Resistência bacteriana: o uso indiscriminado de antimicrobianos indicados para tratamento de afecções orais tem sido discutido como fonte importante de resistência bacteriana. Este estudo apresenta cepas resistentes e discute novas formas de aplicação dos medicamentos.

1. Evaluation of Subgingival Bacteria in the Dog and
Susceptibility to Commonly Used Antibiotics
Mirko Radice, DVM; Piera Anna Martino, DBSc, PhD; Alexander M. Reiter, Dip! Tzt, Dr med vet
progression from a healthy periodontium to gingivitis and
Summary: periodontitis, there is a shift from a gram-positive oriented,
aerobic facultative flora to a predominantly gram-negative,
The aim of the present investigation was to ex'aluate the anaerobic flora." Periodontopathogens are bacteria that cause
subgingival aerobic and anaerobic flora of 13 dogs with gingivitis and periodontitis. A catalase-positive form ofthe gram
periodontal disease and the susceptibility of these bacteria negative Porphyromonas gingivaUs is considered to be the key
to antibiotics currently approved in Italy for ti-eatment of periodontopathogen in cats and dogs''-''-- and is recognized as P
canine infections. Of the anaerobic bacteria, Bacteroides giilae.-'' Other canine and feline Porphyromonas organisms
fragilis was most frequently isolated, followed by include P. assacharolytica, P. cangingivalis, P canoris, P. cansulci,
Peptostreptococciis + Porphyromonas gingivaUs and P. endodontalis, P. circumdentaria, P. crevioricanis, P. salivosa.. P.
Prevotella intermedia. Ofthe aerobic bacteria, a-hemolytic denticanis, and P. gingivicanis."'''-" Additional black-pigmented
Streptococcus was most frequently isolated, ofien associated anaerobic bacteria associated with periodonta! disease include
with Escherichia coli or Pctsteurella multocida. Resistance Pre'Otella intennedia--' and Bacteroides spp."'"-''" Pathogen-
of anaerobic and aerobic bacteria to various antibiotics was related oral spirochetes also are considered to play an important
generally high. Anaerobic bacteria appeared to be role in periodontal disease, but cultivation studies in cats and dogs
susceptible to amoxicillin + clavulanic acid, doxycycline, have only been reported sparsely.*"'-'^
and erythromycin; aerobic bacteria appeared to be Previous studies showed that amoxicillin + clavulanic acid
susceptible to amoxicillin + clavulanic acid, erythromycin, and clindamycin had high in vitro susceptibility against anaerobes
gentamycin, and sulfa-trimethoprim. Bacteroides fragilis and enrofloxacin high in vitiv susceptibility against aerobes from
was resistant to all of the antibiotics tested. The emerging subgingival plaque samples in cats and dogs,'"'' Although
worldwide problem of bacterial resistance to antibiotics periodontal disease is caused by bacteria, antibiotic therapy should
resulting from overuse and misuse of antibiotics is not be the primary treatment strategy,'*^-"' Unfortunately, there is a
discussed J Vet Dent 23 (4); 219 - 224,2006 tendency among veterinarians to use antibiotics as part of the
management of any animal with periodontal disease or other oral
condition. Resistance of plaque bacteria to antibiotics has clearly
been demonstrated in humans,**^' and a similar pattern of bacterial
Introduction
resistance development may be present in cats and dogs.
Periodontal disease is an infectious condition of the tooth
supporting tissues (gingiva, periodontal ligament,, alveolar bone, The aim of the present investigation was to evaluate the
and cementum) and is considered to be the most common disease subgingival flora (aerobic and anaerobic bacteria) of dogs with
in companion animals. The accumulation of plaque on tooth periodontal disease and the susceptibility of these bacteria to
surfaces is responsible for tiie development of gingivitis and antibiotics currently approved in Italy for treatment of canine
periodontitis.' infections. Furthermore, the emerging problem of bacterial
Gingivitis is inflammation ofthe gingiva and is reversible, if resistance to antibiotics in human and veterinary medicine is
plaque is removed by home or professional oral hygiene reviewed.
procedures.^ In addition to toxins and tissue-destructive enzymes
produced by periodontopathogenic bacteria, the host's response to Materials and Methods
plaque leads to the release of agents from damaged neutrophils Thirteen chent-owned dogs with various degrees of
that can cause injury to the body's own tissues.' hiflammation periodontal disease (ranging from gingivitis to periodontitis as
may spread along the periodontal space and ultimately progresses assessed by means of periodontal probing) were included in this
to periodontitis, which is diagnosed as loss of attachment study. There were three Yorkshire terriers, one German shepherd,
(gingival recession, résorption of alveolar bone, and formation of one poodle, and eight mixed-breed dogs. Two dogs received
periodontal pockets). The periapical region ofthe tooth root may sporadic oral hygiene at home, A professional scaling and
become affected, leading to retrograde pulpal infection. Thus, polishing had been performed on all dogs 6-months prior to
endodontic disease can occur as a result of severe periodontal sample collection. Antibiotics had been given to most ofthe dogs
disease. Eventually the tooth becomes mobile and is lost due to in the past for conditions other than periodontal disease. No
spontaneous exfoliation or professional extraction.' attempt was made to assess details of antibiotic history because
Gingivitis and periodontitis are referred to as 'bacterial owners were not able to verify names of antibiotics used, dates
infections', but several hundred bacterial species have been and routes of administration, duration of therapies, etc. However,
identified to date in normal and diseased mouths of cats and dogs must not have received antibiotic therapy for at least 2-weeks
' With maturation of plaque in subgingival areas and before sample collection to be included in the study.
J,VET,DENT Vol. 23 No. 4 December 2006 219

2. Sample collection was performed under general anesthesia at the detachment of microbial cells. Two dilutions (Logio) were
the right maxillary canine tooth (104) and the right maxillary made for all samples that were plated on Tryptic Soy Agar plates
fourth premolar tooth (108) since both teeth had been excluded witb 5 % sheep blood'' for aerobic bacteria and on Bnicella Agar^
from prior periodontai probing, A sterile endodontic paper point for anaerobic bacteria. The plates were incubated aerobically for
was inserted into the depth of the gingival sulcus or periodontai 24 to 48-hours at 37°C, and anaerobicalV for 48 to 72-hours at
pocket at buccal aspects of the teeth. The paper point was 37°C.
removed after a few seconds and placed into tubes containing a The anaerobic flora was identified by growth on Bnicella
transport liquid media (thioglycollate broth)-' for growth of Agaf, a medium containing Vit K and haemin. Gram's staining,
aerobic and anaerobic bacteria. The samples were immediately Schaifer & Fulton's staining for spores, and API System 20A'
transported to the reference laboratory and were vortexed to allow were used as biochemical reference methods.
Aerobic bacteria were identified by their macroscopic {e.g..,
morphology of colonies, presence of hemolysis) and microscopic
Table 1 {using Gram-staining) characteristics; moreover, biochemical
Signalment of the 13 dogs enrolled in the study. tests were performed using macro- or micrometbods*^. For the
identification oí Streptococcus strains, the presence of hemolysis
Variable n % (a partial or ß total) and the growth on Mitis SalivariusAgar^, a
Male 11 84.6 medium for tbe isolation and identification of the streptococci of
Sex the oral cavity, were evaluated. For identification oí Pasteurella
Female 2 15.4
multocida, the lack of growth on Mac Conkey Aga)' was
< 5 years 3 23.1 evaluated.
Age 5-10 years 7 53.8 Evaluation of microbial sensitivity/resistance to antibiotics
was performed using the Kirby-Bauer reference method or the
> 10 years 3 23.1
agar disk diffusion test. A bacterial suspension, performed in
<12kg 8 61.5 saline buffer (0.9 % NaCl), was delivered onto a Mueller-Hinton
Weight
12+kg 5 38.5 plate, and then the disks containing different antibiotic molecules
were placed on the plate. After incubation at 37°C under aerobic
Mixed 10 76.9
Diet or anaerobic atmosphere for 24 to 48-hours, the susceptibility of
Dry 3 23.1 each microorganism was recorded to the following antibiotics:
amikacin, amoxicillin + clavulanic acid, doxycycline,
erythromycin, gentamycin, kanamycin, metronidazole (only for
anaerobes), and sulfa-trimethoprim.^
Table 2
Isolation of anaerobic bacteria. Results
Results of variables of signalment (sex, age, weight, and diet)
Anaerobic bacteria Percent (%)
of the 13 dogs enrolled in the study are reported in Table 1. The
Peplostreptococcus + Porphyromonas majority of dogs were male (84.6 %), 5 to 10-years of age (53.8
gingivaiis 30.8
%), < 12.0 kg (61.5 %), and eating a mixed (soft and dry) diet
Bacteroides fragilis 46.1
(76.9 %).
Prevotella Intermedia 23.1
100 Of the anaerobic bacteria (Table 2), Bacteroides fi-agilis was
most frequently isolated from subgingival samples, followed by
Peptostreptococcus + Porphyromonas gingivaiis, and Prevotella
Anaerobic bacteria intermedia. Of the aerobic bacteria (Table 3), a-haemolytic
Streptococcus was most frequently isolated, often associated with
Peptostreptococcus + Escherichia coli or Pasteurella multocida.
Porphyromonas gingivaiis Susceptibility of anaerobic and aerobic bacteria to various
antibiotics is shown in Tables 4-8. Resistance of isolated bacteria
to tested antibiotics was generally high. Anaerobic bacteria
appeared to be susceptible to amoxicillin + clavulanic acid,
doxycycline, and erythromycin, while aerobic bacteria appeared
to be susceptible to amoxicillin + clavulanic acid, erythromycin,
gentamycin, and sulfa-trimetboprim. Bacteroides fragilis was
Prevotella
intermedia resistant to all of the antibiotics tested.
Bacteroides
fragilis Discussion
The aim of the present investigation was to evaluate the
subgingival aerobic and anaerobic bacterial flora of 13 dogs with
220 J.VET.DENT Vol. 23 No, 4 December 2006

3. periodontal disease and the susceptibility of these bacteria to veterinarians, and diagnostic uncertainty. Several recent studies
antibiotics currently approved in Italy for treatment of canine showed that pediatricians prescribe antibiotics significantly more
infections. Except for the high prevalence of Bacteroidesß-agilis, often, if they perceive parents expect them, and significantly less
the predominant subgingival flora obtained in this study confirms often, if they feel parents do not expect them."^** The best way to
results reported in previous studies."•"•"'•'^•-"'-'- Of the anaerobic combat this situation is to educate patients/patient owners and
bacteria, Bacteroides fragilis was most frequently isolated, doctors/veterinarians to decrease both demand and over-
followed by Peptostreptococcus + Porphyromonas gingivalis and prescribing. Unfortunately, there is a tendency to use antibiotics as
Prevotella intermedia. The reason for the unusually high part of the management of any animal with periodontal disease or
prevalence oí Bacteroides fi-agilis is not clear. Differing results other oral condition, although there is no apparent justification for
between isolation studies may be due to differences in study this practice. Similar to dogs in the present study, resistance of
methodology, including sample population utilized and isolation plaque bacteria to antibiotics has clearly been demonstrated in
techniques applied. Of the aerobic bacteria, a-haemolytic
Streptococcus was most frequently isolated, often associated with
Escherichia coli or Pasteurella nndtocida. Table 3
The fast growth rate, high concentration of cells, genetic isolation of aerobic bacteria.
processes of mutation and selection, and ability to exchange genes
account for the extraordinary adaptation and evolution of Aerobic bacteria Percent {%)
bacteria.'" For these reasons bacterial resistance to antibiotics may a-hemolytic Sireptococcus + E. coli 38
take place very rapidly in evolutionary time. Risk factors a-hemolytic Streptococcus + P. fvultocida 38
responsible for the emergence and spread of resistant bacteria a-hemoiytic Streptococcus + E. coli
+ P. muitocida 8
include: (1) antibiotic use; (2) reservoirs for resistance; (3)
a-hemolytic Streptococcus + E. coli
medical advances; and (4) societal changes.""' Antibiotics make + S. intermedius 8
conditions favorable for overgrowth of some bacteria, including a-hemolytic Streptococcus
those that possess mechanisms of drug resistance. If a resistant S, intermedius + P. muitocida 8
organism is present, antibiotics will create 'selective pressure' 100
favoring the growth ofthat organism. A number of studies have
demonstrated conclusively that the development of bacterial
Aerobic bacteria a-hemolytic Streptococcus
resistance to antibiotics is correlated with the level of antibiotic + E. coli -h P. muttocida
use.'"^*' Antibiotic resistance of nosocomial pathogens in hospitals, a-fiemolytic Streptococcus
nursing homes, day-care centers, and animal facilities is increased + E. cell + S. intermedius
by the transfer of individuals already colonized by resistant a-hemolytic Streptccoccus
organisms from one location to another. Progress in the treatment a-iiemolytic + S. intermedius
Streptococcus + P. multocida
of many diseases has led to an increased life span of humans and E. coii
animals. Consequently, with advanced age, chronic disease or
immunosuppression, individuals can be more susceptible to
bacterial infections, resulting in greater use of antibiotics.
Worldwide spread of bacterial resistance to antibiotics has
occurred due to the increased mobility of today's society.-"-
Pet animal numbers have substantially increased in modem a-hemolytic Streptococcus
+ P. muitocida
society, and attention is increasingly devoted to pet welfare.
Antibiotics are frequently used in small animal practice, with
heavy use of broad-spectrum agents such as amoxicillin +
clavulanic acid, cephalosporins, and ñuoroquinoIones. The Table 4
practice of antibiotic overuse and misuse in cats and dogs has
contributed to the development of Staphylococcus spp., Antibiotic activity versus Prevotella intermedia.
Escherichia coli and various other bacteria that are resistant to
antibiotics."'"^^ The role of pets in the dissemination of bacterial Antibiotic Sensitivity (%) Resistance (%)
resistance to antibiotics has been given relatively little attention Amikacin - 100
when compared with that of food animals, and a marked contrast Amoxicillin-^CIavuianic acid 66.7 33,3
is evident between the current policies on antibiotic usage in Doxycycline 33.3 66.7
companion and food animals. However, the possible transfer of Erythromycin 66.7 33.3
resistant bacteria from cats and dogs to humans has recently been
Gentamycin - 100
acknowledged as a potential threat to public health.""-^*
Kanamycin - 100
One of the biggest problems is inappropriate prescribing of Metronidazole - 100
antibiotics. There are many reasons for this, including demand Suifa-trimethoprim 100
-
from patients/patient owners, time pressure on physicians/
J,VET,DENT, Vol. 23 No, 4 December 2006 221

4. Table 5 Table 6
Antibiotic activity versus Bacteroides fragilis. Antibiofic activify versus Porphyromonas gingivalis
Peptostreptococcus.
Antibiotic Sensitivity (%) Resistance (%) Antibiotic Sensitivity (%) Resistance (%)
Amikacin - 100 Amikacin 25 75
Amoxicillin+Clavulanic acid - 100 Amoxicillin+Clavulanic acid 75 25
Doxycycline - 100 Doxycycline 100 -
Erythromycin - 100 Erythromycin 25 75
Genlamycin - 100 Gentamycin 25 75
Kanamycin - 100 Kanamycin 25 75
Metronidazole - 100 Metronidazole 25 75
Sulfa-trimethoprim - 100 Sulfa-trimethoprim - 100
Table 7 Table 8
Antibiotic activity versus a-haemolytic Streptococcus -f £ Antibiofic activity versus a-haemolyflc Streptococcus + P.
coli. multccida.
Antibiotic Sensitivity (%) Resistance (%) Antibiotic Sensitivity (%) Resistance (%}
Amikacin 20 80 Amikacin - 100
Amoxicillin+Clavulanic acid 40 60 Amoxicillin+Clavulanic acid - 100
Doxycycline 20 80 Doxycycline - 100
Erythrcmycin 20 80 Erythromycin 40 60
Gentamycin 80 20 Gentamycin - 100
Kanamycin 20 80 Kanamycin 100
Sulfa-trimethoprim 60 40 Sulfa-trimethoprim - 100
humans.'"'''' It is therefore imperative to review periodontal
treatment strategies and determine whether systemic antibiotics
Table 9
have a role to play in the management of periodontal disease.
If accumulation of plaqne is prevented, periodontal disease American Veterinary Dental College (AVDC) Position
does not develop." Although this condition is caused by bacteria, Statement on fhe Use of Antibiotics in Veterinary Dentistry.
antibiotic therapy is not considered the primary treatment
strategy.'"^" Instead, treatment of periodontal disease should be The AVDC endorses the use of systemic antibiotics in
directed at mechanical removal or reduction of plaque and veterinary dentistry for treatment of some infectious
calculus accumulation, suppression of the tissue-destructive conditions of the orai cavity Alttiough cuiture and
effects of the inflainmatory response, surgical management of susceptibility testing is rarely performed on individual
patients that have an infection extending from/to the oral
periodonfal pockets, extraction of more severely affected teeth, cavity, ttie selection of an appropriate antibiotic should be
and thorough debridement of extraction sites.' A controlled- based on pubiisfied data regarding susceptibility testing
release local antibiotic delivery system, reaching of the spectra of known oral pathogens. Patients that are
periodontopathogens deep within periodontal pockets, has been scheduled for an oral procedure may benefit from pre-
treatment with an appropriate antibiotic to improve the
described in dogs.^" Professional supra- and subgingival scaling,
health of infected oral tissues. Baoteremia is a recognized
followed by daily tooth brushing, is the 'gold standard" for seguela to dental scaling and other oral procedures.
prevention of periodontal disease.' Home oral hygiene may be Healthy animais are able to overoome this bacteremia
enhanced by offering products that support dietary abrasion or without the use of systemic antibiotics. However, use of a
chemically suppress plaque and calculus accumulation.™ systemically administered antibiotic is recommended to
reduce bacteremia for animals that are immune
Bacteremia secondary to periodontal disease occui"s daily in compromised, have underlying systemic disease (such
patients with periodontal disease, and it is normally rapidly as clinically-evident cardiac, hepatic, and renal diseases)
and/or when severe oral infection is present. Antibiotics
cleared hy the reticulo-endothelial system in the healthy patient."'
should never be considered a monotherapy for treatment
Therefore, for the great majority of otherwise healthy cats and of oral infections, and should not be used as preve •'••/e
dogs presenting with periodontal disease and other oral management of oral conditions. Adopted by the Bo.
conditions, systemic antibiotics are not indicated.''" Bacteremia Directors. April 2005
can be prevented or reduced in severity by rinsing the oral cavity
222 J.VETDENT Vol. 23 No. 4 December 2006

5. di cani con parodontopatie e ioro antibiotioo-sensibilità. Tesi di laurea, Reiatore Dott.ssa
with dilute chlorhexidine gluconate (0.12 %) prior to PA, Marlino, 2003 Facoitâ di Medicina Velennaria, Miiano
commencing the oral procedure. Perioperative systemic
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