Next Article in Journal
Physiological Responses of the Bivalves Mytilus galloprovincialis and Ruditapes decussatus Following Exposure to Phenanthrene: Toxicokinetics, Dynamics and Biomarkers Study
Next Article in Special Issue
Altered miRNA Expression Profiles in the Serum of Beagle Dogs Experimentally Infected with Toxocara canis
Previous Article in Journal
Egg Quality of Italian Local Chicken Breeds: I. Yield Performance and Physical Characteristics
Previous Article in Special Issue
Investigation of the Efficacy of Pyrantel Pamoate, Mebendazole, Albendazole, and Ivermectin against Baylisascaris schroederi in Captive Giant Pandas
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Systematic Review

The Occurrence and Meta-Analysis of Investigations on Sarcocystis Infection among Ruminants (Ruminantia) in Mainland China

1
National Animal Protozoa Laboratory, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
2
Key Laboratory of Animal Epidemiology of the Ministry of Agriculture, College of Veterinary Medicine, China Agricultural University, Beijing 100193, China
*
Author to whom correspondence should be addressed.
Animals 2023, 13(1), 149; https://doi.org/10.3390/ani13010149
Submission received: 9 December 2022 / Revised: 27 December 2022 / Accepted: 28 December 2022 / Published: 30 December 2022

Abstract

:

Simple Summary

Sarcocystis can infect almost all warm-blooded animals, including humans. Ruminants (Ruminantia) are the intermediate hosts for Sarcocystis, representing a potential risk for public health. In China, there are many studies on the prevalence of Sarcocystis. However, the overall prevalence of Sarcocystis infection among ruminants in mainland China remains unclear and relevant risk factors need to be assessed to develop preventive measures. Therefore, we conducted this systematic review and meta-analysis to collect data on the prevalence and risk factors of Sarcocystis in ruminants in mainland China. Based on the results, we discussed the potential factors that may affect the prevalence of Sarcocystis in ruminants and the limitations in the current epidemiological investigation.

Abstract

Sarcocystis is a zoonotic pathogen that threatens public health and the quality of food safety. To determine the Sarcocystis spp. prevalence in ruminants (Ruminantia) in China, we conducted a systematic review and meta-analysis. Data were collected from English databases (PubMed and Web of Science) and Chinese databases (Chinese Web of knowledge (CNKI), Database for Chinese Technical Periodicals (VIP) and Wan Fang databases). A total of 20,301 ruminants from 54 publications were evaluated. The pooled prevalence of Sarcocystis spp. among ruminants in mainland China was 65% (95% CI: 57–72%). Our results indicate that sarcocystosis is prevalent in ruminants, which show significant geographical differences. Therefore, it there is a need for continuous monitoring of infections of Sarcocystis spp. in ruminants to reduce the threat to human health and economic losses to the animal industry.

1. Introduction

Sarcocystis is a food-borne zoonotic pathogen that can infect humans and a variety of animals, there are 196 valid Sarcocystis species [1]. Sarcocystis has an obligate two-host life cycle, the intermediate hosts are usually herbivores, and the definitive hosts are usually carnivores or omnivores. Sarcocystis can form sarcocysts in the striated muscles and central nervous system of domestic animals such as sheep (Ovis aries Linnaeus, 1758), cattle (Bos taurus Linnaeus, 1758), and yaks (Poephagus grunniens Linnaeus, 1766) [1]. At present, a variety of Sarcocystis has been confirmed to have strong pathogenicity. Five known species have been described in cattle: Sarcocystis cruzi Hasselmann, 1926, Sarcocystis hirsuta Moulé, 1888, Sarcocystis hominis Railliet and Lucet, 1891, Sarcocystis rommeli Dubey et al., 2016, and Sarcocystis heydorni Dubey et al., 2015 [2,3]. Among them, humans are the definitive host of S. hominis, which can cause nausea, vomiting, and diarrhea [4]. S. cruzi is the most pathogenic species in cattle, and acute infection can lead to weakness, reduced milk yield, and economic losses in cattle farms [5]. Animals can be infected with Sarcocystis spp. by ingesting water or food contaminated with sporocysts or oocysts [1]. Humans become infected with S. hominis, S. heydorni and Sarcocystis suihominis tadros and Laarman, 1976 by eating undercooked meat containing mature sarcocysts.
Three validated species of Sarcocystis have been described in sheep in China: the pathogenic microscopic Sarcocystis tenella Railliet, 1886, Sarcocystis arieticanis Heydorn, 1985 and the non-pathogenic macroscopic Sarcocystis gigantea Railliet, 1886 [6]. Depending on the number and types of animals infected with Sarcocystis, it can cause anorexia, fever, muscle inflammation, abortion, premature birth, and even death [1]. Furthermore, the formation of sarcocysts in the muscles can affect the appearance and quality of meat, cause waste of meat products, and bring economic losses to animal husbandry. However, diagnosis is difficult due to the lack of specific clinical symptoms of Sarcocystis.
The animal industry is important in China, the annual production of meat from sheep in 2017 was 4851 thousand tons [7], and 66,728,000 tons of beef and 32,012,400 tons of milk in 2020 [8]. The economic significance of Sarcocystis in ruminants and its threat to human health via consumption of infected raw and undercooked meat (e.g., hot pots, roasts) highlights the importance of research on Sarcocystis. In addition, the relatively large number of surveys on the prevalence of Sarcocystis in China makes it necessary to conduct a systematic study to collect these data and to analyze the limitations and strengths of these studies. Meta-analysis and meta-regression are techniques that help to gain insight into the causes of such differences and to describe current knowledge in an evidence-based manner. Therefore, the aim of this study was to analyze the prevalence of Sarcocystis in ruminants and the factors that may influence the prevalence of Sarcocystis in ruminants in mainland China through meta-analysis and meta-regression.

2. Materials and Methods

2.1. Search Strategy and Inclusion Criteria

To evaluate the prevalence of Sarcocystis infection in ruminants, we performed a non-registered systematic review and meta-analysis of the literature published online. This system review and meta-analysis was conducted according to the recommendations of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) [9]. We performed the PRISMA 2020 checklist (Table S1) to ensure the relevant information included was consistent with the study criteria. The meta-analysis was conducted by searching English databases (PubMed, Web of Science) and Chinese databases (Chinese Web of knowledge (CNKI), Database for Chinese Technical Periodicals (VIP), and Wan Fang databases) for publications related to Sarcocystis infection in ruminants in China, from 30 March 1983 to 1 January 2022. We searched databases using the following MeSH (Medical Subject Heading) terms alone or in combination: “Sarcocystis” or “Sarcocystis spp.” And “China” and “cattle” or “yak” or “sheep” or “goats” or “camelus” or “deer” or “ruminants” or “water buffaloes”.
Literature inclusion criteria: (1) the study population was limited to Chinese ruminants; (2) the types of studies were epidemiological and/or molecular studies of Sarcocystis spp. in ruminants; (3) the study must clearly report information on sources of samples, number of samples, infection prevalence of Sarcocystis, and detection methods for Sarcocystis; (4) the languages included in the study were limited to Chinese and English.
Literature exclusion criteria: (1) the source of the reported samples and animal species was unclear, and the data were incorrect or incomplete; (2) samples were not randomly selected; (3) duplicate publications, conference publications, articles given to the editor, review articles, no full text or insufficient information, etc.

2.2. Data Extraction

Data were extracted independently by two investigators (Zhu Zifu and Feng Zixuan) and checked by other authors. From all included publications, we extracted the following information: first author, year of publication, year of sampling, geographical area of study, host, total number of samples examined, number of Sarcocystis spp. positive samples, diagnostic method, and age, gender, or identified species (if reported) (Table 1).

2.3. Statistical Analysis

This study was performed using R software for Meta-Analysis [63]. We used four methods to transform the original data to make them conform to the normal distribution: logarithmic transformation (PLN), logit transformation (PLOGIT), arcsine transformation (PAS), and double arcsine transformation (PFT). Statistical heterogeneity between studies was evaluated using the Cochran‘s Q statistics, p-value, and I2 statistics. The heterogeneity of included studies was used as the basis for selecting the effect model, and heterogeneity was considered insignificant when p > 0.1 and I2 < 50%, when p < 0.05 and I2 > 50%, the heterogeneity was considered significant. When the heterogeneity was not significant, a fixed-effect model was selected; otherwise, a random-effect model was used [64]. We conducted a sensitivity analysis in which one study was removed and the remaining studies were analyzed to assess the potential influence of the presence of outliers on each model per species. To account for sources of heterogeneity, we performed subgroup analyses based on region, host type, year of publication, and diagnostic method. The publication bias was evaluated by trim and fill analysis.

3. Results

3.1. Study Selection and Data Extraction

The search of five databases identified 332 records. After removing duplicate studies and preliminary screening, 244 papers remained. After screening titles and abstracts, 121 papers remained. We were unable to evaluate the full text of one article. After reading the full text, a total of 66 articles were excluded for the following reasons: review articles, non-ruminant animals, lack of Sarcocystis prevalence, and samples not randomly selected. Finally, a meta-analysis of 54 publications was performed, including 73 studies (Figure 1).
The included studies were conducted in 9 provinces in China, including 4 provinces in northwest China, 2 provinces in southwest China, 2 provinces in central China, and 1 province in northeast China (Table 1, Figure S1).

3.2. Prevalence of Sarcocystis in Ruminants in China

In this study, we used the arcsine transformation (PAS) conversion (the value of W was closer to 1, p > 0.05) for rate conversion (Table 2). High heterogeneity was shown in the included studies (χ2 = 8755.27, d.f. = 72, p < 0.001, I2 = 99.2%), the pooled infection rate of Sarcocystis in ruminants in mainland China was 65% (95% CI: 57–72%), as shown in Figure 2. A total of 20,301 ruminant samples were detected, of which 11,555 were positive for Sarcocystis. The detailed Sarcocystis prevalence in ruminants in different articles ranged from 7% to 100%. The presence of publication bias in the included articles could not be directly determined from the funnel plot (Figure S2). Begg’s and Egger’s tests showed that there was no publication bias in the included studies (p = 0.1514 > 0.05, Figure S3). Sensitivity analysis showed that no study had a significant effect on pooled prevalence (Figure S4).

3.3. Subgroup Analysis

The infection rate varied significantly by region in China (p < 0.01), with the highest prevalence of Sarcocystis infection in northwest China (10,205/15,919, 67%, 95% CI: 59–75%) and the lowest in northeast China (7/24, 29%, 95% CI: 13–51%) (Table 3, Figure 3). Significant differences in Sarcocystis infection were found among provinces (χ2 = 30.05, d.f. = 8, p < 0.01, I2 = 99%). The prevalence of Sarcocystis infection (7%) was lowest in Yunnan and highest (100%) in Tibet.
The studies included a variety of animals, including camels (n = 1), cattle (n = 9), goats (n = 6), sheep (n = 34), water buffalo (n = 2), and yaks (n = 21) (Figure S5). There were significant differences in the prevalence of sarcocystosis among the different hosts (χ2 = 6.03, d.f. = 5, p < 0.01, I2 = 99%). Among them, the highest infection rate of Sarcocystis was found in goats (71%, 1788/3528, 95% CI: 40–93%) and the lowest in water buffalo (24%, 58/770, 95% CI: 0–72%).
Our results showed the existence of significant differences (χ2 = 29.07, d.f. = 3, p < 0.01, I2 = 98%) in Sarcocystis infection rates across publication years (Figure S6). The pooled prevalence was significantly higher before 2005 (7771/10,588, 85%, 95% CI: 77–90%) than in 2005–2010 (1048/1998, 46%, 95% CI: 33–60%), 2011–2015 (746/1580, 50%, 95% CI: 30–70%) and after 2016 (1990/6135, 52%, 95% CI: 33–71%).

4. Discussion

This review describes the current knowledge on the prevalence of Sarcocystis among ruminants in mainland China in a systematic manner. All 54 publications included in this study were from naturally infected ruminants in China, including sheep, yaks, cattle, goats, water buffalos, and camels. The included studies were published from 1983 to 2021 and reported data on 20,301 ruminants. The pooled prevalence of Sarcocystis in ruminants was 65% (95% CI: 57–72%), which was lower than the overall prevalence of sarcocystosis in domestic ruminants in Iran (74.40%, 95% CI: 64.01–83.56%) [65]. Although pooled prevalence estimates from different animal species may be considered of limited value, it enables us to statistically define differences in the prevalence of Sarcocystis spp. and may provide information for taking appropriate measures to improve public health.
In this meta-analysis, based on the I2 test, we observed a high degree of heterogeneity regarding the prevalence of Chinese ruminants among eligible studies. This may be related to detection method, age, region, year of sampling, year of publication, and host.
At present, there is no standard serological diagnostic method for the detection of Sarcocystis, which is usually detected by muscle squashing microscopic observation, histological examination, HCl–pepsin digestion method, or molecular detection with specific primers [66]. Most of the studies in this review used morphological observation as the detection method, and the detection rate of this method is closely related to the sample type, sample size, and infection density of Sarcocystis, so the detection rate may be lower than that of the real infection. In addition, PCR identification was performed only on a small number of samples identified as positive by morphological observation, which could not truly reflect the infected species of Sarcocystis in all positive samples.
The age of the animals is considered to be an important factor because the likelihood of animal exposure to parasites increases with age [67]. In this review, only two studies investigated the prevalence of Sarcocystis at different ages. One study reported a significantly higher prevalence of Sarcocystis infection in adult sheep (91.1%, 1912/2108) than in 5–8 months old lambs (68.2%, 101/148) [26]. Another study found that the infection rate (75%, 15/20) and intensity of infection (9.35 sarcocysts/cm2) were significantly higher in adult yaks than in young yaks (10%, 2/20) and (0.15 sarcocysts/ cm2), respectively, indicating an increase in infection rate with the age of the animals [32].
According to the subgroup analysis, there were significant differences in the infection rate of Sarcocystis among ruminants in different regions. The data showed that northwest China had the highest infection rate among the five regions in China, with the research mainly concentrated in Qinghai Province. There was only one study in northeast China, and the results of this study could not truly reflect the infection of Sarcocystis in this area. In addition, in this review, only 9 provinces have reported infection with Sarcocystis in ruminants, and many provinces have not yet reported it.
The infection of ruminants with Sarcocystis is related to their living environment and feeding management. Strengthening the breeding management and reducing the exposure of ruminants to potential sources of Sarcocystis such as wild animals, cats and dogs can greatly reduce the probability of infection in ruminants [68]. According to our analysis, ruminants had the highest rate of Sarcocystis infection before 2005, which might be related to the continuous improvement of feeding management in recent years. However, in this review, there is no information on the feeding management of ruminants and the existence of definitive hosts.
Sarcocystis is a food-borne pathogen which can infect a variety of animals and humans [1]. In this review, the overall prevalence of camels (Camelus dromedarius and Camelus bactrianus, Linnaeus, 1758), cattle, goats (Capra hircus, Linnaeus, 1758), sheep, water buffalo (Bubalus bubalis, Linnaeus, 1758), and yaks was generally higher, at 59%, 56%, 71%, 69%, 24%, and 64%, respectively. Among them, cattle are the intermediate hosts of Sarcocystis spp. Five species of Sarcocystis have been identified in beef, namely S. cruzi, S. hirsuta, S. hominis, S. rommeli, and S. heydorni [2,3]. Humans are the final hosts of S. hominis and S. heydorni, which can cause gastrointestinal distress in humans [4]. In addition to the possibility of zoonosis, there is evidence that these protozoa are related to bovine eosinophilic myositis (BEM), a specific inflammatory myopathy with gray-green lesions that causes carcass necrosis and considerable economic losses [69]. However, there are only nine studies on sarcocystosis in cattle and beef in this systematic review.
This meta-analysis showed that sheep are the most common animal studied in the investigation of sarcocystosis in China, and 34 studies have reported Sarcocystis infection in sheep. The results showed that the pooled infection rate of Sarcocystis spp. was 69% (95% CI: 59–78%) in sheep, which is second only to goats among ruminants in China. Of these, only 3 articles identified infected Sarcocystis species in sheep, which are S. gigantea, S. tenella, and S. arieticanis. Sarcocystis in sheep is widely distributed in the world. The prevalence of Sarcocystis in sheep was reported to be 63.83% in Iran [65], 96.9% in Mongolia [70], 95.8% in Brazil [71], and 13.20% in Egypt [72].
In this systematic review, after sheep, yak became the most common target of sarcocystosis studies in China. Yak meat contains abundant trace elements and essential fatty acids beneficial to human body [73]. Yak meat products are welcomed by consumers because of their excellent quality. There are about 1.3 million yaks in China, accounting for 90% of the world’s yak population [73]. This may reveal why there are many studies on Sarcocystis among yaks in China. The results of this study showed that the prevalence of Sarcocystis spp. was 64% (95% CI: 50–78%), with significant differences in the infection rate of Sarcocystis in yaks in different studies (p < 0.01), which may be related to a variety of factors, such as age of animals, number of samples, and detection methods.
In this systematic review, only 6, 2, and 1 studies were available for goats, water buffalo, and camels, respectively. Although only a few studies were available, it shows that Sarcocystis spp. infection occurs in these animals and deserves further attention. The pooled infection rate of Sarcocystis in goats was 71% (95% CI: 40–93%), which was highest among ruminants. The prevalence of Sarcocystis among goats in China was lower than that reported in Bahia, Brazil (91.6%) [71], and Iran (82.36%, 95% CI: 54.74–98.35%) [65]. Only one study identified infected species of Sarcocystis in goats, S. capracanis and S. hircanis [26]. The pooled infection of water buffalo was 24% (95% CI: 0–72%). The two studies on Sarcocystis of water buffalo were nearly 30 years apart, which showed high heterogeneity (I2 = 96%, p < 0.01) [18,43]. As camels live mainly in desert areas, they are mainly used as vehicles and are not a major source of meat products [74]. In this review, there is only one study on Sarcocystis of camel published in 1994, with an infection rate of 59% (95% CI: 51–65%) [14].
Our meta-analysis has several limitations: (1) the prevalence of Sarcocystis spp. in ruminants has not been reported in many regions of China; (2) the number of eligible studies is limited; (3) most of the studies were of medium or low quality, mainly because few risk factors (e.g., age, sex, and the presence of the final host) were available for analysis of Sarcocystis infection; (4) data on the ruminant living environment are insufficient and there may be different degrees of environmental pollution, which may explain the reason for the differences in the prevalence of Sarcocystis spp.; (5) the detection methods used were relatively simple, and only a few studies reported the infection of Sarcocystis species.

5. Conclusions

This meta-analysis determined the pooled infection rate of Sarcocystis in ruminants, indicating that Sarcocystis is widely present in many regions and animals in China. However, information on risk factors associated with Sarcocystis infection is very limited, and high-quality investigations are needed to further determine Sarcocystis infections in ruminants in China.

Supplementary Materials

The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/ani13010149/s1, Table S1: PRISMA checklist 2020; Figure S1: Forest plot of Sarcocystis infection according to region. Figure S2: Publications bias of studies using trim and fill analysis. Figure S3: Egger’s test for publication bias; Figure S4: Sensitivity analysis of any one included study. Figure S5: Forest plot of Sarcocystis infection according to host. Figure S6: Forest plot of Sarcocystis infection according publication years. Reference [75] are cited in the supplementary materials.

Author Contributions

Conceptualization, J.L.; methodology, Z.Z. and Z.Y.; software, Z.Z., Z.Y. and Z.F.; formal analysis, Z.Z. and Z.Y.; investigation, Z.Z., Z.Y. and Z.F.; data curation, Z.Z., Z.Y., Z.F. and J.L.; writing—original draft preparation, Z.Z. and Z.Y.; writing—review and editing, J.L. and Q.L.; project administration, J.L. and Q.L. All authors have read and agreed to the published version of the manuscript.

Funding

This study was supported by the Beijing Municipal Natural Science Foundation (6212016), and the National Natural Science Foundation of China (31972700).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Full data are available in the references list and Supplementary Files.

Conflicts of Interest

The authors state that there is no conflict of interest.

References

  1. Dubey, J.P.; Calero-Bernal, R.; Rosenthal, B.M.; Speer, C.A.; Fayer, R. Sarcocystis of Animals and Humans, 2nd ed.; CRC Press: Boca Raton, FL, USA, 2016; pp. 1–256. [Google Scholar]
  2. Dubey, J.P.; Moré, G.; van Wilpe, E.; Calero-Bernal, R.; Verma, S.K.; Schares, G. Sarcocystis rommeli, n. sp. (Apicomplexa: Sarcocystidae) from cattle (Bos taurus) and its differentiation from Sarcocystis hominis. J. Eukaryot. Microbiol. 2016, 63, 62–68. [Google Scholar] [CrossRef]
  3. Dubey, J.P.; van Wilpe, E.; Calero-Bernal, R.; Verma, S.K.; Fayer, R. Sarcocystis heydorni, n. sp. (Apicomplexa: Sarcocystidae) with cattle (Bos taurus) and human (Homo sapiens) cycle. Parasitol. Res. 2015, 114, 4143–4147. [Google Scholar] [CrossRef] [PubMed]
  4. Rosenthal, B.M. Zoonotic Sarcocystis. Res. Vet. Sci. 2021, 136, 151–157. [Google Scholar] [CrossRef] [PubMed]
  5. Rubiola, S.; Civera, T.; Panebianco, F.; Vercellino, D.; Chiesa, F. Molecular detection of cattle Sarcocystis spp. in North-West Italy highlights their association with bovine eosinophilic myositis. Parasit. Vectors 2021, 23, 223. [Google Scholar] [CrossRef] [PubMed]
  6. Dong, H.; Lu, Y.Y.; Yang, Y.R. Epidemiology and classification of Sarcocystis in sheep and goat. Chin. J. Zoonoses 2017, 33, 828–836. (In Chinese) [Google Scholar]
  7. Dong, H.; Su, R.J.; Wang, Y.H.; Tong, Z.X.; Zhang, L.X.; Yang, Y.R.; Hu, J.J. Sarcocystis species in wild and domestic sheep (Ovis ammon and Ovis aries) from China. BMC Vet. Res. 2018, 14, 377. [Google Scholar] [CrossRef]
  8. Ying, Z.; Zhu, Z.F.; Yang, X.; Liu, J.; Liu, Q. Prevalence and associated risk factors of Neospora caninum infection among cattle in mainland China: A systematic review and meta-analysis. Prev. Vet. Med. 2022, 201, 105593. [Google Scholar] [CrossRef]
  9. Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A.; PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev. 2015, 4, 1. [Google Scholar] [CrossRef] [Green Version]
  10. Ah, R.Z.; Tan, S.K. Investigation on Sarcocystis infection in Tibetan sheep in Gangcha Country, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 2004, 34, 19. (In Chinese) [Google Scholar]
  11. An, N.; Xin, D.; Shan, B.; Yu, Z.X. Detection of Sarcocystis in yak by microscopy. Chin. Diary Cattl. 2006, 12, 34–35. (In Chinese) [Google Scholar]
  12. Cai, J.Z.; Zhao, M.Y. Investigation on the infection of Taenia and Sarcocystis in cattle and sheep in Tole Pasture. Chin. Q.H. J. Ani. Vet. Sci. 1990, 2, 35–36. (In Chinese) [Google Scholar]
  13. Chen, H.Z. Investigation on Sarcocystis of swine, cattle and sheep in South Henan. Chin. J. Vet. Med. 1989, 7, 26. (In Chinese) [Google Scholar]
  14. Chen, T.J. Post-mortem quarantine investigation and treatment of Sarcocystis in slaughtered camels. Chin. J. Meat Hygiene. 1994, 10, 13. (In Chinese) [Google Scholar]
  15. Chen, L. Investigation on Sarcocystis infection in commercial yaks in Chengduo County, Qinghai Province. Chi. Ani. Hus. Vet. Med. 2012, 44, 111–112. (In Chinese) [Google Scholar]
  16. Chen, X.W.; Wen, T.; Hu, J.J.; Liu, T.T.; Esch, G.W.; Liang, Y.; Li, H.L.; Huang, S. Sarcocystis dehongensis n. sp. (Apicomplexa: Sarcocystidae) from water buffalo (Bubalus bubalis) in China. Parasitol. Res. 2017, 116, 2145–2150. [Google Scholar] [CrossRef]
  17. Dong, S.Z.; Liu, S.G. Investigation on Sarcocystis of goats in Gansu Province. Chin. J. Vet. Sci. Tech. 1984, 10, 37–39. (In Chinese) [Google Scholar]
  18. Geng, T.Y. Investigation on Sarcocystis infection of yaks in Xinghai, Qinghai Province. Chin. J. Vet. Med. 2009, 45, 49. (In Chinese) [Google Scholar]
  19. Guo, Z.P. Investigation on Sarcocystis of sheep carcass in Dilan Country, Qinghai Province. Chi. Ani. H. Insp. 2011, 28, 44. (In Chinese) [Google Scholar]
  20. Han, X.M.; Wu, X.T.; Liu, B.R.; Liu, P.Y.; Tang, X.Y. Examination of zoonotic parasitic diseases in livestock in Xining, Qinghai Province. Chin. J. Zoonoses 2001, 17, 123–124. (In Chinese) [Google Scholar]
  21. Han, L.; Yan, Z.L. Investigation on Sarcocystis infection in sheep in six counties of Qinghai Province. Chin. Ani. H. Insp. 2005, 22, 41. (In Chinese) [Google Scholar]
  22. Hu, J.J.; Huang, S.; Wen, T.; Esch, G.W.; Liang, Y.; Li, H.L. Sarcocystis spp. in domestic sheep in Kunming City, China: Prevalence, morphology, and molecular characteristics. Parasite. 2017, 24, 30. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  23. Hu, J.J.; Huang, S.; Wen, T.; Esch, G.W.; Liang, Y.; Li, H.L. Morphology, molecular characteristics, and demonstration of a definitive host for Sarcocystis rommeli from Cattle (Bos taurus) in China. J. Parasitol. 2017, 103, 471–476. [Google Scholar] [CrossRef] [PubMed]
  24. Hu, J.J.; Liu, T.T.; Liu, Q.; Esch, G.W.; Chen, J.Q.; Huang, S.; Wen, T. Prevalence, morphology, and molecular characteristics of Sarcocystis spp. in domestic goats (Capra hircus) from Kunming, China. Parasitol. Res. 2016, 115, 3973–3981. [Google Scholar] [CrossRef]
  25. Hu, J.J.; Wen, T.; Chen, X.W.; Liu, T.T.; Esch, G.W.; Huang, S. Prevalence, morphology, and molecular characterization of Sarcocystis heydorni sarcocysts from cattle (Bos taurus) in China. J. Parasitol. 2016, 102, 545–548. [Google Scholar] [CrossRef] [PubMed]
  26. Jiang, Y.P.; Liu, J.R.; Miu, L.W.; Li, Z.D.; Luo, Q.G.; Liu, C.S. Investigation on the prevalence of Sarcocystis in sheep in Shihezi area of Xinjiang Province. Chin. J. Vet. Sci. Tech. 1985, 12, 20–22. (In Chinese) [Google Scholar]
  27. Kang, M.; Li, Y.; Shi, W.H.; Xi, J.G.H. Study on the infection of Sarcocystis in the diaphragm of livestock in Hualong Country, Qinghai Province. J. Anhui Agri. Sci. 2013, 41, 1154–1156. (In Chinese) [Google Scholar]
  28. La, M.J.; Ren, Q.C. Investigation on Sarcocystis infection of Tibetan mutton in Maqin Country, Qinghai Province. Chin. J. Vet. Sci. 2004, 40, 50–51. (In Chinese) [Google Scholar]
  29. Li, O.; Xu, T.D.; Li, W.; Sai, Q. Investigation on Sarcocystis of sheep in Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 1989, 2, 12–13. (In Chinese) [Google Scholar]
  30. Li, F.Y. Investigation of Sarcocystis infection in sheep in Angssuto town, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 2007, 4, 33. (In Chinese) [Google Scholar]
  31. Li, S.S. Investigation report on Sarcocystis infection of slaughtered cattle in market. Chin. Q.H. J. Vet. Ani. Vet. Sci. 2014, 44, 26. (In Chinese) [Google Scholar]
  32. Li, C.H.; Cai, J.Z. Investigation of Sarocystis in yaks and sheep in some areas of Qinghai Province. Chin. J. Vet. Sci. 2009, 45, 33–35. (In Chinese) [Google Scholar]
  33. Li, W.; Li, O.; Li, Z.N.; Jiang, Y.S.; Shi, H.N.; Yun, S.M. Investigation on Sarcocystis infection of sheep on a farm in Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 1991, 1, 18–19. (In Chinese) [Google Scholar]
  34. Li, X.W.; Wang, Y.P.; Li, W.L. Investigation of Sarcocystis infection in swine and beef. J. Henan Agri. Sci. 1990, 5, 27–28. (In Chinese) [Google Scholar]
  35. Li, C.Y.; Yun, S.L. Report on inspection of Sarcocystis in sheep carcass. Chin. Q.H. J. Ani. Vet. Sci. 1991, 2, 25. (In Chinese) [Google Scholar]
  36. Liu, X.G.; Yu, J.L.; Zhu, R.; Yan, B.G.; Shen, J.Y. Investigation of Sarcocystis infection in sheep. Chin. J. Meat Hygiene 1996, 10, 10–11. (In Chinese) [Google Scholar]
  37. Ma, D.D.; Cai, J.Z.; Li, C.H.; Lei, M.T.; Sun, J. Investigation of Sarcocystis infection in yaks in Qinghai Province. Chin. Ani. Hus. Vet. Med. 2017, 49, 149–152. (In Chinese) [Google Scholar]
  38. Niang, J.X.; Cai, D.; Yan, Q.L. Investigation of Sarcocystis infection in yaks in Huangnan Area, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 1985, 4, 30–31. (In Chinese) [Google Scholar]
  39. Shan, Q.L.M.; Zhu, C.G.; Ji, R.Y.; Shi, B.; Tang, W.Q.; Suo, L.Q.Y.; Xia, C.Y. Species identification and evolutionary analysis of Sarcocystis from cattle and sheep in Tibet. Chin. Herb. Sci. 2021, 5, 27–30. (In Chinese) [Google Scholar]
  40. Shang, H.Z.; Zhu, X.W.; Qi, Y.X.; Gao, L.Y. Investigation on Sarcocystis infection of cattle and sheep in Tianjun Country, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 1990, 2, 34. (In Chinese) [Google Scholar]
  41. Shi, Y.L. Investigation on Sarcocystis infection of water buffalo and cattle in western Hunan. Chin. Hunan Ani. Hus. Vet. Med. 1991, 2, 34. (In Chinese) [Google Scholar]
  42. Su, X.X.; Xie, C.Y.; Kang, M. Investigation on Sarcocystis infection of Tibetan sheep in Gonghe Country, Qinghai Province. Chin. J. Vet. Sci. 2019, 12, 52–54. (In Chinese) [Google Scholar]
  43. Sun, Y.L.; Ju, J.L.; Su, X.X.; Xie, C.Y.; Li, Y.; Kang, M. Infection survey and morphological characteristics of Sarcocystis spp. in naturally infected Tibetan sheep from Qinghai in northwestern China. Parasitol. Int. 2021, 80, 102219. [Google Scholar] [CrossRef] [PubMed]
  44. Tian, W.F.; Jia, J.; Liang, S.Z.; Niu, H.F. Investigation on Sarcocystis infection of cattle and sheep in Gannan Tibetan Autonomous Prefecture. Chin. Gansu Ani. Hus. Vet. Med. 1989, 2, 16. (In Chinese) [Google Scholar]
  45. Wang, G.L.; Xu, M. Investigation of Sarcocystis infection in cattle in Burqin Country, Xinjiang. Xinjiang J. Ani. Hus. 1989, 2, 36. (In Chinese) [Google Scholar]
  46. Wei, T.; Zhang, P.C.; Han, M.C.; Cai, D.; Liu, Q.H. Investigation on Sarcocystis infection of yak in Zeku Country, Qinghai Province. Chin. J. Trad. Vet. Sci. 1983, 2, 11–15. (In Chinese) [Google Scholar]
  47. Wei, T.; Zhang, P.C.; Dong, M.X.; Sun, Y.J.; Li, W.Y. Investigation on Sarcocystis infection of yaks in Tianzhu, Qinghai Province. Chin. Yak. 1983, 1, 41–44. (In Chinese) [Google Scholar]
  48. Xue, R.; Yan, W.C.; Qian, W.F.; Wang, T.Q.; Zhang, M.; Wei, Z.G.; Han, L.F.; He, B.; Dou, J.C. Prevalence and molecular characterization of Sarcocystis infections of retail beef products from central China. Acta Trop. 2019, 190, 339–343. [Google Scholar] [CrossRef]
  49. Yang, Y.R.; Dong, H.; Su, R.J.; Wang, Y.H.; Wang, R.H.; Jiang, Y.B.; Tong, Z.X. High prevalence of Sarcocystis spp. infections in cattle (Bos taurus) from central China. Parasitol. Int. 2018, 67, 800–804. [Google Scholar] [CrossRef]
  50. Yin, H. Examination of Sarcocystis infection in sheep carcasses in Xunhua Country, Qinghai Province. Chin. J. Vet. Parasitol. 2004, 12, 64. (In Chinese) [Google Scholar]
  51. Zhan, S.X.; Zhao, C.C.; Qi, H.Y.; Jia, Y.Z.; Zhang, Y.H. Investigation of Sarcocystis infection in sheep in Delhi City, Qinghai Province. Chin. Ani. H. Insp. 2001, 1, 28–29. (In Chinese) [Google Scholar]
  52. Zhang, C.W. Investigation on Sarcocystis infection of cattle and sheep in Hualong Country, Qinghai Province. Chin. Mod. Agri. Sci. Tech. 2009, 3, 217. (In Chinese) [Google Scholar]
  53. Zhang, G.L. Investigation on Sarcocystis infection of commercial yaks in Ulan Country, Qinghai Province. Chin. Contemp. Ani. Hus. 2009, 11, 20–21. (In Chinese) [Google Scholar]
  54. Zhang, H.B.; Cang, N.G.; Hou, H.M.; Ah, S.P.; Zhou, M.; Ka, D.Z.; Sun, Y.L.; Kang, M. Investigation of Sarcocystis infection in the diaphragm of cattle and sheep in Zeku Country, Qinghai Province. Chin. Ani. Hus. Vet. Med. 2014, 46, 138. (In Chinese) [Google Scholar]
  55. Zhang, P.C.; Dong, M.X.; Wei, T.; Wang, X.Y.; Xiao, H.; Yang, J.R.; Liang, S.Z. Investigation on Sarcocystis of yak in Luqu Country, Gansu Province. Chin. J. Trad. Vet. Sci. 1987, 6, 18–20. (In Chinese) [Google Scholar]
  56. Zhang, G.C.; Wei, L.; Zhang, Y.C.; Yang, J.Y.; Feng, Z.F.; Bai, Y.Y.; Bao, Z.X.; Wang, L.P.; Han, X.Y. Investigation of Sarcocystis infection in sheep in Datong Country, Qinghai Province. Chin. J. Vet. Parasitol. 2007, 15, 38–39. (In Chinese) [Google Scholar]
  57. Zhang, X.J.; Yang, X.C. Investigation and morphological observation on Sarcocystis of yak in Yushu, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 1989, 6, 20–22. (In Chinese) [Google Scholar]
  58. Zhao, Y.L. Investigation on Sarcocystis infection of commercial sheep in Huzhu Country, Qinghai Province. Chin. Q.H. J. Ani. Vet. Sci. 2011, 41, 59. (In Chinese) [Google Scholar]
  59. Zhao, G. Investigation on the Sarcocystis infection of Tibetan sheep in Heka Town, Xinghai Country. Chin. Ani. Hus. Vet. Med. 2012, 44, 106. (In Chinese) [Google Scholar]
  60. Zhao, W.S.; Yi, G.; Wu, B.; Bu, D.; Cai, R.J.; Ma, W.Z. Investigation on Sarcocystis infection of yak in Dari Country, Qinghai Province. Chin. Q.H. J. Vet. Sci. 1991, 3, 19. (In Chinese) [Google Scholar]
  61. Zhong, W.D. Investigation on Sarcocystis infection of sheep in Minhe Country. Chin. Ani. H. Insp. 2009, 9, 50. (In Chinese) [Google Scholar]
  62. Zhou, W.Y. Sampling survey and analysis of Sarcocystis in commercial livestock in Lenghu area, Qinghai Province. Chin. Ani. H. Insp. 2011, 28, 51–52. (In Chinese) [Google Scholar]
  63. R Core Team. R: A Language and Environment for Statistical Computing; R Foundation for Statistical Computing: Vienna, Austria, 2021; Available online: https://www.R-project.org (accessed on 31 March 2021).
  64. DerSimonian, R.; Laird, N. Meta-analysis in clinical trials revisited. Contemp. Clin. Trials. 2015, 45, 139–145. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  65. Anvari, D.; Narouei, E.; Hosseini, M.; Narouei, M.R.; Daryani, A.; Shariatzadeh, S.A.; Pagheh, A.S.; Gholami, S.; Sarvi, S.; Sargazi, D.; et al. Sarcocystosis in ruminants of Iran, as neglected food-borne disease: A systematic review and meta-analysis. Acta Parasitol. 2022, 65, 555–568. [Google Scholar] [CrossRef] [PubMed]
  66. Tenter, A.M. Current research on Sarcocystis species of domestic animals. Int. J. Parasitol. 1995, 25, 1311–1330. [Google Scholar] [CrossRef] [PubMed]
  67. Zeng, H.; Van Damme, I.; Kabi, T.W.; Šoba, B.; Gabriël, S. Sarcocystis species in bovine carcasses from a Belgian abattoir: A cross-sectional study. Parasit. Vectors. 2021, 14, 271. [Google Scholar] [CrossRef] [PubMed]
  68. van Bree, F.P.J.; Bokken, G.C.A.M.; Mineur, R.; Franssen, F.; Opsteegh, M.; van der Giessen, J.W.B.; Lipman, L.J.A.; Overgaauw, P.A.M. Zoonotic bacteria and parasites found in raw meat-based diets for cats and dogs. Vet. Rec. 2018, 182, 50. [Google Scholar] [CrossRef]
  69. Wouda, W.; Snoep, J.J.; Dubey, J.P. Eosinophilic myositis due to Sarcocystis hominis in a beef cow. J. Comp. Pathol. 2006, 135, 249–253. [Google Scholar] [CrossRef]
  70. Fukuyo, M.; Battsetseg, G.; Byambaa, B. Prevalence of Sarcocystis infection in meat-producing animals in Mongolia. Southeast Asian J. Trop. Med. Public Health 2002, 33, 490–495. [Google Scholar]
  71. Bittencourt, M.V.; Meneses, I.D.; Ribeiro-Andrade, M.; de Jesus, R.F.; de Araújo, F.R.; Gondim, L.F. Sarcocystis spp. in sheep and goats: Frequency of infection and species identification by morphological, ultrastructural, and molecular tests in Bahia, Brazil. Parasitol Res. 2016, 115, 1683–1689. [Google Scholar] [CrossRef]
  72. El-Morsey, A.; Abdo, W.; Zaid, A.A.A.; Sorour, S.S.G. Morphologic and molecular identification of three macroscopic Sarcocystis species infecting domestic sheep (Ovis aries) and cattle (Bos taurus) in Egypt. Parasitol. Res. 2021, 120, 637–654. [Google Scholar] [CrossRef]
  73. Wang, H.B.; Zan, L.S.; Zhang, Y.Y. Profiling of the yak skeletal muscle tissue gene expression and comparison with the domestic cattle by genome array. Animal 2014, 8, 28–35. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  74. Yang, X.; Li, Y.; Wang, Y.; Wang, J.; Lai, P.; Li, Y.; Song, J.; Qi, M.; Zhao, G. Molecular characterization of Blastocystis sp. In Camelus bactrianus in Northwestern China. Animals 2021, 11, 3016. [Google Scholar] [CrossRef] [PubMed]
  75. Page, M.J.; McKenzie, J.E.; Bossuyt, P.M.; Boutron , I.; Hoffmann, T.C.; Mulrow, C.D.; Shamseer, L.; Tetzlaff, J.M.; Akl, E.A.; Brennan, S.E.; et al. The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. BMJ 2021, 372:n71. [Google Scholar] [CrossRef]
Figure 1. PRISMA flowchart of the systematic review and meta-analysis process shows the inclusion and exclusion of studies.
Figure 1. PRISMA flowchart of the systematic review and meta-analysis process shows the inclusion and exclusion of studies.
Animals 13 00149 g001
Figure 2. Forest plot of the prevalence of Sarcocystis infection among ruminants in China. CI: confidence interval. The first column “Study” included “Author + Year” [7,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62].
Figure 2. Forest plot of the prevalence of Sarcocystis infection among ruminants in China. CI: confidence interval. The first column “Study” included “Author + Year” [7,10,11,12,13,14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62].
Animals 13 00149 g002
Figure 3. Prevalence of Sarcocystis infection among ruminants in mainland China.
Figure 3. Prevalence of Sarcocystis infection among ruminants in mainland China.
Animals 13 00149 g003
Table 1. Included studies of Sarcocystis infection in ruminants.
Table 1. Included studies of Sarcocystis infection in ruminants.
First Author, YearHostProvincePeriod of StudyDetection MethodPositive Samples/Total Samples (%)Reference
A et al., 2004Tibetan sheepQinghai2003Macroscopy, LM32/53 (60)[10]
An et al., 2006YaksXinjiang2001LM14/65 (22)[11]
An et al., 2006YaksXinjiang2004LM23/80 (29)[11]
Cai et al., 1990YaksQinghai1988Macroscopy, LM153/210 (73)[12]
Cai et al., 1990Tibetan sheepQinghai1988Macroscopy, LM135/208 (65)[12]
Chen, 1989CattleHenan1985Macroscopy, LM, H&E33/40 (82)[13]
Chen, 1989SheepHenan1985Macroscopy, LM, H&E32/60 (53)[13]
Chen, 1994CamelInner Mongolia1992Macroscopy, LM113/193 (59)[14]
Chen, 2012YaksQinghai2011LM58/214 (27)[15]
Chen et al., 2017Water buffaloYunnann.s.LM, TEM, PCR51/756 (7)[16]
Dong et al., 1984GoatsGansun.s.LM; Pepsin digestion examination1443/3064 (47)[17]
Dong et al., 2018SheepHenan2014–2017LM; Pepsin digestion examination; PCR277/536 (52)[7]
Dong et al., 2018SheepXinjiang2014–2017LM; Pepsin digestion examination; PCR58/102 (57)[7]
Geng, 2009YaksQinghai2008LM227/327 (69)[18]
Guo, 2011SheepQinghai2011Macroscopy, LM201/393 (51)[19]
Han et al., 2001YaksQinghain.s.LM125/200 (62)[20]
Han et al., 2001SheepQinghain.s.LM376/511 (74)[20]
Han et al., 2005SheepQinghain.s.LM74/120 (62)[21]
Hu et al., 2017SheepYunnann.s.LM, TEM, PCR79/86 (92)[22]
Hu et al., 2017CattleYunnann.s.LM, TEM, PCR6/34 (18)[23]
Hu et al., 2016GoatsYunnan2014–2015LM, TEM, PCR174/225 (77)[24]
Hu et al., 2016CattleYunnan2014–2015LM, TEM, PCR173/1630 (11)[25]
Jiang et al., 1985aSheepXinjiangn.s.LM; Pepsin digestion examination1912/2108 (91)[26]
Jiang et al., 1985bSheepXinjiangn.s.LM; Pepsin digestion examination96/148 (65)[26]
Kang, 2013YaksQinghain.s.LM12/30 (40)[27]
Kang, 2013SheepQinghain.s.LM29/31 (94)[27]
La et al., 2014Tibetan sheepQinghai2003LM195/300 (65)[28]
Li et al., 1989SheepQinghai1986LM584/598 (98)[29]
Li, 2007SheepQinghain.s.Macroscopy, LM16/100 (16)[30]
Li, 2014GoatsQinghai2011Macroscopy, LM2/13 (15)[31]
Li, 2014SheepQinghai2011Macroscopy, LM10/150 (7)[31]
Li et al., 2009SheepQinghai2006–2007LM83/101 (82)[32]
Li et al., 2009YaksQinghai2006–2007LM70/121 (58)[32]
Li et al., 1991SheepQinghai1989Macroscopy, LM151/152 (99)[33]
Li et al., 1990CattleHenann.s.LM; Pepsin digestion examination, H&E220/306 (72)[34]
Li et al., 1991SheepQinghai1990Macroscopy, LM114/119 (96)[35]
Liu et al., 1996SheepLiaoningn.s.Macroscopy, LM7/24 (29)[36]
Ma et al., 2017YaksQinghain.s.LM144/390 (37)[37]
Niang et al., 1985YaksQinghai1984LM19/20 (95)[38]
Shan et al., 2021GoatsTibet2019Macroscopy, LM11/11 (100)[39]
Shan et al., 2021SheepTibet2019Macroscopy, LM5/6 (83)[39]
Shan et al., 2021YaksTibet2019Macroscopy, LM22/39 (56)[39]
Shan et al., 2021CattleTibet2019Macroscopy, LM6/6 (100)[39]
Shang et al., 1990YaksQinghai1989LM115/120 (96)[40]
Shang et al., 1990SheepQinghai1989LM186/192 (97)[40]
Shi et al., 1991CattleHunan1990Macroscopy, LM12/26 (46)[41]
Shi et al., 1991Water buffaloHunan1990Macroscopy, LM7/14 (50)[41]
Su et al., 2019Tibetan sheepQinghai2017Macroscopy, LM172/576 (30)[42]
Sun et al., 2021Tibetan sheepQinghai2017–2018LM, H&E, TEM, PCR577/1155 (50)[43]
Tian et al., 1989YaksGansu1985Macroscopy, LM266/286 93)[44]
Tian et al., 1989SheepGansu1985Macroscopy, LM359/391 (92)[44]
Wang et al., 1989CattleXinjiang1988LM63/70 (90)[45]
Wei et al., 1983YaksGansu1982LM139/150 (93)[46]
Wei et al., 1983YaksGansu1981LM; Pepsin digestion examination115/132 (87)[47]
Xue et al., 2019CattleHenan2017LM, H&E, PCR20/62 (32)[48]
Yang et al., 2018CattleHenan2014–2016LM; Pepsin digestion examination, TEM, PCR215/521 (41)[49]
Yin, 2004SheepQinghai2003Macroscopy, LM88/135 (65)[50]
Zhan et al., 2001GoatsQinghai2000Macroscopy, LM74/80 (92)[51]
Zhan et al., 2001SheepQinghai2000Macroscopy, LM51/55 (93)[51]
Zhang, 2009YaksQinghain.s.Macroscopy, LM22/150 (15)[52]
Zhang, 2009SheepQinghain.s.Macroscopy, LM121/200 (60)[52]
Zhang, 2010YaksQinghai2008LM45/134 (34)[53]
Zhang et al., 2014YaksQinghain.s.Macroscopy, LM16/55 (29)[54]
Zhang et al., 2014SheepQinghain.s.Macroscopy, LM56/59 (95)[54]
Zhang et al., 1987YaksGansu1986Macroscopy, LM146/150 (97)[55]
Zhang et al., 2007SheepQinghai2005–2006LM119/200 (59)[56]
Zhang et al., 1989YaksQinghai1986H&E284/286 (99)[57]
Zhao, 2011SheepQinghai2010LM93/150 (62)[58]
Zhao, 2012Tibetan sheepQinghai2010LM106/200 (53)[59]
Zhao et al., 1991YaksQinghai1988Macroscopy, LM126/187 (67)[60]
Zhong, 2009SheepQinghai2007LM234/400 (58)[61]
Zhou, 2011aSheepQinghai2010LM79/150 (53)[62]
Zhou, 2011bGoatsQinghai2010LM84/135 (62)[62]
LM: light microscopy; H&E: hematoxylin-eosin; PCR: polymerase chain reaction; TEM: transmission electron micrograph; n.s.: not specified.
Table 2. Normal distribution test for the normal rate and the different conversion of the normal rate.
Table 2. Normal distribution test for the normal rate and the different conversion of the normal rate.
Conversion FormWp
PRAW0.93510.001641
PLN0.83411.38 × 10−7
PLOGITNaNNA
PAS0.967570.05696
PFT0.964580.03809
PRAW: Original rate; PLN: logarithmic conversion; PLOGIT: logit transformation; PAS: arcsine transformation; PFT: double-arcsine transformation; NaN: meaningless number; NA: missing data.
Table 3. Pooled prevalence of subgroup analysis (region, host and publish year) for Sarcocystis infection in ruminants in mainland China.
Table 3. Pooled prevalence of subgroup analysis (region, host and publish year) for Sarcocystis infection in ruminants in mainland China.
Subgroup VariableNo. StudiesNo. Positive/ No. TestedPrevalence (95% CI)Heterogeneity
Qp-ValueI2 (%)
Region
Northeast China17/2429% (13–51%)0.00--
Central China8816/156554% (42–66%)104.73<0.0193%
Northwest China5510,205/15,91967% (59–75%)4972.27<0.0199%
Southwest China9527/279364% (32–91%)898.07<0.0199%
Host
Camel1113/19359% (51–66%)0.00--
Cattle9748/269556% (31–79%)836.64<0.0199%
Goats61788/352871% (40–93%)209.62<0.0198%
Sheep346707/976969% (59–78%)2928.83<0.0199%
Water buffalo258/77024% (0–72%)15.02<0.0193%
Yaks212141/334664% (50–78%)1473.82<0.0199%
Publish year
<2005337771/10,58885% (77–90%)2738.77<0.0198%
2005–2010121048/199846% (33–60%)337.88<0.0196%
2011–201512746/158050% (30–70%)352.37<0.0194%
>2016161990/613552% (33–71%)1551.60<0.0198%
Total7311,555/20,30165% (57–72%)8755.27<0.0199%
Disclaimer/Publisher’s Note: The statements, opinions and data contained in all publications are solely those of the individual author(s) and contributor(s) and not of MDPI and/or the editor(s). MDPI and/or the editor(s) disclaim responsibility for any injury to people or property resulting from any ideas, methods, instructions or products referred to in the content.

Share and Cite

MDPI and ACS Style

Zhu, Z.; Ying, Z.; Feng, Z.; Liu, Q.; Liu, J. The Occurrence and Meta-Analysis of Investigations on Sarcocystis Infection among Ruminants (Ruminantia) in Mainland China. Animals 2023, 13, 149. https://doi.org/10.3390/ani13010149

AMA Style

Zhu Z, Ying Z, Feng Z, Liu Q, Liu J. The Occurrence and Meta-Analysis of Investigations on Sarcocystis Infection among Ruminants (Ruminantia) in Mainland China. Animals. 2023; 13(1):149. https://doi.org/10.3390/ani13010149

Chicago/Turabian Style

Zhu, Zifu, Zhu Ying, Zixuan Feng, Qun Liu, and Jing Liu. 2023. "The Occurrence and Meta-Analysis of Investigations on Sarcocystis Infection among Ruminants (Ruminantia) in Mainland China" Animals 13, no. 1: 149. https://doi.org/10.3390/ani13010149

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop