Review
Comprehensive molecular epidemiology of Cryptosporidium species in Japan

https://doi.org/10.1016/j.parint.2024.102909Get rights and content

Highlights

  • •
    Cryptosporidium species in Japan, especially C. parvum IIa, show zoonotic risks, highlighting the need to study human-animal links.
  • •
    Water may spread Cryptosporidium spp. in Japan; research shows various species.
  • •
    Investigating water infection routes is crucial.

Abstract

Cryptosporidium species, causing diarrheal illnesses in humans and animals worldwide, are under investigation for their molecular epidemiology in Japan. The study focuses on detecting Cryptosporidium species in humans, animals, water, and the environment, revealing three species in people: C. parvum, C. meleagridis, and C. hominis. Subtype IIa of the C. parvum gp60 gene is prevalent, indicating potential zoonotic transmission. Animal studies identified sixteen species, mainly cattle and pets, with C. parvum (subtype IIa) common in cattle and C. canis and C. felis prevalent in pets. Additionally, C. bovis and C. ryanae were found in cattle and sika deer. Knowledge gaps exist, particularly in water and environmental source typing, with limited research revealing five species and five genotypes, suggesting a significant role of water in transmission. Further research is needed to understand the molecular diversity and transmission dynamics across humans, animals, water, and the environment in Japan.

Introduction

Diarrheal diseases are a prominent cause of death worldwide, especially among children under the age of five. According to recent research in human populations, young children in poor nations, cryptosporidiosis ranks as the second most important cause of moderate-to-severe diarrhea [1]. Cryptosporidium species are ubiquitous protozoan parasites known to cause diarrheal illness in humans and a wide range of animals [2]. In recent years, there has been growing recognition of the importance of molecular epidemiology in understanding the transmission dynamics and genetic diversity of Cryptosporidium [3]. While considerable research has been conducted on Cryptosporidium epidemiology globally, there remains a need for focused investigations within specific geographic regions to elucidate local patterns of transmission [4]. Many studies have documented the burden of diarrheal diseases, which accounted for 1.6 million recorded fatalities in 2017 [5].
Japan, a country known for its advanced healthcare system and meticulous surveillance, has not escaped the clutches of Cryptosporidium. Despite its advanced sanitation systems and stringent water quality regulations, Cryptosporidium infections continue to pose a public health concern in Japan, particularly among vulnerable populations such as children and immunocompromised individuals.
Animals are also prone to cryptosporidiosis. In young ruminants in particular, severe diarrhea and mortality from Cryptosporidium spp. can result in large financial losses [6]. Furthermore, the integration of molecular epidemiology with traditional epidemiological methods has enhanced our ability to track Cryptosporidium outbreaks and identify high-risk populations in Japan. The predominant Cryptosporidium species responsible for human infections in Japan include C. hominis and C. parvum, consistent with global trends [7].
However, the emergence of novel species and genotypes, such as C. cuniculus and C. meleagridis, highlights the dynamic nature of Cryptosporidium transmission within the region [7]. Zoonotic transmission from domestic and wild animal reservoirs further complicates the epidemiological landscape, emphasizing the need for a multidisciplinary approach to understanding Cryptosporidium epidemiology in Japan. Numerous Cryptosporidium species, including C. parvum, C. meleagridis, C. canis, C. felis, and C. ubiquitum, are zoonotic, causing illnesses that infect humans through animal contact, waterborne transmission, and foodborne transmission [3,8]. These species can cause human infections with cryptosporidiosis.
In this review, we aim to provide a comprehensive overview of the molecular epidemiology of Cryptosporidium species in Japan, by integrating findings from diverse studies and identifying research priorities, we seek to contribute to developing targeted interventions to mitigate the burden of cryptosporidiosis in Japan and beyond.

Section snippets

Study overview

For this review, various electronic resources were used, such as Google Scholar, ResearchGate, PubMed, ScienceDirect, Scopus, and pertinent articles from local newspapers. The data sources included publications from 1986 to 2023 that dealt with the detection of Cryptosporidium spp. in water and environmental samples from Japan. Microscopy is the standard approach used to identify these parasites; however, it does not distinguish between species or subtypes. We therefore also included studies

Diagnostic tools used to detect Cryptosporidium species in Japan

In Japan, oocysts in fecal samples are routinely identified visually using PCR and microscopy to diagnose Cryptosporidium species. In addition, molecular biological techniques such as immunochromatographic testing, nested PCR, polymerase chain reaction (PCR), and enzyme-linked immunosorbent assay (ELISA) are used. Microscopic diagnosis is less expensive but also less accurate and time-consuming. But there are also differences in the specificity and sensitivity of the immunological tests used to

Discussion

Research into Cryptosporidium has made significant strides in Japan, yet certain obstacles remain. Most investigations have relied on established molecular diagnostic methods, such as gp60-based PCR sequencing for subtyping in prevalence studies and SSU rRNA, COWP, HSP70 tools for species identification. Topics of investigation that require attention include alterations in the prevalence and epidemiology of cryptosporidiosis in humans, the impact of concentrated animal feeding operations on

Conclusion

This review underscores the significant genetic diversity of Cryptosporidium species prevalent among humans, animals, water sources, and the environment in Japan. Managing the zoonotic transmission of Cryptosporidium spp. in Japan is challenging due to local human practices closely linked with animals as a sustainable food supply. Implementing better disease prevention and control strategies for livestock is imperative to minimize environmental contamination and safeguard the health of humans

CRediT authorship contribution statement

Mohammad Hazzaz Bin Kabir: Writing – original draft, Resources, Funding acquisition, Formal analysis, Data curation, Conceptualization. Kentaro Kato: Writing – review & editing, Supervision, Resources, Funding acquisition, Conceptualization.

Declaration of competing interest

The authors declare that they have no financial or personal conflicts that could negatively influence their contributions to this study.

Acknowledgements

This study was supported by Grants-in-Aid for the Japan Society for the Promotion of Science (JSPS) Fellows (ID No. P21101; JSPS/OF498), and Scientific Research (B) from the Ministry of Education, Culture, Science, Sports, and Technology (MEXT) of Japan, and by a Livestock Promotional Subsidy from the Japan Racing Association.

References (165)

  • Y. Koyama et al.

    Isolation of Cryptosporidium andersoni Kawatabi type in a slaughterhouse in the northern island of Japan

    Vet. Parasitol.

    (2005)
  • R. Fayer et al.

    Prevalence of Cryptosporidium species and genotypes in mature dairy cattle on farms in eastern United States compared with younger cattle from the same locations

    Vet. Parasitol.

    (2007)
  • M. Santín et al.

    A longitudinal study of cryptosporidiosis in dairy cattle from birth to 2 years of age

    Vet. Parasitol.

    (2008)
  • M. Ikarashi et al.

    First description of heterogeneity in 18S rRNA genes in the haploid genome of Cryptosporidium andersoni Kawatabi type

    Vet. Parasitol.

    (2013)
  • M. Matsubayashi et al.

    Genetical survey of novel type of Cryptosporidium andersoni in cattle in Japan

    Vet. Parasitol.

    (2008)
  • S. Nagano et al.

    Detection of a mixed infection of a novel Cryptosporidium andersoni and its subgenotype in Japanese cattle

    Vet. Parasitol.

    (2007)
  • M. Matsubayashi et al.

    Infectivity of a novel type of Cryptosporidium andersoni to laboratory mice

    Vet. Parasitol.

    (2005)
  • S. Nagano-Koyashiki et al.

    Infectivity of Cryptosporidium andersoni Kawatabi type relative to the small number of oocysts in immunodeficient and immunocompetent neonatal and adult mice

    Parasitol. Int.

    (2013)
  • M. Kváč et al.

    Cryptosporidium scrofarum n. sp. (Apicomplexa: Cryptosporidiidae) in domestic pigs (Sus scrofa)

    Vet. Parasitol.

    (2013)
  • R. Fayer

    Taxonomy and species delimitation in Cryptosporidium

    Exp. Parasitol.

    (2010)
  • F. Schubnell et al.

    Occurrence, clinical involvement and zoonotic potential of endoparasites infecting swiss pigs

    Parasitol. Int.

    (2016)
  • Z. Cui et al.

    A canine model of experimental infection with Cryptosporidium canis

    Exp. Parasitol.

    (2018)
  • M. Matsubayashi et al.

    First record of Cryptosporidium infection in a raccoon dog (Nyctereutes procyonoides viverrinus)

    Vet. Parasitol.

    (2004)
  • F. Murakoshi et al.

    Detection and genotyping of Cryptosporidium spp. in large Japanese field mice, Apodemus speciosus

    Vet. Parasitol.

    (2013)
  • U. Ryan

    Cryptosporidium in birds, fish and amphibians

    Exp. Parasitol.

    (2010)
  • L. Xiao et al.

    Molecular characterization of species and genotypes of Cryptosporidium and Giardia and assessment of zoonotic transmission

    Int. J. Parasitol.

    (2008)
  • A.J. Appelbee et al.

    Giardia and Cryptosporidium in mammalian wildlife--current status and future needs

    Trends Parasitol.

    (2005)
  • R.M. Chalmers et al.

    Epidemiology of anthroponotic and zoonotic human cryptosporidiosis in England and Wales, 2004-2006

    Epidemiol. Infect.

    (2011)
  • G.A. Roth et al.

    Global, regional, and national age-sex-specific mortality for 282 causes of death in 195 countries and territories, 1980–2017: a systematic analysis for the global burden of disease study 2017

    Lancet

    (2018)
  • E.S. El-Alfy et al.

    Cryptosporidium species and cryptosporidiosis in Japan: a literature review and insights into the role played by animals in its transmission

    J. Vet. Med. Sci.

    (2020)
  • N. Abe et al.

    Subgenotype analysis of Cryptosporidium parvum isolates from humans and animals in Japan using the 60-kDa glycoprotein gene sequences

    Parasitol. Res.

    (2006)
  • G. Masuda et al.

    Cryptosporidium diarrhea developing in two Japanese adults--one in AIDS and the other in a normal host. Research group for infectious enteric diseases, Japan

    Kansenshogaku Zasshi

    (1991)
  • S. Amer et al.

    Molecular analysis of Cryptosporidium parvum HNJ-1 isolated in Japan

    J. Vet. Med.Sci.

    (2010)
  • H. Yoshida et al.

    An outbreak of cryptosporidiosis suspected to be related to contaminated food, October 2006, Sakai City, Japan

    Jpn. J. Infect. Dis.

    (2007)
  • K. Kagawa et al.

    Cryptosporidiosis in a transplant recipient with severe intractable diarrhea: detection of Cryptosporidium oocysts by intestinal biopsies

    Transpl. Infect. Dis.

    (2018)
  • N. Abe

    Genotype analysis of Cryptosporidium meleagridis isolates from humans in Japan

    Jpn. J. Infect. Dis.

    (2010)
  • Y. Asano et al.

    An outbreak of gastroenteritis associated with Cryptosporidium meleagridis among high school students of dormitory in Ehime, Japan

    Annual Report of Ehime Prefecture Institute of Public Health and Environmental Science.

    (2006)
  • K. Yagita et al.

    Molecular characterization of Cryptosporidium isolates obtained from human and bovine infections in Japan

    Parasitol. Res.

    (2001)
  • T. Endo et al.

    What is learned from cryptosporidiosis outbreak cases in Japan, proceedings of the 3rd Japan-U.S. governmental conference on drinking water quality management and wastewater control

    (2004)
  • T. Kuroki et al.

    An outbreak of waterborne cryptosporidiosis in Kanagawa, Japan

    Kansenshogaku Zasshi

    (1996)
  • N. Yamamoto et al.

    Outbreak of cryptosporidiosis after contamination of the public water supply in Saitama prefecture, Japan, in 1996

    Kansenshogaku Zasshi

    (2000)
  • T. Yamazaki et al.

    Clinical features of Japanese children infected with Cryptosporidium parvum during a massive outbreak caused by contaminated water supply

    Kansenshogaku Zasshi

    (1997)
  • S. Ichinohe et al.

    Secondary transmission of cryptosporidiosis associated with swimming pool use

    Jpn. J. Infect. Dis.

    (2005)
  • M. Takagi et al.

    An outbreak of cryptosporidiosis associated with swimming pools

    Kansenshogaku Zasshi

    (2008)
  • H. Yokoi et al.

    Cryptosporidium outbreak in a sports center

    Jpn. J. Infect. Dis.

    (2005)
  • N. Abe et al.

    An imported case of mixed infection by Giardia and Cryptosporidium parasites in Japan

    Seikatsu Eisei.

    (2005)
  • Y. Masago et al.

    Genotyping of Cryptosporidium spp. in water by denaturing gradient gel electrophoresis (DGGE)

    Environ. Eng. Res.

    (2005)
  • Y. Masago et al.

    Quantification and genotyping of Cryptosporidium spp. in river water by quenching probe PCR and denaturing gradient gel electrophoresis

    Water Sci. Technol.

    (2006)
  • K. Ono et al.

    Contamination of river water by Cryptosporidium parvum oocysts in western Japan

    Appl. Environ. Microbiol.

    (2001)
  • N. Abe et al.

    Multilocus genotypic analysis of Cryptosporidium isolates from cockatiels, Japan

    Parasitol. Res.

    (2010)
    • View full text
    © 2024 Elsevier B.V. All rights are reserved, including those for text and data mining, AI training, and similar technologies.