Accepted Manuscript

Microbiology and Antibiotic Sensitivity of Head and Neck Space Infections of

Odontogenic Origin. Differences in Inpatient and Outpatient Management

Dr Nils Heim, MD, DMD, Dr Anton Faron, MD, Dr Valentin Wiedemeyer, MD, DMD,
Prof. Dr Rudolf Reich, MD, DMD, phD, Head of department, Dr Markus Martini, MD,
DMD, Chief resident
PII: S1010-5182(17)30251-2
DOI: 10.1016/j.jcms.2017.07.013
Reference: YJCMS 2736

To appear in: Journal of Cranio-Maxillo-Facial Surgery

Received Date: 17 December 2016

Revised Date: 10 June 2017
Accepted Date: 20 July 2017

Please cite this article as: Heim N, Faron A, Wiedemeyer V, Reich R, Martini M, Microbiology and
Antibiotic Sensitivity of Head and Neck Space Infections of Odontogenic Origin. Differences in
Inpatient and Outpatient Management, Journal of Cranio-Maxillofacial Surgery (2017), doi: 10.1016/
j.jcms.2017.07.013.

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 ACCEPTED MANUSCRIPT
Title page

Title:

Microbiology and Antibiotic Sensitivity of Head and Neck Space Infections of Odontogenic
Origin. Differences in Inpatient and Outpatient Management

Authors:

1. Dr. Heim, Nils (MD, DMD)1 – Corresponding author – nils.heim@web.de

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2. Dr. Faron, Anton (MD)1 – anton.faron@ukb.uni-bonn.de

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3. Dr. Wiedemeyer, Valentin (MD, DMD)1 – valentin.wiedemeyer@ukb.uni-bonn.de

4. Prof. Dr. Dr. Reich, Rudolf (MD, DMD, phD - Head of department)1 – rudolf.reich@ukb.uni-

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bonn.de

5. Dr. Dr. Martini, Markus (MD, DMD – Chief resident)1 – markus.martini@ukb.uni-bonn.de

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1 Department fot Oral and Cranio-Maxillo and Facial Plastic Surgery
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Full name of department:
Department for Oral and Cranio-Maxillo and Facial Plastic Surgery
(Head: Prof. Dr. Dr. Rudolf H. Reich)
University of Bonn, Germany
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Corresponding author:
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Dr. Nils Heim

Abteilung für Mund-, Kiefer- und

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Plastische Gesichtschirurgie - Universitätsklinikum Bonn

Sigmund-Freud-Strasse 25, Haus 11, 2. OG

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D- 53127 Bonn
Germany

Contact:
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phone
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0049 (0) 228 287 16867

fax
0049 (0) 228 287 22604
e-mail
nils.heim@ukb.ubi-bonn.de

Financial disclosure
There are no financial disclosures or commercial interests from
any authors.
Conflict of interest
There were no conflicts of interest.
Acknowledgments
None
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Microbiology and Antibiotic Sensitivity of Head and Neck Space Infections of
Odontogenic Origin. Differences in Inpatient and Outpatient Management.

Introduction
Patients have been afflicted by orofacial infections since medical records began (Huang et al.,
2006). The microbial flora of orofacial infections of odontogenic origin are typically
polymicrobial (Nair, 2004). In 1928, Alexander Fleming proved that Penicillium notatum was
able to destroy colonies of Staphylococcus aureus. It took more than another decade before

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Howard Florey and Ernst Chain developed a powdered form of Penicillin that could be admitted
to patients. The use of this first antibiotic changed the way odontogenic infections were treated.
As an outcome of evolution, only 4 years after mass production of the first antibiotics, antibiotic-
resistant microorganisms were observed. In order to obtain solutions to rising resistance rates,

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synthetic antibiotics are being continually developed (Hawkey, 2000).

Dental abscesses usually occur secondary to caries, trauma, or insufficient dental treatment (Shu

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et al., 2000). The main symptoms of an acute dental abscess are swelling, pain, erythema, and
hyperthermia (Robertson et al., 2009). Suppuration is often localized to the affected tooth, but
can also spread into other spaces, and can be potentially life threatening as a result of airway
compromise, septicemia, cavernous sinus thrombosis, brain abscess, and shock, if not treated at

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an early stage (Boscolo-Rizzo and Da Mosto, 2009; Tavakoli et al., 2013; DeAngelis et al., 2014).
The majority of dental abscesses can be treated sufficiently by surgical intervention, such as
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incision and drainage of pus (Islam et al., 2008). Bacteria are undoubtedly the main pathogens of
odontogenic abscesses. Nevertheless, pathogenesis of dental abscess is complex, and a single
causative pathogen cannot be identified (Azenha et al., 2012; Daramola et al., 2009).
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The aim of this study was to evaluate whether susceptibility and resistances of bacteria to
antibiotics have an influence on how patients have to be treated (inpatient or outpatient
management) or not. Secondly, the aim was to highlight the susceptibility rate of isolated strains
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to the tested antibiotics.

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Patients and Methods

A 28-month retrospective study evaluated hospital records of 107 patients who had been
treated for head and neck infections of odontogenic origin. All patients in this study underwent
surgical incision and drainage. Patient characteristics reviewed were gender, age, bacteria
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identified, and antibiotic resistance from culture and sensitivity. The specimens were obtained
by performing a swab of the lesions using Transwab – M40-Amies (gel medium). In order to
eliminate the microbial flora on skin and mucosa, disinfection of affected tissue was performed
before incision. Intraoral disinfection was achieved using chlorhexidine, and extraoral
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disinfection was carried out with povidone-iodine. Extraoral incision was performed in 52 cases
of single-space intraoral infection, and in 55 cases of multiple-space infection.
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All patients who underwent inpatient management received IV antibiotic therapy during and
after surgery. The antibiotic therapy for outpatient-managed patients was ampicillin/sulbactam
375mg, administered twice a day (in the morning and evening) for adult patients. Children were
treated with the same medication, with dose adapted to the infants’ weight. If a patient affirmed
a penicillin allergy, we administered clindamycin 600mg three times a day. Children received
lower doses according to their bodyweight. In cases in which the dentist had already initiated
therapy with amoxicillin or clindamycin, we stuck to that medication, and additionally
performed sufficient incision and drainage of the abscess.
The standard antibiotic therapy for inpatient-managed patients consisted of
ampicillin/sulbactam, administered three times a day in a dose according to the patients’ body
weight (<70kg = 3×/2g; >70kg = 3×/3g). Renal dysfunction was checked and the dose was
adjusted if necessary. If patients reported allergic reactions or skin sensations in connection
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with previously administered penicillin, clindamycin (600mg three times a day) was
administered instead. Again, children received lower doses according to their body weight.

Results
There were 65 male (61%) and 42 female (39%) patients, ranging in age from 5 to 91 years,
with a mean age of 48.3 years (±21 SD). 52 patients underwent outpatient management and 55
patients inpatient management. Where there were signs of rapidly spreading infection, multiple-
space infections, or potentially life-threatening conditions secondary to airway compromise or
septicemia, patients underwent inpatient management.

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Of the outpatient-managed patients, 40 received ampicillin/sulbactam (ampi) and 10 patients
received clindamycin (clinda). In two cases we advised the patients to continue the antibiotic
therapy with amoxicillin 1000mg (amox) twice a day.

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Inpatient-managed patients received IV antibiotic therapy. 51 patients received
ampicillin/sulbactam (ampi). In two cases we additionally administered metronidazole, and in

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one case cotrimoxazole was also administered. In all three cases a severe infection led us to the
decision for additional antibiotic therapy. A microbiologist was consulted in order to suggest the
drug of choice. Four patients received clindamycin, due to a prior-reported allergic reaction to
penicillin. In two cases, one additional antibiotic was administered (metronidazole and

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ciprofloxacin) (Figure 1). AN
A total of 92 bacterial strains were isolated from 107 patients, accounting for 0.86 isolates per
patient. Swabs from 37 patients showed no growth from cultures. Candida albicans (11 isolates)
and Candida dublinensis (1 isolate) were also identified. The bacteria were found to be 71.7%
gram-positive. Gram-negative specimens were isolated in 28.3% of cultures.
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Of the 92 isolated strains, 73 were aerobic (Table 1) and 19 anaerobic (Table 2).
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Overall, 46 bacterial strains were isolated from patients who underwent outpatient treatment,
and 34 bacterial strains from those who underwent inpatient treatment. 32.6% of the strains
isolated from outpatient-treated individuals showed resistances against one or more of the
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tested antibiotics. Isolated strains of inpatient treated individuals showed resistances in 52.9%
of cases.
The predominantly isolated microorganisms were Staphylococci, Streptococci, and Prevotella. Of
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all isolates, Staphylococci accounted for 18.5% (17 isolates), group C Streptococci for 14.1% (13
isolates), viridans Streptococci for 18.5% (17 isolates) and Prevotella for 15.2% (14 isolates).
Antibiotics evaluated for resistance included ampicillin, cefazolin, clindamycin, erythromycin,
gentamicin, levofloxacin, metronidazole, penicillin, piperacillin/tazobactam, and
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sulfamethoxazole/trimethoprim.
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Staphylococci showed susceptibility to ampicillin (100%), cefazolin (100%), clindamycin (82.4%

– outpatient management (o): 1; inpatient management (i): 2), erythromycin (76.5% – o: 2; i: 2),
gentamicin (100%), levofloxacin (82.4% – o: 2; i: 1), penicillin (58.8% – o: 5; i: 2),
piperacillin/tazobactam (100%), and sulfamethoxazole/trimethoprim (100%).

Viridans Streptococci demonstrated sensitivity rates to ampicillin (100%), cephazolin (100%),

clindamycin (84.6% – o: 0; i: 2), erythromycin (100%), gentamicin (92.3% – o: 1; i: 0),
levofloxacin (100%), penicillin (100%), piperacillin/tazobactam (100%), and
sulfamethoxazole/trimethoprim (92.3% – o: 1; i: 0).

Group C Streptococci exhibited susceptibility to ampicillin (92.3% – o: 0; i: 1), cephazolin (100%),

clindamycin (84.6% – o: 1; i: 1), erythromycin (100%), levofloxacin (100%), penicillin (100%),
piperacillin/tazobactam (100%), and sulfamethoxazole/trimethoprim (92.3% – o: 0; i: 1).
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Prevotella exhibited susceptibility to penicillin (100%), clindamycin (78.6% – o: 3; i: 0),
gentamicin (100%), and levofloxacin (100%).

Regarding the distribution of bacterial strains and resistances found in the four most common
bacteria (Staphylococcus, group C Streptococci, viridans Streptococci, and Prevotella),
Staphylococcus was found in 10 cases in outpatient management with six resistant isolated
strains (60%). In seven cases Staphylococcus was found in patients who were treated under
inpatient conditions and was resistant in five instances (71.4%). Group C Streptococci were
found in four outpatient cases (one resistant strain = 25%) and nine inpatient cases (three
resistant strains = 33%). Viridans Streptococcus appeared in 12 outpatient cases (two resistant

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strains = 16.6%) and five inpatient cases (two resistant strains = 40%). Prevotella was mostly
isolated in patients treated under outpatient conditions (13 strains, of which three were
resistant = 23.1%). In one case a non-resistant Prevotella strain was isolated in an inpatient-

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treated abscess (Figure 2).

Discussion

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Dental abscess is a frequently occurring infection routinely treated as an office procedure.
Certain factors, such as host resistance, anatomy, and virulence of the bacteria, are of vital
importance regarding the spread of infection. This study investigates patients with head and
neck infections of odontogenic origin, who were either treated under inpatient or outpatient

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conditions. All patients received surgical incision and drainage.
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The mean age of our patients was 48.3 years (±21 SD), which is slightly higher than in other
studies (Sanchez et al., 2011; Zirk et al., 2016). We observed a male dominance (61%), which
was similar to recent studies (Zirk et al., 2016).
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Currently only little literature on outpatient-management of head and neck infection is available.
All patients presented the typical clinical findings of pain and swelling (Robertson et al., 2009).
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All 52 patients treated under outpatient conditions reported with single-space involvement,
whereas multiple-space infections were reported in most of the 55 patients treated under
inpatient conditions. In fact multiple-space infections of odontogenic origin of the head and neck
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are seen more frequently (Storoe et al., 2001).

Bacteria that were isolated included both aerobic and anaerobic species (Stefanopoulos and
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Kolokotronis, 2004). Staphylococci were one of the four predominantly isolated bacteria.
Historically, Staphylococcus species have not been considered members of the oral flora or to
play a preponderant role in the pathogenesis of head and neck infections of odontogenic origin.
However, recent studies have showed that Staphylococci are more frequent colonizers of the oral
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cavity than previously thought (Smith et al., 2008), and have been reported in up to 17.5% of
acute dental abscesses (Walia et al., 2014). Our results were slightly higher, with a Staphylococci
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rate of of 18.5%.
Viridans and group C Streptococci are commonly implicated in dental abscess. The viridans
group of Streptococci includes the oralis, mitis, sanguinis, salivarius, and mutans groups (Fowell
et al., 2012).
Prevotella species have been reported as the most common isolates in different studies (Siquiera
and Rocas, 2009). In our present study, 14 strains (15.2%) of Prevotella species were isolated.
This finding correlates with the other studies reported in the literature (Kuriyama et al., 2012).
Of the total 92 isolates, 73 (79.3%) were aerobes, of which 63 were Gram-positive aerobes
(86.3%) and 10 were Gram-negative aerobes (13.6%). The difference between the Gram-
positive and the Gram-negative aerobes was significant. Out of the 92 isolates, 19 were
anaerobes (20.7%). Our findings showed a significant difference between the incidence of
aerobes and anaerobes. Furthermore, particular attention must be paid to the use of antibiotics
effective against Gram-negative organisms, with 28.3% of the isolated strains in our study being
Gram-negative.
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Candida albicans was isolated in 11 cases (12%) and Candida dublinensis in one case (1.1%). The
occurrence of Candida in the pus of odontogenic abscesses was higher than reported in
literature (Walia et al., 2014).

Our study had an average of 0.86 isolate per sample from 107 patients. This is significantly
lower than for samples obtained by aspiration, with up to 3.3 isolates per sample (Lewis, 1985).
In terms of samples collected by swabbing – similar to the procedure we performed – our results
were slightly lower compared with other studies, ranging from 1.1 to 1.4 isolates per sample
(Hunt and Meyer, 1983; Epstein and Scoop, 1977).

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In 37 cases (34.6 %) swabs showed no results of bacterial growth. Reasons for this might
include the pus composition (Madigan et al., 2012). In advanced abscesses leucocytes can
weaken or eliminate so many of the bacteria that isolating and cultivating any becomes unlikely.

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Nevertheless, bacterial strains are still present in the abscess.

Resistance to the tested antibiotics in Staphylococcus was noted in 11 cases (64.7%) with a low

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susceptibility to penicillin (58.8%). This correlates with other studies reported in the literature
(Barker, 1999). Outpatient-treated patients showed a higher rate of resistance (five cases), than
patients treated under inpatient conditions (two cases). These findings lead us to assume that
the differences in susceptibility of Staphylococcus in dental abscess, treated under either

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inpatient or outpatient conditions, show no evidence for the rate of spreading or the
development of serious, progressive symptoms. Reduced susceptibility was also noted to
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clindamycin (83.4%), erythromycin (76.5%), and levofloxacin (83.4%). However, there was no
significant difference between the strains treated under inpatient or outpatient conditions.

Viridans Streptococci were isolated in 17 cases and showed resistance in two cases in each group
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(inpatient vs. outpatient management). However, 12 of the isolated microorganisms were found
in the outpatient-treated group, while only five were found in the inpatient-treated group. Thus,
the percentage of resistant bacteria was significantly higher in the inpatient group (40%), than
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in the outpatient group (16.6%). Viridans Streptococci viridans were 100% susceptible to
penicillin as well as to erythromycin and cephazolin, which correlates with findings in the
literature (Kuriyama, 2002). The rate of susceptibility to clindamycin was 84.6%. Both resistant
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strains were found in the inpatient group. These findings show that penicillin still appears to be
a highly effective antibiotic in the treatment of viridans Streptococci.
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Group C Streptococci showed a slightly higher resistance rate in the inpatient group (Figure 2).
100% of the isolates were susceptible to penicillin, while only 84.6% susceptibility to
clindamycin was noted. The high susceptibility to penicillin suggests that it should be used in
preference against group C Streptococci, whereas clindamycin should not be used as the first-
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resort antibiotic.
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Prevotella was the predominant Gram-negative isolate (53.8%) (Warnke et al., 2008). In
contradiction to the literature, Prevotella showed no resistance to penicillin in our study
(Boyanova, 2010). Surprisingly, only one of 14 cases (7.1%) of Prevotella had to be treated
under inpatient conditions. Prevotella showed a 78.6% sensitivity rate to clindamycin, whereas
it exhibited high susceptibility to gentamicin (100%) and levofloxacin (100%). Thus,
clindamycin was not shown to be an effective drug of choice against Prevotella.

Patients who required inpatient treatment tended to have multiple-space abscesses. Statistical
analysis showed inpatients to have significantly higher numbers of resistant microorganisms
(52.9%) than outpatients (32.6%). However, it is conjecturable that microorganisms causing
serious progressive symptoms, and showing greater tendency to spread, are more likely to be
resistant to the regular antibiotics, with the consequent complications requiring inpatient
management, including administration of IV antibiotics. Cultures and sensitivities commonly
showed greater growth in aerobes (79.3%) than in anaerobes. The most common bacteria
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isolated were Staphylococci, viridans Streptococci, group C Streptococci and Prevotella.
Staphylococci showed a susceptibility rate of 58.8% to penicillin, whereas viridans Streptococci,
group C Streptococci, and Prevotella were 100% susceptible to penicillin.
Clindamycin showed a reduced susceptibility rate in all of the four predominant groups of
microorganism (Figure 2).

Conclusion
Microorganisms that show low susceptibility to one or more of the standard antibiotic therapy
regimes have a significantly higher chance of causing serious health problems, a tendency to
spread, and are more likely to require inpatient management, with administration of IV

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antibiotics.
Penicillin continues to be a highly effective antibiotic against viridans Streptococci, group C
Streptococci and Prevotella, whereas clindamycin could not be shown to be effective as an

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empirical drug of choice for a large number of odontogenic infections.

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Conflict of interest/ethical approval:

No conflict of interest.
No ethical approval needed.

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Table and figure legends:
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Table 1. Number of aerobic organisms. Gram (+/−); shape: c = coccus, r = rod, fungus
Table 2. Number of anaerobic organisms. Gram (+/−); shape: c=coccus, r=rod
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Figure 1. Administered antibiotics in inpatient (ip) and outpatient (op) management. ampi =
ampicillin/sulbactam; clinda = clindamycin; amoxi = amoxicillin; metro = metronidazole; cotrim
= cotrimoxazole; cipro = ciprofloxacin
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Figure 2. Microorganisms categorised into inpatient and outpatient isolates, and according to
antibiotic resistances.
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Table 1

Aerobic organisms

Strains Gram Shape Number of aerobes

Actinobacter baumanii − c/r 1

Candida albicans + Fungus 11
Candida dubliniensis + Fungus 1
Citrobacter freundii − r 1

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Enterobacter cloacae − r 1
Gemella haemolysans + c 1
Hämophilus parainfluenza − r 3

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Klebsiella oxytoca − r 3
Pseudomonas putida − r 1
Staphylococcus + c 17

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Group A Streptococcus + c 1
Group C Streptococcus + c 13
Group K Streptococcus + c 1
Streptococcus gordonii + c 1

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S. viridans Group + c 17
Total 73
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Table 2

Anaerobic organisms

Bacterial strains Gram Shape Number of anaerobes

Bacteroides uniformis − r 1
Enterococcus + c 2
Fusobacterium − r 1
Parvimonas micra + c 1

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Prevotella − r 14
Total 19

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Figure 2

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