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perspectives                    in nutrition



 The volume and composition                                                                            of human                           milk in
 poorly nourished communities
 A review1
 Derrick      B. Jelliffe      and    E. F. Patrice         Jelliffe




              “How is it that poor men’s wives, who                          have no cold fowl or port wine on which to be




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              coshered   up, nurse their children     without                difficulty, whereas  the wives of rich men, who eat
              and drink everything     that is good, cannot                  do so, we will for the present  leave to the doctors
              and mothers    to settle between    them.”

                                                                                                                             Anthony      Trollope      (1847)


    The question          of the composition            and vol-                   comparison             of breast          feeding        and formula
ume of breast milk produced                   by mothers         on                feeding        as they exist in the nutritional,                          hy-
different       planes       of nutrition         at different                     gienic,      and economic                circumstances             usually
phases      of lactation        is a major     issue in pedi-                      found in villages               and urban shanty                towns in
atnic public        health       in the world,       especially                    resource-poor,                less       developed           countries,
in resource-poor           countries.                                              mainly       in the subtropics                and tropics          (77).
    Fundamentally,            ultimate     concerns       are the                      Considerations                of the volume               and com-
nutritional       adequacy         of such milk for young                          position        of breast         milk in poorly             nourished
infants     in relation        to calories,      proteins,       vi-               communities              can only be made                   in relation
tamins,      and minerals,           and the physiological                         to other         ecological           circumstances            affecting
and practical         efficacy      of supplementing            the                both mother             and baby (66, 77). However,
maternal       on infant        diets, when or if neces-                           this paper           attempts           to draw together                 the
sary.                                                                              main       relevant         information              from      different
    However,          it must be stressed              that infant                 parts of the world,                  in which widely              varying
feeding       cannot       be considered           in relation       to            cultural,        genetic,        economic,          and nutritional
the dietary          supply       of nutrients         alone,      but             circumstances               prevail.         Differences,             when
rather      in an ecological             context.      For exam-                   they exist,          may be related                mainly       to nutri-
ple , with regard              to breast        feeding       in less              tion,     to physical             overwork            and/or        to en-
developed           countries,          the nutritional           and              vironmental            psychosocial            stress. Other van-
health       consequences             of the prevention             of             abbes such as maternal                          parasitic        diseases
diarnheab        disease , the lactation               contracep-                  and genetic             physiological             differences           may
tive phenomenon,                  and the economic                and              be more           relevant          than presently              appneci-
agnonomic          considerations            have to be borne                      ated. Variations               in results        in different         stud-
in mind at the same time (77).                                                     ies are difficult          to interpret,           especially         those
    Conversely,          for the majority           of the world,                  of minor          degree,         because         of dissimilarities
breast       feeding        cannot        only be compared                         in times and methods                     of sampling          and anal-
with adequate              feeding         with cow’s        milk        -         ysis, in types and levels of maternal                              under-
that is with sufficient              formula       available      and
with      reasonable            home        hygiene.       From        a                ‘From    the School     of Public Health,    University                  of
practical       point-of-view,           it is more       usually     a            California,     Los Angeles,    California 90024.


492                   The American       Journal    of Clinical        Nutrition      31: MARCH           1978,    pp. 492-515.         Printed      in U.S.A.
VOLUME              AND        COMPOSITION                OF HUMAN                           MILK                                                               493


nutrition,           and        in degrees             of environmental
psyshosocial                stress.

Methods
     Recent      work has reemphasized                         the possibility            of
very considerable             variations         in findings            as a result of
using different          biochemical            methods          . This       is particu-
larly so with regard to protein                    (91).
     The actual         obtaining        of representative                   samples      of                                                                                     ri;u ProcIs.ocin
human        milk poses          unique         problems              as the normal                                                                                                  Alveokts
destination        is the baby’s stomach                   and not a test-tube
or laboratory         container.        The ejection               of breast milk is
mediated        by the psychosomatic                    let-down           reflex (Fig.
 1). Milk production             is proportional              to the secretion            of       FIG . 2 . Prolactin      reflex . Sucking      stimulation     on
anterior      pituitary       hormone        ,   prolactin         ,   resulting      from     breast generates     nerve impulses      which pass to the an-
nipple stimulation            (“prolactin          reflex”)          (Fig. 2), and to          tenor   pituitary,  which secretes      prolactin.      This is car-
the degree        of intra-alveolar            tension,         related        to empty-       ried in the bloodstream         to the breast , where it acts in
ing.    Methods        used     must , therefore             ,    avoid interfering            the alveoli causing      milk secretion    . The     prolactin  pro-
with normal          mechanisms            as much as possible,                     but in     duced is proportional        to the amount       of sucking    stim-
fact, all do so considerably.                      As Hytten               (48) noted,         ulus.




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“the sucking of a baby has, for the mother,                                   psycholog-
ical overtones           beyond       the mere local stimulation                          of   nipple    stimulation                         (and reflex   prolactin                        secretion).
the areola and nipple; and the mechanical                                 replacement          Important      reducers                        of such stimulation                        are comple-
of this local stimulus               cannot         hope to be an entirely                     mentary            bottle      feeds     (allaitement                   mixte)          and       the       early
effective      substitute        for   the   baby”.                                            introduction                of semisolid         foods.
    Diurnal      variations     in milk volume       and composition                              Likewise , questions   of total ouptut      are often based
have been noted (50, 104, 105). The invariable                          and                    on day-time  estimations.   In fact, in traditional     cultures,
considerable         difference     in fat content       between      fore-                    the baby sleeps by the mother’s       side and must obtain
and hind-milk         (1 to 2 g/100 ml) means that the time of                                 considerable                  quantities           as    “night      feedings”                 (A      .   Omo-
sampling      during a feeding        can be significant.                                      lulu, personal     communication).
    In addition,         in some areas of the world,             seasonal                          Two methods         can be used                               to try to measure      the
variation     has been noted - for example,             lower levels of                        volume    produced    -   test feeding                            and expression   (48):
ascorbic     acid in the “hungry          season”   in parts of Africa
(130).     Such seasonal         changes      have long been recog-                            Test     feeding            (test      weighing)
nized by dairy farmers.           The stage of lactation       is another
                                                                                                   In this venerable   technique,                                  the baby                  is weighed
variable,      as is frequency,          intensity   and duration         of
                                                                                               before   and after each feeding.                                  Difficulties                are numer-
                                                                                               ous      and       obvious.             Results          depend          on      the      vigor            of     the
                                                                                               infant and the success of the mother-baby                      interaction.
                                                                                               To ensure larger, more measurable                   samples,       it may be
                                                                                               considered       preferable      for mothers      to nurse their babies
                                                                                               at prescribed          intervals     rather    than on demand               - as
                                                                                               under nonexperimental              conditions     at home . Expensive,
                                                                                               accurate     scales are required          to measure     relatively      small
                                                                                               weight     increases       in an uncooperative         infant . There          is
                                                                                               considerable                  likelihood            of   interference                  with      the        emo-
                                                                                               tionally-sensitive                      let-down         reflex in the unnatural,                            anx-
                                                                       lldk                    iety-producing                      circumstances             and embarrassment                             inev-
                                                                           Alveoko,
                                                                                               itably         created          by      the     investigation,                which           often             have
                                                                                               been carried out in hospitals.        Practically,     there may be
                                                                                               a need for continuous       surveillance         to ensure   that no
                                                                                               feeding   takes place between        weighings,       and, as noted
                                                                                               earlier, ideally this should be on a 24-hr basis, which is
                                                                                               almost never possible.
     FIG. 1 . Letdown               reflex:    the key to successful             lac-
                                                                                               Expression
tation.      Sucking        stimulation         on the breast         generates
nerve      impulses        that pass to the posterior                   pituitary                   Milk may be expressed            from the breast          manually
that secretes        oxytocin        . This   passes via the bloodstream                       and by some form of mechanical                 or electrical       pump.
to the breast,         where it acts on the myoepithelial                     cells,           These methods         can be used to estimate           total output,
surrounding          the milk-containing             alveoli,   causing        their           and, of course,          are required      if samples        are to be
contraction.         This expresses            the milk from the alveoli                       obtained    for analysis.
into the lacteals.             The sequence          is also known          as the                  The same      difficulties    exist as with test feeding.
“milk ejection          reflex.”        Importantly,     it can be inhibited                   Indeed   , anxiety    can be greater      with expression         , espe-


by anxiety        (Fig. 3) and enhanced                by confidence.                          cially with an unfamiliar,            uncomfortable         apparatus,
494                                                              JELLIFFE        AND       JELLIFFE

possibly      combined        with concern       over     feeding    the    baby        poorly      nourished         women        (4) Recent           .  stud-
later    with    the expressed        milk.     Also,      the influence        of
                                                                                        ies in Guatemala               have suggested                 that fat
expression        on prolactin     secretion      ,   compared      with suck-
ling by the baby,         is unknown.
                                                                                        loss may be the main mechanism                             by which
                                                                                        such mothers          can continue          to lactate         (124a).
Results                                                                                     Many        accounts       from       different          parts       of
                                                                                        the world suggest            that malnourished                 women
    Comparative                 results have varied in differ-                         often      lactate     with unexpectedly                 little clini-
ent studies.     In             some,       expression     has given                   cabby obvious            deterioration           of their          nutri-
greater    volumes;                  in others,       test weighing.                   tional status.         However,         in recent years there
Sometimes       daily               outputs      have been calcu-                      may be increasing                evidence         of shorter           pe-
bated from       the               amount        obtained     at one                   nods       of satisfactory           lactation        then previ-
feeding    only. In              all cases, it is apparent         that                ously,      at least in some parts of the world.
results are only                approximations.                                        The effect of maternal                 malnutrition            may be
                                                                                       partly      hormonal,          with decreased               secretion
Maternal            nutrition
                                                                                       of cortisol       and possibly         prolactin       (55a)        Cer-       .


     Comparisons             are also made more difficult                              tainby the cumulative                 effects      of sequential
 by variables              in the nutritional                     status       of      reproductive            cycles,       including          prolonged
 mothers,         both between               mothers          in a partic-             lactation,         can bead to general                   “maternal




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 ubar group           and between              various          communi-               depletion,”          as shown by progressive                     weight
 ties, and by the possibilities                             of different               loss and a prematurely                      aged      appearance
 degrees        of adaptation               (53).       The nutrients                  (78 , 1 24a)         More specific
                                                                                                                        .          nutrient         deficien-
 involved,         the degree           and duration               of depri-           cies may occur with repeated                        reproductive
 vation,      methods          of nutritional               assessment,                cycles        for example
                                                                                                        -                , an     increasingly            large
 and the previous                  nutritional           situation         and         goiter,     anemia,       osteomalacia,            or nutritional
 stores can have many and varying                                combina-              edema (78).
 tions. There             may, for example,                    be consid-
 enable      difference             between          the nutritional                   Environmental                        psychosocial             stress
 past and present              histories          in poorer           women                Under-appreciated                 in the past has been
 in Sao Paobo,             Brazil,       (106a)        in Ibadan,           Ni-        the effect         of environmental                   psychosocial
genia (8-12),             and in Southern                 India (37).                  stress     from       poverty          and unemployment,
     An aspect            of the situation                about         which          from poor housing                and crime , from ilbegiti-
 nothing       is known           is the effect of the nutri-                          macy and family                instability,       and from cub-
tional      status        of the pregnant                  mothers           to-       tural confusion           and uncertainty              on lactation
wards the end of gestation                         on the sensitive,                   performance,           probably           manifested        through
developing            mammary             glands        of the female                  the     effect      of anxiety              on the         bet-down
fetus (89).                                                                            reflex       and possibly
                                                                                                    -                        on the secretion                of
     More       directly,         the physiological                   weight           various      hormones,           such as contisob.            This is
gain in pregnancy,                   about        one-third           due to           mainly of concern              in urban slums and shanty
deposition           of subcutaneous                  fat (“lactation                  towns.       Despite         these       differences,         certain
stores”2)       ;   can vary considerably                        from the              general     findings       seem to be usual and enable
 1 2 .5 kg suggested               for Western             women          to 5         principles      to be suggested              on which practical
kg (or even weight                   boss) reported              in poorly             action     can be based.             These       can be consid-
fed communities                 (53)     .  Dietary          inadequacy                ered under          three       headings-volume,                 com-
in pregnancy                may sometimes                    be compli-                position,       and adequacy                of breast        milk in
cated      by associated               hard work and by re-                            poorly nourished              communities.
stnictive      food customs.                However,            culturally
defined         customs           or physiological                    adjust-          Volume
ments       may bead to less energy                        expenditure                     Well-nourished                        mothers.           To interpret    the
in pregnancy             and lactation.                                                adequacy                   of yields           of breast      milk in mothers
     Likewise,           in all communities,                      lactation
itself leads           to weight           loss. In very ill-fed                           2   An           estimated       average      increase     in body   fat   of 4 kg
mothers,         this can sometimes                   be as much as
                                                                                       (9 Ib) represents      an energy                   store  of some   35,000         kcal,
7 kg after              a year-even                 leading           to the           enough    to subsidize        lactation                by nearly  300 kcal         daily
development               of nutritional             edema           in very           for 3 to 4 months       (53).
VOLUME            AND      COMPOSITION               OF HUMAN                               MILK                                                            495


in communities                 with defective               nutrition,            it   TABLE                 1
is plainly       important           to compare              results        with       Mean intake                         of breast      milk in Swedish                       babies        (1945).
those       from          well-nourished                 communities.                                                                                         Volume        (mean)
                                                                                                            Age
Unfortunately,                such data are scanty,                         out-                                                                     Girls                                  Boy’.
of-date , and difficult                 to compare             because          of                          inc                                                        ml
differences           in technique             and sampling,                 and                             1                                       576                                    645
because         of recent            back of interest                   in the                               2                                       704                                    750
whole subject              of lactation.                                                                     3                                       733                                    798
    In scientific           and international                    literature,                                 6                                       740                                    817

the figure          of 850 mb/day                 is usually           quoted
for the volume               of milk produced                   in the first
                                                                                       TABLE                 2
6 months.           However,           review of the literature                        Daily      volume                    of breast      milk        in Swedish                women              (1975)
of 20 to 25 years ago shows that this was an                                           (91).
arbitrary        estimate          and selected              as an easy-
                                                                                                       Month                                   No.    of                         Breast      milk
to-remember                round         number           based         on an                     postpartum                               mothers                                 volume

“assumption”               in 1950 in the United                      Nations                                    -                                                                    ml
Committee             on Calorie           Requirements                  (34a).                        0-’/2                                     15                             558±83
                                                                                                      /2-            l/2                         11                             724 ± 117
It has become                  sanctified          by repetition                 in




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                                                                                                 1’/2-3’/2                                       12                             752 ± 177
subsequent               international                reports             (34b,                  3’/2-6’/2                                       12                             756 ± 140
 150a) and in the United                         States,        where         the
first (1953)              recommended                  dietary           allow-
ances for babies               were based on the assump-                               the intakes     of 26 healthy     totally   breast     fed
tion that 850 ml of breast                            milk would                be     babies   in lllinois,    with the following       results
produced            from        1 to 3 months                    and 1400              (in mb/day)      (lila).
from 4 to 6 months                   (139a).
    Typical          daily      outputs          of mature               breast                Month                             Mean                         Mm.                            Max.
milk in well-nourished                      women          in the first 6                         1                             606.3                        294.5                          996.1
months        of life can often be less than antici-                                              2                             601.4                        322.0                          892.4
pated      -  between           600 to 700 mb/day                        rather                   3                             625.5                        400.2                          899.9

than the 850 mb/day often quoted,                                     accord-
ing to a recent               interpretation               by Thomson                      In Sweden,         test weighing            by mothers           gave
and Black             (138)       of the data collected                         by     daily volumes             which         were higher,              with a
Morrison          up to 1952 (101).                  However,             much         mean of 838 mb/day (134a).
variation          occurred          between            the results             of         Various        studies        have        been       undertaken
different         investigations,               depending              on the          which have sometimes                     shown         minor       varia-
methods         used and the type of subjects.                               For       tions between           the volume            produced          by each
example,            a Detroit            series       of studies             and       breast,      and on different                 days or times               of
other early investigations                       contained             profes-         nursing.       Diurnal          variation        in the amount
sional     wet-nurses             (104,        105), whose                “con-        secreted       has also been                noted,        often      with
ditioned”          lactation        performance               can be par-              maximal        yields        in the early            morning          and
ticulanly      impressive.                                                             lowest yields towards                evening.
    Carefully          conducted            investigation              of 363              Results      concerning            variation        with age or
babies      of normal            Swedish           mothers            was un-          parity     of mother           have been rightly                 termed
dertaken          30 years ago by Wallgren                              (145),         “confused         and inconclusive.”                   Variation          in
using test-weighing                  at home for 2 consecu-                            volume       of milk secreted              between          individual
tive days (Table                1 Recently,
                                   ).                     L#{246}nnerdal et            women       is recognized            as being considerable,
al. (91) estimated                  the yield of 53 mothers                            although       difficulties        in making           comparisons
in the same country                   by test-weighing                  (Table         are great,       including         variation         in the weight
2)  .   Despite          different           detailed          techniques              and sucking          vigor of the baby                   Breast       size           .


and the intervening                   time between                  the stud-          does not appear             to be related          to yield, being
ies, the results are quite similar.                                                    more an indication                of mammary               fat. How-
    Very recent             studies       show the difficulty                    in    ever, the influence               of emotional             factors      on
interpreting            variation         in results.          For exam-               milk yield has recently                  been reendorsed                by
ple, Picciano              determined              by test weighing                    Lindbbad       et al. (88b) who found that hospi-
496                                                             JELLIFFE          AND      JELLIFFE

 talization            of      healthy           Swedish             mothers              limits by the mother                       has no physiological
 merely         to collect            samples          of milk,           blood           effect on the volume                    of milk secreted.                  This
 and feces caused                   a significant            drop of 210                  seems endocrinobogicalby                         explicable          in light
 mb/24 hr.                                                                                of the renal antidiunetic,                         water-sparing              ef-
     Variation            in yield with “later”                     lactation             fect of pnolactin                (77). The common                       belief
 is difficult         to judge          in webb-nourished                   corn-        that fluid intake               affects milk yield probably
 rnunities        as, until the resurgence                        of interest           operates            more          through             a “sympathetic
 in breast          feeding          of recent           years,        nursing           magic”         effect       on confidence                  (“fluid       in =
 into the second                  semester         of life or longer                    fluid out”),           and hence on the psychosomatic
 has not been usual in Western                             industrialized                “let-down           reflex.”         Conversely,             in what has
 countries.            Also,        there      seems          little doubt              been termed               a “low solute , continuous                        con-
 that the main stimulus                        responsible             for the          tract species”,                such as man,                  human         milk
 volume         of milk produced                   is the amount                 of     with an approximately                          87% water             content
 sucking       at the breast,             and hence of prolactin                        is also the young baby’s                         source        of fluid, as
 secreted.         This is shown                by “induced                bacta-       well as nourishment,                       even in solely breast
 tion”      in some traditional                     societies          and by           fed infants,            including          such a hot climate                   as
 recently        introduced             “adoptive           lactation”          or      Jamaica         (la).
nelactation          in nonbactating             American             women,                 Dominating              considerations                 of the “nor-




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who wish to breast                      feed their adopted                     ba-      mab range”             of milk volume                secreted        by well-
bies. (143a)            In both, frequent                 sucking         at the        nourished           mothers           are difficult          questions          of
breast       is the main factor                     in initiating             and       sampling,            very great              differences            in tech-
continuing           milk secretion.              Likewise,           24% of            nique and timing of collection                             of specimens,
a series         of twins            have been             shown          to be         and individual                 variation            between           women
solely        breast-fed             adequately              for 3 to 6                 and in the same woman , both from day to
months          (1). Also,             the “perpetual,”                    on at        day and as lactation                   progresses          .  As a gener-
beast very prolonged,                      high output              by tnadi-           abization,         technique            and method              of calcuba-
tional       wet-nurses             is in part a reflection                     of      tion often            appear         to play a major                  robe in
continuing           vigorous          sucking        stimulus         by suc-          the final figure brought                      forward.
cessive        hungry          customers.            In fact, the vol-                       Poorly       nourished            mothers.          Estimations            of
ume of milk secreted                           has to be viewed                         the volume               of breast           milk produced                 have
 against       the pattern             of infant         feeding         in the         also been undertaken                        in a variety            of coun-
 particular          family        (or culture)             and the con-                tries      in Asia             and       Africa,           and      in New
 sequent         degree         of sucking            stimulus          and its         Guinea        .   The results              have been              extracted
 effect on the pnolactin                     secretion.                                 from published                  information              and these            ap-
     The common                concept        of the “normal                 pat-       proximations               are presented               in Table 3 De-     .


tern”      in Western-type                   cultures         is of rise in             spite differences                 in methods               of collection,
output       in the first month                  or so , followed               by      sampling,          and analysis,             and bevels and forms
a decline             thereafter           to a plateau                 lasting         of maternal               undernutrition,                 it seems          that
approximately                  until      the baby             is about           6     the volumes               produced            were usually              some-
months           old, followed                by a slow                decline          what below those reported                             from well-noun-
thereafter.            Consideration               of lactation              pat-       ished countries               in Europe            and North Amer-
terns      elsewhere              and the previously                       men-         ica.
tioned        results         in twins,          in wet-nurses,                  in          Volumes             reported            varied          greatly         and
induced          lactation,           and in nelactation,                    sug-       seem to be lowest in communities                                 with poor
gest that the Western                      pattern        may not be a                  levels of nutrition                 and with inadequate                       liv-
biological          inevitable,           but rather            a response              ing conditions,                 whether           urban        (Cobombo,
to a particular                pattern        of sucking             stimula-           Sri Lanka          (30)) or rural (New Guinea                            High-
tion.                                                                                   lands       (5)) . However,                 working           approxima-
     Very few studies                   have been undertaken                            tions      in round             figures         can be suggested:
on dietary             effects        on the volume                   of milk           between           500 to 700 mb/day                        in the first 6
produced           in well-nourished                 women.           By con-           months of life,400 to 600 mb/day                                        in the
trast,     numerous              investigations              have shown                 second        6 months            and 300 to 500 mb/day in
that variation              in water intake              between            wide        the second              year.       The few studies                    under-
VOLUME             AND        COMPOSITION                       OF HUMAN               MILK                                                  497

 TABLE              3
 Approximate                      quantities       of milk     produced         daily     at different          periods     of lactation         in some      poorly         nourished
 communities0

                             Country                                                                                                                                                     24 months
                                                                      1-6   months                       6-12    months                          12-24   months
                            reference                                                                                                                                                    and   above

 India(15,16)                                                  600ml                                 SOOml                            350ml
 India      (Baroda)                 (116,      117)           600 (3 mo)
                        .                                      (350-1100)
                                                               735 (3 mo)
                                                               (540-1100)
 New       Guinea             (Chimbu)            (142)        525 ml                                525 ml                           343 ml                                        343-142            ml
 Biak Island (60)                                              427 ml                                390-430       ml                 127-338       ml                              243 ml
 New Guinea   (14)                                             720 ml                                660 ml                           705 ml                                        488 ml
 New Guinea   (5)                                              400 ml                                400 ml                           400 ml
    Chimbu              and         Maprik
 New       Guinea             (5)                              600 ml                                600 ml                           600   ml
    Baiyer   River
 New    Guinea     (108)                                                                             350-480       ml                 270-360       ml (12-18 mo)                   230-300            ml
                                                                                                                                      200-210       ml (12-24 mo)
 Ajamaru
 Nubuai                                                                                              310-410       ml                 250-340       ml (12-18 mo)




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                                                                                                                                      150-210       ml (18-24 mo)
 Egypt (45)
    Healthy                                                    922 ml
    Malnourished                                               733    ml
 Sri Lanka           (30)                                      475 ml                      495 ml                                     506 ml
 Nigeria        (Benin)                 (81)                   555 ml (2-3          mo)     590 ml (6-9                   mo)         606 ml (13-18           mo)
 Uganda            (122a)                                                         660 ml (2-12  mo)
    a    Results            not      strictly     comparable         as varying         collection        techniques            and   methods       of sampling            used.



 taken      in the third            year of lactation               show                                     palan       showed           an increase            in volume           se-
 very considerable              differences,          varying        from                                    creted,      from 420 to 540 ml in poorly                           nour-
 230 to 488 mb/day.                                                                                          ished      Indian        women          after protein           supple-
      Also, it is well recognized                in practice           that                                  mentation          (from 61 g/day to 90 g/day (36)).
 the output        of extremely          malnourished             moth-                                      Similar        results       were       obtained         in Western
 ers     in families            declines        and        ultimately                                        Nigeria       by Bassir using a vegetable                       protein
 ceases,      with fatal consequences                  for the nurs-                                         supplement-30                  g of soya flour daily (10).
 ing baby           (71).      The      nutritional          point        at                                 Another         study in India, where inadequately
 which       human         lactation       becomes           seriously                                       nourished          mothers          were fed with milk bis-
 inhibited       or ceases in famine                circumstances                                            cuits, showed             a rise in serum             albumen         par-
 is not known , but early marasmus                              (in the                                      abbebed by increase                in albumen          in the breast
 first 9 months             of life) a solely             breast        fed                                  milk,      presumably               by “spill-oven”               (26b).
babies       may be occurring              increasingly           in the                                     Also , an early investigation                    in 1 93 1 , showed
babies        of very         poorly       nourished           women                                         that an increase             in output        could be achieved
living in conditions                 of severe         psychosocial                                          in New Zealand                  women         by increasing            the
stress      - for example           , in   Karachi        , Pakistan                                         calorie      and/on        the protein          intake      (27). Re-
(89). Sometimes               in some countries              this may                                        cently,      a study in England                   seemed        to sug-
be partly         “contraceptive            manasmus,”              from                                     gest that poor lactation                    could be rebated             to
further       interference          with breast          milk secre-                                         inadequate          energy         reserves          in the form of
                                                                                                                                                                       -


tions by oral estrogen-containing                         contracep-                                         subcutaneous              fat laid down              in pregnancy,
tive pills. In pants of the world with seasonal                                                              and      calorie        intakes         in lactation.           In the
food shortages               (“hungry         seasons”),           as in                                     United       Kingdom,           slimming         diets in lactating
Central        Africa,       the daily output              may drop                                          mothers        lead to “an immediate                    reduction        in
by 100 to 200 ml (l43a).                                                                                     milk supply” (148).
     Supplementation.                Limited         studies        have                                        A recent            detailed        investigation           was re-
been carried           out on the effect of supplemen-                                                       ported        by Edozien              and co-workers                from
tation      of the mother’s             diet on output.               Go-                                    Nigeria,       (31b) when they showed                        that pro-
498                                                                              JELLIFFE                   AND    JELLIFFE


tein       supplementation               of      the      lactating                                               less than in dairy      cows,    but it should        be
mother’s         diet increased         the milk produced                                                         remembered       that such farm       animals     have
and weight          in the baby, but not the protein                                                              been bred to produce          much greater       yields
content        of the milk (Table                 4). Similarly,                                                  than are required     by the offspring     (138).
Sosa et al. (128a)                demonstrated              a rapid
                                                                                                                  Composition
increase        in milk production              in a malnour-
ished Guatemalan               woman        following         an im-                                                    The biochemical                 composition              of human
proved        diet, particularly           calories      and pro-                                                 milk has been examined                           in different             parts
 tein.                                                                                                            of the world          .   Approximate              comparisons              can
     As usual , those concerned                    with the pro-                                                  be made between                  various        communities,                and
 duction        of cow’s       milk as a business,                  the                                           with well-nourished                     mothers,           for protein,
 dairy farmers,          have infinitely         more practical                                                   fat, lactose,           vitamins,         and calcium,              keeping
 knowledge           than those concerned                 with hu-                                                in mind            previously           mentioned              difficulties
 man milk and breast                 feeding.        Thus,      Lind-                                             posed         by variations             with sampling                (period
 blad and colleagues                 quoted        the following                                                  in lactation             cycle , time of day ; single , re-
 aphorism         from Morrison’s            1948 Handbook                                                        peated          or 24 hr; seasons;                   one subject               or
 of Stockmen            (101) which may not be com-                                                               pooled           specimens,            etc.),       with       laboratory
                                                                                                                   techniques           and with bevels of difficulties                           in




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 pleteby      correct      for the human,              but is cer-
  tainby generally         so:                                                                                     maternal          nutrition       (Table         5) . Interpretation
      “Any inadequacy             in the ration         or fault in                                                of such comparisons                     is made much greaten
  the methods            of care or management                      will                                           by recent           realizations            of the physiological
  generally       manifest     itself in the yield of milk,                                                        variations           that      occur        in well-fed             healthy
  rather      than      by a change            in its chemical                                                     women           successfully          breast feeding              their ba-
  composition”                                                                                                     bies.
      However,         the effect of increasing              the ma-                                                     Protein.        The protein             content          of human
  ternal     diet on human             milk output           may be                                                 milk has been described                      as varying          between
                                                                                                                    1 .0 to 1 .6 g/100                     ml in well-nourished
 TABLE     4                                                                                                        women.           In 1952,            Morrison           reported            the
 Effect of maternal                dietary          supplementation                      with                       mean of European                   analyses         to be 1 .6 g/l00
 protein          on the volume              and protein           content               of breast                  ml and American                    1 .2 g/lOO ml (101).                      He
 milkand            weight   gained            by baby           (Nigeria)               31b.0
                                                                                                                    suggested           that differences                 in methods               of
                                                       Daily     protein       intake                               estimation           may be mainly                responsible,             and
           Variable’
                                     .     50g           lOOg                   25g                bOg
                                                                                                                    that 1 .2 g/100              ml probably             represented              an
                                         nitially                            initially
                                                                                                                    overall         mean    .   A study           in Britain            showed
  No. of subjects                           7              7                    3                      3             1 .3 g/100         ml (29a).          There       seems little evi-
  Totalmilksolids                         13.8d          13.4                  12.0                  11.9           dence         for significant              diurnal         variation           or
      (g/lOOml)                          ±1.3           ±0.9                  ±0.6                 ±0.5             fluctuation          with age on parity.
  Milk protein                              1 .61          1 .57                 1 .20                1.25
      (g/lOOml)                          ±0.15          ±0.19                 ±0.21                ±0.23
                                                                                                                          However,            very      recent        Swedish             studies
  Milklactose                                8.1               7.9                 7.3                 8.0           (1975)         have shown             the “true           protein        con-
        (g/lOOml)                        ±0.9            ±1.0                 ±1.4                 ±1.8              tent” to be only 0.8 to 0.9%                            in apparently
  Milkproduced                      742                872                   817                 1059                well-nourished                women            in that            country,
        (g/day)                     ±16                ±32                 ±59                   ±63
                                                                                                                     when         determined            by amino             acid analysis
  Milkconsumed                       617               719                   777                  996
     (g/day)                        ±15                ±10          ±38                          ±74
                                                                                                                     (91). These             investigators            pointed          out that
  Weightgainedby                          30.4            45#{149}7e 10.5                          32.2e             earlier       analyses        of breast           milk were made
        baby(g/day)                      ±3.6            ±2.0         ±3.6                       ±10.1               with the same methods                          as used for cow’s
        0 Subjects          were    fed the           initial        diets        for the first              14      milk. In fact, it is now recognized                                that the
      days and then a diet providing              100 g protein       per day                                        relatively        low protein,            low solute character-
      for the next 14 days. Results          for each subject      represent                                          istics of breast            milk place the human                         as a
      the mean        values    for milk samples        collected       during
                                                                                                                      continuous            contact,        frequent          suckling          spe-
      days   8 to 14 (for initial      diet)    and days     21 to 28 (for
      diet  providing        100 g protein      per day).        b Duration
                                                                                                                      cies in infancy,               with rather              slow growth,
      of lactation          for all subjects             was between                        30     and       90       and also permits               breast       milk to be the only
      days.            C   Duration      of            lactation   was                      over     100              supply of water as well as nutrients.
      days.     ii Results   are mean                    values + SD.                         e Signifi-
                                                                                                                           Retrospective              examination                of analyses
      cantly different     at the 0.05                    level from the                     unsupple-
      mented   subjects.
                                                                                                                       undertaken            with similar            methods            in Brus-
VOLUME               AND          COMPOSITION                  OF HUMAN              MILK                                           499


TABLE        5

Fat, lactose,           protein,           and calcium           content        of mature         human      milk    from   some      well-nourished             and poorly
nourished            communities”

                                    Country     (reference)                                                  Fat              Lactose                  Protein                  Calcium

                                                                                                                             g/IOO    ml                                       mgIlOO     ml

Well-Nourished

American(92)                                                                                               4.5                 6.8                      1.1                        34.0
British(87)                                                                                                4.78                6.95                     1.16                       29.9
Australian       (150)                                                                                                                                                        28.6-30.7
British    (29a)                                                                                           4.2                 7.4                      1.3
Poorly-Nourished

Indian(17)                                                                                                 3.42                7.51                     1.06                      34.2
BantuS.Africa(144)                                                                                         3.90                7.10                     1.35                      28.7
Chimbu,        New         Guinea           Highlands           (142)                                      2.36                7.34                     1.01
New       Hebrides          (111)                                                                          3.8                 5.0                      1.40                     25.8
Wuppertal,             Germany                                                                             3.59                                         1.20
       (Immediately                 Post      World       War      II)   (42)
Nauru(19)                                                                                                                                               1.60
Ibadan,       Nigeria         (88 months)               (62)                                                                                  1 .20 (0.59-1.79)
New       Guinea         (Biak)       (60)                                                                                                        0.83-0.9




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Alexandria,     Egypt               (45)
   Healthy                                                                                                 4.43                6.65                    1.09
   Malnourished                                                                                            4.01                6.48                    0.93
New Guinea          (14)                                                                                   2.3                6.48                     0.93
Sri Lanka      (30)                                                                                        2.8                6.8                      1.5
Brazil   (21)
   Higheconomic                                                                                            3.9                6.8                      1.3                       20.8
   Loweconomic                                                                                             4.2                6.5                      1.3                       25.7
Pakistan   (139)                                                                                                                                       1.2
Tanzania    (25)                                                                                  Often    below      2%
Nigeria(Ibadan)(102)                                                                                       4.05               7.67                     1.22
   a   Modified          from        Gopalan          and Belavady              (37),     with     added     data.



sels, Belgium      (129) in 1954 and in Tokyo,                                                             although         the lysine        and methionine               levels
Japan     (1 23) shows similar          “low”    levels for                                                were lower.
“true   protein   content”       as with recent       Swed-                                                    Varying        results     have been obtained                  with
ish figures.                                                                                               estimations         of the protein          content       with what
     In poorer,    technically       developing        coun-                                               is termed        by modern           Western        cultural       defi-
tries,   the average        protein      content     of the                                                nition      “prolonged           lactation”           that is into
                                                                                                                                                                     -


milk    of inadequately           nourished       mothers,                                                 the second         year of life and later. Some have
based        on        previously                 used          methods            of     total            found a decline,             some a rise, and others                  no
nitrogen             assessment,   is usually      surprisingly                                            material       change.
high-in        fact, a low normal              (1 .0 to 1 .1 g/                                                The effect of maternal                dietary      suppbemen-
 100 ml), although              the range       may be quite                                               tation     on protein          content        does not appear
wide (Table         5).                                                                                    to have been investigated                   adequately.         How-
     In some places with probably                   poorer       flu-                                      ever, in the protein               supplementation               study
trition,     analyses       with older        methods         have                                         carried      out by Gopaban,               the increased            out-
sometimes         shown      the protein        content      to be                                         put of milk was associated                        with a come-
lower (0.8 to 0.9%).                 However,         in a care-                                           sponding        fall in protein          concentration,            with
fully carried        out study of poorly              nourished                                            the result that the total protein                    output      in 24
women       in Karachi,         Pakistan,      the “true pro-                                              hr was not significantly                    altered       (36, 37).
tein content,”          determined          by an exchange                                                 Also,      modern         laboratory         methods         such as
chromatography              after     acid hydrolysis           and                                        immunoelectrophoresis,                    which       enables        ac-
adding      up the calculated              amino       acid resi-                                          curate      quantities        and measurement                  of the
dues, was 0.8 ± 0.1 g/100                    ml (89). These                                                individual        proteins      of milk to be made were
results    are similar        to those obtained            by like                                         not available          at the time of earlier                studies.
techniques        in Sweden,         Belgium,       and Japan,                                                 Recent       investigations          by L#{246}nnendal et al.
500                                                               JELLIFFE          AND     JELLIFFE

 (91) have shown                    many unexplained                       vania-         breast     milk (or cow’s milk based                     formula)
tions in healthy,                   well-fed           women-for                ex-       appears      to be reflected         in the fatty acids in
ample,         in “milk-specific                      proteins,”            those         the infant’s      subcutaneous         fat.
synthesized              by the mammary                         gland,          no-            The relevance        of the fatty acid (and cho-
 tabby ct-lactalbumin                      and lactoferrin                .    The        lestenol)    contents      of human        milk is currently
decrease         in total nitrogen                   in the first period                  under consideration            in relation        to the deveb-
of lactation,            for example              in the first month,                     opment       of the central         nervous         system      and
was mainly due to a dramatic                                drop in secre-                atheroma        in adults      in industrialized             coun-
tory IgA bevel.                                                                           tries. In developing            regions,       the pobyenoic
    Fat (lipid)         . The significance                  of the fat con-               fatty acids may be diminished                    in the breast
tent of milk has been under-emphasized.                                            It     milk of malnourished             mothers,       with possible
is the main source                     of calories;              it contains              ill-consequences         in relation        to brain growth
fat soluble           vitamins,            especially           vitamin          A;       (25).
it is also the source                    of essential             fatty acids                Lactose.       The third “proximate                principle,”
needed        for the growth                  and development                     of      lactose,       is generally        recognized             as being
the central            nervous            system           (24b).        Lastly,          most constant            in concentration             and shows
the higher fat in the after-milk                              may act as a                no diurnal        variation.      Morrison’s            (101)      fig-
physicochemical                    appetite            control         for the            une based         on 1010        samples         examined             in




                                                                                                                                                                     Downloaded from www.ajcn.org by on August 22, 2009
suckling        baby (44).                                                                various        American        and European                  studies
    Earlier        estimations              of the fat content                    of      showed        a mean of 7.2 g/100 ml, while Kon
milk in webb-nourished                         communities                in the          and Mawson             found     6.9 g/100            ml in 586
United       States and Britain                      showed         means of              samples        of mature         milk (87).            In poorly
4.5 (93) and 4.78 g/100                               ml (87),          respec-           nourished         mothers,      lactose       also does not
lively. A more recent                       1977 study showed                       a     seem to vary very much (Table                           5) (range
mean of 4.2 g/100 ml (29a).                                                               6.43 to 7.51 g/l00            ml), except          in one study
    Results         from poorly              fed women               in devel-            in the New Hebrides                where        5.0      g/100      ml
oping countries                  have demonstrated                       consid-          was reported         (111).
enable variation                  (Table        5). However,                some              Calories.      The calorie        intake        from breast
recent      work has suggested                         that the fat may                   milk is a product            of the volume              (as taken
sometimes             be considerably                     reduced,           even         by the baby) and its caloric                 content,          which
down to 1 g/100 ml (24b). Under these                                                     is primarily        derived      from fat. In well-fed
circumstances              ,    the calorie              content          of the          communities,            the caloric          content           varies
milk may be much decreased                                     with signifi-              greatly.      Macy and Kelly (92) give a mean
cant lessening                of energy            intake       (24a).         The        figure of 75 kcab/100            ml (range           45 to 119).
significance           of a bower fat content                       has to be             The recent        United     Kingdom          report        showed
related      to inadequate                 energy         intake in pneg-                 a mean of 70 kcab/100 ml (29a).
nancy,        with         an inadequate                     subcutaneous                     In poorly nourished communities,                             both
“fat bank”             (53),        as well as to the diet in                             the volume secreted and the fat, the main
lactation        itself.                                                                  calorie-containing constituent, (and other
    The fatty acid pattern                        of breast          milk can             nutrients) may be less than in well-fed                       moth-
be altered           to some extent                   without        affecting            ens.
milk volume               or milk fat output                   by variation
                                                                                          Vitamins
in the types of dietary                    fat (especially              if these
are extreme)                 (25a)       on by changes                    in the              Vitamin       A . The        concentration       is influ-
calorie       intake           (57,       147).          During          energy           enced       by the adequacy             of the diet of the
equilibrium,               milk fat resembles                       the fatty             mother         in pregnancy           and lactation.       The
acid pattern            of dietary           fat, but when inade-                         vitamin       A content         of breast       milk is often
quate      calories           are eaten,             the fat in human                     much lower in poorer                 populations     of some
milk follows            the composition                   of human            sub-        developing         countries       (India , Ceylon , Indo-
cutaneous           depot fat. The major factor influ-                                    nesia,     Jordan),       where      this nutrient     is mar-
encing      the fatty acid composition                             of milk is             ginal, than in Europe                and North      America.
the carbohydrate                    supply          in the diet. Ulti-                    Maternal         serum       bevels are also low. The
mately,         the fatty acid composition                                of the          intake      is generally       higher     in the spring and
VOLUME           AND       COMPOSITiON             OF HUMAN            MILK                                        501


summer           months          due to greaten               supplies         of        Niacin.        Although            human        milk is bow in
dark       green        leafy        and yellow               vegetables.            actual      niacin,       it has a high potential                    niacin
Particularly           high levels            of netinob            (vitamin         value because               this vitamin           may be synthe-
A) have           been        noted        in Western               Nigeria,         sized from the amino acid, tryptophan.
presumably            because          of the widespread                    use          Vitamin         B12. Low bevels of vitamin                            B12
of palm oil in cooking                    (102).                                     have      been        found         in the milk              of poorer
     In a recent         comparative              investigation           , the      vegetarian         women           in Bombay.           Also, in var-
vitamin        A content           of breast         milk was signifi-               ious      parts        of India            the      “syndrome               of
cantly       higher         in normal             Swedish           mothers          tremors”           have        been       described            in solely
than in nonpnivileged                       Ethiopian             mothers,           breast      fed babies,           and has been ascribed                     to
whose        milk showed               greater         concentrations                deficient       B12 in the mother’s                 milk (59).
of f3-carotene             (35).                                                         Vitamin        C. The level of ascorbic                         acid in
     Kcn and Mawson                   (87) found that supple-                        breast milk is subject                 to variations          in dietary
mentation           with vitamin             A, before           and after           intake      in developing              countries,         particularly
partunition          or later during                lactation,          bed to      with the seasonal                 availability         of fresh fruits
the secretion              of milk richer                in vitamin            A     and vegetables.               In webb-nourished                 mothers,
than normally               produced.            In Central            Amer-        human          milk contains              an average            of 4 mg/
ica, Arroyave               et al. (3) observed                    a rise in         100 ml of vitamin                C. In Botswana               (formerly




                                                                                                                                                                      Downloaded from www.ajcn.org by on August 22, 2009
the breast           milk vitamin              A levels           after the         Bechuanaband),                   Squires        (130)        found        the
introduction            of vitamin          A fortified           sugar.            content         to be 1 .7 mg/100                    ml in the dry
    Vitamin         D. As well-known,                      levels of fat-           season        and 2.7 mg/100                  ml in the wet sea-
soluble        vitamin         D are low in both human                              sons. The subjects                    were poorly             nourished
and bovine            milks. However,                  the recent          dis-     Tswana         women.
covery        that breast             milk contains                a water-              Since the ascorbic                 acid contant            of breast
soluble         conjugate           of vitamin              D with sub-             milk is greater               than that of blood                   plasma,
phate (87a) producing                     the same anti-nachitic                    which        is generally             below       2.5 mg/100              ml,
potential          as milk formulas                     fortified         with      secretory          activity        in the mammary                    glands
conventional             vitamin         D explains              the clini-         must play a part in determining                            the bevel of
cally well-recognized                   rarity of rickets               in the      vitamin        C in milk. Apparent                     adaptation           to
breast fed.                                                                         low maternal             intakes        of vitamin         C has been
    Thiamine.           The thiamine               content        of breast         noted       in Banoda,            India (117)           and the Phil-
milk in areas with a high incidence                                of infan-        ippines        (132).        The possibility              of placental
tile beriberi          has been found to be low, due                                synthesis        in pregnancy              has been suggested.
to insufficient            maternal          stores and intake                in    Certainly         both the placenta                 and the breasts
communities               with diets            largely         based        on     may be abbe to actively                           secrete         ascorbic
polished          rice (66)         .   Under          these         circum-        acid for the offspring.                     Levels       of fobic acid
stances,         a specific          form       of malnutrition               -     and vitamin              B6 seem            to reflect          maternal
infantile       beriberi       -   occurs exclusively                 in nor-       nutritional         status       (106a,       85).
mab-seeming              breast       fed babies,             and is due
to a thiamine-deficient                       diet in the mother
                                                                                    Vitamin        supplementation
during        pregnancy             and lactation             .    It is so
characteristic           in time of onset that the 2 to                                 Deodhar        and Ramakrishnan              (28) carried
5 month          mortality         has been suggested                    as an      out a dietary        survey among          women       in South
age-specific           rate for this condition                         in the       India with special            reference       to pantothenic
regions       at risk.                                                              acid, riboflavin,         nicotinic     acid, ascorbic       acid
    Riboflavin.           Human          milk is a good source                      and thiamin.          Subsequently,          the breast      milk
of riboflavin,            provided          the maternal               diet is      was analyzed           for the concentrations              of the
adequate. However,                     in South           India,       Gopa-        same      vitamins.       A positive         and significant
ban and Belavady                  (37) found            an average            of    correlation        was found         between       dietary     in-
only 17.2 pg/100                  ml of riboflavin                in breast         take and vitamin            content     of the milk for the
milk, as compared                   with a value of about 25                        vitamins      investigated,         which underlines          the
g/100          ml found            by Kon and Mawson                          in    need for an adequate                diet for the lactating
Britain (87).                                                                       women.         The content           of all the vitamins
502                                                      JELLIFFE        AND     JELLIFFE

increased        steadily        with the dose of supple-                          In this regard,           it is often     insufficiently
mentation.                                                                     appreciated          that the RDA’s          given      for in-
    In a more            recent      investigation,           supple-          fants are themselves            derived   from estimated
mentation         with ascorbic           acid, nicotinic         acid,        intakes        of breast    fed babies,      with an addi-
riboflavin,        thiamin,        pantothenic          acid, cyan-            tional safety factor added for the less certain
ocobalamin,             biotin,      pyridoxine,          and folic            situation        of infants     fed on cow’s milk for-
acid was undertaken.                   As a result,            the vi-         mulas       (70). This is the case, for example,
tamin content            of the milk increased               steadily          with the very high RDA                  of iron (1 0 mg/
with the dose used in supplementation                             (29).        day) for the first 6 months                 of life , which
    Calcium       .   Levels       of calcium         reported          in     can not be attained            with human       milk.
the milk of webb-fed mothers                      vary consider-                   The derivation          of RDA’s      for infants        are
ably. The calcium                 content      in poorly         nour-         often      not understood            by pediatricians          or
ished mothers              has been reported               to range            nutritionists,        so that the advertising         of corn-
from “normal”               levels to somewhat              bow con-           mercial        baby foods can issue the following
centrations          (Table      5). Again,        differences          in     appeal      to “logic”:
sampling         and technique                may be in part
responsible.                                                                          “A stimulating     exercise   for professionals would
    Levels of other minerals                   will not be con-                   be sorting one’s beliefs about breast feeding         into




                                                                                                                                                                     Downloaded from www.ajcn.org by on August 22, 2009
                                                                                  those based on scientific       fact and those stemming
sidered       here,      but are presented               elsewhere
                                                                                  from hearsay       and emotion.     One could thus more
(77). Early analyses                are given by Morrison                         objectively      counsel          that     growing       membership           in
and others          (101).      The question           of the con-                lay organizations             dedicated              to breast     feeding.
tent of trace minerals                 will be much             under             Many    sincerely          believe      that          breast   milk is all
                                                                                  sufficient    without       any     supplementation            for at least
investigation           in coming          years,      in relation
                                                                                  six months       if not     the     full duration         of breast   feed-
both      to nutritional            need      and to possible                     ing.  The     fallacy of this concept    is obvious if one
effects     of environmental               pollution.                             compares       the nutrient  content  of breast milk with
                                                                                  recommended          RDA          for    infants.”
Adequacy
    The nutritional               adequacy        of breast        milk            The inanity         of this comment                is apparent
for the infant              can be roughly             assessed       by       especially        in view of the biological                   adapta-
measuring            24-hr output          and chemical           corn-        tion that has occurred                    over hundreds                of
position       , or    by the recording            of satisfactory             mibbenia. Carried            to extremes,          this argument
growth,         “good health”            and absence         of clini-         would      mean       that breast         milk was unfit for
cab malnutrition.                                                              consumption           by human          babies,        without       ad-
    Adequacy             of nutrients.           The       “nutrient           ditional      iron and vitamins.
needs”        of the baby during the exterogestate                                 The RDA’s            of protein         and calories           sug-
fetal stage           are not derived             only from the                gested      for infants        have been derived                 from
diet, but also from fetal stores                       acquired        in      breast     milk estimations,             feeding        with cow’s
utero,      from the placental               transfusion        (iron)         milk based          formulas        and from the impon-
and, to a limited                and variable         extent      from         tant,     but special,          studies        by Fomon             and
ultraviolet          irradiation        of the skin (vitamin                   May (1958)           on babies bottle fed ad bibiturn
D). The recommended                       daily dietary         allow-         with pasteurized            breast milk (33). Based on
ances        (RDA)            for babies          are     estimated            their findings,           it has been            suggested         that
mainly “by analogy                 with breast fed infants,”                   infants     need:      1 st month           836 mb/day
                                                                                                                                 -              (pro-
and yet it is agreed                 increasingly         that pres-           tein 2.6 g/kg; cab 143kg);                   6th month-990
entby available              data on the composition                   of      ml/day      (protein       1 .7 g/kg; cal 90k).
human         milk is incomplete               and out-of-date.                    However,          as noted          earlier,        outputs        in
Fomon         (34) rightly notes the need for more                             well-nourished           women       actually        nursing      their
modern            studies,       and remarks            that    “until         babies often supply less than this, a common
such data are available,                   many of our calcu-                  range being 600-700                 mb/day for the first 6
lations      rebating        to nutrients        in human          milk        months          (138). Among               poorly nourished
will be likely              to be misleading”.                 Recent          tropical        communities             estimated           volumes
Swedish          studies      (91) on the protein             content          often seem to range from 500-700                               mb/day
of breast milk give urgency                    to this comment.                during      the first six months              (Table       4).
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review
The Volume And Composition Of Human Milk In Poorly Nourished Communities   A Review

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The Volume And Composition Of Human Milk In Poorly Nourished Communities A Review

  • 1. perspectives in nutrition The volume and composition of human milk in poorly nourished communities A review1 Derrick B. Jelliffe and E. F. Patrice Jelliffe “How is it that poor men’s wives, who have no cold fowl or port wine on which to be Downloaded from www.ajcn.org by on August 22, 2009 coshered up, nurse their children without difficulty, whereas the wives of rich men, who eat and drink everything that is good, cannot do so, we will for the present leave to the doctors and mothers to settle between them.” Anthony Trollope (1847) The question of the composition and vol- comparison of breast feeding and formula ume of breast milk produced by mothers on feeding as they exist in the nutritional, hy- different planes of nutrition at different gienic, and economic circumstances usually phases of lactation is a major issue in pedi- found in villages and urban shanty towns in atnic public health in the world, especially resource-poor, less developed countries, in resource-poor countries. mainly in the subtropics and tropics (77). Fundamentally, ultimate concerns are the Considerations of the volume and com- nutritional adequacy of such milk for young position of breast milk in poorly nourished infants in relation to calories, proteins, vi- communities can only be made in relation tamins, and minerals, and the physiological to other ecological circumstances affecting and practical efficacy of supplementing the both mother and baby (66, 77). However, maternal on infant diets, when or if neces- this paper attempts to draw together the sary. main relevant information from different However, it must be stressed that infant parts of the world, in which widely varying feeding cannot be considered in relation to cultural, genetic, economic, and nutritional the dietary supply of nutrients alone, but circumstances prevail. Differences, when rather in an ecological context. For exam- they exist, may be related mainly to nutri- ple , with regard to breast feeding in less tion, to physical overwork and/or to en- developed countries, the nutritional and vironmental psychosocial stress. Other van- health consequences of the prevention of abbes such as maternal parasitic diseases diarnheab disease , the lactation contracep- and genetic physiological differences may tive phenomenon, and the economic and be more relevant than presently appneci- agnonomic considerations have to be borne ated. Variations in results in different stud- in mind at the same time (77). ies are difficult to interpret, especially those Conversely, for the majority of the world, of minor degree, because of dissimilarities breast feeding cannot only be compared in times and methods of sampling and anal- with adequate feeding with cow’s milk - ysis, in types and levels of maternal under- that is with sufficient formula available and with reasonable home hygiene. From a ‘From the School of Public Health, University of practical point-of-view, it is more usually a California, Los Angeles, California 90024. 492 The American Journal of Clinical Nutrition 31: MARCH 1978, pp. 492-515. Printed in U.S.A.
  • 2. VOLUME AND COMPOSITION OF HUMAN MILK 493 nutrition, and in degrees of environmental psyshosocial stress. Methods Recent work has reemphasized the possibility of very considerable variations in findings as a result of using different biochemical methods . This is particu- larly so with regard to protein (91). The actual obtaining of representative samples of ri;u ProcIs.ocin human milk poses unique problems as the normal Alveokts destination is the baby’s stomach and not a test-tube or laboratory container. The ejection of breast milk is mediated by the psychosomatic let-down reflex (Fig. 1). Milk production is proportional to the secretion of FIG . 2 . Prolactin reflex . Sucking stimulation on anterior pituitary hormone , prolactin , resulting from breast generates nerve impulses which pass to the an- nipple stimulation (“prolactin reflex”) (Fig. 2), and to tenor pituitary, which secretes prolactin. This is car- the degree of intra-alveolar tension, related to empty- ried in the bloodstream to the breast , where it acts in ing. Methods used must , therefore , avoid interfering the alveoli causing milk secretion . The prolactin pro- with normal mechanisms as much as possible, but in duced is proportional to the amount of sucking stim- fact, all do so considerably. As Hytten (48) noted, ulus. Downloaded from www.ajcn.org by on August 22, 2009 “the sucking of a baby has, for the mother, psycholog- ical overtones beyond the mere local stimulation of nipple stimulation (and reflex prolactin secretion). the areola and nipple; and the mechanical replacement Important reducers of such stimulation are comple- of this local stimulus cannot hope to be an entirely mentary bottle feeds (allaitement mixte) and the early effective substitute for the baby”. introduction of semisolid foods. Diurnal variations in milk volume and composition Likewise , questions of total ouptut are often based have been noted (50, 104, 105). The invariable and on day-time estimations. In fact, in traditional cultures, considerable difference in fat content between fore- the baby sleeps by the mother’s side and must obtain and hind-milk (1 to 2 g/100 ml) means that the time of considerable quantities as “night feedings” (A . Omo- sampling during a feeding can be significant. lulu, personal communication). In addition, in some areas of the world, seasonal Two methods can be used to try to measure the variation has been noted - for example, lower levels of volume produced - test feeding and expression (48): ascorbic acid in the “hungry season” in parts of Africa (130). Such seasonal changes have long been recog- Test feeding (test weighing) nized by dairy farmers. The stage of lactation is another In this venerable technique, the baby is weighed variable, as is frequency, intensity and duration of before and after each feeding. Difficulties are numer- ous and obvious. Results depend on the vigor of the infant and the success of the mother-baby interaction. To ensure larger, more measurable samples, it may be considered preferable for mothers to nurse their babies at prescribed intervals rather than on demand - as under nonexperimental conditions at home . Expensive, accurate scales are required to measure relatively small weight increases in an uncooperative infant . There is considerable likelihood of interference with the emo- tionally-sensitive let-down reflex in the unnatural, anx- lldk iety-producing circumstances and embarrassment inev- Alveoko, itably created by the investigation, which often have been carried out in hospitals. Practically, there may be a need for continuous surveillance to ensure that no feeding takes place between weighings, and, as noted earlier, ideally this should be on a 24-hr basis, which is almost never possible. FIG. 1 . Letdown reflex: the key to successful lac- Expression tation. Sucking stimulation on the breast generates nerve impulses that pass to the posterior pituitary Milk may be expressed from the breast manually that secretes oxytocin . This passes via the bloodstream and by some form of mechanical or electrical pump. to the breast, where it acts on the myoepithelial cells, These methods can be used to estimate total output, surrounding the milk-containing alveoli, causing their and, of course, are required if samples are to be contraction. This expresses the milk from the alveoli obtained for analysis. into the lacteals. The sequence is also known as the The same difficulties exist as with test feeding. “milk ejection reflex.” Importantly, it can be inhibited Indeed , anxiety can be greater with expression , espe- by anxiety (Fig. 3) and enhanced by confidence. cially with an unfamiliar, uncomfortable apparatus,
  • 3. 494 JELLIFFE AND JELLIFFE possibly combined with concern over feeding the baby poorly nourished women (4) Recent . stud- later with the expressed milk. Also, the influence of ies in Guatemala have suggested that fat expression on prolactin secretion , compared with suck- ling by the baby, is unknown. loss may be the main mechanism by which such mothers can continue to lactate (124a). Results Many accounts from different parts of the world suggest that malnourished women Comparative results have varied in differ- often lactate with unexpectedly little clini- ent studies. In some, expression has given cabby obvious deterioration of their nutri- greater volumes; in others, test weighing. tional status. However, in recent years there Sometimes daily outputs have been calcu- may be increasing evidence of shorter pe- bated from the amount obtained at one nods of satisfactory lactation then previ- feeding only. In all cases, it is apparent that ously, at least in some parts of the world. results are only approximations. The effect of maternal malnutrition may be partly hormonal, with decreased secretion Maternal nutrition of cortisol and possibly prolactin (55a) Cer- . Comparisons are also made more difficult tainby the cumulative effects of sequential by variables in the nutritional status of reproductive cycles, including prolonged mothers, both between mothers in a partic- lactation, can bead to general “maternal Downloaded from www.ajcn.org by on August 22, 2009 ubar group and between various communi- depletion,” as shown by progressive weight ties, and by the possibilities of different loss and a prematurely aged appearance degrees of adaptation (53). The nutrients (78 , 1 24a) More specific . nutrient deficien- involved, the degree and duration of depri- cies may occur with repeated reproductive vation, methods of nutritional assessment, cycles for example - , an increasingly large and the previous nutritional situation and goiter, anemia, osteomalacia, or nutritional stores can have many and varying combina- edema (78). tions. There may, for example, be consid- enable difference between the nutritional Environmental psychosocial stress past and present histories in poorer women Under-appreciated in the past has been in Sao Paobo, Brazil, (106a) in Ibadan, Ni- the effect of environmental psychosocial genia (8-12), and in Southern India (37). stress from poverty and unemployment, An aspect of the situation about which from poor housing and crime , from ilbegiti- nothing is known is the effect of the nutri- macy and family instability, and from cub- tional status of the pregnant mothers to- tural confusion and uncertainty on lactation wards the end of gestation on the sensitive, performance, probably manifested through developing mammary glands of the female the effect of anxiety on the bet-down fetus (89). reflex and possibly - on the secretion of More directly, the physiological weight various hormones, such as contisob. This is gain in pregnancy, about one-third due to mainly of concern in urban slums and shanty deposition of subcutaneous fat (“lactation towns. Despite these differences, certain stores”2) ; can vary considerably from the general findings seem to be usual and enable 1 2 .5 kg suggested for Western women to 5 principles to be suggested on which practical kg (or even weight boss) reported in poorly action can be based. These can be consid- fed communities (53) . Dietary inadequacy ered under three headings-volume, com- in pregnancy may sometimes be compli- position, and adequacy of breast milk in cated by associated hard work and by re- poorly nourished communities. stnictive food customs. However, culturally defined customs or physiological adjust- Volume ments may bead to less energy expenditure Well-nourished mothers. To interpret the in pregnancy and lactation. adequacy of yields of breast milk in mothers Likewise, in all communities, lactation itself leads to weight loss. In very ill-fed 2 An estimated average increase in body fat of 4 kg mothers, this can sometimes be as much as (9 Ib) represents an energy store of some 35,000 kcal, 7 kg after a year-even leading to the enough to subsidize lactation by nearly 300 kcal daily development of nutritional edema in very for 3 to 4 months (53).
  • 4. VOLUME AND COMPOSITION OF HUMAN MILK 495 in communities with defective nutrition, it TABLE 1 is plainly important to compare results with Mean intake of breast milk in Swedish babies (1945). those from well-nourished communities. Volume (mean) Age Unfortunately, such data are scanty, out- Girls Boy’. of-date , and difficult to compare because of inc ml differences in technique and sampling, and 1 576 645 because of recent back of interest in the 2 704 750 whole subject of lactation. 3 733 798 In scientific and international literature, 6 740 817 the figure of 850 mb/day is usually quoted for the volume of milk produced in the first TABLE 2 6 months. However, review of the literature Daily volume of breast milk in Swedish women (1975) of 20 to 25 years ago shows that this was an (91). arbitrary estimate and selected as an easy- Month No. of Breast milk to-remember round number based on an postpartum mothers volume “assumption” in 1950 in the United Nations - ml Committee on Calorie Requirements (34a). 0-’/2 15 558±83 /2- l/2 11 724 ± 117 It has become sanctified by repetition in Downloaded from www.ajcn.org by on August 22, 2009 1’/2-3’/2 12 752 ± 177 subsequent international reports (34b, 3’/2-6’/2 12 756 ± 140 150a) and in the United States, where the first (1953) recommended dietary allow- ances for babies were based on the assump- the intakes of 26 healthy totally breast fed tion that 850 ml of breast milk would be babies in lllinois, with the following results produced from 1 to 3 months and 1400 (in mb/day) (lila). from 4 to 6 months (139a). Typical daily outputs of mature breast Month Mean Mm. Max. milk in well-nourished women in the first 6 1 606.3 294.5 996.1 months of life can often be less than antici- 2 601.4 322.0 892.4 pated - between 600 to 700 mb/day rather 3 625.5 400.2 899.9 than the 850 mb/day often quoted, accord- ing to a recent interpretation by Thomson In Sweden, test weighing by mothers gave and Black (138) of the data collected by daily volumes which were higher, with a Morrison up to 1952 (101). However, much mean of 838 mb/day (134a). variation occurred between the results of Various studies have been undertaken different investigations, depending on the which have sometimes shown minor varia- methods used and the type of subjects. For tions between the volume produced by each example, a Detroit series of studies and breast, and on different days or times of other early investigations contained profes- nursing. Diurnal variation in the amount sional wet-nurses (104, 105), whose “con- secreted has also been noted, often with ditioned” lactation performance can be par- maximal yields in the early morning and ticulanly impressive. lowest yields towards evening. Carefully conducted investigation of 363 Results concerning variation with age or babies of normal Swedish mothers was un- parity of mother have been rightly termed dertaken 30 years ago by Wallgren (145), “confused and inconclusive.” Variation in using test-weighing at home for 2 consecu- volume of milk secreted between individual tive days (Table 1 Recently, ). L#{246}nnerdal et women is recognized as being considerable, al. (91) estimated the yield of 53 mothers although difficulties in making comparisons in the same country by test-weighing (Table are great, including variation in the weight 2) . Despite different detailed techniques and sucking vigor of the baby Breast size . and the intervening time between the stud- does not appear to be related to yield, being ies, the results are quite similar. more an indication of mammary fat. How- Very recent studies show the difficulty in ever, the influence of emotional factors on interpreting variation in results. For exam- milk yield has recently been reendorsed by ple, Picciano determined by test weighing Lindbbad et al. (88b) who found that hospi-
  • 5. 496 JELLIFFE AND JELLIFFE talization of healthy Swedish mothers limits by the mother has no physiological merely to collect samples of milk, blood effect on the volume of milk secreted. This and feces caused a significant drop of 210 seems endocrinobogicalby explicable in light mb/24 hr. of the renal antidiunetic, water-sparing ef- Variation in yield with “later” lactation fect of pnolactin (77). The common belief is difficult to judge in webb-nourished corn- that fluid intake affects milk yield probably rnunities as, until the resurgence of interest operates more through a “sympathetic in breast feeding of recent years, nursing magic” effect on confidence (“fluid in = into the second semester of life or longer fluid out”), and hence on the psychosomatic has not been usual in Western industrialized “let-down reflex.” Conversely, in what has countries. Also, there seems little doubt been termed a “low solute , continuous con- that the main stimulus responsible for the tract species”, such as man, human milk volume of milk produced is the amount of with an approximately 87% water content sucking at the breast, and hence of prolactin is also the young baby’s source of fluid, as secreted. This is shown by “induced bacta- well as nourishment, even in solely breast tion” in some traditional societies and by fed infants, including such a hot climate as recently introduced “adoptive lactation” or Jamaica (la). nelactation in nonbactating American women, Dominating considerations of the “nor- Downloaded from www.ajcn.org by on August 22, 2009 who wish to breast feed their adopted ba- mab range” of milk volume secreted by well- bies. (143a) In both, frequent sucking at the nourished mothers are difficult questions of breast is the main factor in initiating and sampling, very great differences in tech- continuing milk secretion. Likewise, 24% of nique and timing of collection of specimens, a series of twins have been shown to be and individual variation between women solely breast-fed adequately for 3 to 6 and in the same woman , both from day to months (1). Also, the “perpetual,” on at day and as lactation progresses . As a gener- beast very prolonged, high output by tnadi- abization, technique and method of calcuba- tional wet-nurses is in part a reflection of tion often appear to play a major robe in continuing vigorous sucking stimulus by suc- the final figure brought forward. cessive hungry customers. In fact, the vol- Poorly nourished mothers. Estimations of ume of milk secreted has to be viewed the volume of breast milk produced have against the pattern of infant feeding in the also been undertaken in a variety of coun- particular family (or culture) and the con- tries in Asia and Africa, and in New sequent degree of sucking stimulus and its Guinea . The results have been extracted effect on the pnolactin secretion. from published information and these ap- The common concept of the “normal pat- proximations are presented in Table 3 De- . tern” in Western-type cultures is of rise in spite differences in methods of collection, output in the first month or so , followed by sampling, and analysis, and bevels and forms a decline thereafter to a plateau lasting of maternal undernutrition, it seems that approximately until the baby is about 6 the volumes produced were usually some- months old, followed by a slow decline what below those reported from well-noun- thereafter. Consideration of lactation pat- ished countries in Europe and North Amer- terns elsewhere and the previously men- ica. tioned results in twins, in wet-nurses, in Volumes reported varied greatly and induced lactation, and in nelactation, sug- seem to be lowest in communities with poor gest that the Western pattern may not be a levels of nutrition and with inadequate liv- biological inevitable, but rather a response ing conditions, whether urban (Cobombo, to a particular pattern of sucking stimula- Sri Lanka (30)) or rural (New Guinea High- tion. lands (5)) . However, working approxima- Very few studies have been undertaken tions in round figures can be suggested: on dietary effects on the volume of milk between 500 to 700 mb/day in the first 6 produced in well-nourished women. By con- months of life,400 to 600 mb/day in the trast, numerous investigations have shown second 6 months and 300 to 500 mb/day in that variation in water intake between wide the second year. The few studies under-
  • 6. VOLUME AND COMPOSITION OF HUMAN MILK 497 TABLE 3 Approximate quantities of milk produced daily at different periods of lactation in some poorly nourished communities0 Country 24 months 1-6 months 6-12 months 12-24 months reference and above India(15,16) 600ml SOOml 350ml India (Baroda) (116, 117) 600 (3 mo) . (350-1100) 735 (3 mo) (540-1100) New Guinea (Chimbu) (142) 525 ml 525 ml 343 ml 343-142 ml Biak Island (60) 427 ml 390-430 ml 127-338 ml 243 ml New Guinea (14) 720 ml 660 ml 705 ml 488 ml New Guinea (5) 400 ml 400 ml 400 ml Chimbu and Maprik New Guinea (5) 600 ml 600 ml 600 ml Baiyer River New Guinea (108) 350-480 ml 270-360 ml (12-18 mo) 230-300 ml 200-210 ml (12-24 mo) Ajamaru Nubuai 310-410 ml 250-340 ml (12-18 mo) Downloaded from www.ajcn.org by on August 22, 2009 150-210 ml (18-24 mo) Egypt (45) Healthy 922 ml Malnourished 733 ml Sri Lanka (30) 475 ml 495 ml 506 ml Nigeria (Benin) (81) 555 ml (2-3 mo) 590 ml (6-9 mo) 606 ml (13-18 mo) Uganda (122a) 660 ml (2-12 mo) a Results not strictly comparable as varying collection techniques and methods of sampling used. taken in the third year of lactation show palan showed an increase in volume se- very considerable differences, varying from creted, from 420 to 540 ml in poorly nour- 230 to 488 mb/day. ished Indian women after protein supple- Also, it is well recognized in practice that mentation (from 61 g/day to 90 g/day (36)). the output of extremely malnourished moth- Similar results were obtained in Western ers in families declines and ultimately Nigeria by Bassir using a vegetable protein ceases, with fatal consequences for the nurs- supplement-30 g of soya flour daily (10). ing baby (71). The nutritional point at Another study in India, where inadequately which human lactation becomes seriously nourished mothers were fed with milk bis- inhibited or ceases in famine circumstances cuits, showed a rise in serum albumen par- is not known , but early marasmus (in the abbebed by increase in albumen in the breast first 9 months of life) a solely breast fed milk, presumably by “spill-oven” (26b). babies may be occurring increasingly in the Also , an early investigation in 1 93 1 , showed babies of very poorly nourished women that an increase in output could be achieved living in conditions of severe psychosocial in New Zealand women by increasing the stress - for example , in Karachi , Pakistan calorie and/on the protein intake (27). Re- (89). Sometimes in some countries this may cently, a study in England seemed to sug- be partly “contraceptive manasmus,” from gest that poor lactation could be rebated to further interference with breast milk secre- inadequate energy reserves in the form of - tions by oral estrogen-containing contracep- subcutaneous fat laid down in pregnancy, tive pills. In pants of the world with seasonal and calorie intakes in lactation. In the food shortages (“hungry seasons”), as in United Kingdom, slimming diets in lactating Central Africa, the daily output may drop mothers lead to “an immediate reduction in by 100 to 200 ml (l43a). milk supply” (148). Supplementation. Limited studies have A recent detailed investigation was re- been carried out on the effect of supplemen- ported by Edozien and co-workers from tation of the mother’s diet on output. Go- Nigeria, (31b) when they showed that pro-
  • 7. 498 JELLIFFE AND JELLIFFE tein supplementation of the lactating less than in dairy cows, but it should be mother’s diet increased the milk produced remembered that such farm animals have and weight in the baby, but not the protein been bred to produce much greater yields content of the milk (Table 4). Similarly, than are required by the offspring (138). Sosa et al. (128a) demonstrated a rapid Composition increase in milk production in a malnour- ished Guatemalan woman following an im- The biochemical composition of human proved diet, particularly calories and pro- milk has been examined in different parts tein. of the world . Approximate comparisons can As usual , those concerned with the pro- be made between various communities, and duction of cow’s milk as a business, the with well-nourished mothers, for protein, dairy farmers, have infinitely more practical fat, lactose, vitamins, and calcium, keeping knowledge than those concerned with hu- in mind previously mentioned difficulties man milk and breast feeding. Thus, Lind- posed by variations with sampling (period blad and colleagues quoted the following in lactation cycle , time of day ; single , re- aphorism from Morrison’s 1948 Handbook peated or 24 hr; seasons; one subject or of Stockmen (101) which may not be com- pooled specimens, etc.), with laboratory techniques and with bevels of difficulties in Downloaded from www.ajcn.org by on August 22, 2009 pleteby correct for the human, but is cer- tainby generally so: maternal nutrition (Table 5) . Interpretation “Any inadequacy in the ration or fault in of such comparisons is made much greaten the methods of care or management will by recent realizations of the physiological generally manifest itself in the yield of milk, variations that occur in well-fed healthy rather than by a change in its chemical women successfully breast feeding their ba- composition” bies. However, the effect of increasing the ma- Protein. The protein content of human ternal diet on human milk output may be milk has been described as varying between 1 .0 to 1 .6 g/100 ml in well-nourished TABLE 4 women. In 1952, Morrison reported the Effect of maternal dietary supplementation with mean of European analyses to be 1 .6 g/l00 protein on the volume and protein content of breast ml and American 1 .2 g/lOO ml (101). He milkand weight gained by baby (Nigeria) 31b.0 suggested that differences in methods of Daily protein intake estimation may be mainly responsible, and Variable’ . 50g lOOg 25g bOg that 1 .2 g/100 ml probably represented an nitially initially overall mean . A study in Britain showed No. of subjects 7 7 3 3 1 .3 g/100 ml (29a). There seems little evi- Totalmilksolids 13.8d 13.4 12.0 11.9 dence for significant diurnal variation or (g/lOOml) ±1.3 ±0.9 ±0.6 ±0.5 fluctuation with age on parity. Milk protein 1 .61 1 .57 1 .20 1.25 (g/lOOml) ±0.15 ±0.19 ±0.21 ±0.23 However, very recent Swedish studies Milklactose 8.1 7.9 7.3 8.0 (1975) have shown the “true protein con- (g/lOOml) ±0.9 ±1.0 ±1.4 ±1.8 tent” to be only 0.8 to 0.9% in apparently Milkproduced 742 872 817 1059 well-nourished women in that country, (g/day) ±16 ±32 ±59 ±63 when determined by amino acid analysis Milkconsumed 617 719 777 996 (g/day) ±15 ±10 ±38 ±74 (91). These investigators pointed out that Weightgainedby 30.4 45#{149}7e 10.5 32.2e earlier analyses of breast milk were made baby(g/day) ±3.6 ±2.0 ±3.6 ±10.1 with the same methods as used for cow’s 0 Subjects were fed the initial diets for the first 14 milk. In fact, it is now recognized that the days and then a diet providing 100 g protein per day relatively low protein, low solute character- for the next 14 days. Results for each subject represent istics of breast milk place the human as a the mean values for milk samples collected during continuous contact, frequent suckling spe- days 8 to 14 (for initial diet) and days 21 to 28 (for diet providing 100 g protein per day). b Duration cies in infancy, with rather slow growth, of lactation for all subjects was between 30 and 90 and also permits breast milk to be the only days. C Duration of lactation was over 100 supply of water as well as nutrients. days. ii Results are mean values + SD. e Signifi- Retrospective examination of analyses cantly different at the 0.05 level from the unsupple- mented subjects. undertaken with similar methods in Brus-
  • 8. VOLUME AND COMPOSITION OF HUMAN MILK 499 TABLE 5 Fat, lactose, protein, and calcium content of mature human milk from some well-nourished and poorly nourished communities” Country (reference) Fat Lactose Protein Calcium g/IOO ml mgIlOO ml Well-Nourished American(92) 4.5 6.8 1.1 34.0 British(87) 4.78 6.95 1.16 29.9 Australian (150) 28.6-30.7 British (29a) 4.2 7.4 1.3 Poorly-Nourished Indian(17) 3.42 7.51 1.06 34.2 BantuS.Africa(144) 3.90 7.10 1.35 28.7 Chimbu, New Guinea Highlands (142) 2.36 7.34 1.01 New Hebrides (111) 3.8 5.0 1.40 25.8 Wuppertal, Germany 3.59 1.20 (Immediately Post World War II) (42) Nauru(19) 1.60 Ibadan, Nigeria (88 months) (62) 1 .20 (0.59-1.79) New Guinea (Biak) (60) 0.83-0.9 Downloaded from www.ajcn.org by on August 22, 2009 Alexandria, Egypt (45) Healthy 4.43 6.65 1.09 Malnourished 4.01 6.48 0.93 New Guinea (14) 2.3 6.48 0.93 Sri Lanka (30) 2.8 6.8 1.5 Brazil (21) Higheconomic 3.9 6.8 1.3 20.8 Loweconomic 4.2 6.5 1.3 25.7 Pakistan (139) 1.2 Tanzania (25) Often below 2% Nigeria(Ibadan)(102) 4.05 7.67 1.22 a Modified from Gopalan and Belavady (37), with added data. sels, Belgium (129) in 1954 and in Tokyo, although the lysine and methionine levels Japan (1 23) shows similar “low” levels for were lower. “true protein content” as with recent Swed- Varying results have been obtained with ish figures. estimations of the protein content with what In poorer, technically developing coun- is termed by modern Western cultural defi- tries, the average protein content of the nition “prolonged lactation” that is into - milk of inadequately nourished mothers, the second year of life and later. Some have based on previously used methods of total found a decline, some a rise, and others no nitrogen assessment, is usually surprisingly material change. high-in fact, a low normal (1 .0 to 1 .1 g/ The effect of maternal dietary suppbemen- 100 ml), although the range may be quite tation on protein content does not appear wide (Table 5). to have been investigated adequately. How- In some places with probably poorer flu- ever, in the protein supplementation study trition, analyses with older methods have carried out by Gopaban, the increased out- sometimes shown the protein content to be put of milk was associated with a come- lower (0.8 to 0.9%). However, in a care- sponding fall in protein concentration, with fully carried out study of poorly nourished the result that the total protein output in 24 women in Karachi, Pakistan, the “true pro- hr was not significantly altered (36, 37). tein content,” determined by an exchange Also, modern laboratory methods such as chromatography after acid hydrolysis and immunoelectrophoresis, which enables ac- adding up the calculated amino acid resi- curate quantities and measurement of the dues, was 0.8 ± 0.1 g/100 ml (89). These individual proteins of milk to be made were results are similar to those obtained by like not available at the time of earlier studies. techniques in Sweden, Belgium, and Japan, Recent investigations by L#{246}nnendal et al.
  • 9. 500 JELLIFFE AND JELLIFFE (91) have shown many unexplained vania- breast milk (or cow’s milk based formula) tions in healthy, well-fed women-for ex- appears to be reflected in the fatty acids in ample, in “milk-specific proteins,” those the infant’s subcutaneous fat. synthesized by the mammary gland, no- The relevance of the fatty acid (and cho- tabby ct-lactalbumin and lactoferrin . The lestenol) contents of human milk is currently decrease in total nitrogen in the first period under consideration in relation to the deveb- of lactation, for example in the first month, opment of the central nervous system and was mainly due to a dramatic drop in secre- atheroma in adults in industrialized coun- tory IgA bevel. tries. In developing regions, the pobyenoic Fat (lipid) . The significance of the fat con- fatty acids may be diminished in the breast tent of milk has been under-emphasized. It milk of malnourished mothers, with possible is the main source of calories; it contains ill-consequences in relation to brain growth fat soluble vitamins, especially vitamin A; (25). it is also the source of essential fatty acids Lactose. The third “proximate principle,” needed for the growth and development of lactose, is generally recognized as being the central nervous system (24b). Lastly, most constant in concentration and shows the higher fat in the after-milk may act as a no diurnal variation. Morrison’s (101) fig- physicochemical appetite control for the une based on 1010 samples examined in Downloaded from www.ajcn.org by on August 22, 2009 suckling baby (44). various American and European studies Earlier estimations of the fat content of showed a mean of 7.2 g/100 ml, while Kon milk in webb-nourished communities in the and Mawson found 6.9 g/100 ml in 586 United States and Britain showed means of samples of mature milk (87). In poorly 4.5 (93) and 4.78 g/100 ml (87), respec- nourished mothers, lactose also does not lively. A more recent 1977 study showed a seem to vary very much (Table 5) (range mean of 4.2 g/100 ml (29a). 6.43 to 7.51 g/l00 ml), except in one study Results from poorly fed women in devel- in the New Hebrides where 5.0 g/100 ml oping countries have demonstrated consid- was reported (111). enable variation (Table 5). However, some Calories. The calorie intake from breast recent work has suggested that the fat may milk is a product of the volume (as taken sometimes be considerably reduced, even by the baby) and its caloric content, which down to 1 g/100 ml (24b). Under these is primarily derived from fat. In well-fed circumstances , the calorie content of the communities, the caloric content varies milk may be much decreased with signifi- greatly. Macy and Kelly (92) give a mean cant lessening of energy intake (24a). The figure of 75 kcab/100 ml (range 45 to 119). significance of a bower fat content has to be The recent United Kingdom report showed related to inadequate energy intake in pneg- a mean of 70 kcab/100 ml (29a). nancy, with an inadequate subcutaneous In poorly nourished communities, both “fat bank” (53), as well as to the diet in the volume secreted and the fat, the main lactation itself. calorie-containing constituent, (and other The fatty acid pattern of breast milk can nutrients) may be less than in well-fed moth- be altered to some extent without affecting ens. milk volume or milk fat output by variation Vitamins in the types of dietary fat (especially if these are extreme) (25a) on by changes in the Vitamin A . The concentration is influ- calorie intake (57, 147). During energy enced by the adequacy of the diet of the equilibrium, milk fat resembles the fatty mother in pregnancy and lactation. The acid pattern of dietary fat, but when inade- vitamin A content of breast milk is often quate calories are eaten, the fat in human much lower in poorer populations of some milk follows the composition of human sub- developing countries (India , Ceylon , Indo- cutaneous depot fat. The major factor influ- nesia, Jordan), where this nutrient is mar- encing the fatty acid composition of milk is ginal, than in Europe and North America. the carbohydrate supply in the diet. Ulti- Maternal serum bevels are also low. The mately, the fatty acid composition of the intake is generally higher in the spring and
  • 10. VOLUME AND COMPOSITiON OF HUMAN MILK 501 summer months due to greaten supplies of Niacin. Although human milk is bow in dark green leafy and yellow vegetables. actual niacin, it has a high potential niacin Particularly high levels of netinob (vitamin value because this vitamin may be synthe- A) have been noted in Western Nigeria, sized from the amino acid, tryptophan. presumably because of the widespread use Vitamin B12. Low bevels of vitamin B12 of palm oil in cooking (102). have been found in the milk of poorer In a recent comparative investigation , the vegetarian women in Bombay. Also, in var- vitamin A content of breast milk was signifi- ious parts of India the “syndrome of cantly higher in normal Swedish mothers tremors” have been described in solely than in nonpnivileged Ethiopian mothers, breast fed babies, and has been ascribed to whose milk showed greater concentrations deficient B12 in the mother’s milk (59). of f3-carotene (35). Vitamin C. The level of ascorbic acid in Kcn and Mawson (87) found that supple- breast milk is subject to variations in dietary mentation with vitamin A, before and after intake in developing countries, particularly partunition or later during lactation, bed to with the seasonal availability of fresh fruits the secretion of milk richer in vitamin A and vegetables. In webb-nourished mothers, than normally produced. In Central Amer- human milk contains an average of 4 mg/ ica, Arroyave et al. (3) observed a rise in 100 ml of vitamin C. In Botswana (formerly Downloaded from www.ajcn.org by on August 22, 2009 the breast milk vitamin A levels after the Bechuanaband), Squires (130) found the introduction of vitamin A fortified sugar. content to be 1 .7 mg/100 ml in the dry Vitamin D. As well-known, levels of fat- season and 2.7 mg/100 ml in the wet sea- soluble vitamin D are low in both human sons. The subjects were poorly nourished and bovine milks. However, the recent dis- Tswana women. covery that breast milk contains a water- Since the ascorbic acid contant of breast soluble conjugate of vitamin D with sub- milk is greater than that of blood plasma, phate (87a) producing the same anti-nachitic which is generally below 2.5 mg/100 ml, potential as milk formulas fortified with secretory activity in the mammary glands conventional vitamin D explains the clini- must play a part in determining the bevel of cally well-recognized rarity of rickets in the vitamin C in milk. Apparent adaptation to breast fed. low maternal intakes of vitamin C has been Thiamine. The thiamine content of breast noted in Banoda, India (117) and the Phil- milk in areas with a high incidence of infan- ippines (132). The possibility of placental tile beriberi has been found to be low, due synthesis in pregnancy has been suggested. to insufficient maternal stores and intake in Certainly both the placenta and the breasts communities with diets largely based on may be abbe to actively secrete ascorbic polished rice (66) . Under these circum- acid for the offspring. Levels of fobic acid stances, a specific form of malnutrition - and vitamin B6 seem to reflect maternal infantile beriberi - occurs exclusively in nor- nutritional status (106a, 85). mab-seeming breast fed babies, and is due to a thiamine-deficient diet in the mother Vitamin supplementation during pregnancy and lactation . It is so characteristic in time of onset that the 2 to Deodhar and Ramakrishnan (28) carried 5 month mortality has been suggested as an out a dietary survey among women in South age-specific rate for this condition in the India with special reference to pantothenic regions at risk. acid, riboflavin, nicotinic acid, ascorbic acid Riboflavin. Human milk is a good source and thiamin. Subsequently, the breast milk of riboflavin, provided the maternal diet is was analyzed for the concentrations of the adequate. However, in South India, Gopa- same vitamins. A positive and significant ban and Belavady (37) found an average of correlation was found between dietary in- only 17.2 pg/100 ml of riboflavin in breast take and vitamin content of the milk for the milk, as compared with a value of about 25 vitamins investigated, which underlines the g/100 ml found by Kon and Mawson in need for an adequate diet for the lactating Britain (87). women. The content of all the vitamins
  • 11. 502 JELLIFFE AND JELLIFFE increased steadily with the dose of supple- In this regard, it is often insufficiently mentation. appreciated that the RDA’s given for in- In a more recent investigation, supple- fants are themselves derived from estimated mentation with ascorbic acid, nicotinic acid, intakes of breast fed babies, with an addi- riboflavin, thiamin, pantothenic acid, cyan- tional safety factor added for the less certain ocobalamin, biotin, pyridoxine, and folic situation of infants fed on cow’s milk for- acid was undertaken. As a result, the vi- mulas (70). This is the case, for example, tamin content of the milk increased steadily with the very high RDA of iron (1 0 mg/ with the dose used in supplementation (29). day) for the first 6 months of life , which Calcium . Levels of calcium reported in can not be attained with human milk. the milk of webb-fed mothers vary consider- The derivation of RDA’s for infants are ably. The calcium content in poorly nour- often not understood by pediatricians or ished mothers has been reported to range nutritionists, so that the advertising of corn- from “normal” levels to somewhat bow con- mercial baby foods can issue the following centrations (Table 5). Again, differences in appeal to “logic”: sampling and technique may be in part responsible. “A stimulating exercise for professionals would Levels of other minerals will not be con- be sorting one’s beliefs about breast feeding into Downloaded from www.ajcn.org by on August 22, 2009 those based on scientific fact and those stemming sidered here, but are presented elsewhere from hearsay and emotion. One could thus more (77). Early analyses are given by Morrison objectively counsel that growing membership in and others (101). The question of the con- lay organizations dedicated to breast feeding. tent of trace minerals will be much under Many sincerely believe that breast milk is all sufficient without any supplementation for at least investigation in coming years, in relation six months if not the full duration of breast feed- both to nutritional need and to possible ing. The fallacy of this concept is obvious if one effects of environmental pollution. compares the nutrient content of breast milk with recommended RDA for infants.” Adequacy The nutritional adequacy of breast milk The inanity of this comment is apparent for the infant can be roughly assessed by especially in view of the biological adapta- measuring 24-hr output and chemical corn- tion that has occurred over hundreds of position , or by the recording of satisfactory mibbenia. Carried to extremes, this argument growth, “good health” and absence of clini- would mean that breast milk was unfit for cab malnutrition. consumption by human babies, without ad- Adequacy of nutrients. The “nutrient ditional iron and vitamins. needs” of the baby during the exterogestate The RDA’s of protein and calories sug- fetal stage are not derived only from the gested for infants have been derived from diet, but also from fetal stores acquired in breast milk estimations, feeding with cow’s utero, from the placental transfusion (iron) milk based formulas and from the impon- and, to a limited and variable extent from tant, but special, studies by Fomon and ultraviolet irradiation of the skin (vitamin May (1958) on babies bottle fed ad bibiturn D). The recommended daily dietary allow- with pasteurized breast milk (33). Based on ances (RDA) for babies are estimated their findings, it has been suggested that mainly “by analogy with breast fed infants,” infants need: 1 st month 836 mb/day - (pro- and yet it is agreed increasingly that pres- tein 2.6 g/kg; cab 143kg); 6th month-990 entby available data on the composition of ml/day (protein 1 .7 g/kg; cal 90k). human milk is incomplete and out-of-date. However, as noted earlier, outputs in Fomon (34) rightly notes the need for more well-nourished women actually nursing their modern studies, and remarks that “until babies often supply less than this, a common such data are available, many of our calcu- range being 600-700 mb/day for the first 6 lations rebating to nutrients in human milk months (138). Among poorly nourished will be likely to be misleading”. Recent tropical communities estimated volumes Swedish studies (91) on the protein content often seem to range from 500-700 mb/day of breast milk give urgency to this comment. during the first six months (Table 4).