Microsporidia - Emergent Pathogens in the Global Food Chain

G D Stentiford¹, -J J Becnel², L M Weiss³, P J Keeling⁴, E S Didier⁵, B-A P Williams⁶, S Bjornson⁷, M-L Kent⁸, M A Freeman⁹, M J F Brown¹⁰, E-R Troemel¹¹, K Roesel¹², Y Sokolova¹³, K F Snowden¹⁴, L Solter¹⁵

Affiliations

¹ Pathology and Molecular Systematics Team, Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Barrack Road, Weymouth, Dorset DT4 8UB, UK.
² United States Department of Agriculture (USDA) Agricultural Research Center (ARS), Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), 1600 South West 23rd Drive, Gainesville, FL, 32608, USA.
³ Albert Einstein College of Medicine, 1300 Morris Park Avenue, Forchheimer 504, Bronx, NY 10641, USA.
⁴ Canadian Institute for Advanced Research, Botany Department, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, V6T 1Z4 Canada.
⁵ Division of Microbiology, Tulane National Primate Research Center and Department of Tropical Medicine, School of Public Health and Tropical Medicine, Tulane University, 1440 Canal Street, New Orleans, LA 70112, USA.
⁶ Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope, Stocker Road, Exeter EX4 4QD, UK.
⁷ Department of Biology, Saint Mary's University, 923 Robie Street, Halifax, Nova Scotia, Canada.
⁸ Departments of Microbiology and Biomedical Sciences, 220 Nash Hall, Oregon State University, Corvallis, OR 97331, USA.
⁹ Ross University School of Veterinary Medicine, St. Kitts, West Indies.
¹⁰ School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK.
¹¹ University of California, San Diego, 4202 Bonner Hall, 9500 Gilman Drive #0349, La Jolla, CA 92093-0349, USA.
¹² International Livestock Research Institute, c/o Freie Universität Berlin, Institute of Parasitology and Tropical Veterinary Medicine, Robert-von-Ostertag-Strasse 7-13, Berlin, 14163 Germany.
¹³ Department of Comparative Biomedical Sciences, Louisiana State University, School of Veterinary Medicine, 1909 Skip Bertman Drive, Baton RougeLA 70803, USA.
¹⁴ Texas A&M University, College of Veterinary Medicine and Biomedical Sciences, Department of Veterinary Pathobiology, Mailstop 4467, College Station, TX 77843-4467, USA.
¹⁵ Illinois Natural History Survey, Prairie Research Institute at the University of Illinois at Urbana-Champaign, 1816 South Oak Street, Champaign, IL 61820, USA. Electronic address: lsolter@illinois.edu.

PMID: 26796229
PMCID: PMC4818719
DOI: 10.1016/j.pt.2015.12.004

Review

Microsporidia - Emergent Pathogens in the Global Food Chain

G D Stentiford et al. Trends Parasitol. 2016 Apr.

. 2016 Apr;32(4):336-348.

doi: 10.1016/j.pt.2015.12.004. Epub 2016 Jan 19.

Authors

Affiliations

¹ Pathology and Molecular Systematics Team, Centre for Environment, Fisheries and Aquaculture Science (CEFAS), Barrack Road, Weymouth, Dorset DT4 8UB, UK.
² United States Department of Agriculture (USDA) Agricultural Research Center (ARS), Center for Medical, Agricultural, and Veterinary Entomology (CMAVE), 1600 South West 23rd Drive, Gainesville, FL, 32608, USA.
³ Albert Einstein College of Medicine, 1300 Morris Park Avenue, Forchheimer 504, Bronx, NY 10641, USA.
⁴ Canadian Institute for Advanced Research, Botany Department, University of British Columbia, 3529-6270 University Boulevard, Vancouver, BC, V6T 1Z4 Canada.
⁵ Division of Microbiology, Tulane National Primate Research Center and Department of Tropical Medicine, School of Public Health and Tropical Medicine, Tulane University, 1440 Canal Street, New Orleans, LA 70112, USA.
⁶ Biosciences, College of Life and Environmental Sciences, University of Exeter, Geoffrey Pope, Stocker Road, Exeter EX4 4QD, UK.
⁷ Department of Biology, Saint Mary's University, 923 Robie Street, Halifax, Nova Scotia, Canada.
⁸ Departments of Microbiology and Biomedical Sciences, 220 Nash Hall, Oregon State University, Corvallis, OR 97331, USA.
⁹ Ross University School of Veterinary Medicine, St. Kitts, West Indies.
¹⁰ School of Biological Sciences, Royal Holloway University of London, Egham, Surrey, TW20 0EX, UK.
¹¹ University of California, San Diego, 4202 Bonner Hall, 9500 Gilman Drive #0349, La Jolla, CA 92093-0349, USA.
¹² International Livestock Research Institute, c/o Freie Universität Berlin, Institute of Parasitology and Tropical Veterinary Medicine, Robert-von-Ostertag-Strasse 7-13, Berlin, 14163 Germany.
¹³ Department of Comparative Biomedical Sciences, Louisiana State University, School of Veterinary Medicine, 1909 Skip Bertman Drive, Baton RougeLA 70803, USA.
¹⁴ Texas A&M University, College of Veterinary Medicine and Biomedical Sciences, Department of Veterinary Pathobiology, Mailstop 4467, College Station, TX 77843-4467, USA.
¹⁵ Illinois Natural History Survey, Prairie Research Institute at the University of Illinois at Urbana-Champaign, 1816 South Oak Street, Champaign, IL 61820, USA. Electronic address: lsolter@illinois.edu.

PMID: 26796229
PMCID: PMC4818719
DOI: 10.1016/j.pt.2015.12.004

Erratum in

Microsporidia-Emergent Pathogens in the Global Food Chain (Trends in Parasitology 32, 336-348; April 2, 2016).
Stentiford GD, Becnel JJ, Weiss LM, Keeling PJ, Didier ES, Williams BAP, Bjornson S, Kent ML, Freeman MA, Brown MJF, Troemel ER, Roesel K, Sokolova Y, Snowden KF, Solter LF. Stentiford GD, et al. Trends Parasitol. 2016 Aug;32(8):657. doi: 10.1016/j.pt.2016.06.002. Epub 2016 Jun 27. Trends Parasitol. 2016. PMID: 27365191 No abstract available.

Abstract

Intensification of food production has the potential to drive increased disease prevalence in food plants and animals. Microsporidia are diversely distributed, opportunistic, and density-dependent parasites infecting hosts from almost all known animal taxa. They are frequent in highly managed aquatic and terrestrial hosts, many of which are vulnerable to epizootics, and all of which are crucial for the stability of the animal-human food chain. Mass rearing and changes in global climate may exacerbate disease and more efficient transmission of parasites in stressed or immune-deficient hosts. Further, human microsporidiosis appears to be adventitious and primarily associated with an increasing community of immune-deficient individuals. Taken together, strong evidence exists for an increasing prevalence of microsporidiosis in animals and humans, and for sharing of pathogens across hosts and biomes.

Keywords: aquaculture; farming; immune-suppression; intensive rearing; phylogeny; zoonotic.

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Figures

**Figure 1. Microsporidiosis in Humans**
(A) *Encephalitozoon hellem* keratoconjunctivitis. Areas of corneal damage due to microsporidiosis (arrow). (B) Corneal scraping from a case of microsporidian keratoconjunctivitis demonstrating spores (arrow) of *E. hellem*. (C) Conjunctival biopsy in a case of microsporidian keratoconjunctivitis demonstrating microsporidian spores in cross-section (arrows point to polar tubes, the infective structures). The arrangement of the polar tubes is consistent with *Encephalitozoon*. (D) Intestinal biopsy from a patient with gastrointestinal microsporidiosis and diarrhea due to *Enterocytozoon bieneusi* (arrows point to spores in the apical region of an intestinal epithelial cell). (E) Stool stained with modified trichrome stain (arrows point to spores). PCR confirmed that this infection was due to *E. bieneusi*. (F) Intestinal biopsy from a patient with gastrointestinal microsporidiosis and diarrhea due to *Encephalitozoon intestinalis*.

**Figure 2. Microsporidiosis in Shrimp Farming**
Routine health-checking of shrimp stock throughout the production cycle (A,B) and the application of sensitive and specific diagnostics for known and emergent shrimp pathogens has revealed a host-switching event and emergence of clinical disease caused by the microsporidian parasite *Enterocytozoon hepatopenaeii* in *Penaeus vannamei* from in Asia. The parasite, congeneric with the human pathogen *Enterocytozoon bieneusi*, undergoes similar development within the gut of infected shrimp and is implicated in the multi-billion dollar yield-limiting condition known as early mortality syndrome (EMS).

See this image and copyright information in PMC

References

1. Gajadhar AA, et al. Overview of food- and water-borne zoonotic parasites at the farm level. Rev. Sci. Tech. 2006;25:595–606. - PubMed
1. WHO. First formal meeting of the Foodborne Disease Burden Epidemiology Reference Group (FERG): Implementing Strategy, Setting Priorities and Assigning the Tasks. World Health Organization; 2007.
1. Doyle ME. Foodborne Parasites. A Review of the Scientific Literature. University of Wisconsin-Madison: Food Research Institute; 2003.
1. Centers For Disease Control and Prevention. CDC Estimates of Foodborne Illness in the United States. CDC: CDC 2011 Estimates: Findings; 2011.
1. MacKenzie WR, et al. A massive outbreak in Milwaukee of Cryptosporidium infection transmitted through the public water supply. N. Engl. J. Med. 1994;331:161–167. - PubMed

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Microsporidia - Emergent Pathogens in the Global Food Chain

Affiliations

Microsporidia - Emergent Pathogens in the Global Food Chain

Authors

Affiliations

Erratum in

Abstract

Figures

References

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MeSH terms

Grants and funding

LinkOut - more resources

Full Text Sources

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