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«Molecular identification and epidemiological characterization of cryptosporidiosis and fasciolosis in central Vietnam ...»

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TOHOKU LABORATORY OF SUSTAINABLE

UNIVERSITY ENVIRONMENTAL BIOLOGY

Molecular identification

and epidemiological characterization of

cryptosporidiosis and fasciolosis in central Vietnam

(ベトナム中部におけるクリプトスポリジウム症および肝蛭症の分子疫学的研究)

Nguyen Thi Sam

Dissertation submitted in fulfillment of the requirements for the degree of Doctor (PhD) in Agricultural Sciences, 2013

Advisors:

Prof. Dr. Yutaka Nakai Dr. Nguyen Duc Tan Laboratory of Sustainable Environmental Biology Naruko-Onsen, Osaki, Miyagi 989-6711 Tohoku University, Japan 1 Acknowledgements I would like to express my gratitude to Japanese Government through the JSPS (Japan Society for the Promotion of Science) for the financial support during my study in Japan. After 5 years implementation, the thesis has been completed by contribution of many people who I would like to express my deep gratitude to all of them.

First of all, I would like manifest my gratitude sincerely and deeply to Prof. Dr.

Yutaka Nakai, my Japanese Advisor, who not only has conducted me in study, in scientific research, in writing thesis but also has great encouragement as giving me more power to accomplish my study by the heart of a big teacher.

I would like to express my deep and sincere gratitude to Dr. Nguyen Duc Tan, my Vietnamese Advisor, for his supervision and useful suggestions, which made the completion of this work possible.

I also wish to express my sincere thanks to Assistance Professor Yasuhiro Fukuda and Associate Professor Chika Tada, whose strong supports and kind helps are very important to the completion of my study.

I would also like to thank to all my colleagues in Central Vietnam Veterinary Institute (CVVI), Nha Trang, Vietnam for their supports and sharing experiences, and encouragement to me.

As the same way, I would like to thank to all staff members at the Laboratory of Sustainable Environmental Biology, Tohoku University, Japan, for their assistance and encouragement to me.

I wish to thank summer students of Faculty of Veterinary Medicine, Tay Nguyen University, Dak Lak province, for their help in sample collection.

My appreciation would not be completed without expressing my gratitude to my husband Tran Thanh Quang, my daughters Tran Thanh Tam and Tran Thanh Mai, my parents, my brother and sisters, who have stood by me during this period, thank you very much.

2 Contents List of abbreviations……………………………………...5 General introduction……………………………………..6 Objectives………………………………………………..12 Chapter 1………………………………………………...14 Prevalence and molecular characterization of Cryptosporidium in native beef calves in central Vietnam Chapter 2………………………………………………...30 Prevalence, risk factors and molecular characterization of Cryptosporidium in pigs in central Vietnam Part 1…………………………………………………..30 Prevalence and risk factors associated with Cryptosporidium oocyst shedding in pigs in central Vietnam Part 2…………………………………………………..52 Molecular characterization of Cryptosporidium in pigs in central Vietnam Chapter 3………………………………………………...71 Prevalence and molecular characterization of Cryptosporidium in ostriches (Struthio camelus) on a farm in central Vietnam 3 Chapter 4………………………………………………...92 Prevalence and molecular identification of Fasciolosis in cattle in central Vietnam Part 1………………………………………………….92 Molecular identification of Fasciola spp. (Digenea: Platyhelminthes) in cattle from Vietnam Part 2…………………………………………………115 Prevalence of Fasciola in cattle and of its intermediate host Lymnaea snails in central Vietnam General discussion……………………………………..129 Conclusions and recommendations…………………...133

–  –  –

18S rRNA 18S ribosomal RNA AIDS Acquired immune deficiency syndrome BLAST Basic Local Alignment Search Tool bp Base pair CI Confidence interval COI Cytochrome c oxidase subunit 1 DNA Deoxyribonucleic acid ELISA Enzyme linked immunosorbent assay HIV Human immunodeficiency virus HSP-70 70 kDa heat shock protein ITS Internal transcribed spacer ME Microscopic examination mZN Modified Ziehl Neelsen NDI Nicotinamide adenine dinucleotide dehydrogenase subunit OIE Organization of International Epidemiology PCR Polymerase chain reaction RNA Ribonucleic acid US$ American dollar WHO World Health Organization

5General introduction

6 In 1907, about more than one hundred years ago, Ernest Edward Tyzzer described for the first time a protozoa that was found in the gastric glands of laboratory mice, and that was called Cryptosporidium muris (Xiao et al., 2004). He later described a second species, Cryptosporidium parvum, also from laboratory mice, but differed from the first not only by infecting the small intestine rather than the stomach, but also by smaller size (Xiao et al., 2004). However, over 50 years later the pathogenic role of Cryptosporidium had inceptively been paid attention with outbreaks of diarrhea associated with this parasite in turkeys and calves in the 1950s, 1970s. Furthermore, numerous outbreaks of human cryptosporidiosis due to contaminated food or water have been reported in several industrialized nations, such as the large waterborne cryptosporidiosis outbreak in Milwaukee in 1993 (Mac Kenzie et al., 1994). Subsequently, Cryptosporidium is increasingly recognized as an etiological agent of diarrhea in many species of vertebrates and humans. Nowadays, Cryptosporidium is determined as an protozoan parasite of small intestine, belonging to the phylum Apicomplexa (Xiao et al., 2004; Fayer, 2010). It causes cryptosporidiosis, an important parasitic disease of animals and humans.





Fasciolosis is an important parasitic zoonosis caused by the liver flukes Fasciola hepatica or Fasciola gigantica, the two recognized species in this genus. Fasciolosis is considered as the most common parasitic disease in ruminants in tropical countries, especially in southeast Asia region. The economic losses due to fasciolosis is estimated at least US$3.2 billion annually due to reducing of weight gain, draught capacity, fertility and lactation. Moreover, the disease is increasingly reported in humans, with millions of people are estimated to be infected or at the risk of infection throughout the world. Both Cryptosporidium and Fasciola gain the public concerns not only due to their high prevalence and economic significance to animal husbandry, but also to their zoonotic aspect.

Vietnam is a tropical country, located in South-East Asia region and occupies about 331.688 square kilometers. The country is divided into 64 provinces, and has 3 well-defined regions: The Northern, the Central and the Southern regions, which have different climates due to strong monsoon influences. In most regions, the high temperatures, heavy rainfall and high humidity prevail around the year. While the North 7 has four seasons separately, the Center and the South has two seasons only: the dry season begins from December to August, the rainny season begins from September to December.

Vietnam is a developing country, with more than 70% of population are living on agricultural occupations, such as planting rice and raising animals. Livestock production is an important part of agricultural economy of Vietnam, with number of domestic animals, livestock products, number of farms and livestock products with increase rate are reported in Table 1, Table 2, Table 3 and Table 4, respectively (Data obtained from www.gso.gov.vn).

–  –  –

Parasitic diseases are still common in livestock, causing significant economic losses for husbandry of Vietnam. These include fasciolosis and cryptosporidiosis, moreover, the public health impacts of these parasites have not yet been considered in Vietnam.

–  –  –

In Vietnam, studies on Cryptosporidium are very limited. Although Cryptosporidium is recognized as an ubiquitous pathogen for cattle, with estimated prevalence of 30% has been reported, the data on prevalence and genetic profiles are still spare. Likewise, little is known about cryptosporidiosis in pigs and birds in Vietnam. Thus, it is necessary to obtain more information about prevalence and genotype distribution of Cryptosporidium in domestic animals in Vietnam.

Fasciolosis is common in herbivorous animals in Vietnam, with estimated prevalences ranged between 20-90%. Fasciolosis is also an emerging zoonotic disease in Vietnam, especially in Binh Dinh, Khanh Hoa and Phu Yen provinves, central region. In 9 2011, more than 700 cases have been detected in Binh Dinh province. Several studies have shown that F. gigantica is the main cause of human and animal fasciolosis in the north of Vietnam, and Lymnaeid snails have been described as intermediate hosts of Fasciola spp. However, there is little information available on fasciolosis in cattle and snails in central Vietnam. This knowledge gap hinders our understanding of the prevalence and dynamic transmission of fasciolosis in this region. Therefore it is neccessary to investigate the prevalence of natural Fasciola infections in the definitive host (cattle) and intermediate (Lymnaea snails) hosts in these three representative provinces of central Vietnam, and thereby, to extend our understanding on the status of fasciolosis in this area. Such knowledge will be useful in the constructing of preventive and control programs for fasciolosis in Vietnam.

10

References

Fayer, R., 2010. Taxonomy and species delimitation in Cryptosporidium. Exp. Parasitol.

124: 90-97.

Mac Kenzie, W.R., Hoxie, N.J., Proctor, M.E., Gradus, M.S., Blair, K.A., Peterson, D.E., Kazmierczak, J.J., Addiss, D.G., Fox, K.R., Rose, J.B., et al., 1994. A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N. Engl. J. Med. 331: 161-167.

Xiao, L., Fayer, R., Ryan, U., Upton, S.J., 2004. Cryptosporidium taxonomy: Recent advances and implications for public health. Clin. Microbiol. Rev. 17: 72-97.

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1. To estimate the prevalence of cryptosporidiosis and fasciolosis in common domestic animals in Vietnam, using modified Ziehl-Nelseen staining method for cryptosporidiosis and coprological method for fasciolosis.

2. To identify which Cryptosporidium species/genotypes and which Fasciola spp.

harboring in domestic animals in Vietnam, using molecular genotyping tools.

3. To assess the zoonotic importance of Cryptosporidium spp. and Fasciola spp. in Vietnam, and thereby to evaluate the current situation of cryptosporidiosis and fasciolosis in domestic animals in Vietnam.

–  –  –

1 Published in: Nguyen, S.T., Fukuda, Y., Tada, C., Sato, R., Duong, B., Nguyen, D.T., Nakai, Y., 2012. Molecular characterization of Cryptosporidium in native beef calves in central Vietnam. Parasitology Research 111: 1817-1820.

14

Abstract

The aims of this study were to investigate the prevalence of Cryptosporidium and to characterize the genotype distribution of Cryptosporidium isolates in native beef calves 2-6 months old in Dak Lak province, central Vietnam. The presence of Cryptosporidium oocysts was determined using the modified Ziehl-Neelsen (mZN) staining method. The overall prevalence on the sample and herd levels were 18.9% (44/232) and 50% (20/40), respectively. Genotyping based on PCR and sequence analysis of the 18S rRNA gene revealed occurrence of the two non-zoonotic species Cryptosporidium ryanae and C.

bovis, with the former as a dominant species in the animals. The absence of the zoonotic species C. parvum in calves examined suggests that the native beef calves 2-6 months old in the study area are unlikely to contribute to human cryptosporidiosis transmission.

15

Introduction

Cryptosporidiosis caused by the apicomplexan protozoa Cryptosporidium is increasingly recognized as an important gastrointestinal infection in livestocks and humans (Xiao et al., 2004). The disease is transmitted by ingestion of Cryptosporidium oocysts, either directly via the fecal-oral route, or indirectly through contaminated food or drinking water (Fayer, 2010). In immunocompetent individuals, the disease causes a selflimiting infection, but it leads persistent or recurrent infection for neonates and immunocompromised ones, particularly those with AIDS (Fayer, 2010).

Of more than 20 recognized Cryptosporidium species (Xiao, 2010; Fayer, 2010), following four species: C. parvum, C. bovis, C. ryanae, and C. andersoni are frequently detected from cattle. Recent studies in dairy cattle conducted in industrialized nations have shown that the intestinal species C. parvum, ascribed to caused sporadic cases and outbreaks of diarrhea in cattle and humans, is considered most pathogenic, while the intestinal species C. bovis, C. ryanae and the abomasum species C. andersoni are less pathogenic (Xiao, 2010). The species of Cryptosporidium found in dairy cattle are agespecific, with C. parvum predominates in pre-weaned calves, C. bovis and C. ryanae are mostly found in post-weaned calves, and C. andersoni is primarily detected in adult cattle (Santin et al., 2004; Fayer et al., 2006). Thus far, most studies on the epidemiology of Cryptosporidium in cattle have been done with dairy breeds in industrialized nations.

There have only been a few studies on the molecular characterization of Cryptosporidium in dairy cattle, and fewer such studies in native beef cattle from developing countries (Xiao, 2010; Fayer et al., 2010; Feng et al., 2012). Cryptosporidiosis appears to be a neglected disease in developing countries, especialy in Asian countries (Xiao, 2010).

In Vietnam, Cryptosporidium is known as a ubiquitous pathogen for cattle (Nguyen et al., 2007) and pigs (Nguyen et al., 2012). In 2007, C. parvum and C.



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