Water buffalo as sentinel animals for schistosomiasis surveillance

Jose Ma M Angeles Lydia R Leonardo Yasuyuki Goto Masashi Kirinoki Elena A Villacorte Hassan Hakimi Kharleezelle J Moendeg Seungyeon Lee Pilarita T Rivera Noboru Inoue Yuichi Chigusa Shin-ichiro Kawazu About the authors

Introduction

About 75% of human pathogens are zoonotic, meaning that they are communicated from animals to humans.11.  Slingenbergh JI, Gilbert M, de Balogh KI, Wint W. Ecological sources of zoonotic diseases. Rev Sci Tech. 2004 Aug;23(2):467-84. PMID:15702714 Schistosomiasis is a zoonotic disease with a complex transmission cycle involving aquatic snails and least 40 species of mammals, which serve as reservoir hosts. Worldwide, more than 700 million people are at risk of schistosomiasis and over 240 million people are infected with the parasite.22.  Schistosomiasis [Internet]. Geneva: World Health Organization; 2014. Available from: Available from: http://www.who.int/schistosomiasis/en/ [cited 2015 April 27].
http://www.who.int/schistosomiasis/en/...
Schistosomiasis has been eliminated in Japan and the coastal plains of China by a combination of medical treatment, health education, improved water quality and sanitation and snail control through environmental modification, molluscicide and new farming methods. The World Health Organization (WHO) targets elimination of schistosomiasis in the Eastern Mediterranean, the Caribbean, Indonesia and the Mekong river basin by 2015, and in the Western Pacific, the Americas and selected African countries by 2020.33.  Accelerating work to overcome the global impact of neglected tropical diseases; a roadmap for implementation.; Geneva: World Health Organization 2012. Available from: Available from: http://www.who.int/neglected_diseases/NTD_RoadMap_2012_Fullversion.pdf [cited 2015 April 27].
http://www.who.int/neglected_diseases/NT...
Here we argue that elimination guidelines for schistosomiasis should include surveillance of the animal reservoir.

Transmission patterns

Mapping of the transmission patterns in humans and animals can lead to a better understanding of transmission of schistosomiasis between different host species. Parts of China, Indonesia and the Philippines are endemic for schistosomiasis caused by Schistosoma japonicum. Cattle, water buffalo, goats, dogs, pigs and rats are potentially important reservoir hosts for this parasite because of their contact with humans. Other animals including cats and horses are not significant contributors because of their limited contact with contaminated water.44.  Wang TP, Vang Johansen M, Zhang SQ, Wang FF, Wu WD, Zhang GH, et al. Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui province, China. Acta Trop. 2005 Nov-Dec;96(2-3):198-204. http://dx.doi.org/10.1016/j.actatropica.2005.07.017PMID:16188215
http://dx.doi.org/10.1016/j.actatropica....

Grazing ruminants including goats, cattle and water buffalo are exposed to the parasite in transmission sites such as rice paddies. However, goats do not contribute much to transmission as they are uncommon in areas where schistosomiasis is endemic. Cattle and water buffalo are the major animal reservoirs contributing to human transmission of S. japonicum.44.  Wang TP, Vang Johansen M, Zhang SQ, Wang FF, Wu WD, Zhang GH, et al. Transmission of Schistosoma japonicum by humans and domestic animals in the Yangtze River valley, Anhui province, China. Acta Trop. 2005 Nov-Dec;96(2-3):198-204. http://dx.doi.org/10.1016/j.actatropica.2005.07.017PMID:16188215
http://dx.doi.org/10.1016/j.actatropica....
77. , Wang TP Shrivastava J, Johansen MV, Zhang SQ, Wang FF, Webster JP. Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. Int J Parasitol. 2006 Oct;36(12):1317-25. http://dx.doi.org/10.1016/j.ijpara.2006.06.011PMID:16876170
http://dx.doi.org/10.1016/j.ijpara.2006....
In China, bovine defecation is thought to be the main cause of environmental contamination.66.  Jiang Z, Zheng QS, Wang XF, Hua ZH. Influence of livestock husbandry on schistosomiasis transmission in mountainous regions of Yunnan Province. Southeast Asian J Trop Med Public Health. 1997 Jun;28(2):291-5. PMID:9444008Molecular studies have also suggested that transmission is through bovines rather than other domesticated animals.77. , Wang TP Shrivastava J, Johansen MV, Zhang SQ, Wang FF, Webster JP. Does multiple hosts mean multiple parasites? Population genetic structure of Schistosoma japonicum between definitive host species. Int J Parasitol. 2006 Oct;36(12):1317-25. http://dx.doi.org/10.1016/j.ijpara.2006.06.011PMID:16876170
http://dx.doi.org/10.1016/j.ijpara.2006....
Cattle are less capable of recovering from infection than water buffalo.88.  Yang J, Fu Z, Feng X, Shi Y, Yuan C, Liu J, et al. Comparison of worm development and host immune responses in natural hosts of Schistosoma japonicum, yellow cattle and water buffalo. BMC Vet Res. 2012;8(1):25. http://dx.doi.org/10.1186/1746-6148-8-25PMID:22414188
http://dx.doi.org/10.1186/1746-6148-8-25...
Despite the fact that buffalo are capable of clearing the parasite, they are a major reservoir host because they are repeatedly exposed to the parasite when pulling ploughs in rice paddies.99.  Li YS, McManus DP, Lin DD, Williams GM, Harn DA, Ross AG, et al. The Schistosoma japonicum self-cure phenomenon in water buffaloes: potential impact on the control and elimination of schistosomiasis in China.. Int J Parasitol 2014 Mar;44(3-4):167-71. http://dx.doi.org/10.1016/j.ijpara.2013.10.007PMID:24440417
http://dx.doi.org/10.1016/j.ijpara.2013....

In rice-growing regions, water buffalo are a good choice of sentinel animal. In Anhui and Sichuan provinces of China, re-emergence of schistosomiasis in humans was attributed to the high prevalence of schistosome infection among cows and water buffalo.1010.  Lu DB, Wang TP, Rudge JW, Donnelly CA, Fang GR,. Webster JP Contrasting reservoirs for Schistosoma japonicum between marshland and hilly regions in Anhui, China-a two-year longitudinal parasitological survey. Parasitology. 2010 Jan;137(1):99-110. http://dx.doi.org/10.1017/S003118200999103XPMID:19723358
http://dx.doi.org/10.1017/S0031182009991...
1111.  Carlton EJ, Bates MN, Zhong B, Seto EYW, Spear RC. Evaluation of mammalian and intermediate host surveillance methods for detecting schistosomiasis reemergence in southwest China. PLoS Negl Trop Dis. 2011;5(3):e987. http://dx.doi.org/10.1371/journal.pntd.0000987PMID:21408127
http://dx.doi.org/10.1371/journal.pntd.0...
These human infections could be avoided by setting up a sensitive animal surveillance system to detect infection in animals and, by treating them promptly, preventing further contamination of the environment.

Diagnostic tests

Microscopic examination of stool samples is a standard test for several parasitic diseases, including schistosomiasis. However, microscopy has low sensitivity in diagnosing schistosomiasis among water buffalo due to the large volume of bovine excreta. Therefore, a more sensitive and specific diagnostic test is needed to identify schistosomiasis-free areas and prevent re-emergence of the disease. In previous studies, polymerase chain reaction (PCR)1212.  Wu HW, Qin YF, Chu K, Meng R, Liu Y, McGarvey ST, et al. High prevalence of Schistosoma japonicum infection in water buffaloes in the Philippines assessed by real-time polymerase chain reaction. Am J Trop Med Hyg. 2010 Apr;82(4):646-52. http://dx.doi.org/10.4269/ajtmh.2010.09-0638PMID:20348514
http://dx.doi.org/10.4269/ajtmh.2010.09-...
and recombinant antigen-based enzyme-linked immunosorbent assay (ELISA)1313.  Angeles JM, Goto Y, Kirinoki M, Asada M, Leonardo LR, Rivera PT, et al. Utilization of ELISA using thioredoxin peroxidase-1 and tandem repeat proteins for diagnosis of Schistosoma japonicum infection among water buffaloes.. PLoS Negl Trop Dis 2012;6(8):e1800. http://dx.doi.org/10.1371/journal.pntd.0001800PMID:22953018
http://dx.doi.org/10.1371/journal.pntd.0...
have been found to be useful in identifying S. japonicumin stool samples. Surveillance can also be carried out in abattoirs where cattle and buffalo are slaughtered. Documentation of the original source of livestock then allows schistosome-infested sites to be located.

Medical and veterinary approaches

The complexity of zoonotic schistosomiasis transmission has been a major hindrance to elimination of the disease. Definitive, intermediate and reservoir host factors as well as social and environmental influences should all be considered in the control of this disease. An integrated approach with the cooperation of human and animal health agencies will improve the chances of success.1414.  Zinsstag J, Schelling E, Wyss K, Mahamat MB. Potential of cooperation between human and animal health to strengthen health systems. Lancet. 2005 Dec 17;366(9503):2142-5. http://dx.doi.org/10.1016/S0140-6736(05)67731-8PMID:16360795
http://dx.doi.org/10.1016/S0140-6736(05)...

Current control strategies for schistosomiasis include mass drug administration and health education of human hosts. Japan eliminated schistosomiasis before praziquantel was available through snail control measures including molluscicides, construction of cement ditches and land reclamation. However due to the toxicity of molluscicides and the variety of habitats occupied by intermediate host snails, large-scale snail control is not safe or practical. Disease control in the animal reservoir has also been shown to be cost-effective in other zoonotic diseases, including brucellosis1515.  Roth F, Zinsstag J, Orkhon D, Chimed-Ochir G, Hutton G, Cosivi O, et al. Human health benefits from livestock vaccination for brucellosis: case study. Bull World Health Organ. 2003;81(12):867-76. PMID:14997239 and rabies.1616.  Zinsstag J, Dürr S, Penny MA, Mindekem R, Roth F, Gonzalez SM, et al. Transmission dynamics and economics of rabies control in dogs and humans in an African city. Proc Natl Acad Sci USA. 2009 Sep 1;106(35):14996-5001. http://dx.doi.org/10.1073/pnas.0904740106PMID:19706492
http://dx.doi.org/10.1073/pnas.090474010...

In working towards the elimination of schistosomiasis, selective treatment or isolation of infected animals may be the most practical approach. Providing toilets and health education to reduce open defecation by humans would also reduce the risk of infection for both humans and animals. Veterinarians and public health professionals need to work together in the battle against zoonotic schistosomiasis.

References

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    Zinsstag J, Dürr S, Penny MA, Mindekem R, Roth F, Gonzalez SM, et al. Transmission dynamics and economics of rabies control in dogs and humans in an African city. Proc Natl Acad Sci USA. 2009 Sep 1;106(35):14996-5001. http://dx.doi.org/10.1073/pnas.0904740106PMID:19706492
    » http://dx.doi.org/10.1073/pnas.0904740106

Publication Dates

  • Publication in this collection
    July 2015

History

  • Received
    18 June 2014
  • Reviewed
    14 Jan 2015
  • Accepted
    23 Jan 2015
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