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Article

Seasonal Prevalence of Gastrointestinal Parasites in Macaques (Macaca thibetana) at Mount Emei Scenic Area in China

by
Jiandong Yang
1,
Samuel Kumi Okyere
2,
Jie Zheng
3,
Buyuan Cao
2 and
Yanchun Hu
2,*
1
College of Animal Sciences and Technology, Sichuan Agricultural University, Chengdu 611130, China
2
Key Laboratory of Animal Disease and Human Health of Sichuan Province, College of Veterinary Medicine, Sichuan Agricultural University, Chengdu 611130, China
3
Forestry Management Agency of Mount Meishan, Meishan 614200, China
*
Author to whom correspondence should be addressed.
Animals 2022, 12(14), 1816; https://doi.org/10.3390/ani12141816
Submission received: 29 June 2022 / Revised: 11 July 2022 / Accepted: 12 July 2022 / Published: 15 July 2022
(This article belongs to the Section Veterinary Clinical Studies)
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Abstract

:

Simple Summary

Gastrointestinal parasites may affect the health of macaques directly or indirectly, thereby exposing primates to conservational risks. Gastrointestinal parasites cause various health conditions such as apathy, diarrhea, malaise and weight loss. However, there is still a dearth of knowledge about the population of intestinal parasites in the macaques kept in the Mount Emei scenic spot. Therefore, using the microscopic detection method, the population of gastrointestinal parasites in fecal samples of monkeys at the Mount Emei scenic spot was estimated. The results showed that Gongylonema spp. and Entamoeba spp. were dominant gastrointestinal parasites in the fecal samples of monkeys at the Mount Emei scenic spot. This is the first reported study on gastrointestinal parasites in monkeys at the Mount Emei Scenic and will help in designing a future road map for parasitic disease monitoring and control in wild-life habitats, as well as provide epidemiological data on parasites in monkeys in the Mt. Emei Scenic Area at Sichuan, China.

Abstract

The aim of the study was to elucidate the prevalence of intestinal parasites in macaques at the Mt. Emei Scenic Area of Sichuan, China. A total of 168 fecal samples were collected from yellow (n = 31), black (n = 19), new (n = 57), Leidongping (n = 57) and Wuxiangang (n = 4) macaques from 2019 to 2020. The fecal samples were tested for various gastrointestinal parasites following the microscopic detection method. The results showed that the total prevalence rate of the intestinal parasite was 51.19% (86/168), whereas the intestinal parasite with the highest prevalence was Gongylonema spp. (26.79%) for helminth and Entamoeba spp. (18.45%) for protozoa. Interestingly, the highest prevalence of intestinal parasites was observed during the summer season (86.21%), and the lowest was observed during the winter season (7.14%). There was a positive correlation observed between the human contact frequency and total prevalence rate of the intestinal parasites (p < 0.05); however, there was no correlation between the human contact frequency and total prevalence of the intestinal parasites at different seasons (p > 0.05). In conclusion, the dominant parasites Gongylonema spp. and Entamoeba spp. cause various diseases that may be transmitted to humans and other animals; therefore, there is a need for a proper management system, such as parasite control measures and population protection in the Mt. Emei Scenic Area of Sichuan, China.

1. Introduction

Knowledge of gastrointestinal tract (GIT) parasites provides important information for the management of wild animals in scenic areas, as these parasites pose a threat to the population of other wild and domestic animals, as well as tourists [1]. Gastrointestinal parasites reside in the small intestine (duodenum, ileum, jejunum) and large intestine (caecum, colon and rectum) [2]. Gastrointestinal parasites release their infectious propagules in the fecal matter of their hosts, which, when ejected, results in the buildup of infectious agents in the habitat, thereby increasing their transmission [3]. Infections by gastrointestinal parasites, including helminth and protozoans, have been reported in wild animals [4]. As a national second-class protected animal, macaques in the Mount Emei Tibetan area are a unique monkey species in China [5]. Macaques belong to the family of Mammalia and order Primate [6]. Macaques are non-human primates (NHP) mostly found in Africa, Asia and America [7,8]. Rhesus macaque share many common structural, physiology, immunity and heredity traits with humans [9]. For example, the homology of the nucleic acid sequence between macaques and humans was reported to be more than 95% [10]; hence, rhesus monkeys are important experimental animals in scientific research [11,12,13]. In recent years, the passenger flow at the Mount Emei scenic spot has increased rapidly. Moreover, macaques in the Mount Emei scenic spot have frequent contact with tourists who are allowed to take photos and play with the monkeys. However, these macaques serve as hosts for a large number of parasites, which are communicable to humans who are in contact with them. Therefore, their frequent contact with tourists possesses a potential health threat [14].
Gastrointestinal parasites may affect the health of macaques directly or indirectly, thereby exposing primates to conservational risks [15]. Numerous studies have identified, isolated and reported various gastrointestinal parasites in non-human primates [16,17,18]. The infection of intestinal parasites in rhesus monkeys kept in scenic spots affects the health of monkeys, as well as tourists and other domestic animals who visit those tourist sites [19,20]. Many studies have reported cases of human infection caused by intestinal parasites after contact with animals kept in the zoo, wildlife centers and ecological scenic areas in Africa, Southeast Asia and Southern China [21,22,23]. Wild or captive animals are significant in the epidemiology of various zoonotic diseases [24]. Gastrointestinal parasites cause various health conditions such as apathy, diarrhea, malaise and weight loss. However, there is still a dearth of knowledge about the population of intestinal parasites in macaques kept in the Mount Emei scenic spot. Parasitological studies are vital to appreciate the life cycle of parasites and the potential transmission route to other animals and humans [25]. Therefore, to evaluate and manage the effect of gastrointestinal parasites on any animal population dynamics, it is essential to evaluate their prevalence in wildlife populations [26]. The present study was undertaken to examine the status of gastrointestinal helminth and protozoan parasites in macaques at the Mount Emei scenic spot to help in designing future road maps in parasitic disease monitoring and control in wildlife habitats, as well as provide epidemiological data on parasites in monkeys, for education on public health and disease prevention.

2. Materials and Methods

2.1. Study Areas and Examined Monkeys

This study was carried out in the southwestern part of China (Figure 1). The study period was from 15 March 2019 (Spring season) to 16 January 2020 (Winter season). A total of 168 fecal samples were collected from seemingly healthy macaques (1–20 years old) of both sexes in the ecological area of the Emei Mountain scenic spot in the Sichuan province. The macaques had no anthelmintic treatment in the previous years, and these macaques had no direct contact with other monkeys and livestock. The macaques from the Mount Emei scenic spot were recorded and grouped according to their geographical location and special characteristics:
(1)
Yellow macaques group (n = 31): the range of their activity was from Qingyinge to the ecological area. The group was characterized by yellow hair color and had more young monkeys in the population.
(2)
Black macaques group (n = 19): the range of their activity was from near the trestle and cable bridge in the ecological area. The group was characterized by their dark brown color.
(3)
New macaques group (n = 57): the range of their activity was from the ecological area to the upper section of Hongchunping. These macaques migrated to the ecological area near Jiulaodong in hongchunping. Their population was characterized by light brown hair color.
(4)
Leidongping macaques group (n = 57): the range of activity was from the Leishen temple to Jinding ropeway near Leidongping. Their hair color was mostly grayish brown.
(5)
Wuxiangang macaques group (n = 4): the range of their activity was from the Wuxiangang station to Qingyin Pavilion. This group was characterized by their unwillingness to be in contact with tourists.

2.2. Sample Collection

A total of 168 fecal samples from the yellow (n = 31), black (n = 19), new (n = 57), Leidongping (n = 57) and Wuxiangang (n = 4) macaques in the ecological area were collected between the periods of 15 March to 1 April (spring), 25 August to 10 September (summer), 15 June to 1 July (Autumn) 2019 and 2 January to 16 January (winter) 2020 from the Emei Mountain scenic spot. After clinical examination, the monkeys were initially anesthetized with intramuscular 15 mg/kg ketamine and 0.5 mg/kg acepromazine (HangZhou Testsea biotechnology Co., Ltd. Hangzhou, China), and fecal samples were aseptically collected directly from the rectum by disposable rectal gloves, placed into plastic bags and stored in polystyrene foam containers with recyclable ice, maintaining a temperature of about 4 °C within the container. The containers were labeled and then transferred to the Department of Clinical Veterinary Medicine, Sichuan Agricultural University for parasitological examination.
The occurrence time, location, contact times (including group photos, direct contact behaviors such as agonistic behavior of macaques and indirect contact behaviors including feeding and snatching) and the contact frequency between tourists and macaques (contact times/haunting time) of each of the monkey group were recorded daily.

2.3. Microscopic Examination of Fecal Parasites

Fecal samples were microscopically examined for helminth eggs and larvae following the method described previously [2].

2.4. Calculation of Prevalence Rate

Prevalence rate was calculated according to the formula by Thanasuwan et al. [27].
Prevalence (%) = number of macaques with parasites/total number of macaque × 100.

2.5. Statistical Analysis

All the data obtained were analyzed using SPSS 21.0 statistical software program. The chi-square test was used to determine the statistical significance of the different prevalence of endoparasites between macaque groups and seasons, respectively. Pearson’s correlation test was used to determine the relationship between the contact frequency and the intestinal parasite prevalence rate in the various macaque groups and seasons. In all the analyses, the confidence level was 95%, and statistical analyses were considered significant if p < 0.05 and highly significant if p < 0.01.

3. Results

3.1. Population and Daily Contact Frequency of Macaque in Various Seasons

The sampling time of each season was controlled within 10~20 days. The contact time between the macaques and tourists was recorded daily (including direct contact behaviors such as group photos, agonistic behaviors and indirect contact behaviors such as feeding and snatching). The daily contact frequency of the tourists was also calculated. See Table 1 and Table 2 for details.

3.2. Microscopic Examination Results and Analysis

A total of 168 fecal samples of the five formed groups of macaques were examined, and a total of 11 parasites were detected: 4 protozoa spp.—Sphaerozoum fuscum, Balantidium coli, Entamoeba, Blastocysts spp.—and 7 helminths spp.—Trematoda spp., Gongylonema spp., Cestoda, Ascaris lumbricoides, Enterobius vermicularis, Ancylostoma duodenale and Physaloptera. The total infection rate of the parasites was 51.19%. Among the helminth, Gongylonema spp. was highly detected in the fecal samples with a prevalence rate of 26.79% followed by Cestoda (4.17%), Ancylostoma duodenale (3.57%), Trematoda spp. (2.38%), Physaloptera spp. (1.79%), Ascaris lumbricoides (1.19%) and Enterobius vermicularis (0.60%). Moreover, among the protozoa, Entamoeba spp. had the highest prevalence rate (18.45%) followed by Sphaerozoum fuscum (14.29%), Blastocysistis spp. (2.98%) and Balantidium coli (1.19%). The species and prevalence rates of the intestinal parasites in the five macaque groups in the Mount Emei area are shown in Table 3 and Figure 2.

3.3. The Prevalence of the Intestinal Parasite in the Macaque Groups

The prevalence rate of the intestinal parasite in the macaque groups is represented in Table 3. The prevalence rate of the intestinal parasite was arranged in the descending order of prevalence as follows; black macaque 89.47% (17/19), yellow macaque 80.64% (25/31), leidongping macaque 40.35% (23/57), new macaque 35.09% (20/57) and wuxiangang 25% (1/4). It was also observed that the black macaque group recorded the highest rate of intestinal parasite prevalence as compared to the other macaque groups (p < 0.05). In addition, we observed no significant difference in the rate of intestinal parasite prevalence among the yellow, leidongping and wuxiangang macaque groups (p > 0.05, p > 0.01). We also observed that the total intestinal prevalence rate significantly correlated with the contact frequency of tourists (r = 0.8479, p = 0.0348) (Figure 3).

3.4. The Prevalence of the Intestinal Parasite during Different Seasons

Table 4 shows the results of the rate of prevalence of intestinal parasites in macaques in different seasons. The rate of prevalence was arranged in descending order of prevalence as follows: summer 86.21% (50/58), spring 61.29% (19/31), autumn 56.52% (13/23) and winter 7.14% (4/56). We observed that the summer season had the highest rate of prevalence of intestinal parasites compared with the other seasons (p < 0.05). Moreover, we also observed no significant correlation between the contact frequency and the prevalence rate of macaques during different seasons (r = 0.8349, p = 0.0825) (Figure 4).

4. Discussion

Mount Emei is a famous tourist attraction with a dense population flow and a spot where macaques have more contact with tourists. Humans and pets visiting scenic spots carry pathogens [28] and may transmit these pathogens when they are in direct or indirect contact with an animal in these scenic spots [29].
Among the intestinal parasites detected in the fecal samples of the macaques in the Mount Emei scenic area, Gongylonema spp., Entamoeba spp., Sphaerozoum fuscum, Cestoda spp. and Ascaris lumbricoides were the most dominant intestinal parasites, probably due to poor hygienic environment in the scenic area, untreated drinking water and free monkey contact with tourists. These observations were similar to the previous report [30]. In addition, we observed that the rate of prevalence of the intestinal parasites among the various groups of macaques was different, and thus we speculated that these differences could be caused by the difference in the geographical locations of the macaques in the scenic area, which was consistent with reports by Antonelli et al. [31]. However, there is a need for further studies.
Gongylonema spp., especially Gongylonema pulchrum (gullet worm), has been identified in many mammals [32,33]. Numerous cases of Gongylonema spp. infection with associated pathological lesions and clinical signs have been reported in monkeys and other vertebrates [34].
Entamoeba [35] is the species of amoeba that causes human infection and pathogenicity. They are free-living amoebas in water, air and soil, which were reported in the past as posing no threat to humans. However, few records of human infection with histolytic amoeba have been found in recent years [36], but their infection routes were not from their contact with other primates but mostly from water and soil source infections [37]. Entamoeba histolytica of Entamoeba spp. causes amoeba dysentery and liver abscesses [38]. E. histolytica trophozoites degrade the mucus layer, lyse epithelial cells and invade leukocytes [35,39]. E. histolytica also alters active electrolyte transport, secretion and malabsorption [40].
Adult tapeworms (Cestoda) are found in the small intestine. Cestoda infections are usually asymptomatic but may cause abdominal distress, dyspepsia, anorexia (or increased appetite), nausea, localized pain and diarrhea [41].
Sphaerozoum fuscum is a common and harmful parasite found in the intestine of most animals. It causes conditions such as emaciation, anemia, dysentery and growth inhibition [42].
Ancylostoma duodenale is the most common parasitic infection in countries with poor access to adequate water, sanitation and hygiene [43]. Ancylostoma duodenale has been reported to cause upper gastrointestinal bleeding [44]. Hookworms may cause Löffler syndrome with coughing, wheezing, eosinophilia and sometimes hemoptysis [45].
Ascaris lumbricoides is a common nematode parasite in humans and has been associated with intestinal pathology, respiratory symptoms and malnutrition in children from endemic areas [46]. Ascaris lumbricoides infects about 820 million people and is prevalent in at least 103 of 218 countries worldwide [47,48].
Numerous studies have reported that seasons can influence the growth and development of various endo- and ecto-parasites [31,49]. Thus, low temperatures affect the rate of growth, development and metabolism of parasites [50]. A study by Viljoen et al. [51] showed that clear seasonal patterns of parasite prevalence and abundance emerged with peaks during the summer season for mites and the winter season for cestodes. In the present study, the highest prevalence rate was recorded during the summer season, and this may be related to many helminths developing during the summer season [52].
Contact between humans and animals is unavoidable [53], which may result in the natural transmission of parasites and zoonotic diseases [54]. Therefore, in this study, Pearson correlation analysis was used to determine whether there was a possible relationship between the frequency of human contact and the prevalence rate of the intestinal parasites, as well as the frequency of seasonal human contact and the seasonal prevalence rate of the intestinal parasites. The results showed a positive correlation between the prevalence rate of the intestinal parasites and human contact with the monkeys, indicating a high probability of monkeys transmitting these intestinal parasites to tourists (vice versa). This finding was inconsistent with the previous study by Elbahy et al., [52]. However, there was no significant correlation between the seasonal prevalence rate of the parasites and seasonal human contact with monkeys.

5. Conclusions

The presence of gastrointestinal helminth and protozoa parasites with known ill impact on macaques may threaten the survival of these monkeys, as well as tourists and other animals living in the Mount Emei scenic area. Based on our parasitological results, we found various gastrointestinal endoparasites in the macaques in the Mount Emei scenic area. Among them, Gongylonema spp. and Entamoeba were the prevalent parasites, whereas Gongylonema spp., Entamoeba spp., Ascaris lumbricoides, Ancylostoma duodenale and Cestoda were the dominant zoonotic parasites in the gastrointestinal tract of the macaques. Therefore, restrictions to reduce direct human (tourists) contact with macaques, proper facility management, keeping good sanitary conditions of the scenic area and regular deworming of monkeys are recommended. In addition, we suggest further research to be conducted to determine the intensity of infection, parasitic diseases and mode of transmission of parasites and possible mitigating strategies to strengthen the management of the scenic area.

Author Contributions

Conceptualization, J.Y., S.K.O., J.Z. and B.C.; Data curation, J.Y., S.K.O., J.Z. and B.C.; Formal analysis, J.Y., S.K.O., J.Z. and B.C.; Funding acquisition, J.Y. and Y.H.; Investigation, J.Y. and Y.H.; Methodology, J.Y., S.K.O., J.Z. and B.C.; Project administration, J.Y., J.Z. and Y.H.; Resources, J.Y., J.Z. and Y.H.; Software, J.Y., S.K.O. and J.Z.; Supervision, Y.H.; Validation, J.Y., J.Z. and Y.H.; Visualization, Y.H.; Writing—original draft, J.Y., S.K.O., J.Z. and B.C.; Writing—review and editing, J.Y., S.K.O., J.Z. and Y.H. All authors have read and agreed to the published version of the manuscript.

Funding

This research was supported by grants from the project of Investigation on Population and Epidemic Disease of Tibetan macaque in Mount Emei (No. 015H4102).

Institutional Review Board Statement

This study was approved by the Institutional Animal Care and Use Committee of Sichuan Agricultural University, Sichuan, China, under the permit number DKY-B2019603005. All experiments were conducted in accordance with the Sichuan Agricultural University (SAU) Laboratory Animal Welfare and Ethics guidelines.

Informed Consent Statement

Not applicable.

Data Availability Statement

The data presented in this study are available on request from the corresponding author.

Acknowledgments

We would like to thank the management of the Emei Mountain Scenic Area for the great support we had in the field survey and the cooperation of the staff in the Scenic Area during the sampling.

Conflicts of Interest

We wish to confirm that there is no known conflict of interest associated with this publication, and there has been no significant financial support for this work that could have influenced its outcome.

References

  1. Daszak, P.; Cunningham, A.A.; Hyatt, A.D. Emerging infectious diseases of wildlife-threats to biodiversity and human health. Science 2000, 287, 443–449. [Google Scholar] [CrossRef] [PubMed]
  2. Bhat, R.A.; Tak, H.; Bhat, B.A.; Dar, J.R.; Ahmed, R. Gastrointestinal helminth parasites of wild ungulates in Hirpora Wildlife Sanctuary, Kashmir, India. J. Parasit. Dis. 2022, 147, 1–7. [Google Scholar] [CrossRef]
  3. Soulsby, E.J.L. Textbook of Veterinary Clinical Parasitology, Vol I; Helminth Oxford Blackwell Scientific: London, UK, 1982. [Google Scholar]
  4. Sprenger, L.K.; Yoshitani, U.Y.; Buzatti, A.; Molento, M.B. Occurrence of gastrointestinal parasites in wild animals in State of Paraná, Brazil. An. Acad. Bras. Ciências 2018, 90, 231–238. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Tibetannet. Available online: https://en.tibet3.com/photo/2017-02-23/2346.html (accessed on 2 May 2022).
  6. Salegio, E.A.; Bresnahan, J.C.; Sparrey, C.J.; Camisa, W.; Fischer, J.; Leasure, J.; Buckley, J.; Nout-Lomas, Y.S.; Rosenzweig, E.S.; Moseanko, R.; et al. A unilateral cervical spinal cord contusion injury model in non-human primates (Macaca mulatta). J. Neurotrauma 2016, 33, 439–459. [Google Scholar] [CrossRef] [Green Version]
  7. Peña, J.C.; Ho, W.Z. Non-human primate models of tuberculosis. Microbiol. Spectr. 2016, 4, 1–13. [Google Scholar] [CrossRef] [Green Version]
  8. Modolo, L.; Salzburger, W.; Martin, R.D. Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony. Proc. Natl. Acad. Sci. USA 2005, 102, 7392–7397. [Google Scholar] [CrossRef] [Green Version]
  9. Chan, A.W. Progress and prospects for genetic modification of nonhuman primate models in biomedical research. ILAR J. 2013, 54, 211–223. [Google Scholar] [CrossRef] [Green Version]
  10. Roodgar, M.; Babveyh, A.; Nguyen, L.H.; Zhou, W.; Sinha, R.; Lee, H.; Hanks, J.B.; Avula, M.; Jiang, L.; Jian, R.; et al. Chromosome-level de novo assembly of the pig-tailed macaque genome using linked-read sequencing and HiC proximity scaffolding. Gigascience 2020, 9, giaa069. [Google Scholar] [CrossRef]
  11. Li, Z.H.; He, X.P.; Li, H.; He, R.Q.; Hu, X.T. Age-associated changes in amyloid-β and formaldehyde concentrations in cerebrospinal fluid of rhesus monkeys. Zoöl. Res. 2020, 41, 444–448. [Google Scholar] [CrossRef]
  12. Nogueira, R.; Peltier, N.E.; Anzai, A.; DeAngelis, G.C.; Martínez-Trujillo, J.; Moreno-Bote, R. The effects of population tuning and trial-by-trial variability on information encoding and behavior. J. Neurosci. 2020, 40, 1066–1083. [Google Scholar] [CrossRef]
  13. Vierboom, M.P.M.; Breedveld, E.; Keehnen, M.; Klomp, R.; Bakker, J. Pain Relief in Nonhuman Primate Models of Arthritis. Methods Mol. Biol. 2017, 1559, 411–417. [Google Scholar] [PubMed]
  14. Wang, Z. Analysis of zoonosis between wild animals and humans. Spec. Econ. Anim. Plants. 2008, 7, 17–18. [Google Scholar]
  15. Moudgil, A. Studies on the Prevalence and Management of Parasitic Infections in Zoo Animals. Master’s Dissertation, University of Lisbon, Lisbon, Portugal, 2015. [Google Scholar]
  16. Islam, S.; Rahman, M.K.; Uddin, M.H.; Rahman, M.M.; Chowdhury, M.N.U.; Hassan, M.M.; Magalhaes, R.S.; Islam, A. Prevalence and diversity of gastrointestinal parasites in free-ranging rhesus macaques (Macaca mulatta) in different land gradients of Bangladesh. Am. J. Primatol. 2022, 84, e23345. [Google Scholar] [CrossRef] [PubMed]
  17. Adrus, M.; Zainudin, R.; Ahamad, M.; Jayasilan, M.A.; Abdullah, M.T. Gastrointestinal parasites of zoonotic importance observed in the wild, urban, and captive populations of non-human primates in Malaysia. J. Med. Primatol. 2019, 48, 22–31. [Google Scholar] [CrossRef]
  18. Debenham, J.J.; Tysnes, K.; Khunger, S.; Robertson, L.J. Occurrence of Giardia, Cryptosporidium, and Entamoeba in wild rhesus macaques (Macaca mulatta) living in urban and semi-rural North-West India. Int. J. Parasitol. Parasites Wildl. 2017, 6, 29–34. [Google Scholar] [CrossRef]
  19. Li, J.; Cui, Z.; Li, X.; Zhang, L. Review of zoonotic amebiasis: Epidemiology, clinical signs, diagnosis, treatment, prevention and control. Res. Vet. Sci. 2021, 136, 174–181. [Google Scholar] [CrossRef]
  20. Otranto, D.; Deplazes, P. Zoonotic nematodes of wild carnivores. Int. J. Parasitol. Parasites Wildl. 2019, 9, 370–383. [Google Scholar] [CrossRef]
  21. Samad, M.A. Public health threat caused by zoonotic diseases in Bangladesh. Bangladesh J. Vet. Med. 2013, 9, 95–120. [Google Scholar] [CrossRef] [Green Version]
  22. Moshfe, A.; Mowlavi, G.; Mobedi, I.; Cheraghzade, R.; Askarian, S.; Mohammadi, R.; Nouripour, S.; Zahabioun, F.; Imani, P.; Mirsepahi, N. Fauna of zoontic parasites of stray dogs in yasouj suburbs in 2008. N. Z. Nurs. J. Kai Tiaki 2011, 75, 14. [Google Scholar]
  23. Mpofu, T.J.; Nephawe, K.A.; Mtileni, B. Prevalence of gastrointestinal parasites in communal goats from different agro-ecological zones of South Africa. Vet. World 2020, 13, 26–32. [Google Scholar] [CrossRef] [Green Version]
  24. Wobeser, G. Disease in Wild Animals: Investigation and Management; Spinger: Berlin, Germany, 2007; 393p. [Google Scholar]
  25. Macpherson, C.N. Human behaviour and the epidemiology of parasitic zoonoses. Int. J. Parasitol. 2005, 35, 1319–1331. [Google Scholar] [CrossRef] [PubMed]
  26. Bogale, B.; Chanie, M.; Melaku, A.; Fentahun, T.; Berhanu, A. Occurrence, Intensity and Parasite Composition of Gastrointestinal Helminth Parasites in Walia Ibex (Capra walie) at Semien Mountains National Park, Natural World Heritage Site, Northern Ethiopia. Acta Parasitol. Glob. 2014, 5, 19–25. [Google Scholar]
  27. Thanasuwan, S.; Piratae, S.; Tankrathok, A. Prevalence of gastrointestinal parasites in cattle in Kalasin Province, Thailand. Vet. World 2021, 14, 2091–2096. [Google Scholar] [CrossRef] [PubMed]
  28. Learmonth, M.J. Human-Animal Interactions in Zoos: What Can Compassionate Conservation, Conservation Welfare and Duty of Care Tell Us about the Ethics of Interacting, and Avoiding Unintended Consequences? Animals 2020, 10, 2037. [Google Scholar] [CrossRef] [PubMed]
  29. Hongqian, F.; Lanlan, F. A study on zoonotic taeniasis in ancient and modern times. Agric. Archaeol. 2006, 000, 248–249. [Google Scholar]
  30. Wei, M.; Feng, M.; Guan, Y.; Zhou, H.; Fu, Y.; Cai, J.; Cheng, X. Study on the genetic diversity of Entamoeba knowlesi strains infected by wild macaques in China. In Proceedings of the 16th National Academic Conference and the 7th International Symposium on Parasitology of the Professional Committee of Zoology Society of China, Jiangxi, China, 18 October 2017. [Google Scholar]
  31. Antonelli, L.; Foata, J.; Quilichini, Y.; Marchand, B. Influence of season and site location on European cultured sea bass parasites in Corsican fish farms using indicator species analysis (IndVal). Parasitol. Res. 2016, 115, 561–568. [Google Scholar] [CrossRef]
  32. Setsuda, A.; Varcasia, A.; Scala, A.; Ozawa, S.; Yokoyama, M.; Torii, H.; Suzuki, K.; Kaneshiro, Y.; Corda, A.; Dessì, G.; et al. Gongylonema infection of wild mammals in Japan and Sardinia (Italy). J. Helminthol. 2018, 94, 1–8. [Google Scholar] [CrossRef]
  33. Setsuda, A.; Da, N.; Hasegawa, H.; Behnke, J.M.; Rana, H.B.; Dhakal, I.P.; Sato, H. Intraspecific and interspecific genetic variation of Gongylonema pulchrum and two rodent Gongylonema spp. (G. aegypti and G. neoplasticum), with the proposal of G. nepalensis n. sp. for the isolate in water buffaloes from Nepal. Parasitol. Res. 2016, 115, 787–795. [Google Scholar] [CrossRef]
  34. Adkesson, M.J.; Langan, J.N.; Paul, A. Evaluation of control and treatment of Gongylonema spp. infections in callitrichids. J. Zoo Wildl. Med. Off. Publ. Am. Assoc. Zoo Vet. 2007, 38, 27–31. [Google Scholar] [CrossRef] [PubMed]
  35. Mortimer, L.; Chadee, K. The immunopathogenesis of Entamoeba histolytica. Exp. Parasitol. 2010, 126, 366–380. [Google Scholar] [CrossRef]
  36. Wang, N.; Han, M.; Qu, S.; Jiang, X.; Shi, W.; Feng, X.; Dan, J. Research progress of pathogenic amoeba vaccine. J. Jilin Med. Coll. 2019, 40, 4. [Google Scholar]
  37. Chen, Y.; Chen, B.; Xie, H.; Xie, X.; Jiang, D. Clinical characteristics and prognosis of 6 cases of histolytic amebiasis. J. Trop. Med. 2019, 19, 1285–1287. [Google Scholar]
  38. Kantor, M.; Abrantes, A.; Estevez, A.; Schiller, A.; Torrent, J.; Gascon, J.; Hernandez, R.; Ochner, C. Entamoeba Histolytica: Updates in Clinical Manifestation, Pathogenesis, and Vaccine Development. Can. J. Gastroenterol. Hepatol. 2018, 2018, 4601420. [Google Scholar] [CrossRef] [Green Version]
  39. Lejeune, M.; Rybicka, J.M.; Chadee, K. Recent discoveries in the pathogenesis and immune response toward Entamoeba histolytica. Future Microbiol. 2009, 4, 105–118. [Google Scholar] [CrossRef] [PubMed]
  40. Halliez, M.C.; Buret, A.G. Gastrointestinal Parasites and the Neural Control of Gut Functions. Front. Cell. Neurosci. 2015, 9, 452. [Google Scholar] [CrossRef]
  41. Heyneman, D. Chapter 89: Medical Microbiology. In Cestodes, 4th ed.; Baron, S., Ed.; University of Texas Medical Branch at Galveston: Galveston, TX, USA, 1996; Available online: https://www.ncbi.nlm.nih.gov/books/NBK8399/ (accessed on 13 May 2022).
  42. Wang, Z.; Liu, P.; Kuang, S.; Shu, H.; Huang, M. A case of diagnosis and prevention of Sphaerozoum fuscum occurred in Lophura nythemera. South China For. Sci. 2015, 43, 64. [Google Scholar] [CrossRef]
  43. Aziz, M.H.; Ramphul, K. Ancylostoma. In StatPearls [Internet]; StatPearls Publishing: Treasure Island, FL, USA, 2022. [Google Scholar]
  44. Ronquillo, A.C.; Puelles, L.B.; Espinoza, L.P.; Sánchez, V.A.; Luis Pinto Valdivia, J. Ancylostoma duodenale as a cause of upper gastrointestinal bleeding: A case report. Braz. J. Infect. Dis. 2019, 23, 471–473. [Google Scholar] [CrossRef]
  45. Pearson, R. Hookworm Infection. Medical Topics & Chapters. Available online: https://www.msdmanuals.com/professional/infectious-diseases/nematodes-roundworms/hookworm-infection (accessed on 18 May 2022).
  46. Hagel, I.; Giusti, T. Ascaris lumbricoides: An overview of therapeutic targets. Infect. Disord. Drug Targets 2010, 10, 349–367. [Google Scholar] [CrossRef] [Green Version]
  47. World Health Organization. Guideline: Preventive Chemotherapy to Control Soil-Transmitted Helminth Infections in At-Risk Population Groups; World Health Organization: Geneva, Switzerland, 2017. [Google Scholar]
  48. World Health Organization. Soil-Transmitted Helminth Infections. Retrieved from World Health Organization Website. Available online: https://www.who.int/news-room/fact-sheets/detail/soil-transmitted-helminth-infections (accessed on 16 November 2020).
  49. de Melo Hoshino, É.; Tavares-Dias, M. Interannual and Seasonal Variation in Protozoan and Metazoan Parasite Communities of Hemibrycon surinamensis, a Characid Fish Inhabiting the Brazilian Amazon. Acta Parasit. 2019, 64, 479–488. [Google Scholar] [CrossRef]
  50. Wharton, D.A. Parasites and low temperatures. Parasitology 1999, 119, S7–S17. [Google Scholar] [CrossRef]
  51. Viljoen, H.; Bennett, N.C.; Ueckermann, E.A.; Lutermann, H. The role of host traits, season and group size on parasite burdens in a cooperative mammal. PLoS ONE 2011, 6, e27003. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  52. Elbahy, N.M.; Elkhtam, A.O.; AbouLaila, M.; Abdelaziz, A.R. Prevalence of different flatworms infecting ruminants in Menoufia Governorate. J. Curr. Vet. Res. 2015, 9, 66–77. [Google Scholar] [CrossRef]
  53. Thompson, A.; Kutz, S. Introduction to the Special Issue on ‘Emerging Zoonoses and Wildlife’. Int. J. Parasitol. Parasites Wildl. 2019, 9, 322. [Google Scholar] [CrossRef]
  54. Rahman, M.T.; Sobur, M.A.; Islam, M.S.; Ievy, S.; Hossain, M.J.; El Zowalaty, M.E.; Rahman, A.T.; Ashour, H.M. Zoonotic Diseases: Etiology, Impact, and Control. Microorganisms 2020, 8, 1405. [Google Scholar] [CrossRef] [PubMed]
Animals 12 01816 g001 550
Figure 1. This map shows the summary of the study area (Emei Mountain scenic spot) and the geographical distribution of macaques: (1) yellow macaques group; (2) black macaques group; (3) new macaques group; (4) Leidongping macaques group; (5) Wuxiangang macaques group.
Figure 1. This map shows the summary of the study area (Emei Mountain scenic spot) and the geographical distribution of macaques: (1) yellow macaques group; (2) black macaques group; (3) new macaques group; (4) Leidongping macaques group; (5) Wuxiangang macaques group.
Animals 12 01816 g001
Animals 12 01816 g002 550
Figure 2. Gastrointestinal parasite presents in fecal samples of macaques. (a) Ascaris eggs; (b) trematoda eggs; (c) enterobius eggs; (d) physaloptera eggs; (e) ancylostoma duodenale eggs spp.; (f) cestoda egg.
Figure 2. Gastrointestinal parasite presents in fecal samples of macaques. (a) Ascaris eggs; (b) trematoda eggs; (c) enterobius eggs; (d) physaloptera eggs; (e) ancylostoma duodenale eggs spp.; (f) cestoda egg.
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Animals 12 01816 g003 550
Figure 3. Correlation between the contact frequency and total intestinal parasite prevalence rate.
Figure 3. Correlation between the contact frequency and total intestinal parasite prevalence rate.
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Animals 12 01816 g004 550
Figure 4. Correlation between the contact frequency and seasonal intestinal parasite prevalence.
Figure 4. Correlation between the contact frequency and seasonal intestinal parasite prevalence.
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Table
Table 1. Population of monkeys during the four seasons.
Table 1. Population of monkeys during the four seasons.
Population
Season		Yellow Macaque Group in the Ecological AreaBlack Macaque Group in the Ecological AreaNew Macaque in the Ecological AreaLeidongping MacaqueWuxiangang MacaqueTotal
Spring9479231
Summer1491617258
Autumn5369023
Winter332822056
Total311957574168
Table
Table 2. Contact frequency of different groups of macaques with humans.
Table 2. Contact frequency of different groups of macaques with humans.
MonkeysNumber of SamplesHaunt Time Every Day
(h)		Haunt LocationDaily Exposure Time
(n)		Contact Frequency
(n/h)
Yellow macaque312.6Near Qingyin Pavilion16.16.2
Black macaque192.9Suspension bridge in ecological area16.45.7
New macaque573.2Sandaoqiao, suspension bridge in ecological area14.14.4
Leidongping macaque576.1Leidongping stand19.53.2
Wuxiangang macaque40.6Wuxiangang station0.30.5
Table
Table 3. Total prevalence rate of the intestinal parasites in macaques.
Table 3. Total prevalence rate of the intestinal parasites in macaques.
PopulationYellow Macaque Group in the Ecological Area (n = 31)Black Macaque Group in the Ecological Area
(n = 19)		New Macaque in the Ecological Area (n = 57)Leidongping
Macaque
(n = 57)		Wuxiangang
Macaque
(n = 4)		Total
(n = 168)
ParasitesDN
(n)		PR
(%)		DN
(n)		PR
(%)		DN
(n)		PR
(%)		DN
(n)		PR
(%)		DN
(n)		PR
(%)		DN
(n)		PR
(%)
Ascaris lumbricoides26.450023.51000021.19
Entamoeba spp.1238.71736.8458.77712.28003118.45
Blastocysistis spp.0015.2635.26000052.98
Enterobius vermicularis00000011.750010.60
Trematoda spp.0015.2623.5111.750042.38
Cestoda spp.516.130011.7523.510074.17
Gongylonema spp.1341.941263.16610.561322.811254526.79
Ancylostoma duodenale0015.2635.2623.510063.57
Physaloptera spp.000011.7523.510031.79
Balantidium coli13.2315.2600000021.19
Sphaerozoum fuscum825.8115.26712.2858.771252414.29
Total2580.651789.472035.092340.351258651.19
DN—Detection number, PR—Prevalence rate.
Table
Table 4. Prevalence of intestinal parasites during different seasons.
Table 4. Prevalence of intestinal parasites during different seasons.
Season/Population
Parasites		Spring (n = 31)Summer (n = 58)Autumn (n = 23)Winter (n = 56)Total (n = 168)
DN
(n)		PR
(%)		DN
(n)		PR
(%)		DN
(n)		PR
(n)		DN
(n)		PR
(%)		DN
(n)		PR
(%)
Ascaris lumbricoides13.2311.7214.3511.7942.38
Entamoeba spp.003153.4500003118.45
Blastocysistis spp.0046.90000042.38
Enterobius vermicularis000014.350010.60
Trematoda spp.0011.72313.040044.76
Cestoda spp.13.2346.90313.040084.17
Gongylonema spp.1548.381831.03939.1335.364526.79
Ancylostoma duodenale0058.6214.350063.57
Physaloptera spp.0035.17000031.79
Balantidium coli13.2311.72000021.19
Sphaerozoum fuscum412.901627.5928.70002213.10
Total1961.295086.211356.5247.148651.19
DN—Detection number, PR—prevalence rate.
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Yang, J.; Okyere, S.K.; Zheng, J.; Cao, B.; Hu, Y. Seasonal Prevalence of Gastrointestinal Parasites in Macaques (Macaca thibetana) at Mount Emei Scenic Area in China. Animals 2022, 12, 1816. https://doi.org/10.3390/ani12141816

AMA Style

Yang J, Okyere SK, Zheng J, Cao B, Hu Y. Seasonal Prevalence of Gastrointestinal Parasites in Macaques (Macaca thibetana) at Mount Emei Scenic Area in China. Animals. 2022; 12(14):1816. https://doi.org/10.3390/ani12141816

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Yang, Jiandong, Samuel Kumi Okyere, Jie Zheng, Buyuan Cao, and Yanchun Hu. 2022. "Seasonal Prevalence of Gastrointestinal Parasites in Macaques (Macaca thibetana) at Mount Emei Scenic Area in China" Animals 12, no. 14: 1816. https://doi.org/10.3390/ani12141816

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