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The global molecular epidemiology of microsporidia infection in sheep and goats with focus on Enterocytozoon bieneusi: a systematic review and meta-analysis

Abstract

Background

Microsporidia is a zoonotic pathogen with health consequences in immunocompromised patients. Small ruminants are a potential reservoir of microsporidia for humans in their vicinity. Hence, we aimed to evaluate the molecular prevalence of microsporidian infections with emphasis on Enterocytozoon bieneusi genotypes among sheep and goats at a global scale through systematic review and meta-analysis approach.

Methods

The standard protocol of preferred reporting items for systematic reviews and meta-analyses (PRISMA) guidelines were followed. Eligible prevalence studies on small ruminant microsporidiosis, published from 1 January 2000 until 15 April 2021 were gathered using systematic literature search in PubMed, Scopus, Web of Science and Google Scholar databases. Inclusion and exclusion criteria were applied. The point estimates and 95% confidence intervals were calculated using a random-effects model. The variance between studies (heterogeneity) was quantified by I2 index.

Results

In total, 25 articles (including 34 datasets) were included for final meta-analysis. The pooled molecular prevalence of microsporidia in sheep and goats was estimated to be 17.4% (95% CI: 11.8–25%) and 16% (95% CI: 11.2–22.4%), respectively. Likewise, the overall prevalence of E. bieneusi was estimated to be 17.4% (95% CI: 11.8–25%) for sheep and 16.3% (95% CI: 11.3–22.8%) for goats. According to internal transcribed spacer (ITS) gene analysis, E. bieneusi with genotypes BEB6 (15 studies) and COS-1 (nine studies) in sheep, and CHG3 (six studies) and BEB6 (five studies) in goats were the highest reported genotypes.

Conclusion

The present results highlight the role of sheep and goats as reservoir hosts for human-infecting microsporidia. Therefore, this global estimate could be beneficial on preventive and control measures.

Introduction

Microsporidia are a diverse group of zoonotic pathogens parasitizing invertebrates (insects) and vertebrates (fish, birds and mammals) [1]. Enterocytozoon bieneusi and Encephalitozoon spp. (i.e., Enc. intestinalis, Enc. hellem, and Enc. cuniculi) are two well-known genera among microsporidian species [2], with E. bieneusi being responsible for over 90% of animal and human cases [3]. A distinctive stage in the microsporidian life cycle is the formation of infective spores, which potentially contaminate the environment including water supplies and foodstuff [4,5,6]. Clinical infection is frequently eminent in immunocompromised patients, manifesting as malabsorption with subsequent chronic diarrhea as well as wasting diathesis [7, 8]. Additionally, microsporidian infections in immunocompetent subjects are asymptomatic but important, since these individuals are carriers of infective spores as a significant epidemiological concern [7]. Previously, the global prevalence of microsporidia infections was estimated among HIV-positive patients, rendering a 11.8% (95% CI: 10.1–13.4%) pooled prevalence [9]. A considerably high total prevalence of microsporidia infection was, also, calculated among cat populations worldwide [29.7% (95% CI: 19.7–42.2%)] [10], rather than in dogs [23.1% (95% CI: 13.5–36.8%)] [11]. As mentioned previously, E. bieneusi is the most prevalent genus among other microsporidian species, which demands molecular approaches to be exactly identified and genotyped [12]. Molecular techniques based on the variations in the nucleotide sequence of the internal transcribed spacer (ITS) region of the rRNA gene are mostly preferred for the identification of E. bieneusi genotypes [12]. Until now, over 200 distinct genotypes of E. bieneusi have been identified in humans, animals or both [13]. Small ruminants (sheep and goat) contribute a major role in the production of various dairy products worldwide [14, 15]. Diarrhea is a common intestinal sequela of microsporidian infections in small ruminants, causing considerable mortality and production loss [5, 16]. As well, there are some reports of raw milk contamination by microsporidian agents in sheep and goats [5, 17]. However, little is known on the molecular prevalence and genotype distribution of microsporidia, particularly E. bieneusi genotypes, in small ruminants. Thereby, the present systematic review and meta-analysis was done to evaluate the molecular prevalence of microsporidian infections with emphasis on Enterocytozoon bieneusi genotypes among sheep and goats at a global scale.

Methods

Information sources and systematic search

The present systematic review and meta-analysis was performed based on the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement [18]. Four international databases (PubMed, Scopus, Web of Science and Google Scholar) were excavated to gather relevant records on the molecular prevalence of microsporidia infection in sheep and goats published between 1 January 2000 and 15 April 2021. The search process was accomplished using MeSH terms alone or in combination: (Microsporidium” OR “Microsporidia” OR “Microspora” OR “Enterocytozoon bieneusi” OR “Encephalitozoon spp.”) AND (“Prevalence” OR “Epidemiology”) AND ("Small Ruminant" OR "Sheep” OR “Goat”). In addition, the bibliographic list of initially found papers was manually searched to find other relevant citations.

Inclusion criteria, study selection and data extraction

The inclusion criteria for the present systematic review were as follows: (1) abstracts and/or full-texts published in English language; (2) cross-sectional original papers or short reports estimating the molecular prevalence of microsporidia infection in sheep and goats; (3) utilization of different molecular methods; (4) papers providing total sample size and positive samples; and (5) published online from 1 January 2000 until 15 April 2021. Two independent reviewers evaluated the articles based on determined inclusion criteria and possible contradictions in cases of study selection or extraction procedure were obviated by discussion and consensus. Also, those articles on microsporidia infection in humans or other animals, studies that used non-molecular diagnostics, experimental investigations in small ruminants, as well as review papers, cohort, case-reports, case series, and editorials were all excluded. In the following, a set of required information, including first author’s last name; year of publication; continent; country; small ruminant species (sheep or goats); number of examined animals; number of animals with a positive test result, age, gender, molecular methods, identified parasite species and gene targets were precisely extracted.

Study quality assessment

The Joanna Briggs Institute (JBI) checklist is a qualitative index for inclusion of articles [19], providing ten questions with four options including, Yes, No, Unclear, and Not applicable. Briefly, a study can be awarded a maximum of one star for each numbered item. Those papers with a total score of 4–6 and 7–10 points were assigned as moderate and high quality, respectively.

Meta-analysis

The comprehensive meta-analysis Bio stat v2.2 software was employed for meta-analysis procedure [10, 11, 20]. Calculation of the pooled prevalence of microsporidia infection among small ruminants and 95% confidence intervals (CIs) was done using random-effects model (REM), which enhances the distribution of true effect sizes among studies [21, 22]. Subgroup analysis was, also, performed in order to reveal the weighted prevalence based on continent, country, and type of ruminants (sheep and goats). Moreover, the probable association of microsporidia prevalence with age and gender was determined using REM-based odd ratio (OR) estimation. The heterogeneity between studies was computed via I2 index and the Cochrane’s Q statistics [10, 11, 23]. Funnel plot was used to show the probability of publication bias [24]. Forest plot diagram was utilized to represent the pooled prevalence (with 95% CI) of microsporidia infection in sheep and goats.

Results

Following comprehensive systematic search (Fig. 1), 1715 records were initially retrieved, among which many duplicate/non-eligible articles were removed and only 25 papers were finally eligible to undergo meta-analysis [16, 25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48]. Of note, 9 out of 25 studies possessed more than one dataset (Table 1), so that 34 datasets (20 datasets for sheep and 14 for goat) were reviewed and required data were extracted. Table 1 shows the results of the quality assessment based on the JBI checklist, rendering acceptable quality for all articles.

Fig. 1
figure1

PRISMA flow diagram describing included/excluded studies

Table 1 All the studies investigating the global prevalence of microsporidia species in sheep and goats according to molecular methods

All datasets represented molecular characterization of microsporidia infections in small ruminants from 8 countries located at 4 continents, including Asia (26 datasets, 9925 animals), Europe (four datasets, 169 animals), Africa (three datasets, 212 animals) and America (one dataset, 125 animals) (Tables 1 and 2). China possessed the most published literature with 17 studies and 24 datasets. Most studies focused on E. bieneusi and only one study reported Enc. intestinalis in goats [34] (Table 1). In addition, one study out of the total study focused only on the detection of Enc. cuniculi in goats [30]. A relatively moderate weighted prevalence of microsporidia infection was obtained for both sheep 17.4% (95% CI: 11.8–25%) and goats 16% (95% CI: 11.2–22.4%) (Additional file 1: Figs. S1 and 2). Similar pooled prevalence rates were estimated for E. bieneusi in both sheep 17.4% (95% CI: 11.8–25%) (Fig. 2) and goats 16.3% (95% CI: 11.3–22.8%) (Fig. 3). The molecular determination of E. bieneusi genotypes was frequently accomplished using ITS gene, and genotypes BEB6 (15 studies) and COS-1 (nine studies) in sheep, and CHG3 (six studies) and BEB6 (five studies) in goats were the most prevalent among all other genotypes (Table 1). America and Asia continents showed the highest total prevalence rates with 19.2% (95% CI: 13.2–27.1%) and 17.6% (95% CI: 13.1–23.3%), respectively, followed by Europe 10.2% (95% CI: 1.4–48.3%), and Africa 8.7% (95% CI: 2.9–23.6%) (Table 2). It is noteworthy that Table 2 demonstrates data on country-based prevalence of microsporidia infection.

Table 2 Subgroup analysis of continents, countries and animal type (sheep and goats), based on molecular methods
Fig. 2
figure2

The pooled molecular prevalence of E. bieneusi infection in sheep

Fig. 3
figure3

The pooled molecular prevalence of E. bieneusi infection in goats

A positive association was observed between microsporidia infection with age (≤ 3 months) (OR = 2.044; 95% CI, 1.35–3.093%) and male gender (OR = 3.169; 95% CI, 2.215–4.535%) (Table 3). The included studies had a significant publication bias based represented in the funnel plot (Additional file 1: Fig. S3 for sheep and Additional file 1: Fig. S4 for goats).

Table 3 Gender and age associated with microsporidia infection among sheep and goats worldwide

Discussion

The health of animals and human are tightly interconnected within the environmental context, what is called as the One Health approach [49]. Domestic animals such as sheep and goats are in close contact with humans in rural areas and may contribute to some zoonotic pathogens including microsporidia infections [46]. Hence, a global evaluation of the pooled prevalence of microsporidia infections in small ruminants seems necessary.

The present systematic review and meta-analysis showed that microsporidia infection, with particular emphasis on E. bieneusi, is more prevalent in sheep (17.4%) than in goats (16.3%). Most microsporidia species are able to infect the gastrointestinal tract, while some species occupy the urinary tract, hence being found in urine samples. In this meta-analysis, only one study examined the molecular prevalence of Enc. cuniculi in urine samples, which was negative for all samples [30].

Although most studies used the nested PCR technique, some studies used the PCR and real-time SYBR green techniques. The most important advantage of nested PCR compared to the other two methods is that it could detect low amounts of microsporidia due to its high specificity [50, 51]. Moreover, nested PCR with the ITS gene is able to identify different E. bieneusi genotypes [51], whereas PCR with SSU rRNA gene fails to identify genotypes [52]. Genotyping of E. bieneusi using ITS gene sequence has been the most preferred and the gold standard method in recent decades, offering adequate information on pathogenicity and source of the organism [53]. Reportedly, BEB6, COS-1, and CHG3 of E. bieneusi have been the most prevalent genotypes among ruminants, in particular sheep and goats [39, 42, 53]. Of note, other less common zoonotic genotypes (Peru 6 and I), were also found in the present review, mostly isolated from humans and small ruminants [53]. This indicates to the possible environmental transmission of infective spores between humans and small ruminants. However, many samples from these animals and humans should be genotyped to endorse the zoonotic transmission of the genotypes.

China possessed the largest dataset (24 datasets) with a pooled prevalence rate of 17.9%, while only 7 other countries had reported microsporidia infection in sheep and goats. Still little is known regarding microsporidian infections in small ruminants in many countries worldwide, particularly in those nations having traditional animal husbandry system. As shown in Table 2, some key countries have few studies which implicates the need for further studies and more attention to sheep and goats microsporidiosis in these countries. It is noteworthy that information derived from the Europe (three studies), Africa (two studies), and America (one study) must be interpreted cautiously, because of paucity of studies (Table 2). There are several risk factors involved in the distribution of the microsporidian agents, including climatic variation, type of animal husbandry, parasite control measures, Human Development Index (HDI), etc. [11, 54]. Traditional animal husbandry systems facilitate the access of small ruminants to other domestic, wild and stray animals or close contact with environmental sources (e.g., consumption of spores contaminated water and food) [1, 7, 20, 51]. As such, different animals, water resources, and vegetables play a crucial role in maintaining the microsporidia cycle. Therefore, sheep and goats may be considered as a major reservoir of microsporidia, which subsequently may be responsible for the outbreaks of human microsporidiosis.

In the present meta-analysis, we found a higher microsporidia prevalence in ≤ 3 months and male animals, being statistically significant. Younger animals have immature and/or deficient immune status, hence they may be more susceptible to the microsporidia infection [26, 27], as substantiated by the higher prevalence in this review.

This systematic review and meta-analysis has some limitations and the results presented here should be interpreted with respect to these limitations, comprising lack of prevalence information in many countries; low sample size in some studies; and lack of risk factor (i.e., age and gender) and clinical symptoms (i.e., gastrointestinal disorders) assessment in most studies. Moreover, although this is a global meta-analysis on the molecular prevalence of microsporidia in sheep and goats, only eligible published studies were included, and it is possible that useful data were missed from the ‘grey’ literature. Also, online registration in PROSPERO failed, because data were already extracted. Considering these limitations, it is noteworthy to say that our results may be not precisely reflect the true prevalence, and the presented numbers are apparent prevalence rates. Nevertheless, it is believed what we had reported here is close to true microsporidia prevalence in sheep and goats within a global context.

Conclusion

This study showed a relatively high prevalence of microsporidia infection in sheep and goats worldwide, which could be directed towards better control and prevention of microsporidia infection in sheep and goats. Further, the findings of the present study should be taken into account by the health care authorities, physicians, veterinarians of the countries. The high-risk groups including immunocompromised patients must receive accurate and valid information about the risk of contact with the infected these ruminants. We suggest performing further studies to clarify the global prevalence of microsporidiosis based on molecular methods, which would be a guide to the establishment of appropriate public health interventions.

Availability of data and materials

Not applicable.

References

  1. 1.

    Didier ES. Microsporidiosis: an emerging and opportunistic infection in humans and animals. Acta Trop. 2005;94(1):61–76. https://doi.org/10.1016/j.actatropica.2005.01.010.

    CAS  Article  PubMed  Google Scholar 

  2. 2.

    Weiss LM. Microsporidia: emerging pathogenic protists. Acta Trop. 2001;78(2):89–102. https://doi.org/10.1016/S0001-706X(00)00178-9.

    CAS  Article  PubMed  Google Scholar 

  3. 3.

    Wang SS, Wang RJ, Fan XC, Liu TL, Zhang LX, Zhao GH. Prevalence and genotypes of Enterocytozoon bieneusi in China. Acta Trop. 2018;1(183):142–52. https://doi.org/10.1016/j.actatropica.2018.04.017.

    CAS  Article  Google Scholar 

  4. 4.

    Izquierdo F, Hermida JAC, Fenoy S, Mezo M, González-Warleta M, del Aguila C. Detection of microsporidia in drinking water, wastewater and recreational rivers. Water Res. 2011;45(16):4837–43. https://doi.org/10.1016/j.watres.2011.06.033.

    CAS  Article  PubMed  Google Scholar 

  5. 5.

    Yildirim Y, Al S, Duzlu O, Onmaz NE, Onder Z, Yetismis G, et al. Enterocytozoon bieneusi in raw milk of cattle, sheep and water buffalo in Turkey: Genotype distributions and zoonotic concerns. Int J Food Microbiol. 2020;2(334): 108828. https://doi.org/10.1016/j.ijfoodmicro.2020.108828.

    CAS  Article  Google Scholar 

  6. 6.

    Stentiford G, Becnel J, Weiss L, Keeling P, Didier E, Bjornson S, et al. Microsporidia–emergent pathogens in the global food chain. Trends Parasitol. 2016;32(4):336–48. https://doi.org/10.1016/j.pt.2015.12.004.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. 7.

    Didier ES, Weiss LM. Microsporidiosis: current status. Curr Opin Infect Dis. 2006;19(5):485. https://doi.org/10.1097/01.qco.0000244055.46382.23.

    Article  PubMed  PubMed Central  Google Scholar 

  8. 8.

    Weiss LM. Clinical syndromes associated with microsporidiosis. In: Weiss LM, Becnel JJ, editors. Microsporidia: pathogens of opportunity. 1st ed. United Kingdom: John Wiley & Sons, Inc.; 2014. p. 371–401.

    Google Scholar 

  9. 9.

    Wang ZD, Liu Q, Liu HH, Li S, Zhang L, Zhao YK, et al. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasit Vectors. 2018;11(1):1–9. https://doi.org/10.1186/s13071-017-2558-x.

    Article  PubMed  PubMed Central  Google Scholar 

  10. 10.

    Taghipour A, Ghodsian S, Shajarizadeh M, Sharbatkhori M, Khazaei S, Mirjalali H. Global prevalence of microsporidia infection in cats: a systematic review and meta-analysis of an emerging zoonotic pathogen. Prev Vet Med. 2021. https://doi.org/10.1016/j.prevetmed.2021.105278.

    Article  PubMed  Google Scholar 

  11. 11.

    Taghipour A, Bahadory S, Khazaei S. A systematic review and meta-analysis on the global prevalence of microsporidia infection among dogs: a zoonotic concern. Trop Med Health. 2020;48(1):1–10. https://doi.org/10.1186/s41182-020-00265-0.

    Article  Google Scholar 

  12. 12.

    Santin M, Fayer R. Enterocytozoon bieneusi genotype nomenclature based on the internal transcribed spacer sequence: a consensus. J Eukaryot Microbiol. 2009;56(1):34–8. https://doi.org/10.1111/j.1550-7408.2008.00380.x.

    CAS  Article  PubMed  Google Scholar 

  13. 13.

    Santín-Durán M: Enterocytozoon bieneusi. In: Biology of Foodborne Parasites. Boca Raton: CRC Press, 2015: 149–174.

  14. 14.

    Boyazoglu J, Morand-Fehr P. Mediterranean dairy sheep and goat products and their quality: a critical review. Small Rumin Res. 2001;40(1):1–11. https://doi.org/10.1016/S0921-4488(00)00203-0.

    CAS  Article  PubMed  Google Scholar 

  15. 15.

    Hilali M, El-Mayda E, Rischkowsky B. Characteristics and utilization of sheep and goat milk in the Middle East. Small Rumin Res. 2011;101(1–3):92–101. https://doi.org/10.1016/j.smallrumres.2011.09.029.

    Article  Google Scholar 

  16. 16.

    Shi K, Li M, Wang X, Li J, Karim MR, Wang R, et al. Molecular survey of Enterocytozoon bieneusi in sheep and goats in China. Parasit Vectors. 2016;9(1):1–8. https://doi.org/10.1186/s13071-016-1304-0.

    CAS  Article  Google Scholar 

  17. 17.

    Vecková T, Sak B, Samková E, Holubová N, Kicia M, Zajączkowska Ż, et al. Raw Goat’s Milk, Fresh and Soft Cheeses as a Potential Source of Encephalitozoon cuniculi. Foodborne Pathog Dis. 2021. https://doi.org/10.1089/fpd.2021.0017.

    Article  PubMed  Google Scholar 

  18. 18.

    Moher D, Shamseer L, Clarke M, Ghersi D, Liberati A, Petticrew M, et al. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst Rev. 2015;4(1):1–9.

    Article  Google Scholar 

  19. 19.

    Joanna Briggs Institute. Joanna Briggs Institute reviewers’ manual: 2014 edition/supplement. Australia: The Joanna Briggs Institute, The University of Adelaide; 2014.

    Google Scholar 

  20. 20.

    Taghipour A, Bahadory S, Abdoli A, Javanmard E. A systematic review and meta-analysis on the global molecular epidemiology of microsporidia infection among rodents: a serious threat to public health. Acta Parasitol. 2021;27:1–3.

    Google Scholar 

  21. 21.

    Khatami A, Bahadory S, Ghorbani S, Saadati H, Zarei M, Soleimani A, et al. Two rivals or colleagues in the liver? Hepatit B virus and Schistosoma mansoni co-infections: a systematic review and meta-analysis. Microb Pathog. 2021;17: 104828. https://doi.org/10.1016/j.micpath.2021.104828.

    Article  Google Scholar 

  22. 22.

    Khatami A, Pormohammad A, Farzi R, Saadati H, Mehrabi M, Kiani SJ, et al. Bovine Leukemia virus (BLV) and risk of breast cancer: a systematic review and meta-analysis of case-control studies. Infect Agents Cancer. 2020;15(1):1–8. https://doi.org/10.1186/s13027-020-00314-7.

    Article  Google Scholar 

  23. 23.

    Khademvatan S, Majidiani H, Khalkhali H, Taghipour A, Asadi N, Yousefi E. Prevalence of fasciolosis in livestock and humans: a systematic review and meta-analysis in Iran. Comp Immunol Microbiol Infect Dis. 2019;1(65):116–23. https://doi.org/10.1016/j.cimid.2019.05.001.

    Article  Google Scholar 

  24. 24.

    Egger M, Smith GD, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34. https://doi.org/10.1136/bmj.315.7109.629.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. 25.

    Valenčáková A, Danišová O. Molecular characterization of new genotypes Enterocytozoon bieneusi in Slovakia. Acta Trop. 2019;1(191):217–20. https://doi.org/10.1016/j.actatropica.2018.12.031.

    CAS  Article  Google Scholar 

  26. 26.

    Stensvold CR, Beser J, Ljungström B, Troell K, Lebbad M. Low host-specific Enterocytozoon bieneusi genotype BEB6 is common in Swedish lambs. Vet Parasitol. 2014;205(1–2):371–4. https://doi.org/10.1016/j.vetpar.2014.06.010.

    Article  PubMed  Google Scholar 

  27. 27.

    Ye J, Xiao L, Wang Y, Guo Y, Roellig DM, Feng Y. Dominance of Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotype BEB6 in sheep in Inner Mongolia. China Vet Parasitol. 2015;210(3–4):235–9. https://doi.org/10.1016/j.vetpar.2015.04.011.

    Article  PubMed  Google Scholar 

  28. 28.

    Qi M, Zhang Z, Zhao A, Jing B, Guan G, Luo J, et al. Distribution and molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi amongst grazing adult sheep in Xinjiang, China. Parasitol Int. 2019;71:80–6. https://doi.org/10.1016/j.parint.2019.04.006.

    Article  PubMed  Google Scholar 

  29. 29.

    Lores B, Del Aguila C, Arias C. Enterocytozoon bieneusi (microsporidia) in faecal samples from domestic animals from Galicia, Spain. Mem Inst Oswaldo Cruz. 2002;97:941–5.

    CAS  Article  Google Scholar 

  30. 30.

    Abu-Akkada SS, Ashmawy KI, Dweir AW. First detection of an ignored parasite, Encephalitozoon cuniculi, in different animal hosts in Egypt. Parasitol Res. 2015;114(3):843–50. https://doi.org/10.1007/s00436-014-4247-4.

    Article  PubMed  Google Scholar 

  31. 31.

    Chang Y, Wang Y, Wu Y, Niu Z, Li J, Zhang S, Wang R, Jian F, Ning C, Zhang L. Molecular characterization of Giardia duodenalis and Enterocytozoon bieneusi isolated from Tibetan sheep and Tibetan goats under natural grazing conditions in Tibet. J Eukaryot Microbiol. 2020;67(1):100–6. https://doi.org/10.1111/jeu.12758.

    CAS  Article  PubMed  Google Scholar 

  32. 32.

    Chen D, Wang SS, Zou Y, Li Z, Xie SC, Shi LQ, et al. Prevalence and multi-locus genotypes of Enterocytozoon bieneusi in black-boned sheep and goats in Yunnan Province, southwestern China. Infect Genet Evol. 2018;1(65):385–91. https://doi.org/10.1016/j.meegid.2018.08.022.

    Article  Google Scholar 

  33. 33.

    da Silva Fiuza VR, Lopes CW, Cosendey RI, de Oliveira FC, Fayer R, Santín M. Zoonotic Enterocytozoon bieneusi genotypes found in Brazilian sheep. Res Vet Sci. 2016;1(107):196–201. https://doi.org/10.1016/j.rvsc.2016.06.006.

    CAS  Article  Google Scholar 

  34. 34.

    Al-Herrawy AZ. Microsporidial spores in fecal samples of some domesticated animals living in Giza. Egypt Iran J Parasitol. 2016;11(2):195.

    PubMed  Google Scholar 

  35. 35.

    Li WC, Wang K, Gu YF. Detection and genotyping study of Enterocytozoon bieneusi in sheep and goats in East-central China. Acta Parasitol. 2019;64(1):44–50. https://doi.org/10.2478/s11686-018-00006-8.

    CAS  Article  PubMed  Google Scholar 

  36. 36.

    Askari Z, Mirjalali H, Mohebali M, Zarei Z, Shojaei S, Rezaeian T, et al. Molecular detection and identification of zoonotic microsporidia spore in fecal samples of some animals with close-contact to human. Iran J Parasitol. 2015;10(3):381.

    PubMed  PubMed Central  Google Scholar 

  37. 37.

    Zhou HH, Zheng XL, Ma TM, Qi M, Cao ZX, Chao Z, et al. Genotype identification and phylogenetic analysis of Enterocytozoon bieneusi in farmed black goats (Capra hircus) from China’s Hainan Province. Parasite. 2019. https://doi.org/10.1051/parasite/2019064.

    Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Peng XQ, Tian GR, Ren GJ, Yu ZQ, Lok JB, Zhang LX, et al. Infection rate of Giardia duodenalis, Cryptosporidium spp. and Enterocytozoon bieneusi in cashmere, dairy and meat goats in China Infect. Genet Evol. 2016;41:26–31. https://doi.org/10.1016/j.meegid.2016.03.021.

    Article  Google Scholar 

  39. 39.

    Peng JJ, Zou Y, Li ZX, Liang QL, Song HY, Li TS, et al. Occurrence of Enterocytozoon bieneusi in Chinese Tan sheep in the Ningxia Hui Autonomous Region. China Parasitol Res. 2019;118(9):2729–34. https://doi.org/10.1007/s00436-019-06398-4.

    Article  PubMed  Google Scholar 

  40. 40.

    Li W, Li Y, Li W, Yang J, Song M, Diao R, et al. Genotypes of Enterocytozoon bieneusi in livestock in China: high prevalence and zoonotic potential. PLoS ONE. 2014;9(5): e97623. https://doi.org/10.1371/journal.pone.0097623.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  41. 41.

    Udonsom R, Prasertbun R, Mahittikorn A, Chiabchalard R, Sutthikornchai C, Palasuwan A, et al. Identification of Enterocytozoon bieneusi in goats and cattle in Thailand. BMC Vet Res. 2019;15(1):1–7. https://doi.org/10.1186/s12917-019-2054-y.

    CAS  Article  Google Scholar 

  42. 42.

    Yang H, Mi R, Cheng L, Huang Y, An R, Zhang Y, et al. Prevalence and genetic diversity of Enterocytozoon bieneusi in sheep in China. Parasit Vectors. 2018;11(1):1. https://doi.org/10.1186/s13071-018-3178-9.

    Article  Google Scholar 

  43. 43.

    Wu Y, Chang Y, Chen Y, Zhang X, Li D, Zheng S, et al. Occurrence and molecular characterization of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi from Tibetan sheep in Gansu. China Infect Genet Evol. 2018;64:46–51. https://doi.org/10.1016/j.meegid.2018.06.012.

    CAS  Article  PubMed  Google Scholar 

  44. 44.

    Zhang Q, Cai J, Li P, Wang L, Guo Y, Li C, et al. Enterocytozoon bieneusi genotypes in Tibetan sheep and yaks. Parasitol Res. 2018;117(3):721–7. https://doi.org/10.1007/s00436-017-5742-1.

    Article  PubMed  Google Scholar 

  45. 45.

    Zhang Q, Zhang Z, Ai S, Wang X, Zhang R, Duan Z. Cryptosporidium spp., Enterocytozoon bieneusi, and Giardia duodenalis from animal sources in the Qinghai-Tibetan Plateau Area (QTPA) in China. Comp Immunol Microbiol Infect Dis. 2019;67:101346. https://doi.org/10.1016/j.cimid.2019.101346.

    Article  PubMed  Google Scholar 

  46. 46.

    Zhao W, Zhang W, Yang D, Zhang L, Wang R, Liu A. Prevalence of Enterocytozoon bieneusi and genetic diversity of ITS genotypes in sheep and goats in China. Infect Genet Evol. 2015;1(32):265–70. https://doi.org/10.1016/j.meegid.2015.03.026.

    Article  Google Scholar 

  47. 47.

    Jiang Y, Tao W, Wan Q, Li Q, Yang Y, Lin Y, et al. Zoonotic and potentially host-adapted Enterocytozoon bieneusi genotypes in sheep and cattle in northeast China and an increasing concern about the zoonotic importance of previously considered ruminant-adapted genotypes. Appl Environ Microbiol. 2015;81(10):3326–35. https://doi.org/10.1128/AEM.00328-15.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  48. 48.

    Zhang Y, Mi R, Yang J, Wang J, Gong H, Huang Y, et al. Enterocytozoon bieneusi genotypes in farmed goats and sheep in Ningxia, China. Infect Genet Evol. 2020;1(85): 104559. https://doi.org/10.1016/j.meegid.2020.104559.

    CAS  Article  Google Scholar 

  49. 49.

    Mackenzie JS, Jeggo M. The One Health approach—why is it so important? Basel: Multidisciplinary Digital Publishing Institute; 2019.

    Book  Google Scholar 

  50. 50.

    Jaroenlak P, Sanguanrut P, Williams BA, Stentiford GD, Flegel TW, Sritunyalucksana K, et al. A nested PCR assay to avoid false positive detection of the microsporidian Enterocytozoon hepatopenaei (EHP) in environmental samples in shrimp farms. PLoS ONE. 2016;11(11): e0166320. https://doi.org/10.1371/journal.pone.0166320.

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  51. 51.

    Javanmard E, Mirjalali H, Niyyati M, Jalilzadeh E, Tabaei SJ, Aghdaei HA, et al. Molecular and phylogenetic evidences of dispersion of human-infecting microsporidia to vegetable farms via irrigation with treated wastewater: one-year follow up. Int J Hyg Environ Health. 2018;221(4):642–51. https://doi.org/10.1016/j.ijheh.2018.03.007.

    Article  PubMed  Google Scholar 

  52. 52.

    Mirjalali H, Mohebali M, Mirhendi H, Gholami R, Keshavarz H, Meamar AR, et al. Emerging intestinal microsporidia infection in HIV+/AIDS patients in Iran: microscopic and molecular detection. Iran J Parasitol. 2014;9(2):149.

    PubMed  PubMed Central  Google Scholar 

  53. 53.

    Thellier M, Breton J. Enterocytozoon bieneusi in human and animals, focus on laboratory identification and molecular epidemiology. Parasite. 2008;15(3):349–58. https://doi.org/10.1051/parasite/2008153349.

    CAS  Article  PubMed  Google Scholar 

  54. 54.

    Javanmard E, Niyyati M, Ghasemi E, Mirjalali H, Aghdaei HA, Zali MR. Impacts of human development index and climate conditions on prevalence of Blastocystis: a systematic review and meta-analysis. Acta Trop. 2018;1(185):193–203. https://doi.org/10.1016/j.actatropica.2018.05.014.

    Article  Google Scholar 

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Acknowledgements

We thank the scientists and personnel of the Medical Parasitology Department in Tarbiat Modares University of Medical Sciences, Tehran, for their collaboration.

Funding

This research did not receive any specific grant from funding agencies in public, commercial, or not-for-profit sectors.

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All authors contributed to study design. AT contributed to all parts of the study. AT and SB contributed to study implementation. AT and SB collaborated in the analysis and interpretation of data. AT, SB, and EJ collaborated in the manuscript writing and revision. All the authors commented on the drafts of the manuscript and approved the final version of the article. All authors read and approved the final manuscript.

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Correspondence to Ali Taghipour.

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Supplementary Information

Additional file 1.

Figure S1. The pooled molecular prevalence of microsporidia infection in sheep. Figure S2. The pooled molecular prevalence of microsporidia infection in goats. Figure S3. Publication bias using funnel plot. Publication bias in sheep datasets. Funnel plot displaying prevalence data for all included publications (n = 20). Each circle represents reported prevalence from one individual study. Please note wide value distribution outside the funneled area indicating significant publication bias. Figure S4. Publication bias using funnel plot. Publication bias in goat’s datasets. Funnel plot displaying prevalence data for all included publications (n = 14). Each circle represents reported prevalence from one individual study. Please note wide value distribution outside the funneled area indicating significant publication bias.

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Taghipour, A., Bahadory, S. & Javanmard, E. The global molecular epidemiology of microsporidia infection in sheep and goats with focus on Enterocytozoon bieneusi: a systematic review and meta-analysis. Trop Med Health 49, 66 (2021). https://doi.org/10.1186/s41182-021-00355-7

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Keywords

  • Microsporidia
  • Enterocytozoon bieneusi
  • Sheep
  • Goat
  • Meta-analysis