Next Article in Journal
The Acari Hypothesis, III: Atopic Dermatitis
Previous Article in Journal
Genetics and Pathogenicity of Natural Reassortant of Infectious Bursal Disease Virus Emerging in Latvia
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Pathogens
Volume 11
Issue 10
10.3390/pathogens11101082
pathogens-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Phylogenetic Groups, Pathotypes and Antimicrobial Resistance of Escherichia coli Isolated from Western Lowland Gorilla Faeces (Gorilla gorilla gorilla) of Moukalaba-Doudou National Park (MDNP)

by
Leresche Even Doneilly Oyaba Yinda
1,*,
Richard Onanga
1,
Pierre Philippe Mbehang Nguema
2,
Etienne François Akomo-Okoue
2,
Gontran Nsi Akoue
3,
Neil Michel Longo Pendy
4,
Desire Otsaghe Ekore
1,
Roméo Wenceslas Lendamba
1,
Arsène Mabika-Mabika
1,
Jean Constant Obague Mbeang
2,
Natacha Poungou
2,
Ibrahim
5,
Jacques François Mavoungou
2 and
Sylvain Godreuil
6
1
Laboratory of Bacteriology, Interdisciplinary Medical Research Center of Franceville, Franceville P.O. Box 769, Gabon
2
Microbiology Laboratory, Research Institute for Tropical Ecology, Libreville P.O. Box 13354, Gabon
3
École Normale Supérieure (ENS), Libreville P.O. Box 17009, Gabon
4
Laboratory of Vector Ecology, Interdisciplinary Medical Research Center of Franceville, Franceville P.O. Box 769, Gabon
5
Laboratory of Biology, University of Science and Technology of Masuku, Franceville P.O. Box 913, Gabon
6
Laboratoire de Bactériologie, CHU de Montpellier, UMR MIVEGEC (IRD, CNRS, Université de Montpellier), 34295 Montpellier, France
*
Author to whom correspondence should be addressed.
Pathogens 2022, 11(10), 1082; https://doi.org/10.3390/pathogens11101082
Submission received: 1 July 2022 / Revised: 27 July 2022 / Accepted: 28 July 2022 / Published: 23 September 2022
Browse Figures
Review Reports Versions Notes

Abstract

:
(1) Background: Terrestrial mammals in protected areas have been identified as a potential source of antimicrobial-resistant bacteria. Studies on antimicrobial resistance in gorillas have already been conducted. Thus, this study aimed to describe the phylogroups, pathotypes and prevalence of antimicrobial resistance of Escherichia coli isolated from western lowland gorilla’s faeces living in MDNP. (2) Materials and Methods: Ninety-six faecal samples were collected from western lowland gorillas (Gorilla gorilla gorilla) during daily monitoring in the MDNP. Sixty-four E. coli isolates were obtained and screened for phylogenetic and pathotype group genes by polymerase chain reaction (PCR) after DNA extraction. In addition, antimicrobial susceptibility was determined by the disk diffusion method on Mueller Hinton agar. (3) Results: Sixty-four (64%) isolates of E. coli were obtained from samples. A high level of resistance to the beta-lactam family, a moderate rate for fluoroquinolone and a low rate for aminoglycoside was obtained. All E. coli isolates were positive in phylogroup PCR with a predominance of A (69% ± 11.36%), followed by B2 (20% ± 19.89%) and B1 (10% ± 8.90%) and low prevalence for D (1% ± 3.04%). In addition, twenty E. coli isolates (31%) were positive for pathotype PCR, such as EPEC (85% ± 10.82%) and EPEC/EHEC (15% ± 5.18%) that were obtained in this study. The majority of these MDR E. coli (DECs) belonged to phylogenetic group A, followed by MDR E. coli (DECs) belonging to group B2. (4) Conclusion: This study is the first description of MDR E. coli (DECs) assigned to phylogroup A in western lowland gorillas from the MDNP in Gabon. Thus, wild gorillas in MDNP could be considered as asymptomatic carriers of potential pathogenic MDR E. coli (DECs) that may present a potential risk to human health.

1. Introduction

Many zoonoses are associated with ecological imbalances linked to deforestation, human population expansion, changes in agricultural practices and encroachment on wildlife habitats [1]. The intensification of these human activities within previously isolated wildlife habitats is a key factor in the emergence of infectious diseases [2,3]. Certainly, the spread of zoonotic diseases in human populations is a phenomenon on which particular attention has been paid [4,5,6]. On the other hand, the ever-increasing anthropization of wildlife habitats also favours the emergence of diseases in wildlife [2,7].
These zoonoses, caused by pathogenic microorganisms such as enterobacteria (such pathogenic E. coli), have been a human public health problem for decades [8,9]. Indeed, many studies have shown that wildlife [3,5,10,11,12,13], including wild primates, could transmit pathogens to humans [14,15,16,17]. Pathogenic E. coli strains belong to phylogenetic groups B2 and D [18,19,20], while commensal or wild-type strains, associated with phylogenetic groups B1 and A, are more frequently isolated in environment [21,22]. Pathogenic E. coli (DECs) are classified as enteropathogenic (EPEC), enterohemorrhagic (EHEC), enterotoxigenic (ETEC), entero-invasive (EIEC), enteroaggregative (EAEC) and diffuse adhesion (DAEC) E. coli [23].
Indeed, while habitat loss and poaching are recognized threats to the survival of great apes [24,25], infectious diseases are emerging as the real challenge facing the conservation of wildlife biodiversity. For example, the listing of the western lowland gorilla (Gorilla gorilla gorilla) in the IUCN Red List of Threatened Species (Version 2015.4. www.iucnredlist.org, accessed on 31 March 2022) is a consequence of the great apes massacre caused by the Zaire strain of the Ebola virus; thousands of common chimpanzees (Pan troglodytes troglodytes) and lowland gorillas in Central Africa were indeed decimated during this epidemic [26,27,28].
In addition, multidrug-resistant (MDR) pathogens, mainly enterobacteria, have been associated with increased mortality rates in humans and animals, including non-human primates (NHPs) [29]. Indeed, the close phylogenetic relationship between humans and other human species such as non-human primates, combined with the expansion of the human–animal interface, facilitates the transmission of pathogens between species, leading to morbidity and mortality in great ape populations worldwide [14,15,30,31,32,33,34,35,36].
Many substantiated cases of transmission of human pathogens to non-human primates [37], including chimpanzees [14] and mountain gorillas [15], have resulted from interactions (hunting, ecotourism, research activities, etc.) between humans and non-human primates.
Indeed, exchange of E. coli between humans, domestic animals and apes has been reported in densely populated areas of western Uganda. In Uganda, habituated groups of wild apes are visited daily by researchers and tourists, such as chimpanzees in Kibale [38] and mountain gorillas in Bwindi Impenetrable National Park [39].
In the forest of Moukalaba-Doudou National Park (MDNP), Gabon, ecotourism is being introduced due to the human habituation of groups of western lowland gorillas (Gorilla gorilla gorilla) [40,41]. The protection of human and animal populations, especially great apes, from mutual transmission of epidemics is therefore important [42].
Enterobacteriaceae, particularly Escherichia coli, Klebsiella spp., Enterobacter cloacae, Proteus mirabilis and Serratia spp., carrying antimicrobial resistance or multidrug-resistant Enterobacteriaceae (MRAE), have already been isolated from wild mammals in protected areas [43,44] and unprotected areas of Gabon [45], with a lower prevalence of bacteria isolated from wildlife compared to humans. Among these EMRAs, EBLSEs have recently been isolated from fruit bats captured in highly anthropized urban areas [45]. The level of antimicrobial-resistant bacteria in wildlife, particularly in western lowland gorillas (Gorilla gorilla gorilla), could reveal the true level of the anthropological impact on wildlife in the PNMD.
In Gabon, studies on antimicrobial resistance of enterobacteria isolated from gorillas in the Lopé National Park [46] and in the MDNP [43,44] have already been conducted. It has also been shown that in protected areas wild types of E. coli carrying natural (intrinsic) resistances predominate over clinical strains carrying acquired resistances [47]. However, there is a lack of data on pathogenic antibiotic resistant E. coli in the wild mammals in protected areas. These pathogenic strains of antimicrobial-resistant or MDR E. coli are potential zoonoses that could be spread to humans [48,49,50,51] and create a real public health problem.
This study aims to describe the phylogenetic groups and pathotypes associated with antimicrobial resistance of E. coli isolated from faecal samples of gorillas living in MDNP (south-western Gabon).

2. Results

2.1. E. coli Found in Gorilla Faecal Samples

Following culture on solid media, isolation and biochemical identification, 64 E. coli isolates were obtained from 96 faecal samples collected from gorillas in the MDNP forest.

2.2. Prevalence of E. coli Phylogroups

Among the 64 E. coli isolates, phylogroup A was predominant (69% ± 11.36%; n = 44/64), followed by phylogroups B2 (20% ± 19.89%; n = 13/64), B1 (10% ± 8.90%; n = 6/64) and D (1% ± 3.04%%; n = 1/64), respectively (Table 1).

2.3. Prevalence of E. coli Pathotypes

Characterization of E. coli pathogenicity genes showed that of the 64 isolates 20 (31% ± 11.36%) carried these genes. Among pathogenic isolates, there was a predominance of the EPEC pathotype (85% ± 10.82%; n = 17/20). Three isolates (15% ± 5.18%; n = 3/20) were positive for the EPEC/EHEC complex pathotype (Table 2).

2.4. Antibiotic Susceptibility Testing

From the 64 E. coli isolates, 62 (97% ± 4.26%) were resistant to at least one antimicrobial agent, and resistance was most frequently observed against the beta-lactam family, such as amoxicillin-clavulanic acid (60% ± 12.03%) followed by imipenem (54% ± 12.23%), ticarcillin (41% ± 12.03%), cefotetan (41% ± 12.03%), piperacillin/tazobactam (36% ± 11.76%), piperacillin (34% ± 11.64%), cefoxitin (33% ± 11.50%) and ertapenem (8% ± 6.57%). In the aminoglycoside family, isolates were resistant to gentamycin (6% ± 7.14%), to tobramycin (5% ± 1.24%), to netylmicin (5% ± 1.24%) and to amikacin (3% ± 5.18%). In the quinolones and fluoroquinolones family, isolates were resistant to nalidixic acid (19% ± 18.49%), to ciprofloxacin (10% ± 7.65%) and to levofloxacin (2% ± 4.26%). In the family of phosphonic acid, isolates were resistant to fosfomycin (11% ± 9.24%). In the family of phenicols, isolates were resistant to chloramphenicol (6% ± 7.14%). Isolates were also resistant to sulfamethoxazole (6% ± 7.14%), to nitrofurantonin (6% ± 7.14%), to tetracycline (6% ± 7.14%) and to levofloxacin (2% ± 4.26%); twelve of the 62 (19% ± 4.26%) were MDR (Figure 1).

3. Discussion

Studies have suggested that the habituation process of wild animals, including gorillas, and tourism activities in their home range are aggravating factors for increased disease transmission mechanisms between humans and wildlife [54,55]. Indeed, the presence of human observers stresses the animals, which increases their susceptibility to microbial diseases [54,55]. In addition, the increase in human–wildlife interactions, including gorillas, greatly facilitates the exchange of potential pathogens [56].
This study is the first identification of MDR E. coli (DECs) isolates assigned to different phylogenetic groups in a wild gorilla population in the PNMD in Gabon. Indeed, previous studies in Gabon have reported the prevalence of antimicrobial resistance in Enterobacteriaceae, including E. coli, isolated from the faeces of unprotected wild mammals from peri-urban areas [45,57], and the faeces of wild mammals from protected areas such as those in the PNMD [43,44] and the Lopé National Park [46]. In addition, studies conducted in the Lopé National Park have characterized E. coli isolates belonging to phylogenetic groups A, B1, B2 and D [46].

3.1. Isolation of E. coli in Wild Gorillas from MDNP

The presence of antimicrobial resistance in Gabon’s national parks has already been described. This study aimed to describe the phylogenetic groups, pathotypes and prevalence of antimicrobial resistance in E. coli isolated from gorillas living in MDNP in Gabon. In our study, the prevalence of E. coli was similar to that reported by Mbehang et al. [45] and Benavides et al. [46] in the gorilla population living in national parks in Gabon. E. coli is one of the enterobacteria frequently described in wildlife [58,59,60].

3.2. Prevalence of Phylogenetic Groups

The phylogenetic clustering method used in this study detected and classified E. coli isolated from gorilla faeces into four groups (A, B1, B2 and D) [52,53]. Groups B2 and D are associated with extraintestinal pathogenic isolates causing diarrheal diseases in humans and animals [18,19,20], while groups A and B1 are associated with commensal isolates [52,53]. However, group B2 and D isolates are less frequently isolated from the environment [59] or fish, frogs and reptiles compared to group A or B1 isolates [22].
Our results revealed the predominance of phylogroups A (44/69%) and B2 (13/21%) and are similar to those obtained by Benavides et al. [46]. Although the number of commensal E. coli isolates is greater than the number of pathotype-carrying E. coli isolates in our results, the finding of the latter would suggest that these wild gorillas are asymptomatic carriers of potentially pathogenic E. coli [61]. The relatively high prevalence of group B2 isolates has previously been associated with herbivorous and omnivorous animals [23] and would suggest a potential transmission of E. coli strains from humans to these gorillas.
The phylogenetic grouping results obtained in the Taï National Park (Ivory Coast), namely group A (68%), followed by group B1 (18%), group D (16%) and group B2 (0.4%) [62], are very similar to those obtained by us. The predominance of phylogroup A was, as in the present study, in agreement with the results obtained by Carlos et al. [63], who concluded that group A is more prevalent in omnivorous hosts, while group B1 is typical of herbivorous hosts. Studies conducted at Minnesota State Zoo showed that phylogenetic groups A, B1, B2 and D were isolated from a captive population of NHPs being tested. In this study, group B1 was the most predominant [64]. These results are similar to those observed in our study on wild gorillas.

3.3. Prevalence of Pathotypes

Detection of E. coli pathotypes revealed that 20 out of 64 (31% ± 11.36%) isolates carried E. coli pathotypes represented mainly by the EPEC group (85% ± 10.82%) followed by the EPEC/EHEC complex (5% ± 5.18%). Similar results were reported by Kolappaswamy et al. [62]. These DECs are most often implicated in the development of diarrhoea in humans and are thought to contribute to the weakening of the host immune system [64,65,66,67,68]. The results of our study suggest that these gorillas are asymptomatic carriers of potentially pathogenic E. coli isolates.
The prevalence of EPEC pathotypes observed in our study is higher than that obtained in wild semi-captive monkeys in India [69]. In addition, EPEC was the most common pathotype isolated from captive and semi-captive populations of non-human primates [62,63,64,65,66,67,68,69,70,71,72]. Similarly, the results observed in our study corroborate those obtained by a team of researchers from the State of Minnesota in the United States for the majority of the primates studied living in a zoo, concerning EHEC and EPEC pathotypes [73]. Indeed, the EPEC pathotype is a major public health problem in developing countries, as it is a significant cause of childhood diarrhoea, sometimes fatal [74,75]. However, this pathotype has different effects on non-human primates, i.e., some react as asymptomatic carriers and others are susceptible and suffer from diarrhoea [70,71,76,77].
The presence of these DECs in the faeces of western lowland gorillas in MDNP suggests potential human transmission through defecation and waste of all kinds produced by the human populations surrounding this protected area, and that these wild animals are important reservoirs of E. coli isolates potentially pathogenic to humans.

3.4. Antibiotic Susceptibility

In our study, the antimicrobial resistance prevalence of E. coli isolates to beta-lactam antimicrobials, such as amoxicillin-clavulanic acid, imipenem, cefotetan, piperacillin and piperacillin-tazobactam, were observed. These results could be due to the contamination of food eaten by the gorillas. Indeed, wild animals, including gorillas in MDNP, can acquire antimicrobial resistant bacteria and AMR genes through improperly disposed antimicrobial chemicals and through environments contaminated with animal faeces and remains [78,79,80,81]. This result could also be explained to a lesser extent by other mechanisms for resistance acquisition, such as horizontal gene exchange among bacteria or naturally acquired resistance [46], or even through the adaptation and evolution of these pathogenic enterobacterial isolates in their environment [82] or the consumption of various foods [46,83]. The results obtained in a very recent study tend to correlate with our observations on the prevalence of antimicrobial resistance in wildlife. According to the authors, antimicrobial-resistant bacteria can contaminate soil and water systems and spread to wildlife [84]. Similar results were also observed in a study conducted in the Apuan Alps Regional Park (Tuscany, Italy) [85].
However, antimicrobial resistance was obtained for aminoglycosides, tetracycline, nitrofurantoin, sulfamethoxazole-trimethoprim and phenicol in our study. Similar results have been observed in studies of terrestrial mammals in protected [45] and unprotected [45,57] areas of Gabon. E. coli is naturally sensitive to these antimicrobials [16]. Therefore, the presence of these resistances in the digestive tract of gorillas could also be explained by the low human consummation of these antibiotics in that area.
The rates of resistance to ciprofloxacin obtained in our study are similar to those observed by Albrechtova et al. in Taï National Park [86]. Janatova et al. [87] obtained similar results in habituated gorillas (Gorilla gorilla gorilla) in the Dzanga-Sangha protected area in CAR, also describing the presence of these resistance genes [87]. Ciprofloxacin is a highly mobile hydrophilic compound, present in high concentrations in aquatic environments such as hospital effluents [88,89]. Despite its low stability with short half-lives, ciprofloxacin has regularly been detected in various aquatic environments such as groundwater and drinking water [88,90,91,92]. This could be partially explained by the wide use of this antimicrobial in the treatment of infections in human populations living around the PNMD [43,44,45]. Additionally, this resistance could be due to the intrinsic exchange of the resistome present in the digestive tract of these animals [82].
In addition, in E. coli, resistance to ciprofloxacin could result from various genetic variations [93,94,95]. Most strains unable to develop a favourable set of mutations in the quinolone resistance determining regions (QRDRs) must rely primarily on the overexpression of efflux pumps [96,97]. Only a few sequence types of E. coli would be able to develop multiple energetically favourable QRDR mutations [97].
The antimicrobial resistance observed in our study could also be related to antimicrobials used in human therapy and consumed locally. This hypothesis had already been proposed [43,44,46]. According to these authors, previous studies had already postulated that contact and subsequent transmission of antimicrobial-resistant bacterial isolates from highly resistant sources, such as humans or livestock, could explain the occurrence of antimicrobial resistance in wildlife [81,98,99,100,101].
The prevalence of antimicrobial resistance obtained in our study is higher than that observed in Bwindi Impenetrable National Park, where tourism and wildlife research activities are conducted. However, the results of this work suggest that habitat overlap between humans, livestock and mountain gorillas could influence the patterns of gastrointestinal bacterial exchange between the species [39]. The low rates of antimicrobial resistance in chimpanzees and monkeys in Taï National Park are thought to be attributed to the naturally evolving resistome, particularly because the monkeys have never been treated with antibiotics—evidence that there was no transmission of multidrug-resistant enteric bacteria, including E. coli, from humans to non-human primates in the park. Hygiene practices employed in the TNP would be effective in protecting Taï NHPs from acquiring multi-drug resistant enteric bacteria from humans [86]. In addition, the results obtained in the study of mountain gorillas in Kibale National Park, Uganda, for chloramphenicol, ciprofloxacin, tetracycline, trimethoprim-sulfamethoxazole and nalidixic acid were lower than our results, while the antimicrobial resistance results for chimpanzees from the same site were closer to ours [102].
The results obtained by Weiss et al. provided further evidence that humans and animals harbour bacteria with phenotypically similar (often identical) antimicrobial resistance profiles to commonly available and tested human antimicrobials [24,39]. However, the proportion of resistant isolates in animals was about three times lower than in humans, to ensure that isolates from domestic animals and wild primates had comparable proportions of resistant isolates. The most common multiple resistance patterns in E. coli isolates from humans were also the most common multiple resistance patterns in E. coli isolates from both livestock and wild primates [102].
However, the results of this work are not consistent with those obtained very recently in nature reserves, protected areas and national parks in the Gambia for a wide range of non-human primates regarding trimethoprim, sulfamethoxazole and tetracycline [103]. Increased contact between animal species greatly facilitates the potential exchange of pathogens [104]. Analyses by the research team also suggested an exchange of E. coli strains between humans and wild non-human primates [103].
The antimicrobial resistance rates obtained in our study were much higher than those observed in the work of Clayton et al. in a Minnesota State Zoo for gentamicin, nalidixic acid, tetracycline, sulfamethoxazole and trimethoprim in gorillas and other non-human primate species studied [73]. The results obtained in this study could be explained by the fact that the majority of the antimicrobials tested had only recently been used, except for ampicillin, which had historically been used in zoos to treat physical injuries, often suffered by humans [73]. However, the prevalence of resistance observed in another previous study of snub-nosed monkeys in zoos in China [105] is very close to the rates obtained in our study. Geographical location, zoological practices and the species of primates examined are many factors that could explain this phenomenon.
Antimicrobial resistance results for chloramphenicol, ciprofloxacin, gentamicin, tetracycline and trimethoprim in Kibale chimpanzees were lower than ours. However, the lack of appreciable resistance to ciprofloxacin, neomycin, gentamicin and ceftiofur in humans or chimpanzees already suggested that local antimicrobial use was responsible for the observed trends. It should be noted that no antimicrobials had ever been administered to the Kibale chimpanzees, but also that antimicrobials are freely available in Uganda and can be used indiscriminately. Thus, the presence of clinically resistant isolates in chimpanzees provided further evidence of the transmission of resistant bacteria or resistance-conferring genetics from humans to chimpanzees [38].

3.5. Association between Antimicrobial-Resistant DECs and Virulence in E. coli

Resistance profiles obtained in our study were diverse. Twelve E. coli isolates showed MDR with a resistance index between 0.22–0.59 in this study (Table 3). The results of this study reveal that the majority of MDR E. coli (DECs) isolates belong to group A and group B1, which group commensal isolates, followed by groups B2 and D, which group pathogenic isolates (Figure 2). Recent studies have reported that antimicrobial resistance and virulence factor carriage are linked, in E. coli populations, to a community setting [106,107]. Furthermore, these data suggested that while the co-occurrence of resistance and virulence in E. coli is partially due to antimicrobial selection pressure, the presence of virulence factors might explain it [106].
Ecological niche, life history and the propensity of causing disease are markers that characterize the different E. coli phylogroups. Thus, groups B2 and D are less frequently isolated from the environment [109]. Regarding human disease, E. coli isolates recovered from extra-intestinal body sites are more likely to belong to phylotypes B2 or D than to groups A or B1 [110,111]. Previous studies have revealed differences in the prevalence of phylogenetic groups within virulent extra-intestinal E. coli [112]. Although the two phylogenetic groups most commonly linked to extra-intestinal E. coli virulence are the aforementioned groups B2 and D, some reports have shown a high frequency of group A (46%) among E. coli causing UTIs in humans [112].
In addition, the existence of resistance diversity in terrestrial mammals, both genotypically and phenotypically, has been previously described in different protected areas in Africa, including Gabon [43,44,45,46], CAR [87], the Ivory Coast [86] and Uganda [38,39]. These results point to the potential for transmission of these MDR E. coli (DECs) from wildlife to humans living close to these areas or often cohabiting with these animals, or vice versa [38,39]. The results obtained in our study would support this hypothesis insofar as the majority of MDR DECs isolated from the faeces of MDNP gorillas belong to phylogenetic group A almost exclusively isolated from humans. This information highlights the existence of a health threat to these endangered animals living in protected areas.

4. Materials and Methods

  • Feld research authorization
The sampling of gorilla faeces in their living area in Moukalaba-Doudou National Park (Figure 3) was carried out in the case of a research study (field research authorization N° 003/20/DG/JBLD).

4.1. Study Area

Faecal samples were collected in the home range of habituated gorillas of MDNP (Figure 3) [113,114,115] from 27 February to 10 March 2020 using the non-invasive method as described in previous studies [44,45].
Pathogens 11 01082 g003 550
Figure 3. Location of the study area [116].
Figure 3. Location of the study area [116].
Pathogens 11 01082 g003

4.2. Sample Collection

Gorilla faeces were collected non-invasively by following gorillas in the forest.
Faeces left behind either following immediate defecation or three hours later were picked up based on the observation of their colour, temperature and consistency. To avoid bias from soil contamination, each faecal sample was collected inside the faecal material, avoiding surfaces exposed to the immediate environment and atmospheric oxygen, and the more reflective surfaces of fresh distal intestine (large intestine) samples using sterilized forceps. It is recommended that as many samples as possible be taken to ensure that a large number of individuals are sampled [43,44]. Each tube containing a faeces sample was stored in a bag in the shade and identified by a number which was transcribed on the tube and referenced in a small booklet next to which the identifiers of the said sample were marked (the diameter of the faeces, the collection area, the GPS point of the location, the name of the gorilla, etc.). Back at the research camp laboratory and after 3 to 4 h of sampling, a small portion of each sample was used to culture the bacteria and the remaining sample was stored/preserved in a solution of 70% physiological water (or phosphate-buffered saline (PBS)) and 30% glycerol. Samples preserved in such conditions could then be stored on the bench, in a bag or in a box, for more than two weeks at room temperature.

4.3. Culture, Isolation and Identification of Colonies

In the bacteriology laboratory of the Interdisciplinary Center for Medical Research of Franceville (CIRMF), the bacteria culture consisted of emulsifying some of the faecal specimens in sterile water and streaking a loopful of the resultant on MacConkey agar medium (MCA) (bioMérieux, France). After eighteen to twenty-four hours of incubation, several colonies (never more than two or three from one medium Petri dish), differentiated by structure and colour, were picked up and streaked in the same medium and incubated in the same conditions. A loop of liquid was removed from the cultures and streaked onto methylene eosin blue agar (EMB) plates (bioMérieux, France) for E. coli isolation. Plates were examined for the characteristic appearance of E. coli (metallic green sheen) and colonies with green metallic sheen were interpreted as E. coli isolates [117,118,119]. Purified green metallic colonies were subjected to biochemical identification using the Api 20 E galleries (bioMérieux, Marcy l’étoile, France) and the VITEK® 2 Compact 15 system (bioMérieux, Marcy l’étoile, France). Isolates were confirmed by using phylogenetic group detection PCR as described by Clermont et al. [52,53].

4.4. Antimicrobial Susceptibility Testing of E. coli Isolates

Antimicrobial susceptibility testing was performed using the Kirby–Bauer disk-diffusion method [120]. The antimicrobial was chosen according to the recommendations of the Clinical Laboratory Standards Institute [121,122]. The antimicrobials tested were amoxicillin/clavulanic acid (AMC, 30 μg), ticarcillin (TIC, 75 µg), piperacillin (PIP, 100 μg), piperacillin/tazobactam (TZP, 100/10 µg), cefoxitin (FOX 30 μg), imipenem (IPM, 10 μg), ertapenem (ETP, 10 μg), amikacin (AMK, 30 μg), gentamycin (GEN, 10 μg), netilmicin (NET, 30 μg), tobramycin (TOB, 10 μg), chloramphenicol (CHL, 30 μg), tetracycline (TET, 30 μg), trimethoprim/sulfamethoxazole (SXT, 25 μg), nalidixic acid (NAL, 30 µg), ofloxacin (OFX, 5 μg), ciprofloxacin (CIP, 5 μg), levofloxacin (LVX, 5 µg), norfloxacin (NFX 10 µg), cefotetan (CTT 30 µg), fosfomycin (FOF, 200 g) and nitrofurantonin (NIT, 300 µg).
The breakpoints provided by the CLSI (2018) were used for the designation of isolates as resistant (R), intermediately susceptible (IS) or susceptible (S). For subsequent data analysis, the isolates with an I result were grouped with the isolates that gave an R result, and defined as resistant. Multidrug-resistant isolates were identified based on the definition of MDR as bacteria that are resistant to three or more classes of antimicrobial agents [84,123].

4.5. Molecular Identification of E. coli Phylogenetic and Pathotype Groups

DNA Extraction

DNA was extracted using the boiling method described by Mbehang Nguema et al. [45]. The characterization of the phylogenetic groups (A, B1, B2 and D) was carried out by amplification of the 3 genes chua, yjiaa and tspe4c2 in multiplex PCR as described by Clermont et al. [52,53] (Table S1). The characterization of the pathotype groups was carried out under the conditions described by Sjöling et al. [124], using primers [125,126,127].

4.6. Data Analysis

The software Excel was used for data analysis, including calculations of the prevalence of E.-coli-carrying genes for detecting phylogenetic groups and pathotypes, the prevalence of antimicrobial resistance and confidence intervals. Adobe Illustrator software was used to design the histograms. The Multiple Antimicrobial Resistance Index was calculated following Krumperman [108]. All statistical analyses were performed using R 4.0.2. To visualize the data, a correspondence analysis was performed with the packages FactoMineR and Factoextra. In order to determine the relationship between the occurrence of EPEC virulence factors, antimicrobial resistance and phylogroups, a generalized linear binomial family model was generated with the stats package version 3.6.2 using the glm function. The best model illustrating this relationship was the one with ΔAIC = 0.

5. Conclusions

This study aimed to describe the phylogenetic groups and pathotypes associated with antimicrobial resistance of E. coli isolates from wild western lowland gorillas in the MDNP, a protected area in Gabon. The presence of these MDR E. coli (DECs), observed in these animals, suggests that they may be reservoirs of potential pathogenic antimicrobial resistant bacteria that would present a health risk to humans, but also the need to deepen our knowledge of their origin and their diffusion mechanisms in different ecological niches. The permanent absence of electricity at the sampling site, the limited time of the field missions, the tertiary nature of the forest, the wild nature of the animals that were the subject of this study, etc., are all limitations that we encountered in the field. However, the results obtained pave the way for other lines of research such as the sequencing of these MDR E. coli (DECs) to generate a phylogenetic tree, and then the study of the diet of these animals which could be a factor limiting the effects of these MDR E. coli (DECs). In addition, the study of the variation in the prevalence of these MDR E. coli (DECs) according to the seasons, etc., would be of great use.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/pathogens11101082/s1, Table S1: Target genes and primers used for the detection of E. coli phylogenetic groups [52,53] and pathotypes [124].

Author Contributions

Formal analysis, L.E.D.O.Y. and N.M.L.P.; investigation, L.E.D.O.Y., R.O. and E.F.A.-O.; methodology, L.E.D.O.Y., R.O., A.M.-M. and P.P.M.N.; project administration, L.E.D.O.Y., R.O., P.P.M.N. and S.G.; resource, G.N.A. and J.C.O.M.; supervision, L.E.D.O.Y., R.O., P.P.M.N., E.F.A.-O., I. and S.G.; Resource, N.P. and J.F.M.; writing—original draft, L.E.D.O.Y.; writing—review and editing, L.E.D.O.Y., R.O., D.O.E., P.P.M.N. and R.W.L. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Acknowledgments

Our thanks go to Jean Bernard LEKANA-DOUKI, Managing, and Etienne François AKOMO-OKOUE, for logistically and technically providing his support for the sampling in Doussala Station.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Chomel, B.B.; Belotto, A.; Meslin, F.-X. Wildlife, exotic pets, and emerging zoonoses. Emerg. Infect. Dis. 2007, 13, 6. [Google Scholar] [CrossRef] [PubMed]
  2. Daszak, P.; Cunningham, A.A.; Hyatt, A.D. Anthropogenic environmental change and the emergence of infectious diseases in wildlife. Acta Trop. 2001, 78, 103–116. [Google Scholar] [CrossRef]
  3. Jones, K.E.; Patel, N.G.; Levy, M.A.; Storeygard, A.; Balk, D.; Gittleman, J.L.; Daszak, P. Global trends in emerging infectious diseases. Nature 2008, 451, 990–993. [Google Scholar] [CrossRef]
  4. Woolhouse, M.E.; Gowtage-Sequeria, S. Host range and emerging and reemerging pathogens. Emerg. Infect. Dis. 2005, 11, 1842. [Google Scholar] [CrossRef] [PubMed]
  5. Wolfe, N.D.; Dunavan, C.P.; Diamond, J. Origins of major human infectious diseases. Nature 2007, 447, 279–283. [Google Scholar] [CrossRef]
  6. Lloyd-Smith, J.O.; Georges, D.; Pepin, K.M.; Pitzer, V.E.; Pulliam, J.R.C.; Dobson, A.P.; Hudson, P.J.; Grenfell, B.T. Epidemic dynamics at the human-animal interface. Science 2009, 326, 1362–1367. [Google Scholar] [CrossRef]
  7. Dobson, A.; Foufopoulos, J. Emerging infectious pathogens of wildlife. Philos. Trans. Royal. Soc. Lond. Ser. B Biol. Sci. 2001, 356, 1001–1012. [Google Scholar] [CrossRef] [PubMed]
  8. Kahn, R.; Clouser, D.; Richt, J. Emerging infections: A tribute to the one medicine, one health concept. Zoonoses Public Health 2009, 56, 407–428. [Google Scholar] [CrossRef]
  9. Richt, J.; Feldmann, H. Emerging zoonoses: Recent advances and future challenges. Zoonoses Public Health 2009, 56, 257. [Google Scholar] [CrossRef]
  10. Kruse, H.; Kirkemo, A.-M.; Handeland, K. Wildlife as source of zoonotic infections. Emerg. Infect. Dis. 2004, 10, 2067. [Google Scholar] [CrossRef]
  11. Rabinowitz, P.; Scotch, M.; Conti, L. Human and animal sentinels for shared health risks. Vet. Ital. 2009, 45, 23. [Google Scholar]
  12. Quammen, D. Spillover: Animal Infections and the Next Human Pandemic; WW Norton & Company: New York, NY, USA, 2012. [Google Scholar]
  13. Quammen, D. Ebola: The Natural and Human History of a Deadly Virus; WW Norton & Company: New York, NY, USA, 2014. [Google Scholar]
  14. Köndgen, S.; Kühl, H.; N’Goran, P.K.; Walsh, P.D.; Schenk, S.; Ernst, N.; Biek, R.; Formenty, P.; Mätz-Rensing, K.; Schweiger, B. Pandemic human vi-ruses cause decline of endangered great apes. Curr. Biol. 2008, 18, 260–264. [Google Scholar] [CrossRef] [PubMed]
  15. Palacios, G.; Lowenstine, L.J.; Cranfield, M.R.; Gilardi, K.V.K.; Spelman, L.; Lukasik-Braum, M.; Kinani, J.-F.; Mudakikwa, A.; Nyirakaragire, E.; Bussetti, A.V.; et al. Human metapneumovirus infection in wild mountain gorillas, Rwanda. Emerg. Infect. Dis. 2011, 17, 711. [Google Scholar] [CrossRef]
  16. Calvignac-Spencera, S.; Leendertza, S.A.J.; Gillespie, T.R.; Leendertza, F.H. Wild great apes as sentinels and sources of infectious disease. Clin. Microbiol. Infect. 2012, 18, 521–527. [Google Scholar] [CrossRef]
  17. Schaumburg, F.; Mugisha, L.; Kappeller, P.; Fichtel, C.; Köck, R.; Köndgen, S.; Becker, K.; Boesch, C.; Peters, G.; Leendertz, F.H. Evaluation of non-invasive biological samples to monitor Staphylococcus aureus colonization in great apes and lemurs. PLoS ONE 2013, 8, e78046. [Google Scholar] [CrossRef]
  18. Nowrouzian, F.L.; Wold, A.E.; Adlerberth, I. Escherichia coli strains belonging to phylogenetic group B2 have superior capacity to persist in the intestinal microflora of infants. J. Infect. Dis. 2005, 191, 1078–1083. [Google Scholar] [CrossRef]
  19. Nowrouzian, F.L.; Wold, A.E.; Adlerberth, I. Enhanced persistence in the colonic microbiota of Escherichia coli strains be-longing to phylogenetic group B2: Role of virulence factors and adherence to colonic cells. Microbes Infect. 2006, 8, 834–840. [Google Scholar] [CrossRef]
  20. Johnson, J.R. Molecular epidemiology and population genetics of extraintestinal pathogenic Escherichia coli. In Population Genetics of Bacteria: A Tribute to Thomas, S. Whittam; ASM Press: Washington, DC, USA, 2011; pp. 91–107. [Google Scholar]
  21. Escobar-Páramo, P.; Le Menac’h, A.; Le Gall, T.; Amorin, C.; Gouriou, S.; Picard, B.; Skurnik, D.; Denamur, E. Identification of forces shaping the commensal Escherichia coli genetic structure by comparing animal and human isolates. Environ. Microbiol. 2006, 8, 1975–1984. [Google Scholar] [CrossRef] [PubMed]
  22. Gordon, D.M.; Cowling, A. The distribution and genetic structure of Escherichia coli in Australian vertebrates: Host and geographic effects. Microbiology 2003, 149, 3575–3586. [Google Scholar] [CrossRef] [PubMed]
  23. Croxen, M.A.; Law, R.J.; Scholz, R.; Keeney, K.M.; Wlodarska, M.; Finlay, B.B. Recent advances in understanding enteric pathogenic Escherichia coli. Clin. Microbiol. Rev. 2013, 26, 822–880. [Google Scholar] [CrossRef] [PubMed]
  24. Goldberg, T.L.; Gillespie, T.R.; Rwego, I.B.; Estoff, E.L.; Chapman, C.A. Forest fragmentation as cause of bacterial transmission among nonhuman primates, humans, and livestock, Uganda. Emerg. Infect. Dis. 2008, 14, 1375. [Google Scholar] [CrossRef] [PubMed]
  25. Cameron, K.; Cranfield, M.; Gaffikin, L.; Kalema-Zikusoka, G.; Köndgen, S.; Leendertz, S.; Lonsdorf, E.; Muehlenbein, M.; Mugisha, L.; Nizeyi, J.B.; et al. Best Practice Guidelines for Health Monitoring and Disease Control in Great Ape Populations; Occasional Paper of the IUCN Species Survival Commission No. 56; IUCN Species Survival Commission: Gland, Switzerland, 2015; p. 56. [Google Scholar]
  26. Walsh, P.D.; Abernethy, K.A.; Bermejo, M.; Beyers, R.; De Wachter, P.; Akou, M.E.; Huijbregts, B.; Mambounga, D.I.; Toham, A.K.; Kilbourn, A.M.; et al. Catastrophic ape decline in western equatorial Africa. Nature 2003, 422, 611–614. [Google Scholar] [CrossRef] [PubMed]
  27. Leroy, E.M.; Rouquet, P.; Formenty, P.; Souquière, S.; Kilbourne, A.; Froment, J.-M.; Bermejo, M.; Smit, S.; Karesh, W.; Rollin, P.E. Multiple Ebola virus transmission events and rapid decline of central African wildlife. Science 2004, 303, 387–390. [Google Scholar] [CrossRef] [PubMed]
  28. Genton, C.; Cristescu, R.; Gatti, S.; Levréro, F.; Bigot, E.; Caillaud, D.; Pierre, J.-S.; Ménard, N. Recovery potential of a western lowland gorilla population following a major Ebola outbreak: Results from a ten year study. PLoS ONE 2012, 7, e37106. [Google Scholar] [CrossRef]
  29. D’Andrea, M.M.; Arena, F.; Pallecchi, L.; Rossolini, M.G. CTX-M-type β-lactamases: A successful story of antibiotic resistance. Int. J. Med. Microbiol. 2013, 303, 305–317. [Google Scholar] [CrossRef]
  30. Lawick-Goodall, J.V. The Shadow of Man; Houghton Mifflin Company: Boston, MA, USA, 1971. [Google Scholar]
  31. Wallis, J. Prevention of disease transmission in primate conservation. Ann. N. Y. Acad. Sci. 2000, 916, 691–693. [Google Scholar] [CrossRef] [PubMed]
  32. Ferber, D. Human diseases threaten great apes. Science 2000, 289, 1277–1278. [Google Scholar] [CrossRef] [PubMed]
  33. Woodford, M.H.; Butynski, T.M.; Karesh, W.B. Habituating the great apes: The disease risks. Oryx 2002, 36, 153–160. [Google Scholar] [CrossRef]
  34. Kaur, T.; Singh, J.; Tong, S.; Humphrey, C.; Clevenger, D.; Tan, W.; Szekely, B.; Wang, Y.; Li, Y.; Muse, E.A.; et al. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees (Pan troglodytes) at Mahale Mountains National Park, Western Tanzania. Am. J. Primatol. 2008, 70, 755–765. [Google Scholar] [CrossRef] [PubMed]
  35. Deem, S.L. Conservation Medicine: A Solution-Based Approach for Saving Nonhuman Primates. In Ethnoprimatology. Developments in Primatology: Progress and Prospects; Waller, M.T., Ed.; Springer: Cham, Switzerland, 2016. [Google Scholar] [CrossRef]
  36. Estrada, A.; Garber, P.A.; Rylands, A.B.; Roos, C.; Fernandez-Duque, E.; Di Fiore, A.; Nekaris, K.A.-I.; Nijman, V.; Heymann, E.W. Impending extinction crisis of the world’s primates: Why primates matter. Sci. Adv. 2017, 3, e1600946. [Google Scholar] [CrossRef] [Green Version]
  37. Gillespie, T.R.; Nunn, C.L.; Leendertz, F.H. Integrative approaches to the study of primate infectious disease: Implications for biodiversity conservation and global health. Am. J. Phys. Anthr. 2008, 137, 53–69. [Google Scholar] [CrossRef] [PubMed]
  38. Goldberg, T.L.; Gillespie, T.R.; Rwego, I.B.; Estoff, E.L.; Chapman, C.A. Patterns of gastrointestinal bacterial exchange between chimpanzees and humans involved in research and tourism in western Uganda. Biol. Conserv. 2007, 135, 511–517. [Google Scholar] [CrossRef]
  39. Rwego, I.B.; Isabirye-Basuta, G.; Gillespie, T.R.; Goldberg, T.L. Gastrointestinal bacterial transmission among humans, mountain gorillas, and livestock in Bwindi Impenetrable National Park, Uganda. Conserv. Biol. 2008, 22, 1600–1607. [Google Scholar] [CrossRef] [PubMed]
  40. Yamagiwa, J. Creating a Future in which Human Beings and Wild Animals Can Live in Harmony in the Tropical Forests of Africa. Japan Science and Technology Agency. 2006. Available online: https://www.jst.go.jp/global/english/kadai/h2006_gabon.html (accessed on 7 November 2013).
  41. Matsuura, N.; Takenoshita, Y.; Yamagiwa, J. Eco-anthropologie et primatologie pour la conservation de la biodiversité: Un projet collaboratif dans le Parc National de Moukalaba-Doudou, Gabon. Rev. Primatol. 2013. [CrossRef]
  42. Alvarez, D.A.K.A.; Völlm, J. Maladies zoonotiques partagées par les gorilles et les humains. Gorilla J. 2004, 29, 17–18. (In French). [Google Scholar]
  43. Nguema, P.P.M.; Okubo, T.; Tsuchida, S.; Fujita, S.; Yamagiwa, J.; Tamura, Y.; Ushida, K. Isolation of multiple drug-resistant enteric bacteria from feces of wild Western Lowland Gorilla (Gorilla gorilla gorilla) in Gabon. J. Vet. Med. Sci. 2015, 77, 619–623. [Google Scholar] [CrossRef]
  44. Nguema, P.P.M.; Tsuchida, S.; Ushida, K. Bacteria culturing and isolation under field conditions of Moukalaba-Doudou National Park, Gabon, and preliminary survey on bacteria carrying antibiotic resistance genes. Tropics 2015, 23, 165–174. [Google Scholar] [CrossRef]
  45. Nguema, P.P.M.; Onanga, R.; Atome, G.R.N.; Mbeang, J.C.O.; Mabika, A.M.; Yaro, M.; Lounnas, M.; Dumont, Y.; Zohra, Z.F.; Godreuil, S.; et al. Characterization of ESBL-producing enterobacteria from fruit bats in an unprotected area of Makokou, Gabon. Microorganisms 2020, 8, 138. [Google Scholar] [CrossRef] [PubMed]
  46. Benavides, J.A.; Godreuil, S.; Bodenham, R.; Ratiarison, S.; Devos, C.; Petretto, M.-O.; Raymond, M.; Escobar-Páramoa, P. No evidence for transmission of antibiotic-resistant Escherichia coli strains from humans to wild western lowland gorillas in Lopé National Park, Gabon. Appl. Environ. Microbiol. 2012, 78, 4281–4287. [Google Scholar] [CrossRef]
  47. Nguema, P.P.M.; Onanga, R.; Atome, G.R.N.; Tewa, J.J.; Mabika, A.M.; Nzambe, J.U.M.; Mbeang, J.C.O.; Essono, P.Y.B.; Bretagnolle, F.; Godreuil, S. High level of intrinsic phenotypic antimicrobial resistance in enterobacteria from terrestrial wildlife in Gabonese national parks. PLoS ONE 2021, 16, e0257994. [Google Scholar]
  48. Guenther, S.; Aschenbrenner, K.; Stamm, I.; Bethe, A.; Semmler, T.; Stubbe, A.; Stubbe, M.; Batsajkhan, N.; Glupczynski, Y.; Wieler, L.H.; et al. Comparable high rates of extended-spectrum-beta-lactamase-producing Escherichia coli in birds of prey from Germany and Mongolia. PLoS ONE 2012, 7, e53039. [Google Scholar] [CrossRef] [PubMed]
  49. Hussain, A.; Shaik, S.; Ranjan, A.; Nandanwar, N.; Tiwari, S.K.; Majid, M.; Baddam, R.; Qureshi, I.A.; Semmler, T.; Wieler, L.H.; et al. Risk of transmission of antimicrobial resistant Escherichia coli from commercial broiler and free-range retail chicken in India. Front. Microbiol. 2017, 8, 2120. [Google Scholar] [CrossRef] [PubMed]
  50. Wieler, L.H.; Ewers, C.; Guenther, S.; Walther, B.; Lübke-Becker, A. Methicillin-resistant staphylococci (MRS) and extended-spectrum beta-lactamases (ESBL)-producing Enterobacteriaceae in companion animals: Nosocomial infections as one reason for the rising prevalence of these potential zoonotic pathogens in clinical samples. Int. J. Med. Microbiol. 2011, 301, 635–641. [Google Scholar] [PubMed]
  51. Mazurek-Popczyk, J.; Pisarska, J.; Bok, E.; Baldy-Chudzik, K. Antibacterial activity of bacteriocinogenic commensal Escherichia coli against zoonotic strains resistant and sensitive to antibiotics. Antibiotics 2020, 9, 411. [Google Scholar] [CrossRef] [PubMed]
  52. Clermont, O.; Bonacorsi, S.; Bingen, E. Rapid and simple determination of the Escherichia coli phylogenetic group. Appl. Environ. Microbiol. 2000, 66, 4555–4558. [Google Scholar] [CrossRef] [PubMed]
  53. Gordon, D.M.; Clermont, O.; Tolley, H.; Denamur, E. Assigning Escherichia coli strains to phylogenetic groups: Multi-locus sequence typing versus the PCR triplex method. Environ. Microbiol. 2008, 10, 2484–2496. [Google Scholar] [CrossRef]
  54. Koneman, E.W.; Allen, S.D.; Janda, W.; Schreckenberger, P.; Winn, W. Diagnostic Microbiology. The Nonfermentative Gram-Negative Bacilli; Lippincott-Raven Publishers: Philadelphia, PA, USA, 1997; pp. 253–320. [Google Scholar]
  55. Baneth, G.; Aroch, I.; Tal, N.; Harrus, S. Hepatozoon species infection in domestic cats: A retrospective study. Vet. Parasitol. 1998, 79, 123–133. [Google Scholar] [CrossRef]
  56. Zogg, A.L.; Zurfluh, K.; Schmitt, S.; Nüesch-Inderbinen, M.; Stephan, R. Antimicrobial resistance, multilocus sequence types and virulence profiles of ESBL producing and non-ESBL producing uropathogenic Escherichia coli isolated from cats and dogs in Switzerland. Vet. Microbiol. 2018, 216, 79–84. [Google Scholar] [CrossRef]
  57. Onanga, R.; Nguema, P.P.M.; Atome, G.R.N.; Mabika, A.M.; Ngoubangoye, B.; Tonda, W.L.K.; Mbeang, J.C.O.; Lebibi, J. Prevalence of Extended-Spectrum β-Lactamases in E. coli of Rats in the Region North East of Gabon. Vet. Med. Int. 2020, 2020, 5163493. [Google Scholar] [CrossRef]
  58. Renaud, F.; Vittecoq, M. Faune Sauvage et Antibiorésistances. In La Revue d’Humanité et Biodiversité; Humanité et Biodiversité: Paris, France, 2015; p. 84. [Google Scholar]
  59. Nys, G. Revue Bibliographique des Antibiorésistances Portées par les Entérobactéries Isolées de Reptiles et Evaluation du Profil de Résistance d’Escherichia coli Isolées de Reptiles en Belgique. Master’s Thesis, Université de Liège, Liège, Belgium, 2021. [Google Scholar]
  60. Aberkane, S. Dépistage et Caractérisation de Bactéries Multirésistantes aux Antibiotiques au Sein d’un Réservoir Aviaire Méditerranéen. Ph.D. Thesis, Université de Montpellier, Montpellier, France, 2017. [Google Scholar]
  61. Waititu, K.K. Molecular Characterization and Antimicrobial Susceptibility Patterns of Escherichia coli in Captive and Wild Olive Baboon (Papio anubis) Gut. Master’s Thesis, Jomo Kenyatta University of Agriculture and Technology, Nairobi, Kenya, 2020. [Google Scholar]
  62. Kolappaswamy, K.; Nazareno, J.; Porter, W.P.; Klein, H.J. Outbreak of pathogenic Escherichia coli in an outdoor-housed non-human primate colony. J. Med. Primatol. 2014, 43, 122–124. [Google Scholar] [CrossRef] [PubMed]
  63. Carlos, C.; Pires, M.M.; Stoppe, N.C.; Hachich, E.M.; Sato, M.I.; Gomes, T.A.; Amaral, L.A.; Ottoboni, L.M. Escherichia coli phylogenetic group determination and its application in the identification of the major animal source of fecal contamination. BMC Microbiol. 2010, 10, 1–10. [Google Scholar] [CrossRef] [PubMed]
  64. Gouali, M.; Weill, F.-X. Les Escherichia coli entérohémorragiques: Des entérobactéries d’actualité. Presse Méd. 2013, 42, 68–75. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Le Bouguénec, C. Diagnostic des différents pathovars d’Escherichia coli responsables de diarrhées chez l’homme. Rev. Francoph. Lab. 1999, 314, 33–37. [Google Scholar]
  66. Szalo, I.M.; Goffaux, F.; Pirson, V.; Piérard, D.; Ball, H.; Mainila, J. Presence in bovine enteropathogenic (EPEC) and enterohaemorrhagic (EHEC) Escherichia coli of genes encoding for putative adhesins of human EHEC strains. Res. Microbiol. 2002, 153, 653–658. [Google Scholar] [CrossRef]
  67. Hu, J.; Torres, A.G. Enteropathogenic Escherichia coli: Foe or innocent bystander? Clin. Microbiol. Infect. 2015, 21, 729–734. [Google Scholar] [CrossRef] [PubMed]
  68. Chen, D.H.; Frankel, G. Enteropathogenic Escherichia Coli: Unravelling Pathogenesis. FEMS Microbiol. Rev. 2005, 29, 83–98. [Google Scholar] [CrossRef] [PubMed]
  69. Milton, A.A.P.; Agarwal, R.K.; Priya, G.B.; Aravind, M.; Athira, C.K.; Rose, L.; Saminathan, M.; Sharma, A.K.; Kumar, A. Captive wildlife from India as carriers of Shiga toxin-producing, Enteropathogenic and Enterotoxigenic Escherichia coli. J. Vet. Med. Sci. 2018, 81, 321–327. [Google Scholar] [CrossRef] [PubMed]
  70. Mansfield, K.G.; Lin, K.-C.; Newman, J.; Schauer, D.; MacKey, J.; Lackner, A.A.; Carville, A. Identification of Enteropathogenic Escherichia coli in Simian Immunodeficiency Virus-Infected Infant and Adult Rhesus Macaques. J. Clin. Microbiol. 2001, 39, 971–976. [Google Scholar] [CrossRef]
  71. Mansfield, K.G.; Lin, K.-C.; Xia, D.; Newman, J.V.; Schauer, D.B.; Mackey, J.; Lackner, A.A.; Carville, A. Enteropathogenic Escherichia coli and Ulcerative Colitis in Cotton-Top Tamarins (Saguinus Oedipus). J. Infect. Dis. 2001, 184, 803–807. [Google Scholar] [CrossRef]
  72. Carvalho, V.d.; Irino, K.; Onuma, D.; Castro, A.F. Random amplification of polymorphic DNA reveals clonal relationships among enteropathogenic Escherichia coli isolated from non-human primates and humans. Braz. J. Med. Biol. Res. 2007, 40, 237–241. [Google Scholar] [CrossRef]
  73. Clayton, J.B.; Danzeisen, J.L.; Trent, A.M.; Emurphy, T.; Johnson, T.J. Longitudinal characterization of Escherichia coli in healthy captive non-human primates. Front. Vet. Sci. 2014, 1, 24. [Google Scholar] [CrossRef] [PubMed]
  74. Sharma, R.; Munns, K.; Alexander, T.; Entz, T.; Mirzaagha, P.; Yanke, L.J.; Mulvey, M.; Topp, E.; McAllister, T. Diversity and distribution of commensal fecal Escherichia coli bacteria in beef cattle administered selected subtherapeutic antimicrobials in a feedlot setting. Appl. Environ. Microbiol. 2008, 74, 6178–6186. [Google Scholar] [CrossRef] [PubMed]
  75. Abreu, A.G.; Bueris, V.; Porangaba, T.M.; Navarro-Garcia, F.; Elias, W.P. Auto transporter protein-encoding genes of diarrheagenic Escherichia coli are found in both typical and atypical enteropathogenic E. coli strains. Appl. Environ. Microbiol. 2012, 79, 4114. [Google Scholar] [CrossRef] [Green Version]
  76. Carvalho, V.M.; Gyles, C.L.; Ziebell, K.; Ribeiro, M.A.; Catão-Dias, J.L.; Sinhorini, I.L.; Otman, J.; Keller, R.; Trabulsi, L.R.; de Castro, A.F.P. Characterization of monkey enteropathogenic Escherichia coli (EPEC) and human typical and atypical EPEC serotype isolates from neotropical nonhuman primates. J. Clin. Microbiol. 2003, 41, 1225–1234. [Google Scholar] [CrossRef]
  77. Chen, F.G. Enteropathogenic Escherichia coli: Unravelling pathogenesis. FEMS Microbiol. Rev. 2005, 29, 83–98. [Google Scholar] [CrossRef]
  78. Drzewiecka, D. Significance and roles of Proteus spp. bacteria in natural environments. Microb. Ecol. 2016, 72, 741–758. [Google Scholar] [CrossRef] [PubMed]
  79. Mwova, J.P. Antimicrobial Resistance Genes Harboured in Enterococci Isolated from the Faeces of Captive Baboons. Ph.D. Thesis, University of Nairobi, Nairobi, Kenya, 2016. [Google Scholar]
  80. Bachiri, T.; Bakour, S.; Ladjouzi, R.; Thongpan, L.; Rolain, J.M.; Touati, A. High rates of CTX-M-15-producing Escherichia coli and Klebsiella pneumoniae in wild boars and Barbary macaques in Algeria. J. Glob. Antimicrob. Resist. 2017, 8, 35–40. [Google Scholar] [CrossRef]
  81. Dolejska, M.; Cizek, A.; Literak, I. High prevalence of antimicrobial-resistant genes and integrons in Escherichia coli isolates from black-headed gulls in the Czech Republic. J. Appl. Microbiol. 2007, 103, 11–19. [Google Scholar] [CrossRef]
  82. Baquero, F.; Martínez, J.L.; Lanza, V.F.; Rodríguez-Beltrán, J.; Galán, J.C.; Millán, A.S.; Cantón, R.; Coque, T.M. Evolutionary pathways and trajectories in antibiotic resistance. Clin. Microbiol. Rev. 2021, 34, e0005019. [Google Scholar] [CrossRef]
  83. Baron, S.A.; Mediannikov, O.; Abdallah, R.; Yimagou, E.K.; Medkour, H.; Dubourg, G.; Elamire, Y.; Afouda, P.; Ngom, I.I.; Angelakis, E. Multidrug-Resistant Klebsiella Pneumoniae Clones from Wild Chimpanzees and Termites in Senegal. Antimicrob. Agents Chemother. 2021, 65, AAC0255720. [Google Scholar] [CrossRef]
  84. Bamunusinghage, N.P.D.; Neelawala, R.G.; Magedara, H.P.; Ekanayaka, N.W.; Kalupahana, R.S.; Silva-Fletcher, A.; Kottawatta, S.A. Antimicrobial Resistance Patterns of Fecal Escherichia coli in Wildlife, Urban Wildlife, and Livestock in the Eastern Region of Sri Lanka, and Differences between Carnivores, Omnivores, and Herbivores. J. Wildl. Dis. 2022, 58, 380–383. [Google Scholar] [CrossRef]
  85. Turchi, B.; Dec, M.; Bertelloni, F.; Winiarczyk, S.; Gnat, S.; Bresciani, F.; Viviani, F.; Cerri, D.; Fratini, F. Antibiotic Susceptibility And Virulence Factors In Escherichia coli From Sympatric Wildlife Of The Apuan Alps Regional Park (Tuscany, Italy). Microb. Drug Resist. 2019, 25, 772–780. [Google Scholar] [CrossRef]
  86. Albrechtova, K.; Papousek, I.; de Nys, H.; Pauly, M.; Anoh, E.; Mossoun, A.; Dolejska, M.; Masarikova, M.; Metzger, S.; Couacy-Hymann, E. Low rates of antimicrobial-resistant Enterobacteriaceae in wildlife in Taï National Park, Côte d’Ivoire, surrounded by villages with high prevalence of multiresistant ESBL-producing Escherichia coli in people and domestic animals. PLoS ONE 2014, 9, e113548. [Google Scholar] [CrossRef] [PubMed]
  87. Janatova, M.; Albrechtova, K.; Petrzelkova, K.J.; Dolejska, M.; Papousek, I.; Masarikova, M.; Cizek, A.; Todd, A.; Shutt, K.; Kalousova, B.; et al. Antimicrobial-resistant Enterobacteriaceae from humans and wildlife in Dzanga-Sangha protected area, Central African Republic. Vet. Microbiol. 2014, 171, 422–431. [Google Scholar] [CrossRef]
  88. Felis, E.; Kalka, J.; Sochacki, A.; Kowalska, K.; Bajkacz, S.; Harnisz, M.; Korzeniewska, E. Antimicrobial pharmaceuticals in the aquatic environment-occurrence and environmental implications. Eur. J. Pharmacol. 2020, 866, 172813. [Google Scholar] [CrossRef] [PubMed]
  89. Verlicchi, P.; Al Aukidy, M.; Galletti, A.; Petrovic, M.; Barceló, D. Hospital effluent: Investigation of the concentrations and distribution of pharmaceuticals and environmental risk assessment. Sci. Total Environ. 2012, 430, 109–118. [Google Scholar] [CrossRef]
  90. Cardoza, L.A.; Knapp, C.W.; Larive, C.K.; Belden, J.B.; Lydy, M.; Graham, D.W. Factors affecting the fate of ciprofloxacin in aquatic field systems. Water Air Soil. Poll. 2005, 161, 383–398. [Google Scholar] [CrossRef]
  91. Hanna, N.; Sun, P.; Sun, Q.; Li, X.; Yang, X.; Ji, X.; Zou, H.; Ottoson, J.; Nilsson, L.E.; Berglund, B.; et al. Presence of antibiotic residues in various environmental compartments of Shandong province in eastern China: Its potential for resistance development and ecological and human risk. Environ. Int. 2018, 114, 131–142. [Google Scholar] [CrossRef]
  92. Reis, E.O.; Foureaux, A.F.S.; Rodrigues, J.S.; Moreira, V.R.; Lebron, Y.A.R.; Santos, L.V.S.; Amaral, M.C.S.; Langea, L.C. Occurrence, removal and seasonal variation of pharmaceuticals in Brasilian drinking water treatment plants. Environ. Pollut. 2019, 250, 773–781. [Google Scholar] [CrossRef]
  93. Marcusson, L.L.; Frimodt-Møller, N.; Hughes, D. Interplay in the selection of fluoroquinolone resistance and bacterial fitness. PLoS Pathog. 2009, 5, e1000541. [Google Scholar] [CrossRef]
  94. Baker, S.; Duy, P.T.; Nga, T.V.T.; Dung, T.T.N.; Phat, V.V.; Chau, T.T.; Turner, A.K.; Farrar, J.; Boni, M.F. Fitness benefits in fluoroquinolone-resistant Salmonella Typhi in the absence of antimicrobial pressure. eLife 2013, 2, e01229. [Google Scholar] [CrossRef]
  95. Machuca, J.; Briales, A.; Labrador, G.; Díaz-de-Alba, P.; López-Rojas, R.; Docobo-Pérez, F.; Martínez-Martínez, L.; Rodríguez-Baño, J.; Pachón, M.E.; Pascual, Á. Interplay between plasmid-mediated and chromosomal-mediated fluoroquinolone resistance and bacterial fitness in Escherichia coli. J. Antimicrob. Chemother. 2014, 69, 3203–3215. [Google Scholar] [CrossRef] [PubMed]
  96. Johnson, J.R.; Johnston, B.; Kuskowski, M.A.; Sokurenko, E.V.; Tchesnokova, V. Intensity and Mechanisms of Fluoroquinolone Resistance within the H 30 and H 30Rx Subclones of Escherichia coli Sequence Type 131 Compared with Other Fluoroquinolone-Resistant, E. coli. Antimicrob. Agents Chemother. 2015, 59, 4471–4480. [Google Scholar] [CrossRef] [Green Version]
  97. Fuzi, M.; Szabo, D.; Csercsik, R. Double-serine fluoroquinolone resistance mutations advance major international clones and lineages of various multi-drug resistant bacteria. Front. Microbiol. 2017, 8, 2261. [Google Scholar] [CrossRef] [PubMed]
  98. Rolland, R.M.; Hausfater, G.; Marshall, B. Antibiotic-resistant bacteria in wild primates: Increased prevalence in baboons feeding on human refuse. Appl. Environ. Microbiol. 1985, 49, 791–794. [Google Scholar] [CrossRef] [PubMed]
  99. Skurnik, D.; Ruimy, R.; Andremont, A.; Amorin, C.; Rouquet, P.; Picard, B.; Denamur, E. Effect of human vicinity on antimicrobial resistance and integrons in animal faecal Escherichia coli. J. Antimicrob. Chemother. 2006, 57, 1215–1219. [Google Scholar] [CrossRef]
  100. Literák, I.; Vanko, R.; Dolejská, M.; Čížek, A.; Karpíšková, R. Resistant Escherichia coli and Salmonella in Russian rooks (Corvus frugilegus) wintering in the Czech Republic. Lett. Appl. Microbiol. 2007, 45, 616–621. [Google Scholar] [CrossRef]
  101. Cohen, M.L. Epidemiology of drug resistance: Implications for a post-antimicrobial era. Science 1992, 257, 1050–1055. [Google Scholar] [CrossRef]
  102. Weiss, D.; Wallace, R.M.; Rwego, I.B.; Gillespie, T.R.; Chapman, C.A.; Singer, R.S.; Goldberg, T.L. Antibiotic-resistant Escherichia coli and class 1 integrons in humans, domestic animals, and wild primates in Rural Uganda. Appl. Environ. Microbiol. 2018, 84, e01632-18. [Google Scholar] [CrossRef]
  103. Foster-Nyarko, E.; Alikhan, N.-F.; Ravi, A.; Thilliez, G.; Thomson, N.M.; Baker, D.; Kay, G.; Cramer, J.D.; O’Grady, J.; Antonio, M.; et al. Genomic diversity of Escherichia coli isolates from non-human primates in the Gambia. Microb. Genom. 2020, 6, mgen000428. [Google Scholar] [CrossRef] [PubMed]
  104. Beatty, A.; Scott, K.; Tsai, P. Achieving Sustainable Global Capacity for Surveillance and Response to Emerging Diseases of Zoonotic Origin: Workshop Summary; National Academies Press: Washington, DC, USA, 2008. [Google Scholar]
  105. He, T.; Wei, R.; Zhang, L.; Sun, L.; Pang, M.; Wang, R.; Wang, Y. Characterization of Ndm-5-Positive Extensively Resistant Escherichia coli Isolates from Dairy Cows. Vet. Microbiol. 2017, 207, 153–158. [Google Scholar] [CrossRef] [PubMed]
  106. Zhang, L.; Levy, K.; Trueba, G.; Cevallos, W.; Trostle, J.; Foxman, B.; Marrs, C.F.; Eisenberg, J.N.S. Effects of selection pressure and genetic association on the relationship between antibiotic resistance and virulence in Escherichia coli. Antimicrob. Agents Chemother. 2015, 59, 6733–6740. [Google Scholar] [CrossRef] [PubMed]
  107. Vega-Manriquez, X.D.; Ubiarco-López, A.; Verdugo-Rodríguez, A.; Hernández-Chiñas, U.; Navarro-Ocaña, A.; Ahumada-Cota, R.E.; Ramírez-Badillo, D.; de León, N.H.-D.; Eslava, C.A. Pet dogs potential transmitters of pathogenic Escherichia coli with resistance to antimicrobials. Arch. Microbiol. 2020, 202, 1173–1179. [Google Scholar] [CrossRef] [PubMed]
  108. Krumperman, P.H. Multiple antibiotic resistance indexing of Escherichia coli to identify high-risk sources of fecal contamination of foods. Appl. Environ. Microbiol. 1983, 46, 165–170. [Google Scholar] [CrossRef]
  109. Walk, S.T.; Alm, E.W.; Calhoun, L.M.; Mladonicky, J.M.; Whittam, T.S. Genetic diversity and population structure of Escherichia coli isolated from freshwater beaches. Environ. Microbiol. 2007, 9, 2274–2288. [Google Scholar] [CrossRef]
  110. Gordon, D.M. The Influence of Ecological Factors on the Distribution and the Genetic Structure of Escherichia coli. EcoSal Plus 2004, 1. [Google Scholar] [CrossRef] [PubMed]
  111. Pérez, C.; Gómez-Duarte, O.G.; Arias, M.L. Diarrheagenic Escherichia coli in children from Costa Rica. Am. J. Trop. Med. Hyg. 2010, 83, 292. [Google Scholar] [CrossRef] [PubMed]
  112. Adib, N.; Ghanbarpour, R.; Solatzadeh, H.; Alizade, H. Antibiotic resistance profile and virulence genes of uropathogenic Escherichia coli isolates in relation to phylogeny. Trop. Biomed. 2014, 31, 17–25. [Google Scholar] [PubMed]
  113. Vande Weghe, J. Les Parcs Nationaux du Gabon: Moukalaba Doudou; Agence Nationale des Parcs Nationaux: Libreville, Gabon, 2012; p. 296. [Google Scholar]
  114. Takenoshita, Y.; Ando, C.; Yamagiwa, J. Fruit phenology of the great ape habitat in the Moukalaba-Doudou National Park, Gabon. Afr. Study Monogr. 2008, 39, 23–39. [Google Scholar]
  115. Takenoshita, Y.; Yamagiwa, J. Estimating gorilla abundance by dung count in the northern part of Moukalaba-Doudou National Park, Gabon. Afr. Study Monogr. 2008, 39, 41–54. [Google Scholar]
  116. Nguelet, F.L.M.; Koumba, C.R.Z.; Mavoungou, J.F.; Nzengue, E.; Akomo-Okoue, E.F.; Nakashima, Y.; Hongo, S.; Ella, G.W.E.; Koumba, L.B.M.; M’batchi, B. Étude de la relation entre l’abondance des grands mammifères frugivores et celle des fruits dans le Parc National de Moukalaba-Doudou, Gabon. Int. J. Biol. Chem. Sci. 2016, 10, 1969–1982. [Google Scholar] [CrossRef]
  117. Oluduro, A.O. Antibiotic-Resistant Commensal Escherichia coli in Faecal Droplets from Bats and Poultry in Nigeria. Vet. Ital. 2012, 48, 297–308. [Google Scholar] [PubMed]
  118. Jaja, I.F.; Green, E.; Muchenje, V. Aerobic mesophilic, coliform, Escherichia coli, and Staphylococcus aureus counts of raw meat from the formal and informal meat sectors in South Africa. Int. J. Environ. Res. Public Health 2018, 15, 819. [Google Scholar] [CrossRef] [PubMed]
  119. Jaja, I.F.; Jaja, C.-J.I.; Chigor, N.V.; Anyanwu, M.U.; Maduabuchi, E.K.; Oguttu, J.W.; Green, E. Antimicrobial resistance phenotype of Staphylococcus aureus and Escherichia coli isolates obtained from meat in the formal and informal sectors in South Africa. BioMed Res. Int. 2020, 2020, 1–11. [Google Scholar] [CrossRef] [PubMed]
  120. Bauer, A.W.; Kirby, W.M.; Sherris, J.C.; Turck, M. Antibiotic susceptibility testing by a standardized single disk method. Am. J. Clin. Pathol. 1966, 45, 149–158. [Google Scholar] [CrossRef]
  121. Clinical and Laboratory Standards Institute. M100: Performance Standards for Antimicrobial Susceptibility Testing, 28th ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2018. [Google Scholar]
  122. Clinical and Laboratory Standards Institute. M100: Performance Standards for Antimicrobial Susceptibility Testing, 20th ed.; Clinical and Laboratory Standards Institute: Wayne, PA, USA, 2010. [Google Scholar]
  123. Ibrahim, M.; Bilal, N.; Hamid, M. Increased multi-drug resistant Escherichia coli from hospitals in Khartoum state, Sudan. Afr. Health Sci. 2012, 12, 368–375. [Google Scholar] [CrossRef]
  124. Sjöling, Å.; Sadeghipoorjahromi, L.; Novak, D.; Tobias, J. Detection of major diarrheagenic bacterial pathogens by multiplex PCR panels. Microbiol. Res. 2015, 172, 34–40. [Google Scholar] [CrossRef] [PubMed]
  125. Kong, R.Y.C.; Lee, S.K.Y.; Law, T.W.F.; Law, S.H.W.; Wu, R.S.S. Detection of major diarrheagenic bacterial pathogens by multiplex PCR panels. Water Res. 2002, 36, 2802–2812. [Google Scholar] [CrossRef]
  126. Rodas, C.; Mamani, R.; Blanco, J.; Blanco, J.E.; Wiklund, G.; Svennerholm, A.-M.; Sjöling, Å.; Iniguez, V. Enterotoxins, colonization factors, serotypes and antimicrobial resistance of enterotoxigenic Escherichia coli (ETEC) strains isolated from hospitalized children with diarrhea in Bolivia. Braz. J. Infect. Dis. 2011, 15, 132–137. [Google Scholar] [PubMed]
  127. Vidal, R.; Vidal, M.; Lagos, R.; Levine, M.; Prado, V. Multiplex PCR for diagnosis of enteric infections associated with diarrheagenic Escherichia coli. J. Clin. Microbiol. 2004, 42, 1787–1789. [Google Scholar] [CrossRef] [Green Version]
Pathogens 11 01082 g001 550
Figure 1. Prevalence of antimicrobial-resistant E. coli isolates.
Figure 1. Prevalence of antimicrobial-resistant E. coli isolates.
Pathogens 11 01082 g001
Pathogens 11 01082 g002 550
Figure 2. Relationship between the occurrence of EPEC virulence factors, antimicrobial resistance and phylogroups of E. coli isolates. This graph shows the correlation between the presence of the EPEC pathotype in gorilla E. coli isolates and their membership of phylogenetic groups that traditionally carry pathogenic isolates in humans, such as groups B2 and D, and the presence of antimicrobial resistance phenotypes used in human therapy. In addition, phylogenetic groups that normally carry non-pathogenic isolates, such as groups A and B1 in humans, are found to carry certain pathogenicity genes such as MDR EPEC, which is very often implicated in diarrhoeal episodes in primates, including humans and gorillas. This graph shows that there are mechanisms for transmission of MDR DECs isolates from humans to gorillas, mostly linked to the presence of phylogenetic group A.
Figure 2. Relationship between the occurrence of EPEC virulence factors, antimicrobial resistance and phylogroups of E. coli isolates. This graph shows the correlation between the presence of the EPEC pathotype in gorilla E. coli isolates and their membership of phylogenetic groups that traditionally carry pathogenic isolates in humans, such as groups B2 and D, and the presence of antimicrobial resistance phenotypes used in human therapy. In addition, phylogenetic groups that normally carry non-pathogenic isolates, such as groups A and B1 in humans, are found to carry certain pathogenicity genes such as MDR EPEC, which is very often implicated in diarrhoeal episodes in primates, including humans and gorillas. This graph shows that there are mechanisms for transmission of MDR DECs isolates from humans to gorillas, mostly linked to the presence of phylogenetic group A.
Pathogens 11 01082 g002
Table
Table 1. Phylogenetic groups of E. coli isolates resulting from the application of the Clermont method [52,53].
Table 1. Phylogenetic groups of E. coli isolates resulting from the application of the Clermont method [52,53].
Subject StudiedSamplechuAyjaATSPE4.C2Phylogroup AssignationFrequency (%)
GorillaFaecal---A (n = 44)69
GorillaFaecal-+-A (n = 0)0
GorillaFaecal--+B1 (n = 6)10
GorillaFaecal++-B2 (n = 0)0
GorillaFaecal+++B2 (n = 13)20
GorillaFaecal+--D (n = 1)1
GorillaFaecal+-+D (n = 0)0
Legend: The phylogenetic types A (ChuA-, YjaA-, TSPE4.C2-), B1 (ChuA-, YjaA-, TSPE4.C2+), B2 (ChuA+, YjaA+, TSPE4.C2+) and D (ChuA+, YjaA-, TSPE4.C2-) have been observed in this study. In contrast, the phylogenetic types A (ChuA-, YjaA+, TSPE4.C2-), B2 (ChuA+, YjaA+, TSPE4.C2-) and D (ChuA+, YjaA-, TSPE4.C2+) were not observed in this study.
Table
Table 2. Pathotype groups of E. coli isolates.
Table 2. Pathotype groups of E. coli isolates.
SamplesPathotype GroupFrequency (%)
FaecalEPEC (n = 17)85
FaecalEPEC/EHEC (n = 3)15
Legend: EPEC (enteropathogenic E. coli), EHEC (enterohemorrhagic E. coli).
Table
Table 3. Phenotypes of antibiotics, phylogroups, pathotypes and MARI [108] of E. coli isolated from western lowland gorilla faeces of MDNP.
Table 3. Phenotypes of antibiotics, phylogroups, pathotypes and MARI [108] of E. coli isolated from western lowland gorilla faeces of MDNP.
IsolateAnimalATBClass Resistance Phenotype Profile PhylogroupPathotypeMARI
E19Gorilla51TICPIPTZPFOXAMC DEPEC0.23
E24Gorilla51TICPIPTZPAMCCTT B2 0.23
E33Gorilla52PIPTZPAMCNALCTT A 0.23
E32Gorilla63PIPTZPAMCTETNALCTT A 0.28
E40Gorilla63PIPTZPIPMAMCFOFTOB AEPEC0.28
E41Gorilla63PIPTZPIPMTETNALCTT A 0.28
E1Gorilla72TICPIPFOXIPMETPFOFCTT A 0.33
E8Gorilla73TICTPZPIPIPMETPFOFCIP A 0.33
E28Gorilla71TICPIPTZPFOXIPMAMCCTT B2 0.33
E45Gorilla82TICPIPTZPFOXIPMAMCNALCTT B1 0.38
E57Gorilla82TICFOXIPMAMCGENAMKTOBNET A 0.38
E59Gorilla82TICFOXIPMAMCGENAMKTOBNET AEPEC0.38
E64Gorilla86FOXIPMTETCHLNALSXTNITCTT AEPEC0.38
E4Gorilla95TZPIPMETPFOFGENTOBCIPNITLEV A 0.42
E7Gorilla93TZPIPMETPAMCFOFGENAMKNITLEV A 0.42
E37Gorilla93TICPIPTZPFOXIPMAMCNALSXTCTT B1 0.42
E50Gorilla93TICPIPTZPFOXIPMAMCNETSXTCTT B1 0.42
E49Gorilla116TICTZPFOXIPMAMCTETCHLNALSXTNITCTT A 0.52
E63Gorilla127TICPIPTZPFOXIPMAMCNETTETCHLNALCIPNIT B2EPEC0.57
E10Gorilla136TICTZPPIPFOXIPMETPAMCFOFTOBCHLNALCIPCTTA 0.61
ATB = antibiotic, MARI = Multiple Antimicrobial Resistance Index, AMC = amoxicillin/clavulanic acid, TIC = ticarcillin, PIP = piperacillin, TZP = piperacillin/tazobactam, FOX = cefoxitin, ETP = ertapenem, IPM = imipenem, CTT = cefotetan, TOB = tobramycin, AMK = amikacin, NET = netilmicin, GEN = gentamycin, NAL = nalidixic acid, CIP = ciprofloxacin, NOR = norfloxacin, OFX = ofloxacin, LVX = levofloxacin, FOF = fosfomycin, TET = tetracycline, SXT = sulfamethoxazole + trimethoprim, CHL = chloramphenicol, NIT = nitrofurantoin, EPEC (enteropathogenic E. coli), EHEC (enterohemorrhagic E. coli). This table includes only resistant E. coli isolates with a resistance index (MARI) between 0.22–0.59 out of 64 isolates tested.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Oyaba Yinda, L.E.D.; Onanga, R.; Mbehang Nguema, P.P.; Akomo-Okoue, E.F.; Nsi Akoue, G.; Longo Pendy, N.M.; Otsaghe Ekore, D.; Lendamba, R.W.; Mabika-Mabika, A.; Mbeang, J.C.O.; et al. Phylogenetic Groups, Pathotypes and Antimicrobial Resistance of Escherichia coli Isolated from Western Lowland Gorilla Faeces (Gorilla gorilla gorilla) of Moukalaba-Doudou National Park (MDNP). Pathogens 2022, 11, 1082. https://doi.org/10.3390/pathogens11101082

AMA Style

Oyaba Yinda LED, Onanga R, Mbehang Nguema PP, Akomo-Okoue EF, Nsi Akoue G, Longo Pendy NM, Otsaghe Ekore D, Lendamba RW, Mabika-Mabika A, Mbeang JCO, et al. Phylogenetic Groups, Pathotypes and Antimicrobial Resistance of Escherichia coli Isolated from Western Lowland Gorilla Faeces (Gorilla gorilla gorilla) of Moukalaba-Doudou National Park (MDNP). Pathogens. 2022; 11(10):1082. https://doi.org/10.3390/pathogens11101082

Chicago/Turabian Style

Oyaba Yinda, Leresche Even Doneilly, Richard Onanga, Pierre Philippe Mbehang Nguema, Etienne François Akomo-Okoue, Gontran Nsi Akoue, Neil Michel Longo Pendy, Desire Otsaghe Ekore, Roméo Wenceslas Lendamba, Arsène Mabika-Mabika, Jean Constant Obague Mbeang, and et al. 2022. "Phylogenetic Groups, Pathotypes and Antimicrobial Resistance of Escherichia coli Isolated from Western Lowland Gorilla Faeces (Gorilla gorilla gorilla) of Moukalaba-Doudou National Park (MDNP)" Pathogens 11, no. 10: 1082. https://doi.org/10.3390/pathogens11101082

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop