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Asian Journal of Animal and Veterinary Advances

Year: 2020 | Volume: 15 | Issue: 1 | Page No.: 13-19
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Research Article

Public Health Risk Due to Some Fecal-borne Pathogens in Zoo Animals and Zookeepers

Gihan K. Abdel-Latef Gihan K. Abdel-Latef's LiveDNA and Asmaa A. Kamel

ABSTRACT

Background and Objectives: Bacterial infections constitute a public health hazards worldwide especially, with the emerging of drug-resistant pathogens. In our study we try to spot light on the role of zoo animals as a source of environmental contamination with drug-resistant pathogens of public health significance. Materials and Methods: About 75 fecal samples were collected from 11 zoo animal species including non-human primates, herbivorous, carnivorous. Moreover 10 zookeeper's stool samples were examined. Samples subjected to bacteriologic, serologic examination; as well antibiogram test was done for identified samples. Results: Bacterial isolation reveals 68 isolates from zoo animals represented as Escherichia coli 58 (85.29%), Pseudomonas species. 4 (5.88%) and Shigella species, 6 (8.82%). All workers' samples reveal Escherichia coli and only one worker sample reveal Shigella species. Failure of isolation of E. coli O157 and Salmonella from both types of samples. Serological identification of Escherichia coli species from zoo animals reveals Escherichia coli O145 in a percent of 17.24%. While that of zookeeper's shows that 10% was Escherichia coli O44, 10% Escherichia coli O164 and 80% were untypable poly (1-3). Antibiotic profile revealed resistance to number of antibiotics, with variant degree of resistance. Escherichia coli revealed resistance to most antibiotic used with most detected resistance to amoxicillin/clavulanic, trimethoprim-sulfamethoxazole, ampicillin, ciprofloxacin, chloramphenicol and ceftriaxone moreover, Shigella species reveal resistance to ceftriaxone, ampicillin, chloramphenicol and amoxicillin/clavulanic. While pseudomonas species revealed 100% resistance to amoxicillin/clavulanic, chloramphenicol, ceftriaxone, tetracycline, ampicillin and trimethoprim-sulfamethoxazole. Conclusion: The results indicated that zoo animals in our country act as a potential source of antimicrobial-resistant zoonotic pathogens.
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INTRODUCTION

Zoos are considered as a public recreational area for people of all ages so the visitors of the zoos are in continuous increase. Unintentionally zoos provide pathogens with a high diversity of species. Animals shed a plethora of pathogenic bacteria in their feces; some of them are of zoonotic importance, including Escherichia coli (E. coli ), Salmonella, Yersinia and Pseudomonas1. According to a recent report, there are more than 25 human infectious disease outbreaks were being attributed to visiting animal exhibits2. Human infection can result from hand-to-mouth ingestion of animal feces, or direct contact with animals, or contaminated surface3. Visitors of petting zoo practices as touching their face after animal contact, lack of hand washing, eating and drinking within animal areas mostly promote these pathogen transmissions4.

Concerning, the fact that the problem of development and spread of antibiotic resistance increasing year by year and now considered a global threat to public health. The crisis of antibiotic resistance attributed to the over and/or misuse of drugs which imperiling the efficacy of the antibiotic used5. Several studies reveal antibiotic resistance E. coli species in wildlife6,7. As there is no previous work on zoo animals in our country, little is known about bacteria of public health importance in zoo animals in our country particularly drug-resistant zoonotic pathogens. So, that we conduct our study to assess the prevalence of some zoonotic bacteria isolated from feces of zoo animals and their antibiotic profile in Beni-Suef Governorate, Egypt.

MATERIAL AND METHODS

Study area and period: A cross-sectional study was done during the period from September, 2018 through April, 2019 in Beni-Suef zoo, Beni-Suef province (coordinates: 29°04 N 31°05 E), Egypt. The Beni-Suef zoo is one of the zoos in Egypt. It was established in 1996 and opened in 1997; it contains many species of zoo animals.

Samples and sampling process
Fecal samples: A total of 75 fecal samples were collected from zoo animals in Beni-Suef Zoo, Egypt. One visit/week during which freshly voided fecal samples were collected from the enclosure floor directly using polyethylene sterile bags and labeled by species. Samples collected including 3 species of non-human primates (Grivet monkeys; Chlorocebus aethiops, Hamadryas baboons; Papio hamadryas and brown capuchin; Cebus apella) in addition to 2 species of carnivores which including African lion; Panther Leo, Hyena; Crocuta crocuta). Finally 6 species of herbivorous animals include Lamma; Lama glama, Pony; Shetland pony, Nile lechwe; Kobus megaceros, goats; Capra aergagrus, Barbary sheep; Ammotragus lervia and Hippo; Hippopotamus amphibious.

Zookeepers stool samples: Human stool samples were collected twice with 2 weeks interval from 5 workers who were closely in contact with animals at the zoo. Samples were collected by following WHO guidelines for the collection of fecal samples8.

Samples were sent directly in a cooler with ice packs to the Hygiene, Zoonoses and Epidemiology laboratory at the Faculty of Veterinary Medicine, Beni-Suef University and stored at 4°C to be tested.

Laboratory examination
Macroscopic examination: All fecal samples were examined visually by naked eyes to detect consistency, presence or absence of blood and/or mucus.

Bacteriologic examination
Isolation of Salmonella and Shigella9: About 1 g from each fecal or stool samples were aseptically transferred into a sterile test tube containing 9 mL of 0.1% sterile buffer peptone water. Buffered peptone water was incubated at 37°C for 24 h. About 1 mL of broth was added to 10 mL of Rappaport Vassiliadis (biolife) and incubated at 41.5±0.5°C for 18-24 h then loopful from each broth was streaked on Salmonella-Shigella agar (SS) and incubated for 18-24 h at 37°C. Suspected colonies (colorless colonies with a black center for Salmonella and colorless colonies for Shigella) were streaked on nutrient slopes for further identification and biochemical characterization using Gram stain, oxidase, indole, methyl red, Voges Proskauer, citrate utilization, triple sugar iron, urease test.

Isolation of E. coli species: loopful from buffered peptone broth after incubation at 37°C for 24 h was streaked onto MacConkey (MAC) agar and Sorbitol MAC agar containing Cefixime Tellurite (CT-SMAC) and incubated at 37°C for 24 h. Presumptive E. coli and E. coli O157 colonies (pink colonies on MAC agar and clear colonies on sorbitol MAC) were streaked onto TSA and testing for indole production10,11. Serological identification of the strains was done in the Clinical Microbiology Unit, Central Health Laboratories of Ministry of Health, Egypt.

Antibiotic profile: All identified isolates were tested for their antimicrobial resistance/susceptibility pattern by disc diffusion method using antibiotic disks of 5.5 mm diameter according to Clinical and Laboratory Standards Institute12. Isolates were tested for sensitivity to ciprofloxacin (CIP15μg), clarithromycin (CLR 15 μg), streptomycin (S 10 μg), amikacin (AMK10 μg), amoxicillin/clavulanic (AMC 30 μg), chloramphenicol (C 30 μg), ampicillin (Am 10 μg), ceftriaxone (CRO 30 μg), tetracycline (TC 30 μg) and trimethoprim-sulfamethoxazole (STX 30 μg), (Oxoid, UK) were used. The diameter of the zones of complete inhibition was measured and compared with the zone size interpretation chart provided by the supplier and was graded as susceptible (S), intermediate (I) and resistant (R).

Statistical analysis: Results were statistically analyzed by use of descriptive analysis to determine the prevalence of infection in examined animal groups as well the percentage of drug resistant pathogens.

RESULTS AND DISCUSSION

Bacterial isolation revealed 68 isolates from zoo animal samples represented as E. coli (85.29%), Pseudomonas species (5.88%) and Shigella species (8.82%). All workers' stool samples showed E. coli and only one worker samples reveal Shigella species. Failure of isolation of E. coli O157 and Salmonella from both types of samples.

Serological identification of E. coli species from zoo animals manifested E. coli O145 in a percent of 17.24%. While that of zookeeper's shows 10% E. coli O44 and 10% E. coli O164. Isolates of E. coli showed resistance to most antibiotic used. Moreover, Shigella species were resistant to ceftriaxone, ampicillin, chloramphenicol and amoxicillin/ clavulanic. While Pseudomonas species revealed 100% resistance to amoxicillin/clavulanic, chloramphenicol, ceftriaxone, tetracycline, ampicillin and trimethoprim-sulfamethoxazole.

As shown in Table 1 and 2, E. coli species was the most predominant microorganism among different examined zoo animal groups (85.29%). From which non-human primates and carnivorous shows 100% isolation rate of E. coli while only goats and barbary sheep from herbivorous species show 67.6 and 100% isolation rate, respectively. Escherichia coli is one of the largest Enterobacteriaceae family which are facultative anaerobic Gram-negative enteric pathogen, it can be disseminated in different ecosystems.

Table 1: Prevalence of bacterial pathogens in examined fecal samples from zoo animal
Zoo animals
Animal species (no. of samples) Non-human primates (No. 16) Carnivorous (No. 7) Herbivorous animals (No. 52) Total
Bacterial isolates (No. 68) Number Percentage Number Percentage Number Percentage Number Percentage
E. coli O157 0 0.00 0 0.0 0 0.0 0 0.00
E. coli spp. 16 27.58 7 12.06 35 60.34 58 85.29
Shigella spp. 6 100.00 0 0.0 0 0.0 6 8.82
Salmonella spp. 0 0.00 0 0.0 0 0.0 0 0.00
Pseudomonas spp. 4 100.00 0 0.0 0 0.0 4 5.88


Table 2: Prevalence of bacterial pathogens in each species of examined zoo animals
Isolated bacteria
E. coli spp. Shigella spp. Pseudomonas spp.
Positive Positive Positive
Animal species
Number of examined samples
 Number Percentage Number Percentage Number Percentage
Non-human primates
Grivet monkeys (Chlorocebus aethiops)
10
 10 100.0 0 0.0 0 0.0
Hamadryas baboons (Papio hamadryas)
4
 4 100.0 4 100.0 4 100.0
Brown capuchin (Cebus apella)
2
 2 100.0 2 100.0 0 0.0
Carnivorous
African lion (Panther Leo)
5
 5 100.0 0 0.0 0 0.0
Hyena (Crocuta crocuta)
2
 2 100.0 0 0.0 0 0.0
Herbivorous
Lamma (Lama glama)
1
 0 0.0 0 0.0 0 0.0
Pony (Shetland pony)
1
 0 0.0 0 0.0 0 0.0
Nile lechwe (Kobus megaceros)
1
 0 0.0 0 0.0 0 0.0
Goats (Capra aergagrus)
34
 23 67.6 0 0.0 0 0.0
Barbary sheep (Ammotragus lervia)
12
 12 100.0 0 0.0 0 0.0
Hippo (Hippopotamus amphibius)
3
 0 0.0 0 0.0 0 0.0


Table 3: Prevalence of bacterial pathogens isolated from in zookeeper's stool samples
  Zookeepers
Samples No. 10 Isolated bacteria Worker 1
Worker 2
Worker 3
Worker 4
Worker 5
E. coli O157 -
-
-
-
-
E. coli spp. +
+
+
+
+
Shigella spp. +
-
-
-
-
Salmonella spp. -
-
-
-
-
Pseudomonas spp. -
-
-
-
-


Table 4: Serological identification of E. coli isolated from examined zoo animals and zookeeper
Zoo animal samples Zookeepers samples
E. coli serogroups Number Percentage Number Percentage
E. coli O145 10 17.24 0.0 0.0
E. coli O44 0 0.00 1.0 10.0
E. coli O164 0 0.00 1.0 10.0
Untypable poly 1-3 48 82.75 8.0 80.0
Total 58 100.00 10.0 100.0

In Trinidad and Tobago India, the prevalence of E. coli in zoo animals was 67%13. As well E. coli was isolated in a percent of 52.6% at Asa Zoological Park Hiroshima Prefecture, Japan14, while 100% isolation rate of E. coli was reported in Joes Zoo, Nigeria15. Although the absence of sorbitol fermenter E. coli O157 in our study, which is a good indicator that zoo animals examined are not an important reservoir of VTEC, strains16. Other E. coli species ranging from nonpathogenic to highly virulent enteropathogens, which can contribute a great risk for both animals and humans, are isolated. Escherichia coli species has the ability to survive in soil, water, feed and manure which act as a source of infection to other zoo animals. Escherichia coli was reported to induce health problems in zoo animals'17. In addition to its potential transmission to zookeepers and visitors15,18.

Shigella species represents 8.82% only from the fecal samples of two species of non-human primates (Hamadryas baboons; Papio hamadryas and Brown capuchin; Cebus apella). Shigellosis was reported in a Vienna zoo in four macaques19. Shigella is a pathogen of primates; mainly responsible for morbidity and mortality in colonized monkeys, it was isolated in a percent of 12%20. Shigella isolated in a percent of 31.66% in china21. The asymptomatic carriers may be present especially in monkeys22. Thus the addition of such carriers either from wild or from other colonies enhance the spread of Shigella infections via fecal-oral route23.

Pseudomonas species represent 5.88% of the isolated pathogens mainly from Hamadryas baboons (Papio hamadryas). Similar isolation rate was reported from zoo animals in japan14. Pseudomonas species are ubiquitous Gram-negative opportunistic pathogen. It can be detected in animal and human fecal samples24. In animals, it is responsible for various infections25. In humans, it can cause respiratory tract infection in immuno compromised persons26. In immuno competent individuals, it may cause otitis, Keratitis and other signs27.

Results in Table 3 demonstrate that examination of zookeeper's stool samples reveals the presence of Shigella spp. in one worker (20%) and E. coli spp. in all worker samples (100%). Shigella was isolated form an animal keeper in Vienna zoo19. Nevertheless, the presence of Shigella in stool samples of zookeepers represents a risk of environmental contamination and cross infection between the workers and the animals and vice versa. Moreover, poor sanitation and crowded conditions constitute additional risk factors28,29. It is noteworthy that, Shigella is a zoonotic organism could be present in workers at the zoo as well non-human primates and vice versa30.

Result of serologic identification of E. coli species from zoo animals as shown in Table 4 reveal E. coli O145 in a percent of 17.24. Escherichia coli O145 are Shiga-toxin E. coli which sometimes referred as non-O157 STECs. It constitutes a multi state outbreak infection in humans due to the ingestion of shredded Romaine Lettuce in the USA31.

Serologic identification of E. coli species from zookeepers shows that 10% was E. coli O44 and 10% was E. coli O164 both constituting a public health risk for humans. Escherichia coli O164 are an Enteroinvasive E. coli (EIEC). Usually it associated with contaminated food or water. It causes 2 outbreaks of in Czechoslovakia where 18/54 becoming ill with transient paresis in lower extremities32. It was isolated from patient suffering from diarrhea at Osaka airport quarantine facility in Japan33. As well, it isolated in a percent of 10% (8/80) from stool of patients with diarrhea attending Abou EI Reesh Hospital, Egypt34.

Escherichia coli O44 is an enteroaggregative E. coli (EAEC) strain. EAEC is an emerging enteric pathogen causing persistent diarrhea and malnutrition in children and immuno compromised individuals in developed countries35. It was isolated from a child with diarrhea from36 Peru in 1983-1984. As well several outbreaks with EAEC were documented inJapan37, Italy38; all were linked with the consumption of contaminated food. It was denoted that EAEC more likely to occur via food borne infection than any other bacterial pathogens even with ETEC39.

Table 5: Antimicrobial resistance pattern (%) of bacteria isolated from zoo animals and zookeepers
Bacterial isolates (No.)
Antibiotic tested (conc.) E. coli spp. (12) Shigella spp. (6) Pseudomonas spp. (4)
  R I S R I S R I S
CIP (15 μg) 66.6 8.3 25.0 50.0 33.3 16.6 0.0 50.0 50.0
CLR (15 μg) 58.3 25.0 16.6 50.0 33.3 16.6 50.0 0.0 50.0
S (10 μg) 50.0 33.3 16.6 50.0 33.3 16.6 0.0 0.0 100.0
AMK (10 μg) 58.3 25.0 16.6 33.3 66.6 0.0 50.0 50.0 0.0
AMC (30 ug) 100 0.0 0.0 66.6 16.6 16.6 100.0 0.0 0.0
C (30 μg) 66.6 25.0 8.33 66.6 33.3 0.0 100.0 0.0 0.0
Am (10 μg) 83.3 8.3 8.3 83.3 16.6 0.0 75.0 25.0 0.0
CRO (30 μg) 66.6 33.3 0.0 66.6 16.6 16.6 100.0 0.0 0.0
TC (30 μg) 41.66 8.3 50.0 50.0 33.3 16.6 100.0 0.0 0.0
STX (30 μg) 66.6 16.6 16.6 50.0 33.3 16.6 100.0 0.0 0.0
S: Sensitive, I: Intermediated, R: Resistant, CIP: Ciprofloxacin, CLR: Clarithromycin, S: Streptomycin, AMK: Amikacin, AMC: Amoxicillin/clavulanic, C: Chloramphenicol, Am: Ampicillin, CRO: Ceftriaxone, TC: Tetracycline, STX: Trimethoprim-sulfamethoxazole

In this study, the isolates exhibit a variant degree of resistance to antibiotics used (Table 5). Our results exhibit that most of the isolates were resistant to one or more antibiotics. Escherichia coli species reveal resistance to most antibiotics. Similar results recorded in japan zoo where 21.1% of E. coli isolates showed resistance to antibiotics14. As well antibiotic resistant E. coli species from wildlife animals was isolated in Portugal40. Most of the antibiotic resistance was to the β-lactams group such as ampicillin, amoxicillin/clavulanic even those of extended-spectrum as ceftriaxone. Authors in china21,41,42, in Catalonia43 and Spain6 reported ESBL-containing E. coli strains in apparently healthy wild animals. This result highlighted the public health risk as these drugs usually used for serious infection treatment in hospitals44.

Shigella species reveals resistance to ceftriaxone, ampicillin, chloramphenicol and amoxicillin/clavulanic. While pseudomonas reveals 100% resistance to amoxicillin/ clavulanic, chloramphenicol, ceftriaxone, tetracycline and trimethoprim-sulfamethoxazole. Pseudomonas species reveal resistance to most antimicrobial used which recorded by other authors45.

CONCLUSION

Although many pathogens are normal inhabitant in the animal guts, the presence of pathogenic species as E. coli, Shigella and pseudomonas especially those resist to drugs indicates that zoo animals may serve as source and melting pool for bacterial resistance especially those of zoonotic potential. Further studies should be made to determine the resistant genes, alternative approaches to control.

SIGNIFICANCE STATEMENT

This study highlighted the significant role and the hidden threat from zoo animals as a source of multi drug-resistant pathogens of public health importance; therefore preventive measures should be implemented to prevent environmental contamination and infection of both man and animals.

ACKNOWLEDGMENT

The authors are grateful to the manager of Beni-Suef zoo and zoo workers for their valuable help.

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