Intestinal parasites in captive wild animals at four zoological gardens in Northeast China

Hongyu Qiu; Huining Yang; Xiaojing Sun; Chengjia Jin; Ximing Zou; Chunren Wang; Qiaocheng Chang

doi:10.4103/2773-0344.350692

ORIGINAL ARTICLE

Year : 2022 | Volume : 2 | Issue : 1 | Page : 11

Intestinal parasites in captive wild animals at four zoological gardens in Northeast China

Hongyu Qiu¹, Huining Yang², Xiaojing Sun³, Chengjia Jin², Ximing Zou⁴, Chunren Wang², Qiaocheng Chang⁵
¹ School of Public Health, Shantou University, Shantou, Guangdong 515041; College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang 163319, P.R. China
² College of Animal Science and Veterinary Medicine, Heilongjiang Bayi Agricultural University, Daqing, Heilongjiang 163319, P.R. China
³ School of Basic Medical Sciences, Xi'an Medical University, Xi'an, Shaanxi 710021, P.R. China
⁴ Harbin North Forest Zoo, Harbin, Heilongjiang 150000, P.R. China
⁵ School of Public Health, Shantou University, Shantou, Guangdong 515041, P.R. China

Date of Submission	26-Dec-2021
Date of Decision	21-Feb-2022
Date of Acceptance	08-Jul-2022
Date of Web Publication	13-Sep-2022

Correspondence Address:
Qiaocheng Chang
School of Public Health, Shantou University, Shantou, Guangdong 515041
P.R. China

Source of Support: None, Conflict of Interest: None

DOI: 10.4103/2773-0344.350692

Abstract

Objective: In order to investigate the prevalence of intestinal parasites in captive wild animals in four zoological gardens in Heilongjiang Province of Northeast China.
Method: From September 2016 to September 2020, fecal samples were collected from Harbin North Forest Zoo, Jiamusi Water Source Mountain Park, Qiqihar Longsha Zoological and Botanical Gardens, and Jixi City Zoo. The morphological identification of eggs or oocysts was carried out using the water washing precipitation method, saturated saline floatation method, and saturated sucrose floatation method.
Results: The overall parasite positive detection rate in the four zoos were 18.33% (33/180), 21.69%(18/83), 22.22%(8/36), and 26.32%(10/38), respectively. The most prevalent parasitic species of Carnivora, Artiodactyla, Perissodactyla, Primates, and Aves were Ascaridoidea, Trichuris spp., and Contracaecum sp. Zoonotic parasites were also observed (Toxocara cati, Spirometra mansoni, Trichostrongylus sp.).
Conclusions: The results are beneficial in assisting zoo management to formulate and implement preventive and control measures against the spread of infectious parasitic diseases among the animals or to humans.

Keywords: Intestinal parasites; Zoo animals; Northeast China

How to cite this article:
Qiu H, Yang H, Sun X, Jin C, Zou X, Wang C, Chang Q. Intestinal parasites in captive wild animals at four zoological gardens in Northeast China. One Health Bull 2022;2:11

How to cite this URL:
Qiu H, Yang H, Sun X, Jin C, Zou X, Wang C, Chang Q. Intestinal parasites in captive wild animals at four zoological gardens in Northeast China. One Health Bull [serial online] 2022 [cited 2023 Mar 31];2:11. Available from: http://www.johb.info/text.asp?2022/2/1/11/350692

Hongyu Qiu, Huining Yang. These authors contributed equally to this work.

1. Introduction

Human beings are facing more complex health problems than ever before, especially in the aspect of zoonosis, which often involves animals, humans and the environment. The background surveys and database construction of wildlife pathogens are of great significance for the prevention and control of zoonosis^[1]. Captive wild animals in zoological gardens can be affected by various intestinal parasites that can present a serious threat to their health, and occasionally zoonotic parasites pose a potential threat to public health and safety. Zoological gardens play a beneficial role in the promotion of animal biodiversity by protecting endangered species. Zoos housing domestic, captive wild, and exotic animals are required to uphold excellent standards of animal health and welfare, and accordingly, the prophylaxis of pathogens is extremely important^[2].

A major concern in zoos is the high risk of environmental contamination due to the confinement of animals in relatively small areas^[3],[4]. In addition, stressful conditions caused by captivity can also diminish their resistance to parasitic diseases^[5]. Intestinal parasites of zoo animals include zoonotic species that can infect humans, which raises public health concerns. Taking appropriate measures to prevent infections either among zoo animals or from animals to humans is of the utmost concern^[5],[6],[7]. The occurrence of parasites in animals housed in zoological gardens might vary according to husbandry practices, disease prophylaxis, and administered treatments^[7].

To obtain a better understanding of intestinal parasitic infections in zoo animals and to assess the potential threat of zoonotic parasites being transmitted to breeders and tourists, we investigated the occurrence of intestinal parasites in four of the largest zoological gardens in Heilongjiang Province in this study.

2. Materials and methods

2.1. Fecal samples collection and examination

From September 2016 to September 2020, samples were collected from Harbin North Forest Zoo (45.31’ N, 126.51’ E), Jiamusi Water Source Mountain Park (46.80’ N,130.40’ E), Qiqihar Longsha Zoological and Botanical Gardens (47.38’ N,123.94’ E), and Jixi City Zoo (45.31’ N,130.90’ E). According to the species and quantity of captive wild animals in the zoos, various proportions of samples were collected randomly from Carnivora, Artiodactyla, Aves, Perissodactyla, Primates, Marsupials, Rodentia, and Proboscidea in the four animal parks. The samples covered most of the animal species in the zoo at the time of sampling. The fecal samples were put into prepared sealable bags, which were labeled, recorded, and taken to the laboratory for storage at 4 °C before being used for testing. The morphological identification of eggs or oocysts was carried out using the water washing precipitation method, saturated saline floatation method, and saturated sucrose floatation method^[8]. Worm species were determined by eggs morphology and host origin. PCR was used to detect Cryptosporidium spp. in animals with diarrhea^[9],[10]. The entire small subunit ribosomal rRNA gene was amplified from samples by conventional polymerase chain reaction by using the forwarding primer 5'-AAC CTG GTT GAT CCT GCC AGT AGT C-3' and reverse primer 5'-TGA TCC TTC TGC AGG TTC ACC TAC G-3'. Each PCR consisted of 35 cycles of denaturation at 94 °C for 45 s, annealing at 60 °C for 45 s, and extension at 72 °C for 60 s, with an initial denaturation at 94 °C for 5 min and a final extension at 72 °Cfor 10 min. The PCR products were cloned and sent to Sangon Company (Shanghai, China) for sequencing from both directions using Sanger sequencing.

3. Results

A total of 337 fecal samples were collected from Harbin Northern Forest Zoo, Qiqihar Longsha Zoological and Botanical Gardens, Jixi City Zoo, and Jiamusi Shuiyuan Mountain Park for analysis. We confirmed 69 positive fecal samples, and the total infection rate was 20.47% (69/337). The total infection rate in Harbin North Forest Zoo was 18.33% (33/180), in which the positive detection rate of Carnivora, Artiodactyla, Perissodactyla, Primates, Aves were respectively 22.81%(13/57), 29.17%(7/24), 50.00%(5/10), 13.64%(3/22), 7.58%(5/66),and no parasite eggs were detected in the feces of Proboscidea. The total infection rate of Qiqihar Longsha Animal and Botanical gardens was 21.69% (18/83); in Carnivora, Artiodactyla, Perissodactyla, Primates and Aves, the positive detection rate were respectively 18.75% (3/16), 15.15%(5/33), 71.43%(5/7), 50.00%(4/8), and 7.14%(1/14), and there were no parasite eggs detected in Rodentia or Marsupials. The total infection rate in Jixi City Zoo was 22.22% (8/36), and the positive detection rate in Carnivora, Artiodactyla, and Aves were respectively 29.41%(5/17), 13.33%(2/15), 33.33%(1/3) and no paresites detected on Primates. The total infection rate in Shuiyuan Mountain Park of Jiamusi was 26.32%(10/38), in which the positive detection rate of Carnivora, Artiodactyla, Primates, and Aves were 23.08%(3/13), 28.57%(2/7), 37.50%(3/8), and 22.22%(2/9), respectively, while no parasite eggs were detected in Perissodactyla [Table 1].

Table 1: Parasite infection of wild animals in four zoos.

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Carnivorous animals in the four zoos were infected with eight parasite species, including Toxascaris (T.) leonina, T. cati, and Spirometra mansoni. Parasitic Ascaridoidea were predominant in carnivorous animals, and T. leonina and T. cati were common in large cats. The parasites in Artiodactyla animals were mainly nematodes, among which Trichuris spp. is the most common infectious parasite. Similarly, primates were mostly infected with Trichuris sp. In general, Aves were infected with three kinds of parasites, Contracaecum sp., Capillaria sp., and Heterakis sp., among which the most severe infections were brought by Contracaecum sp. The Perissodaetyla were infected with five parasites, of which roundworm was the dominant species. Primates in the four zoos were infected with three kinds of parasites, the most common of which was Trichuris sp. In primates, Trichuris spp. are the main species. Trichuris sp. was one of the most common and serious intestinal parasites of the primate Rhinopithecus roxellana and are of great significance to public health; therefore, attention should be paid to these parasites in prevention and control work. The specific types of parasitic infections found are shown in [Table 2]. The morphological pictures of eggs are shown in [supplementary Figure 1[Additional file 1], Figure 2[Additional file 2], Figure 3[Additional file 3], Figure 4[Additional file 4] and Figure 5[Additional file 5]. We observed the widespread occurrence of co-infections. In the Harbin zoo, two lions (Panthera Leo) were infected with T. cati, T.leonina and Ascaris; a tiger (Panthera tigris) was infected with Ascaris and T. cati, and a giraffe (Giraffa camelopardalis) was infected with Oesophagostomum sp. and Trichostrongylus sp. In the Longsha animal and plant garden in Qiqihar, an mouflon (Ovis aries musimon) was infected with Bunostomum trigonocephalum and Trichostrongylus sp., three zebras (Equus burchellii) were infected with Triodontophorus, Strongylus sp. and Cyathostomum sp., and a peacock(Pavo muticus) was infected with Capillaria spp. and Contracaecum sp. And a spotted deer (Cervus nippon) in Jiamusi zoo was infected with Trichostrongylus sp. and Trichuris sp. [Table 3]. Among the four zoos, Jixi City Zoo did not have any co-infections, while Qiqihar Zoo had the highest co-infection rate of 6.3%, Harbin Zoo had a rate of 4.3%, and Jiamusi Zoo had 2.6%.We observed the widespread occurrence of co-infections. Among the four zoos, Jixi City Zoo did not have any co-infections, Qiqihar Zoo had the most mixed infections at 6.3%, Harbin Zoo had a rate of 4.3%, and Jiamusi Zoo had 2.6% co-infections.

Table 2: Species of parasite infection in wild animals in four zoos.

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Table 3: The mixed infection of parasites in wild animals.

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4. Discussion

In our investigation, in order to more accurately express the infection of intestinal parasites in animals, we selected randomly under the premise of covering almost all animal species in sampling. Diarrhea faeces samples were also tested for cryptosporidium. Animals inside the facilities were cleaned daily with high-pressure pipe water. The outdoor facilities with soil and sand were not cleaned daily with water, but the dung was removed daily except the area reserved for savannah animals. Collection of feces were carried out in the morning with the assistance of the animal’s handlers. More than 50% of the tested animal samples were collected in this study. The results can preliminarily represent the prevalence of intestinal parasites in zoos. T. cati was the main parasitic infection of carnivores in this study. A survey of Malaysian zoos also showed that cats easily contract T. cati^[10]. Ascaridoidea members were the dominant species in carnivores. T. cati and T. leonina were the main infectious species in large cats, which is consistent with the results of an investigation by Liu Jianli and Wang Dezhao^[11]. T. cati is a zoonotic parasite that is considered to be an important agent of toxocariasis^[12]. It can pose a threat to the breeding staff and its presence should be monitored. Toxocariasis is a parasitosis that can be transmitted through the placenta or through breastfeeding, and prevention and control precautions should be taken before and after childbirth.

When compared the parasite species in animals in the four zoos, we found similar patterns of infection. The total positive detection rate of the four zoos were lower than that of captive wild animals in a research center in Shaanxi Province (88.9%)^[13], a zoo in Sichuan Province (74.4%)^[14], and a zoo in Henan Province (56.5%)^[15]. Compared with Italian zoos, the infection rate of chimpanzees in Heilongjiang Province was lower in the four zoos , and the parasite infection rate did not reach 100%^[16]. The level of parasitism in the four zoos in Heilongjiang Province was lower than that found in zoos in Romania^[17]. However, we did not collect blood samples from carnivores; therefore, we have no information on the Toxoplasma infection rate, which calls for further attention. Evidence shows that the four zoos in Heilongjiang Province pay closer attention to the prevention and control of parasitic diseases and have higher standards of feeding conditions and health regulations. However, we found evidence of zoonotic parasites in Heilongjiang Province zoos, which requires people to be vigilant and maintain active treatment and prevention measures to avoid the parasites posing a threat to zoo keepers and tourists. The different prevalence rates for parasites recorded in the four zoos indicate the importance of fecal removal, routine surveillance, and selective prophylactic treatments for parasitic diseases within feeding procedures and disease prevention measures.

In conclusion, the findings of this study demonstrated that intestinal parasites were prevalent in captive wild mammals in zoos. The positive detection rate of the four zoos were 18.33%(33/180), 21.69%(18/83), 22.22%(8/36), and 26.32%(10/38), respectively, and the most prevalent parasites in Carnivora, Artiodactyla, Perissodactyla, Primates, and were Ascaridoidea, Trichuris spp., and Contracaecum sp.

Some of the parasitic species detected in this study pose potential or proven zoonotic risks, and these findings underscore the importance of controlling these parasitic diseases to safeguard the health of captive animals, as well as the health of humans working with these animals and tourists.

Funding

The study received no extramural funding.

Authors’ contribution

Chang QC, Wang CR and Zou XM designed the study, searched the literatures, took part in data collection and management, Sun XJ and Jin CJ performed the statistical analysis and interpreted the results of data analysis. Author Yang HN wrote the protocol. Qiu HY and Chang QC prepared the first draft of the manuscript. All authors read and approved the final manuscript.

Conflicts of Interest

The authors declare that there is no conflicts of interest.

Publisher’ s note

The Publisher of the Journal remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

References

1.	Gao George F, Chen JS, Zhao GP, Xu JG, Lu JH. The 697th Xiangshan Science Conference consensus report on One Health and human health. One Health Bullet 2021; 1(1): 3-9
2.	Kelly JD, English AW. Conservation biology and the preservation of biodiversity in Australia: A role for zoos and the veterinary profession. Aust Vet J 1997; 75(8): 568-574.
3.	Lia RP, Traversa D, Laricchiuta P, Dantas-Torres F, Paradies R, Alvinerie M, et al. Efficacy of an in-feed formulation containing ivermectin for the control of intestinal strongyles in captive zebras [Equus burchelli (Gray, 1824)]. Vet Parasitai 2010; 169(1-2): 133-137.
4.	Malan FS, Horak IG, de Vos V, van Wyk JA. Wildlife parasites: Lessons for parasite control in livestock. Vet Parasitai 1997; 71(2-3): 137-153.
5.	Gracenea M, Gómez MS, Torres J, Carné E, Fernández-Morán J. Transmission dynamics of Cryptosporidium in primates and herbivores at the Barcelona zoo: a long-term study. Vet Parasitol 2002; 104(1): 19-26.
6.	Levecke B, Dorny P, Geurden T, Vercammen F, Vercruysse J. Gastrointestinal protozoa in non-human primates of four zoological gardens in Belgium. Vet Parasitol 2007; 148(3-4): 236-246.
7.	Pérez Cordón G, Hitos Prados A, Romero D, Sánchez Moreno M, Pontes A. Intestinal parasitism in the animals of the zoological garden “Peña Escrita” (Almuñecar, Spain). Vet Parasitol 2008; 156(3-4): 302-309.
8.	Taylor MA. Veterinary Parasitology. Oxford. Blackwell Publishing. 2007.
9.	Fagiolini M, Lia RP, Laricchiuta P, Cavicchio P, Mannella R. Gastrointestinal parasites in mammals of two Italian zoological gardens. J Zoo Wildl Med 2010; 41(4): 662-670.
10.	Hussain S, Mohsin Bukhari S, Wang L, Khalid N, Hou Z. Exploration of zoo felids in north-east China for the prevalence and molecular identification of Cryptosporidium spp. Peer J 2021; 9: e11819.
11.	Lim YA, Ngui R, Shukri J, Rohela M, Mat Naim HR. Intestinal parasites in various animals at a zoo in Malaysia. Vet Parasitol 2008; 157(1-2): 154-159.
12.	Wang DZ, Zhang Q, Liu C. Investigation on intestinal ascariasis infection of tigers, lions and leopards in some zoos in Northeast China. Chin J Vet Parasitol 2002; 01: 60.
13.	Cai J, Qiao JY, Zhang X. Observation on Intestinal parasitic morphology and infection in captive rare wildlife in Shaanxi province. Chin J Zool 2009; 44(03): 63-69.
14.	Qi M, Dong HJ, Hu L. Investigation on the prevalence of intestinal parasites in wild animal zoo. China Animal Husband Vet Med 2011; 38(10): 188-191.
15.	Yang N, Qi M, Jian FC. Survey on the infection status of intestinal parasites in captive wild-animals. J Human Agricul Turai Sci 2011; 40(03): 154-157.
16.	Fagiolini M, Lia RP, Laricchiuta P, Cavicchio P, Mannella R. Gastrointestinal parasites in mammals of two Italian zoological gardens. J Zoo Wildl Med 2010; 41(4): 662-670.
17.	Dǎrǎbuş G, Afrenie M, Hotea I, Imre M, Morariu S. Endoparasites in mammals from seven zoological gardens in Romania. J Zoo Wildl Med 2014; 45(2): 239-246.