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Odontology https://doi.org/10.1007/s10266-019-00414-w

ORIGINAL ARTICLE

Aerobic and anaerobic microorganisms and antibiotic sensitivity of odontogenic maxillofacial infections

Emmanuel López‑González1 · Marlen Vitales‑Noyola1 · Ana María González‑Amaro1 · Verónica Méndez‑González1 · Antonio Hidalgo‑Hurtado2 · Rosaura Rodríguez‑Flores3 · Amaury Pozos‑Guillén4

Received: 1 December 2018 / Accepted: 27 January 2019 © The Society of The Nippon Dental University 2019

AbstractThis study aimed to identify the aerobic and anaerobic causal microorganisms of odontogenic infections and their antibiotic sensitivity. Purulent exudates were taken from patients with odontogenic infections by transdermal puncture, and aerobic and anaerobic microorganisms were identified using biochemical tests. Susceptibility to antibiotics was tested using the Kirby-Bauer method; the inhibition halos were measured according to NCCLS, and based on the results, the microorgan-isms were classified as susceptible, intermediate or resistant to each antibiotic. Frequencies of species and percentages of resistance were calculated. The microorganisms associated with odontogenic infections were principally anaerobic (65.3% anaerobic vs. 35.7% aerobic), and the susceptibility to antibiotics was higher in anaerobic than in aerobic microorganisms. The majority of isolated microorganisms (82%) showed susceptibility to amoxicillin/clavulanic acid. The causal agents of odontogenic infections were anaerobic microorganisms, which exhibited high resistance to antibiotics.

Keywords Microorganism · Antibiotic · Odontogenic infection · Aerobic · Anaerobic

Introduction

Odontogenic infections affect the tooth and its supporting structures, are polymicrobial in origin and are caused by both aerobic and anaerobic microorganisms [1, 2]. Odonto-genic infections are clinically classified as (i) periodontitis, (ii) pericoronitis, (iii) jaw inflammation, and (iv) phlegmon of the jaw bone area [3, 4]. The proper and timely manage-ment of these infections is essential for disease outcomes and prognosis in patients. If an odontogenic infection is not treated at an early stage, it generally spreads into contiguous

fascial spaces, may lead to additional complications [4] and can potentially be life threatening as a result of airway compromise, septicemia, cavernous sinus thrombosis, brain abscess, and shock [5]. Other, rare, complications of odon-togenic infections include cervical necrotizing fasciitis, with most reported cases of this pathology being of odontogenic origin [6, 7], and orbital abscess, which is a very rare pres-entation, secondary to an odontogenic complication, but a cause for concern because of the risk of permanent vision loss [8]. These complications are more severe when micro-organisms spread to contiguous spaces; in addition, severity is related to the type of causal pathogen.

Recent years have witnessed significant changes in the spectrum of microorganisms isolated from odontogenic infections [9]. These infections are polymicrobial in nature, and a great variety of causal pathogens, mainly faculta-tive and obligate anaerobic microorganisms, have been described; however, aerobic microorganisms have also been isolated. Gram-positive cocci of the genera Streptococcus, Enterococcus and Peptostreptococcus are mainly isolated from purulent exudates, but bacilli such as Prevotella, Lac-tobacillus and Bacteroides and, in some cases, yeasts such as Candida are also present in these infections [9, 10].

* Amaury Pozos-Guillén apozos@uaslp.mx

1 Endodontics Posgraduated Program, Faculty of Dentistry, San Luis Potosí University, San Luis Potosí, SLP, Mexico

2 Department of Oral and Maxillofacial Surgery, Hospital “Ignacio Morones Prieto”, San Luis Potosí, SLP, Mexico

3 Department of Oral and Maxillofacial Surgery, Hospital No. 50 of Mexican Social Security Institute, San Luis Potosí, SLP, Mexico

4 Basic Sciences Laboratory, Faculty of Dentistry, San Luis Potosi University, Zona Universitaria, Av. Manuel Nava 2, 78290 San Luis Potosí, SLP, Mexico

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The management of odontogenic space infections requires best judgment and skills from a surgeon [4]. The majority of these infections can be successfully treated by an incision of the soft tissue abscess, together with the extraction or root canal therapy of the affected tooth [11]. In addition, incision and drainage procedures are useful in reducing the bacterial load at the infected site. However, when surgical drainage cannot be achieved or the patient shows signs of systemic involvement, antibiotic therapy is indicated [11].

Selection of antibiotics with strong antibacterial activities against oral streptococci and anaerobic bacteria is consid-ered since these microorganisms are primary causes of odon-togenic infections; besides, the frequency of involvement of obligate anaerobes increases with the severity of inflamma-tion [12]. For severe odontogenic infections, antimicrobials with strong antibacterial activities against anaerobic bacteria that produce beta-lactamases are usually selected, after peni-cillin was considered a long-awaited panacea against dental infections. However, rapid evolution of antibiotic resistance in microorganisms has led to the use of more potent antibiot-ics [13]. In several countries, the first-choice drugs for odon-togenic infections include amoxicillin and clavulanic acid/amoxicillin; if there is an allergy to penicillin, ceftriaxone and clindamycin are used [3]. In the cases of severe odon-togenic infections, carbapenem antibiotics can be indicated, such as faropenem, meropenem and doripenem. Owing to the great antimicrobial resistance observed in recent years, it is very important to evaluate the susceptibility and resistance of microorganisms present in odontogenic infections since these infections are considered a public health problem and they worsen the clinical course of other infectious diseases.

The aim of this study was to evaluate the susceptibility to different groups of antibiotics of aerobic and anaerobic microorganisms isolated from purulent exudates of hospital-ized patients with severe odontogenic infections.

Materials and methods

Patients

Fourteen patients with odontogenic infections, who went to the Maxillofacial Surgery Service, were included in this study. All patients answered a questionnaire on medical his-tory and were subjected to oral examination. Laboratory and radiographic tests were performed on all patients. Surgical treatments and/or antibiotic therapy were established to treat the odontogenic infections in the patients. This study was approved by the Institutional Ethics Committee and was con-ducted in accordance with the 1964 Declaration of Helsinki. All patients signed informed consent.

Samples

Purulent exudates were taken through transdermal puncture with a 20-cc syringe after disinfection of the operation area with iodine for 5 min. The collected exudate was placed in two tubes with thioglycolate medium for culturing anaerobic microorganisms (BD BBL, Edo de México, MX), and one tube was placed in an anaerobic chamber (COY Labora-tory Products, Inc., Grass Lake, MI, USA) with 85% nitro-gen, 10% hydrogen and 5% carbon dioxide and incubated at 37 ± 2 °C for 48–72 h, until visible microbial growth appeared. The other tube was placed in a microbiological incubator (FE-1320, Felisa, Jalisco, MX) under aerobic con-ditions for approximately 24–48 h, until microbial develop-ment was observed.

Biochemical identification of microorganisms

The turbidity of samples in thioglycolate medium was meas-ured with a McFarland densitometer (Densimat; bioMérieux, Florence, Italy). The exudate samples were spread on anaer-obic blood agar or blood agar (BD BBL, Edo de México, MX) and incubated under anaerobic or aerobic conditions, respectively, for 24–72 h, until the appearance of micro-bial growth. Macro- and microscopic characteristics were evaluated under a stereoscopic microscope (Leica EZ4D; Singapore), including Gram staining (HYCEL, Jalisco, MX) and the presence of bacterial spores, respectively. Microbial identification was performed with biochemical tests using the following API systems (bioMérieux, SA, Marcy l’Etoile, France) according to the manufacturer’s instructions: API 20 Strep for streptococci and related genera, API 20A for anaerobic microorganisms and API 20C AUX for yeast identification.

Antibiotic susceptibility tests

All isolated microorganisms, except yeasts, were submit-ted to antibiotic susceptibility tests using the Kirby-Bauer method with the following antibiotics: ampicillin/sulbactam (SAM; 20 µg) (BD BBL, Benex, Ltd., Shannon, Ireland), dicloxacillin (DC; 1 µg) (Bio-Rad, México, DF), clinda-mycin (CC; 2 µg), cefoxitin (FOX; 30 µg), cefazolin (CZ; 30 µg), cefotaxime (CTX; 30 µg), piperacillin (PIP; 100 µg), amoxicillin/clavulanic acid (AMC; 20/10 µg), piperacillin/tazobactam (TZP; 100/10 µg), ampicillin (AM; 10 µg), imipenem (IPM; 10 µg), penicillin (P; 10 IU), ceftriaxone (CRO; 30 µg) (Becton, Dickinson and Company, Sparks, MD, USA), and ticarcillin/clavulanic acid (TIM; 75/10 µg) (BD BBL, Benex, Ltd.). The identified microorganisms were spread with a sterile cotton tip on anaerobic blood agar or

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blood agar; discs with antibiotics were placed on agar with sterile forceps, and the plates were incubated for 24–48 h. The measurements of inhibition halos were performed with a Vernier caliper according to the National Committee for Clinical Laboratory Standards (NCCLS) [14]. The results were expressed as resistant (R), intermediate (I) or suscep-tible (S) for each antibiotic.

Statistical analysis

Data are reported as frequencies of species and percentages of resistance.

Results

Clinical data of patients with odontogenic infections

The patients with odontogenic infections showed an equal sex distribution, 50% males and 50% females, and the mean age was 37.5 years. The causal tooth was more frequently the third molar (37.5%), and the more affected aponeurotic space was the submaxillary space (57.1%). All clinical and demographic data are presented in Table 1.

Microorganisms associated with odontogenic infections

Forty-two strains of microorganisms were isolated, and the frequencies of the genera and species are shown in Table 2, classified according to oxygen requirements. The mean number of isolates per patient was 3 strains; 65.3% of the total microorganisms were anaerobic, of which 66.6% were strictly anaerobic (Fig. 1a). All identified aerobic microor-ganisms were Gram-positive cocci (100%), and the anaero-bic microorganisms were more frequently represented by Gram-positive bacilli (85.1%), followed by yeasts (7.4%); we found an equal distribution of Gram-negative bacilli and Gram-positive cocci in 3.7% of the cases (Fig. 1b).

Antibiotic susceptibility of causal microorganisms of odontogenic infections

The antibiotics used were classified according to their family as beta-lactams, cephalosporins, lincosamides and carbap-enems. For all microorganisms, both aerobic and anaerobic, susceptibility to dicloxacillin (a beta-lactam antibiotic) was low (5.5%); however, a high susceptibility of 82% was shown to amoxicillin with clavulanic acid (other beta-lactam anti-biotics) (Fig. 2a). In the cephalosporin family, it was found that the susceptibility to cefazolin (a first-generation cepha-losporin) was 36% and that to ceftriaxone (a third-genera-tion cephalosporin) was 59.7% (Fig. 2b). In the lincosamide

family, the antibiotic used was clindamycin, to which 47.2% of the microorganisms were susceptible (Fig. 2c). In the car-bapenem family, the antibiotic used was imipenem, to which 100% of the microorganisms were susceptible (Fig. 2d). Subsequently, the antibiotic susceptibilities were compared between aerobic and anaerobic microorganisms, and higher percentages of resistance to almost all beta-lactam antibiot-ics were found for anaerobic microorganisms: piperacillin (11.1% vs. 41.6%, aerobic and anaerobic microorganisms, respectively) (Fig. 3a); amoxicillin/clavulanic acid (0% vs. 16.6%, aerobic and anaerobic microorganisms, respectively) (Fig. 3b); dicloxacillin (55.5% vs. 83.3%, aerobic and anaer-obic microorganisms, respectively) (Fig. 3c); piperacillin/tazobactam (0% vs. 8.3%, aerobic and anaerobic micro-organisms, respectively) (Fig. 3d); penicillin (11.1% vs. 16.6%, aerobic and anaerobic microorganisms, respectively) (Fig. 3f); ampicillin (11.1% vs. 25%, aerobic and anaerobic

Table 1 Clinical characteristics of patients with odontogenic infec-tions

Values are given as the mean ± standard deviationa 4–11 K/ulb Some patients underwent two surgical treatments at the maxillofacial surgeon´s consideration

Characteristics Patients

Age (years) 37.5 ± 14.3Gender (%) Female/male 50/50

Evolution time (days) 6.7 ± 3.5Causal tooth (%) First molar 31.2 Second molar 25 Third molar 37.5 Premolar 6.25

Aponeurotic space affected (%) Submasseteric 14.3 Submandibular 57.1 Sublingual 7.1 Submental 7.1 Buccal space 14.3

Levels of leukocytesa 14.1 ± 2.6Antibiotic therapy previous hospitalization (%) Yes/no 85/15

Hospital antibiotic therapy (%) Clindamycin/ceftriaxone 85.7 Clindamycin/dicloxacillin 7.1 Clindamycin/cefotaxime 7.1

Surgical treatment (%)b

 Exodontia 50 Dentoalveolar surgical 28.5 Surgical drainage and debridement 50

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microorganisms, respectively) (Fig. 3g). However, simi-lar percentages of resistance to ampicillin/sulbactam were observed between aerobic and anaerobic microorganisms (11.1% vs. 8.3%, respectively) (Fig. 3e), while the percent-age of resistance to ticarcillin/clavulanic acid was higher for aerobic microorganisms than for anaerobic microorganisms (33.3% vs. 8.3%, respectively) (Fig. 3h). For the cephalo-sporins, we obtained similar results, with higher percentages

of resistance among anaerobic microorganisms: cefoxitin (22.2% vs. 33.3%, aerobic and anaerobic microorganisms, respectively) (Fig. 4a); cefotaxime (11.1% vs. 41.6%, aero-bic and anaerobic microorganisms, respectively) (Fig. 4b); ceftriaxone (11.1% vs. 50%, aerobic and anaerobic micro-organisms, respectively) (Fig. 4c); and cefazolin (22.2% vs. 41.6%, aerobic and anaerobic microorganisms, respec-tively) (Fig. 4d). For clindamycin (lincosamide family), a higher percentage of resistance was observed for anaerobic microorganisms than for aerobic microorganisms (33.3% vs. 41.6%, aerobic and anaerobic, respectively) (Fig. 4e), and 100% of both aerobic and anaerobic microorganisms were susceptible to imipenem.

Comparison of resistance to antibiotics between anaerobic and aerobic microorganisms

For almost all antibiotics (except ampicillin/sulbactam and ticarcillin/clavulanic acid), a higher resistance was observed for anaerobic microorganisms than for aerobic microorgan-isms. The anaerobic microorganisms were threefold more resistant to piperacillin, 1.6-fold more resistant to amoxicil-lin/clavulanic acid, 2.7-fold more resistant to dicloxacillin, 0.8-fold more resistant to piperacillin/tazobactam, 0.5-fold more resistant to each penicillin and amoxicillin, 1.1-fold more resistant to cefoxitin, and threefold more resistant to cefotaxime than were aerobic microorganisms. Ceftriaxone showed the most significant difference in resistance, which was 3.9-fold higher for anaerobic microorganisms than for aerobic microorganisms, while the former were 1.9-fold more resistant to cefazolin and 0.8-fold more resistant to clindamycin than the latter (data not shown).

Table 2 Frequency of isolation of microorganisms from purulent exu-dates of patients with odontogenic infections

Microorganisms

Aerobic Anaerobic

Streptococcus 33.3%  Clostridium 63% S. anginosus 13.3%  C. beijerinckii butyricum 37% S. mitis 6.6%  C. spp 15% S. constellatus 6.6%  C. difficile 3.7% S. equinus 6.6%  C. clostridioforme 3.7%

 C. ramosum 3.7%Lactococcus 33.3% Bifidobacterium 11.1% L. lactis spp cremoris  B. spp 2

Staphylococcus 6.6% Candida 7.4% S. aureus  C. albicans

Aerococcus 6.6% Actinomyces 3.7% A. urinae  A. meyeri odontolyticus

Granulicatella adiacens 6.6% Peptoniphilus asaccharolyticus 3.7%Globicatella sanguinis 6.6% Eggerthella lenta 3.7%Gemella haemolysans 6.6% Bacteroides ovatus thetaiotamicron

3.7%Streptococcus intermedius 3.7%

Fig. 1 Frequencies of identified microorganisms isolated from puru-lent exudates from patients with odontogenic infections. The micro-organisms were classified according to their oxygen requirements and morphological characteristics. a Frequencies of aerobic and anaerobic

microorganisms. b Frequencies of Gram-positive and Gram-negative cocci and bacilli among aerobic and anaerobic microorganisms. a, b Data are presented as the means

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Discussion

Present study evaluated the response at several antibiotics by the causal microorganisms of odontogenic infections in a developing country, where the use and prescription of anti-biotics it not had been regulated until a few years ago, so it’s important to know the public health problem that repre-sented the indiscriminate previous use of antibiotics and its impact in public health institutions.

Odontogenic infections are caused by multiple micro-organisms, mainly anaerobic bacteria, and affect teeth and their supporting structures [2]. These infections are a serious public health problem and are most common in underserved patients, lacking access to healthcare [15], although severe forms of these infections require hospital care.

In this study, we included patients with severe odonto-genic infections, and all patients required hospitalization. The mean time of disease progression was 6.7 days before the patients went to a hospital, and 85% of the patients reported the use of antibiotics before hospitalization. Unfor-tunately, the use of antibiotics causes an increase in bac-terial resistance, and although antibiotic prescriptions are

regulated in some countries, many patients report the use of antibiotics at home [16]. The management of these patients can be significantly improved if infections are treated at early stages; however, on average, these patients seek medical care 1 week after the infection starts, and by that time, the infec-tion usually spreads.

The severity of these infections depends on the tissue affection grade and dissemination of infection to contigu-ous spaces, as well as on several other factors, such as the general state of patient’s health, the presence of systemic disease, immunosuppression, etc. [4, 17, 18]. The spaces most affected by odontogenic infections are submandibular and buccal spaces [19, 20]. In the present study, we found that in 57.1% of the patients, the submandibular space was affected, and in 14.3% of the patients, the buccal and sub-masseteric spaces were affected; because of their anatomic location, it is logical to expect that these facial spaces are most commonly involved. The complications of odonto-genic infections are diverse, and many patients may require admission to an intensive care unit [21]. Even though our patients had severe infections, none presented with rare com-plications. In some cases, deep neck and head infections

Fig. 2 Percentages of susceptibility of causal microorganisms of odontogenic infections to antibiotics from different families. The anti-biotics used were classified into 4 families. a Percentages of suscepti-bility of all microorganisms (aerobic and anaerobic) to beta-lactams. b Percentages of susceptibility of all microorganisms (aerobic and anaerobic) to cephalosporins. c Percentages of susceptibility of all microorganisms (aerobic and anaerobic) to lincosamides. d Percent-

ages of susceptibility of all microorganisms (aerobic and anaerobic) to carbapenems. PIP Piperacillin, AMC Amoxicillin/clavulanic acid, DC dicloxacillin, TZP piperacillin/tazobactam, SAM ampicillin/sul-bactam, P penicillin, AM amoxicillin, TIM ticarcillin/clavulanic acid, CZ cefazolin, FOX cefoxitin, CRO ceftriaxone, CTX cefotaxime, CC clindamycin, IPM imipenem. a–d Data are presented as the means

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can occur, causing true medical airway emergencies [22]; in addition, tonsillopharyngitis and lymphadenitis can be caused by maxillofacial odontogenic infections [23]. Other important factors to consider while treating these infections and not allowing them to spread are severe complications such as necrotizing fasciitis, which can lead to significant skin and soft tissue loss, mediastinitis, vascular thrombosis or rupture, limb loss, organ failure, and death [7].

Odontogenic infections are mainly associated with man-dibular molars, such as the first or third molars [4, 24]; in the sample studied in this study, third molars were most frequently involved. Third molars are the teeth with lim-ited access in the oral cavity; since their location is usually intraosseous, this creates difficulty for good hygiene, and thus these teeth commonly have caries, which can advance and produce other infections in adjacent tissues. Regardless of the causal tooth, the clinical management includes the elimination of the primary cause by extraction of the tooth or endodontic treatment, followed by a suction drainage and antibiotics [25]. An essential factor for the treatment of these infections is performing local procedures, such as drainage and abscess incision, since penetration of antibiotics into oral tissues such as the infected jaw bone and abscess cavity is low, resulting in a low antibiotic concentration at the site of infection [3]. In this study, all patients were treated with extraction of the causal tooth and drainage and debridement,

along with intravenous administration of antibiotics such as clindamycin and ceftriaxone.

Odontogenic infections are mainly caused by anaerobic microorganisms [1, 26], and we found a higher percentage of anaerobes than that of aerobes in purulent exudates from the patients. Gómez-Arámbula et al. have found in a study per-formed on patients from the same admission centers that the microbiota of odontogenic infections was principally formed by Gram-positive cocci, although the presence of Candida albicans was also reported [27]. We detected that all aero-bic microorganisms were Gram-positive cocci of the genus Streptococcus, which is consistent with the data from many studies [10, 28]. Rashi et al., Heim et al., and Chunduri et al., reported in different studies that the microorganisms isolated of these infections are Streptococcus mainly viridans group, up 70% among the aerobic bacteria, whereas Gram-negative and -positive bacillus as Bacteroides and Prevotellas were the most common bacterial species among anaerobes [4, 5, 10]; in these reports they concluded that this type of infec-tions has a mixed environment, which involve the presence of both aerobic and anaerobic microorganisms. The most frequent isolates in our study were from different species of Clostridium. Clostridium spp. are strictly anaerobic, sporu-lating, Gram-positive bacilli; some species are pathogens causing several diseases in humans, including tissue necrosis and have been reported in odontogenic infections [29]. The

Fig. 3 Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to beta-lactams. The microorganisms were classified according to their oxygen requirements into aerobic and anaerobic, and percentages of susceptibility to beta-lactam antibiotics were calculated. a Percentages of susceptibility and resistance of aer-obic and anaerobic microorganisms to piperacillin. b Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to amoxicillin/clavulanic acid. c Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to dicloxacillin. d Percentages of susceptibility and resistance of aerobic and anaero-

bic microorganisms to piperacillin/tazobactam. e Percentages of sus-ceptibility and resistance of aerobic and anaerobic microorganisms to ampicillin/sulbactam. f Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to penicillin. g Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to ampicillin. h Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to ticarcillin/clavulanic acid. R Resist-ant, I intermediate and S susceptible. a–h Data are presented as the means

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methods for the identification of microorganisms include conventional or molecular tests. Molecular tests such as PCR have greater sensitivity and accuracy compared with those of conventional tests; however, we employed in this study biochemical conventional tests since these tests allow iden-tification of causal microorganisms of recent infections, as well as the isolation of microorganisms by growth on cul-ture plates and the performance of antibiotic susceptibility tests, because it is essential for obtaining antibiograms that microorganisms are cultivable.

There are several antibiotics that are used for the treat-ment of odontogenic infections. Although penicillin had been considered the standard treatment for dental infections for a long time, bacteriological spectra of the oral microbiota have shown resistant microorganisms since penicillin was introduced. Newer and more potent antibiotics are needed to fight against causal microorganisms of odontogenic infec-tions. In this study, 14 different antibiotics, such as beta-lactams, cephalosporins, lincosamides and carbapenems, were used to evaluate the susceptibility of microbial isolates from purulent exudates of patients with severe odontogenic infections, and it was found that among the antibiotics tested (except imipenem, which was used as a control antibiotic),

all isolates showed high susceptibility to clavulanic acid/amoxicillin. The use of amoxicillin with clavulanic acid increases the antimicrobial capacity of amoxicillin against bacteria producing beta-lactamases [30]. This antibiotic combination is used for acute bacterial sinusitis, otitis, ton-sillitis, cystitis, severe dental abscesses, and other infections [30]. However, the disadvantages of this antibiotic combi-nation are its high cost and insufficient availability of the intravenous formulation so that other antibiotics of the same family are used in the clinic.

Other antibiotics used are lincosamides, such as clin-damycin, which was most frequently used to treat patients enrolled in this study; however, we observed low suscepti-bility of the isolated microorganisms to this antibiotic. High resistance to this antibiotic has been observed in dentistry in the last years, and therefore, it is progressively less pre-scribed by maxillofacial surgeons and dentists [31, 32]. It should be noted that one of essential causes of bacterial resistance is self-medication, and most of the patients treated had consumed antibiotics before their hospitalization.

Despite the differences in the frequency of microorgan-isms isolated from this type of infections, the pharmacologi-cal management is similar in several countries. Chunduri

Fig. 4 Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to cephalosporins and lincosamides. The microorganisms were classified according to their oxygen require-ments into aerobic and anaerobic, and percentages of susceptibility to antibiotics were calculated. a Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to cefoxitin. b Percentages of susceptibility and resistance of aerobic and anaerobic

microorganisms to cefotaxime. c Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to ceftriaxone. d Percentages of susceptibility and resistance of aerobic and anaero-bic microorganisms to cefazolin. e Percentages of susceptibility and resistance of aerobic and anaerobic microorganisms to clindamycin. R resistant, I intermediate and S susceptible. a–e Data are presented as the means

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et al., reported a good susceptibility at clavulanic acid amox-icillin and amoxicillin alone; in contrast, a high resistance at erythromycin was observed, in patients with orofacial infections in India, where the bacterial resistance represent a serious health problem [10]; similar results were reported by Rashi et al., where the therapy with Co amoxiclav show a good susceptibility at aerobic and anaerobic microorganisms [4]; these results agree with ours. Heim et al., observed in a study where the susceptibility of antibiotics were evaluated in patients with odontogenic infections with inpatient and outpatient management that the microorganisms that show low susceptibility to one or more of the standard antibiotic regimen have a significantly higher chance of causing seri-ous health problems [5]. All these authors concluded that the success management of these infections depend in part, by choosing the proper antibiotic.

When we compared the susceptibility and resistance to the antibiotics tested by classifying the microorganisms into anaerobes and aerobes, we observed in most cases, that the anaerobic microorganisms showed lower percentages of susceptibility than did aerobic microorganisms. Amoxicil-lin/clavulanic acid was the antibiotic combination to which the microorganisms were most susceptible, but the percent-age of susceptibility to this antibiotic among the anaero-bic microorganisms was lower than that among the aerobic microorganisms. The anaerobic microorganisms were more resistant than aerobes because of their virulence factors and the ability to live in a hostile environment without oxygen. In addition, in the oral cavity, microorganisms are mainly present in a biofilm form, which makes them up to 2 − 1000-fold more resistant than the corresponding planktonic forms to the effects of antibiotics [33].

All findings reported in this study support the actual clini-cal management of these patients, as the antibiotics type beta-lactams are the more used in public health institutions in our area; in addition, it is important to highlight that in our Mexican population there aren´t similar studies that include the evaluation of diverse antibiotics in odontogenic max-illofacial infections, so it is essential to carry out further longitudinal studies and evaluate the follow-up of patients in the clinical area. Other important factor to considerer is the necessity to perform similar studies in other popula-tions where the use of antibiotics is not regulated to identify possible bacterial resistance as in this study. Finally, good management, diagnostics, and adequate treatment lead to satisfactory resolution of infection.

Conclusions

The causal microorganisms of odontogenic infections show high resistance to standard antibiotic therapy regimes and cause serious health problems. Amoxicillin/

clavulanic acid is a highly effective antibiotic combination against Streptococcus and anaerobic microorganisms caus-ing odontogenic infections.

Acknowledgements This study was partially supported by PFCE-UASLP 2018 grant.

Compliance with ethical standards

Conflict of interest The authors declare that they have no conflict of interest.

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