Hostname: page-component-586b7cd67f-t7fkt Total loading time: 0 Render date: 2024-11-25T08:59:10.482Z Has data issue: false hasContentIssue false

Global prevalence of Cryptosporidium spp. in pigs: a systematic review and meta-analysis

Published online by Cambridge University Press:  20 March 2023

Yuancai Chen
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Huikai Qin
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Yayun Wu
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Huiyan Xu
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Jianying Huang
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Junqiang Li
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
Longxian Zhang*
Affiliation:
College of Veterinary Medicine, Henan Agricultural University, Zhengzhou 450002, P. R. China
*
Author for correspondence: Longxian Zhang, E-mail: [email protected]

Abstract

Cryptosporidium spp. are significant opportunistic pathogens causing diarrhoea in humans and animals. Pigs are one of the most important potential hosts for Cryptosporidium. We evaluated the prevalence of Cryptosporidium in pigs globally using published information and a random-effects model. In total, 131 datasets from 36 countries were included in the final quantitative analysis. The global prevalence of Cryptosporidium in pigs was 16.3% (8560/64 809; 95% confidence interval [CI] 15.0–17.6%). The highest prevalence of Cryptosporidium in pigs was 40.8% (478/1271) in Africa. Post-weaned pigs had a significantly higher prevalence (25.8%; 2739/11 824) than pre-weaned, fattening and adult pigs. The prevalence of Cryptosporidium was higher in pigs with no diarrhoea (12.2%; 371/3501) than in pigs that had diarrhoea (8.0%; 348/4874). Seven Cryptosporidium species (Cryptosporidium scrofarum, Cryptosporidium suis, Cryptosporidium parvum, Cryptosporidium muris, Cryptosporidium tyzzeri, Cryptosporidium andersoni and Cryptosporidium struthioni) were detected in pigs globally. The proportion of C. scrofarum was 34.3% (1491/4351); the proportion of C. suis was 31.8% (1385/4351) and the proportion of C. parvum was 2.3% (98/4351). The influence of different geographic factors (latitude, longitude, mean yearly temperature, mean yearly relative humidity and mean yearly precipitation) on the infection rate of Cryptosporidium in pigs was also analysed. The results indicate that C. suis is the dominant species in pre-weaned pigs, while C. scrofarum is the dominant species in fattening and adult pigs. The findings highlight the role of pigs as possible potential hosts of zoonotic cryptosporidiosis and the need for additional studies on the prevalence, transmission and control of Cryptosporidium in pigs.

Type
Research Article
Creative Commons
Creative Common License - CCCreative Common License - BY
This is an Open Access article, distributed under the terms of the Creative Commons Attribution licence (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted re-use, distribution and reproduction, provided the original article is properly cited.
Copyright
Copyright © The Author(s), 2023. Published by Cambridge University Press

Introduction

Cryptosporidium is an opportunistic zoonotic parasite found worldwide that infects many vertebrate hosts and typically causes self-limiting diarrhoea in humans and livestock (Kotloff, Reference Kotloff2017; Hatam-Nahavandi et al., Reference Hatam-Nahavandi, Ahmadpour, Carmena, Spotin, Bangoura and Xiao2019). Cryptosporidium is commonly found in the intestines of humans and animals and is transmitted by the fecal–oral route (Bouzid et al., Reference Bouzid, Hunter, Chalmers and Tyler2013). Children, immunodeficient individuals and newborn animals are among the groups that are susceptible to Cryptosporidium infection (Checkley et al., Reference Checkley, White, Jaganath, Arrowood, Chalmers, Chen, Fayer, Griffiths, Guerrant, Hedstrom, Huston, Kotloff, Kang, Mead, Miller, Petri, Priest, Roos, Striepen, Thompson, Ward, Van Voorhis, Xiao, Zhu and Houpt2015). Among animals susceptible to Cryptosporidium, pigs are considered as one of the main reservoir hosts (Qi et al., Reference Qi, Zhang, Xu, Zhang, Xing, Tao and Zhang2020). There are no effective vaccines that can prevent cryptosporidiosis in humans or livestock (Dumaine et al., Reference Dumaine, Tandel and Striepen2020).

Globally, the first report of 3 pig cases of cryptosporidiosis was in 1977 (Kennedy et al., Reference Kennedy, Kreitner and Strafuss1977). Pigs with cryptosporidiosis are characterized by diarrhoea, vomiting, dehydration, reduced daily gain and a lower feed conversion rate (Vítovec and Koudela, Reference Vítovec and Koudela1992; Quílez et al., Reference Quílez, Sánchez-Acedo, Clavel, del Cacho and López-Bernad1996; Enemark et al., Reference Enemark, Ahrens, Bille-Hansen, Heegaard, Vigre, Thamsborg and Lind2003), and the parasites mainly live in the intestinal tract and gallbladder (Fleta et al., Reference Fleta, Sánchez-Acedo, Clavel and Quílez1995). There is considerable genetic variation in the genus Cryptosporidium; there are 44 known species, and more than 120 genotypes of Cryptosporidium have been identified (Ryan et al., Reference Ryan, Feng, Fayer and Xiao2021). Thirteen different Cryptosporidium species/genotypes have been isolated in pigs, namely Cryptosporidium scrofarum (previously Cryptosporidium pig genotype II), Cryptosporidium suis (previously Cryptosporidium pig genotype I), Cryptosporidium muris, Cryptosporidium parvum, Cryptosporidium tyzzeri (previously Cryptosporidium mouse genotype I), Cryptosporidium hominis, Cryptosporidium meleagridis, Cryptosporidium felis, Cryptosporidium andersoni, Cryptosporidium struthioni, Cryptosporidium rat genotype, Cryptosporidium sp. Eire w65.5 and unknown Cryptosporidium genotype from pig slurry (Němejc et al., Reference Němejc, Sak, Květoňová, Hanzal, Janiszewski, Forejtek and Kváč2013b; Wang et al., Reference Wang, Gong, Zeng, Li, Zhao and Ni2021, Reference Wang, Li, Zou, Du, Song, Wang and Chen2022). Cryptosporidium scrofarum and C. suis infections account for more than 90% of cryptosporidiosis in pigs (Feng et al., Reference Feng, Ryan and Xiao2018). Cryptosporidiosis in pigs does not always cause clinical symptoms, and cases of human infection with C. scrofarum and C. suis suggest that these 2 Cryptosporidium species may be zoonotic (Kvác et al., Reference Kvác, Kvetonová, Sak and Ditrich2009c; Moore et al., Reference Moore, Elwin, Phot, Seng, Mao, Suy, Kumar, Nader, Bousfield, Perera, Bailey, Beeching, Day, Parry and Chalmers2016; Sannella et al., Reference Sannella, Suputtamongkol, Wongsawat and Cacciò2019). However, their pathogenicity and infectivity to humans are not well understood; so, they remain a potential threat to human health.

The global pig population was estimated at 952.6 million in 2020 (https://www.fao.org/). In animal husbandry, cryptosporidiosis causes huge economic losses due to weight loss in young animals, stunted growth and reduced production in adult animals (Pumipuntu and Piratae, Reference Pumipuntu and Piratae2018). Pigs are also animals that humans often contact directly or indirectly. Therefore, we performed a systematic review and meta-analysis to assess the global prevalence of Cryptosporidium in pigs. The potential risk factors including region, age and geographical and climatic factors were also analysed. The results describe the distribution characteristics of Cryptosporidium species in different age groups of pigs, and provide a basis for the prevention and control of Cryptosporidium infections.

Materials and methods

Search strategy and selection criteria

We used 5 literature databases (PubMed, Web of Science, the China National Knowledge Infrastructure, VIP Chinese Journals Database and Wanfang Data) to search for studies on the global prevalence of Cryptosporidium in pigs. All published studies on Cryptosporidium in pigs from 31 September 2022 onwards were included. We searched the 2 English databases with the term ‘Cryptosporidium’, ‘Cryptosporidiosis’ cross-referenced with ‘pig’, ‘swine’, ‘hog’, ‘wart’, ‘warthog’, ‘Phacochoerus’, ‘Suidae’, ‘boar’ or ‘piglet’. In the 3 Chinese databases, ‘Cryptosporidium’ (Chinese) and ‘pig’ (Chinese) were used as keywords. We conducted analyses in accordance with the preferred reporting items for systematic reviews and meta-analyses (PRISMA) statement and the PRISMA 2009 checklist (Table S1). The articles for which full text was not available, the first author was not contacted for more research information and/or statistics.

The following clauses were used as the criteria for article exclusion:

  1. 1) the purpose of the study was not the prevalence of Cryptosporidium in pigs;

  2. 2) the total number of pigs tested and the number of pigs that tested positive were not provided;

  3. 3) the testing method was not clearly described;

  4. 4) the sample was a mixture of specimens from multiple pig feces;

  5. 5) the study sample size was less than 20;

  6. 6) the study was a review or a case report.

Quality assessment

We used established methods to evaluate the quality of the studies (Guyatt et al., Reference Guyatt, Oxman, Vist, Kunz, Falck-Ytter, Alonso-Coello and Group2008). Studies with scores of 0 or 1 point were classified as low quality, studies with scores of 2 or 3 points were classified as medium quality, and studies with scores of 4 or 5 points were classified as high quality. A study scored 1 point if it included one of the following items:

  1. 1) a clear research goal;

  2. 2) a clearly defined research period;

  3. 3) a sample size of greater than 200;

  4. 4) a clear detection method;

  5. 5) analysis involving 3 or more influencing factors.

Data extraction

Two authors (Y. C. and H. Q.) separately screened all titles, abstracts and full texts and independently extracted the data. Disagreements were resolved by discussion with Y. W. Y. C. and H. Q. extracted information, including the first author, publication date, country, sampling time, detection method, total samples, positive samples, prevalence, study quality and Cryptosporidium species (Table S2).

Statistical analysis

All data were analysed using Stata version 14.0 (https://www.stata.com). Due to high heterogeneity (I 2 > 50%, P < 0.1) of the data, the random-effects model was used for the meta-analysis. To investigate the potential sources of heterogeneity, sensitivity analysis, subgroup analysis and meta-regression analysis were performed on the extracted data. If a study involved multiple detection methods for Cryptosporidium, the molecular results in the analysis were the first choice. We used sensitivity analysis to test the stability of the data, and the overall study was evaluated using forest plots. We evaluated the effect of selected studies on the pooled prevalence by excluding single studies sequentially (Wang et al., Reference Wang, Liu, Liu, Li, Zhang, Zhao and Zhu2018b). Publication bias of the study was evaluated using a funnel plot and Egger's tests (Egger et al., Reference Egger, Davey Smith, Schneider and Minder1997). The following potential sources of heterogeneity were examined: region (Asia compared to other regions), age (post-weaned compared to the other age groups), presence or absence of diarrhoea (diarrhoea compared to non-diarrhoea) and Cryptosporidium species (C. scrofarum compared to the other species).

The global longitude and latitude span was large, and there were significant geographical differences. The data related to geographic factors were obtained from the National Oceanic and Atmospheric Administration (NOAA, https://gis.ncdc.noaa.gov/maps/ncei/cdo/monthly). We also used subgroup analysis and meta-regression analysis to evaluate the impact of geographical risk factors, including latitude (30°–60° vs others), longitude (<−60° vs others), mean yearly temperature (5–10 °C vs others), mean yearly relative humidity (<60% vs others), mean yearly precipitation (0–400 mm vs others).

Results

Characteristics of studies

A total of 833 publications were initially identified. After screening of the title and abstract, 162 potentially relevant articles were selected for full text search. Of these, 6 were review studies, 9 had incomplete information or only provided prevalence, 6 had sample sizes less than 20, 4 were case reports and 9 lacked full text. In total, 128 publications (including 131 datasets) were of sufficient quality and were considered suitable for meta-analysis (Fig. 1).

Fig. 1. Flow diagram of the selection of eligible studies.

The selected studies came from 36 countries (Fig. 2, Table 1). A total of 71 datasets originated from Asia [China (n = 54), India (n = 2), Indonesia (n = 1), Japan (n = 6), Korea (n = 3), Thailand (n = 1), Turkey (n = 1), Vietnam (n = 3)]. A total of 30 datasets were from countries in Europe [Austria (n = 1), Czech Republic (n = 6), Denmark (n = 2), Germany (n = 2), Ireland (n = 1), Norway (n = 1), Poland (n = 2), Serbia (n = 1), Slovak Republic (n = 2), Spain (n = 8), Sweden (n = 1), Switzerland (n = 1) and the UK (n = 1)]. Eight datasets were from countries in Africa [Ghana (n = 1), Madagascar (n = 1), Malawi (n = 1), Nigeria (n = 3), South Africa (n = 1), Zambia (n = 1)]. A total of 10 datasets were from countries in North America [Canada (n = 4), Trinidad (n = 1), the USA (n = 4), Cuba (n = 1)]. Eight datasets were from South America [Argentina (n = 1), Brazil (n = 4), Colombia (n = 2), Ecuador (n = 1)]. Four datasets were from countries in Oceania [Australia (n = 4)] (Tables 1 and 2). Pre-weaned pigs were described in 48 datasets, post-weaned pigs were described in 63 datasets, fattening pigs were described in 48 datasets and adult pigs were described in 53 datasets. Most datasets lacked information on pig health status. Diarrhoea in pigs was reported in 14 datasets, and no diarrhoea in pigs was reported in 10 datasets (Table 2).

Fig. 2. Map of Cryptosporidium infection in pigs across the world. Prevalence ranges are shown in different colours. [The figure was designed using Arcgis 10.2, and the original vector diagram imported in Arcgis was adapted from Natural Earth (http://www.naturalearthdata.com).]

Table 1. Estimated pooled prevalence of Cryptosporidium infection by country/region

Table 2. Pooled prevalence of Cryptosporidium infection in pigs across the world

a Including C. parvum, C. muris, C. tyzzeri, C. andersoni, C. struthioni, Cryptosporidium spp.

Table 3. Extracted data from included studies for molecular methods of Cryptosporidium species

a Mixed infection

Cryptosporidium infection in pigs by region

The estimated Cryptosporidium prevalence in pigs ranged from 7.1% [95% confidence interval (CI) 3.6–10.5%] to 40.8% (95% CI 20.6–61.0%), with substantial heterogeneity (I 2 = 98.8%, P < 0.001). On a global scale, pooled estimated prevalence of Cryptosporidium infection in pigs was 16.3% (95% CI 15.0–17.6%, 8560/64 809) (Table 2). On 6 continents (Table 2, Figs 3–8), the infection rates of Cryptosporidium in pigs were 14.8% in Asia, 18.3% in Europe, 40.8% in Africa, 13.6% in North America, 7.1% in South America and 9.3% in Oceania. The highest number of studies on Cryptosporidium infections in pigs originated from Asia (n = 71). The highest prevalence rate was reported in South Africa [80.0% (95% CI 71.6–88.4%)], and the lowest prevalence rate was in Germany [0.4% (95% CI 0.1–0.6%)] (Table 1).

Fig. 3. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Asia.

Fig. 4. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Europe.

Fig. 5. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Africa.

Fig. 6. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in North America.

Fig. 7. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in South America.

Fig. 8. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Oceania.

Prevalence related to age, presence or absence of diarrhoea and Cryptosporidium species

The Cryptosporidium infection rate in post-weaned pigs was 25.8% (95% CI 21.8–29.8%, 2739/11 824). This was significantly higher than that in pre-weaned pigs [12.0%, 95% CI 9.9–14.0%, 1061/11 370, odds ratio (OR) 2.93, P < 0.05], fattening pigs (17.4%, 95% CI 14.8–20.0%, 1186/8815, OR 1.94, P < 0.05) and adult pigs (12.7%, 95% CI 10.4–15.1%, 980/9658, OR 2.67, P < 0.05) (Table 2). The infection rate for pigs with diarrhoea was 8.0% (95% CI 5.6–10.3%, 348/4874), while the infection rate for pigs without diarrhoea was 12.2% (95% CI 8.4–15.9%, 371/3501) (Table 2). Seven Cryptosporidium species (C. scrofarum, C. suis, C. parvum, C. muris, C. tyzzeri, C. andersoni, C. struthioni) were detected in pigs globally (Table 3). The prevalence rate of C. scrofarum was 7.9% (95% CI 6.9–8.8%, 1491/23 168) and that of C. suis was 4.7% (95% CI 3.8–5.6%, 1385/25 036) (Table 2). In Europe, C. scrofarum and C. suis infection rates were the highest, at 10.3% (678/6613) and 8.0% (881/10 951), respectively (Table S2).

Prevalence according to geographic and climatic variables

We analysed geographic subgroup factors. The prevalence of Cryptosporidium in pigs in regions with a −30° to 0° latitude range (22.9%, 95% CI 8.3–37.5%, 193/872), 0°–60° longitude range (29.3%, 95% CI 17.9–40.7%, 774/5729), 5–10 °C mean yearly temperature (25.4%, 95% CI 16.3–34.6%, 603/4991), <60% mean yearly relative humidity (21.5%, 95% CI 15.0–28.0%, 627/3921), 800–1200 mm mean yearly precipitation (20.7%, 95% CI 15.5–25.9%, 2006/10 586) was higher than that in other regions (Table S3).

Sensitivity analysis and publication bias

Sensitivity analysis indicated that the analysis was reliable (Figs S1–S6). We often used a funnel plot to measure the publication bias in selected articles. Some points fell outside the funnel and the funnel plot showed obvious asymmetry (Fig. 9). The P value was less than 0.001 by Egger's test (Table S4), indicating that obvious publication bias was found.

Fig. 9. Funnel plot for examination of publication bias of the prevalence estimates of Cryptosporidium infection in pigs across the world.

Sources of heterogeneity by meta-regression analysis

Univariate meta-regression analysis was used to determine the sources of heterogeneity. Age (P < 0.001), Cryptosporidium species (P = 0.002) and latitude (P = 0.028) were the factors that fostered heterogeneity. Region (P = 0.381), presence or absence of diarrhoea (P = 0.367), longitude (P = 0.793), mean temperature (P = 0.345), mean relative humidity (P = 0.356) and mean yearly precipitation (P = 0.548) were the factors that affected heterogeneity (Tables 2 and S3).

Discussion

A meta-analysis based on selected datasets from 36 countries on 6 continents produced an estimate of Cryptosporidium prevalence in pigs. As mentioned in a previous systematic review, Cryptosporidium prevalence in pigs was the highest in Asia, Africa and Europe (Hatam-Nahavandi et al., Reference Hatam-Nahavandi, Ahmadpour, Carmena, Spotin, Bangoura and Xiao2019). Compared with previous study, the prevalence of Cryptosporidium in pigs was the highest in Africa, Europe and Asia in our study. In Europe, the highest infection rate was in the UK (38.6%, 95% CI 33.2–44.1%) (Featherstone et al., Reference Featherstone, Marshall, Giles, Sayers and Pritchard2010), while the lowest rate was in Germany (0.4%, 95% CI 0.1–0.6%) (Wieler et al., Reference Wieler, Ilieff, Herbst, Bauer, Vieler, Bauerfeind and Zahner2001; Epe et al., Reference Epe, Coati and Schnieder2004). Cryptosporidium infection in pigs differs between countries and also in different regions of the same country. In China, 1 study reported an infection rate of only 0.9% (2/216) in pigs in Zhejiang (Liu et al., Reference Liu, Ni, Xu, Wang, Li, Shen and Yin2021), while another study found a much higher infection rate of 26.9% (101/375) in pigs in Shaanxi (Yao et al., Reference Yao, Wang, Wang, Li, Zhao, Song and Zhao2020).

Previous studies demonstrated that the rate of Cryptosporidium infection in pigs was related to age factors (Maddox-Hyttel et al., Reference Maddox-Hyttel, Langkjaer, Enemark and Vigre2006; Featherstone et al., Reference Featherstone, Marshall, Giles, Sayers and Pritchard2010). In our analysis, the Cryptosporidium infection rate in post-weaned pigs was significantly higher than that in pigs of other age groups. This is consistent with other studies (Wang et al., Reference Wang, Qiu, Jian, Zhang, Shen, Zhang and Xiao2010; Yui et al., Reference Yui, Shibahara, Kon, Yamamoto, Kameda and Taniyama2014a, Reference Yui, Nakajima, Yamamoto, Kon, Abe, Matsubayashi and Shibahara2014b; Petersen et al., Reference Petersen, Jianmin, Katakam, Mejer, Thamsborg, Dalsgaard and Enemark2015; Pettersson et al., Reference Pettersson, Ahola, Frössling, Wallgren and Troell2020; Qi et al., Reference Qi, Zhang, Xu, Zhang, Xing, Tao and Zhang2020). Post-weaned piglets may be more susceptible to Cryptosporidium infection due to reduced immunity resulting from the loss of maternal immunity, or it may be due to weaning stress (Maddox-Hyttel et al., Reference Maddox-Hyttel, Langkjaer, Enemark and Vigre2006; Li et al., Reference Li, Guo, Wen, Jiang, Ma and Han2018b). However, other studies revealed slightly divergent results. In Vietnam, the Cryptosporidium infection rate in pre-weaned pigs was higher (24.7%; 67/271) than that in post-weaned pigs (17.2%; 51/296), fattening pigs (7.1%; 7/98) or adult pigs (12.0%; 9/75) (Nguyen et al., Reference Nguyen, Honma, Geurden, Ikarash, Fukuda, Huynh, Nguyen and Nakai2012). In China, 2 studies showed higher rates of Cryptosporidium infection in finishing pigs than in pre-weaned, post-weaned and adult pigs (Chen and Huang, Reference Chen and Huang2007; Wang et al., Reference Wang, Li, Zou, Du, Song, Wang and Chen2022). In general, Cryptosporidium infection in post-weaned pigs has attracted greater attention. However, high rates of Cryptosporidium infection in pigs of other age groups suggest that different management measures among the geographical areas may be involved in infection.

The global prevalence of Cryptosporidium infection in pigs without diarrhoea was higher than that in pigs suffering from diarrhoea (P < 0.05). Most of the articles did not mention the presence or absence of diarrhoea in pigs. Insufficient data collection may also affect the stability of the results. Therefore, the relationship between Cryptosporidium infection and diarrhoea in pigs remains unclear. Experimental infection studies showed that pigs shed a high number of Cryptosporidium oocysts but had no or mild diarrhoea. When Cryptosporidium was co-infected with other enteric pathogens, pigs exhibited significant diarrhoea and had a high mortality rate (Enemark et al., Reference Enemark, Ahrens, Bille-Hansen, Heegaard, Vigre, Thamsborg and Lind2003). These results indicated that feces of apparently healthy pigs may also contain Cryptosporidium oocysts and that prevention of Cryptosporidium transmission in healthy pigs should be considered.

Pre-weaned pigs shed significantly more Cryptosporidium oocysts than older pigs, and this was associated with C. suis infection (Kvác et al., Reference Kvác, Hanzlíková, Sak and Kvetonová2009b). Piglets were more susceptible to C. suis infection, while older pigs were more susceptible to C. scrofarum (Yin et al., Reference Yin, Yuan, Cai, Shen, Jiang, Zhang and Cao2013). Compared with previous studies, C. suis and C. scrofarum are still the dominant species in pigs. Other Cryptosporidium species (C. parvum, C. muris, C. tyzzeri, C. andersoni, C. struthioni) have occasionally been reported in pigs. House mice were the main hosts of C. muris and C. tyzzeri (Feng et al., Reference Feng, Ryan and Xiao2018), and mice on pig farms may be involved in transmitting Cryptosporidium. Cryptosporidium parvum infection in pigs mainly occurred in Europe (Wieler et al., Reference Wieler, Ilieff, Herbst, Bauer, Vieler, Bauerfeind and Zahner2001; Zintl et al., Reference Zintl, Neville, Maguire, Fanning, Mulcahy, Smith and De Waal2007; Kvác et al., Reference Kvác, Sak, Hanzlíková, Kotilová and Kvetonová2009a; García-Presedo et al., Reference García-Presedo, Pedraza-Díaz, González-Warleta, Mezo, Gómez-Bautista, Ortega-Mora and Castro-Hermida2013; Němejc et al., Reference Němejc, Sak, Květoňová, Kernerová, Rost, Cama and Kváč2013a; Rzeżutka et al., Reference Rzeżutka, Kaupke, Kozyra and Pejsak2014; Pettersson et al., Reference Pettersson, Ahola, Frössling, Wallgren and Troell2020), Asia (Katsuda et al., Reference Katsuda, Kohmoto, Kawashima and Tsunemitsu2006; Qi et al., Reference Qi, Zhang, Xu, Zhang, Xing, Tao and Zhang2020; Yao et al., Reference Yao, Wang, Wang, Li, Zhao, Song and Zhao2020; Liu et al., Reference Liu, Ni, Xu, Wang, Li, Shen and Yin2021; Resnhaleksmana et al., Reference Resnhaleksmana, Wijayanti and Artama2021) and North America (Atwill et al., Reference Atwill, Sweitzer, Pereira, Gardner, Van Vuren and Boyce1997; Farzan et al., Reference Farzan, Parrington, Coklin, Cook, Pintar, Pollari and Dixon2011; Budu-Amoako et al., Reference Budu-Amoako, Greenwood, Dixon, Barkema, Hurnik, Estey and McClure2012). Cryptosporidium parvum may play a role in zoonotic transmission on pig farms. Therefore, necessary measures should be taken to reduce contact between breeders and pigs to reduce the transmission of Cryptosporidium from pigs to humans.

Oocysts can survive for a long time under many environmental conditions (Rose et al., Reference Rose, Huffman and Gennaccaro2002; Gorospe, Reference Gorospe2005; Alum et al., Reference Alum, Absar, Asaad, Rubino and Ijaz2014), and a single oocyst is sufficient to infect and cause disease in a susceptible host (Ramirez et al., Reference Ramirez, Ward and Sreevatsan2004). The prevalence of Cryptosporidium in pigs in regions with −30° to 0° latitude range (22.9%, 193/872) and 0°–60° longitude range (29.3%, 774/5729) was higher than that in pigs in other regions. Jagai et al. predicted that climate change would increase the spread of cryptosporidiosis infection, and that this spread would vary by season and location (Jagai et al., Reference Jagai, Castronovo, Monchak and Naumova2009). The prevalence of Cryptosporidium in pigs was higher in areas with a mean yearly precipitation of 800–1200 mm (20.7%, 2006/10 586), mean yearly temperature of 5–10 °C (25.4%, 603/4991) and mean yearly relative humidity of < 60% (21.5%, 627/3921). These results indicated that cryptosporidiosis was more likely to occur in warm and rainy areas. Factors such as rainfall, temperature and humidity influence the life cycle of Cryptosporidium and may influence the timing and intensity of disease outbreaks (Patz et al., Reference Patz, Graczyk, Geller and Vittor2000).

Limitations

The current study has the following limitations:

  1. 1. Some countries had only 1 publication of Cryptosporidium infecting pigs in the past 30 years.

  2. 2. Unpublished data were not included in the analysis.

  3. 3. Data of some conference abstracts were not included in the analysis.

  4. 4. Some publications lacked full text, and these articles were excluded.

  5. 5. Analysis of the factors involved was limited. Factors such as season, feeding model and pig breed may also be sources of heterogeneity.

Even so, we believe that the results of this study are close to the true global prevalence of Cryptosporidium in pigs.

Conclusions

This analysis shows that Cryptosporidium infection in pigs is widespread worldwide. Cryptosporidium can cause high levels of disease, particularly in Africa where infection rates are as high as 40.8%. Cryptosporidium suis is the dominant species in pre-weaned pigs while C. scrofarum is the dominant species in fattening and adult pigs. Pig age is an important risk factor associated with cryptosporidiosis. Age should be considered so that farmers can implement effective management plans based on geographical area and environmental factors and prevent zoonotic transmission. These findings highlight the role of pigs as possible potential hosts of zoonotic cryptosporidiosis and the need for additional studies on the prevalence, transmission and control of Cryptosporidium in pigs.

Supplementary material

The supplementary material for this article can be found at https://doi.org/10.1017/S0031182023000276

Data availability

All data generated or used during the study appear in the submitted article.

Acknowledgements

We thank Accdon-LetPub Editor for editing the English text of a draft of this manuscript.

Author's contribution

L. Z. conceived and designed the study; Y. C., H. Q. and J. L. conducted the study; J. H., Y. C., H. X. and Y. W. collected and analysed the data; Y. C. and L. Z. wrote the manuscript. All the authors have read and approved the final version of the manuscript.

Financial support

This research was funded by the NSFC-Henan Joint Fund Key Project (U1904203) and the Leading Talents of the Central Plains Thousand Talents Program (19CZ0122).

Conflict of interest

None.

Ethical standards

Not applicable.

Footnotes

*

These 2 authors contributed equally to this work.

References

Alum, A, Absar, IM, Asaad, H, Rubino, JR and Ijaz, MK (2014) Impact of environmental conditions on the survival of Cryptosporidium and Giardia on environmental surfaces. Interdisciplinary Perspectives on Infectious Diseases 2014, 210385.10.1155/2014/210385CrossRefGoogle ScholarPubMed
Atwill, ER, Sweitzer, RA, Pereira, MG, Gardner, IA, Van Vuren, D and Boyce, WM (1997) Prevalence of and associated risk factors for shedding Cryptosporidium parvum oocysts and Giardia cysts within feral pig populations in California. Applied and Environmental Microbiology 63, 39463949.10.1128/aem.63.10.3946-3949.1997CrossRefGoogle ScholarPubMed
Bouzid, M, Hunter, PR, Chalmers, RM and Tyler, KM (2013) Cryptosporidium pathogenicity and virulence. Clinical Microbiology Reviews 26, 115134.10.1128/CMR.00076-12CrossRefGoogle ScholarPubMed
Budu-Amoako, E, Greenwood, SJ, Dixon, BR, Barkema, HW, Hurnik, D, Estey, C and McClure, JT (2012) Occurrence of Giardia and Cryptosporidium in pigs on Prince Edward Island, Canada. Veterinary Parasitology 184, 1824.10.1016/j.vetpar.2011.07.047CrossRefGoogle ScholarPubMed
Checkley, W, White, AC Jr, Jaganath, D, Arrowood, MJ, Chalmers, RM, Chen, XM, Fayer, R, Griffiths, JK, Guerrant, RL, Hedstrom, L, Huston, CD, Kotloff, KL, Kang, G, Mead, JR, Miller, M, Petri, WA Jr, Priest, JW, Roos, DS, Striepen, B, Thompson, RC, Ward, HD, Van Voorhis, WA, Xiao, L, Zhu, G and Houpt, ER (2015) A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for Cryptosporidium. The Lancet. Infectious Diseases 15, 8594.10.1016/S1473-3099(14)70772-8CrossRefGoogle ScholarPubMed
Chen, F and Huang, K (2007) Prevalence and phylogenetic analysis of Cryptosporidium in pigs in eastern China. Zoonoses and Public Health 54, 393400.10.1111/j.1863-2378.2007.01078.xCrossRefGoogle ScholarPubMed
Chen, Z, Mi, R, Yu, H, Shi, Y, Huang, Y, Chen, Y and Lin, J (2011) Prevalence of Cryptosporidium spp. in pigs in Shanghai, China. Veterinary Parasitology 181, 113119.10.1016/j.vetpar.2011.04.037CrossRefGoogle ScholarPubMed
Danišová, O, Valenčáková, A and Petrincová, A (2016) Detection and identification of six Cryptospordium species in livestock in Slovakia by amplification of SSU and GP60 genes with the use of PCR analysis. Annals of Agricultural and Environmental Medicine: AAEM 23, 254258.10.5604/12321966.1203886CrossRefGoogle ScholarPubMed
De Felice, LA, Moré, G, Cappuccio, J, Venturini, MC and Unzaga, JM (2020) Molecular characterization of Cryptosporidium spp. from domestic pigs in Argentina. Veterinary Parasitology: Regional Studies and Reports 22, 100473.Google ScholarPubMed
Dumaine, JE, Tandel, J and Striepen, B (2020) Cryptosporidium parvum. Trends in Parasitology 36, 485486.10.1016/j.pt.2019.11.003CrossRefGoogle ScholarPubMed
Egger, M, Davey Smith, G, Schneider, M and Minder, C (1997) Bias in meta-analysis detected by a simple, graphical test. British Medical Journal 315, 629634.10.1136/bmj.315.7109.629CrossRefGoogle ScholarPubMed
Enemark, HL, Ahrens, P, Bille-Hansen, V, Heegaard, PM, Vigre, H, Thamsborg, SM and Lind, P (2003) Cryptosporidium parvum: infectivity and pathogenicity of the ‘porcine’ genotype. Parasitology 126, 407416.10.1017/S0031182003003032CrossRefGoogle ScholarPubMed
Epe, C, Coati, N and Schnieder, T (2004) Results of parasitological examinations of faecal samples from horses, ruminants, pigs, dogs, cats, hedgehogs and rabbits between 1998 and 2002. DTW. Deutsche Tierarztliche Wochenschrift 111, 243247.Google ScholarPubMed
Farzan, A, Parrington, L, Coklin, T, Cook, A, Pintar, K, Pollari, F and Dixon, B (2011) Detection and characterization of Giardia duodenalis and Cryptosporidium spp. on swine farms in Ontario, Canada. Foodborne Pathogens and Disease 8, 12071213.10.1089/fpd.2011.0907CrossRefGoogle ScholarPubMed
Featherstone, CA, Marshall, JA, Giles, M, Sayers, AR and Pritchard, GC (2010) Cryptosporidium species infection in pigs in East Anglia. The Veterinary Record, 9 166, 5152.10.1136/vr.b4771CrossRefGoogle ScholarPubMed
Feng, Y, Ryan, UM and Xiao, L (2018) Genetic diversity and population structure of Cryptosporidium. Trends in Parasitology 34, 9971011.10.1016/j.pt.2018.07.009CrossRefGoogle ScholarPubMed
Feng, S, Jia, T, Huang, J, Fan, Y, Chang, H, Han, S and He, H (2020) Identification of Enterocytozoon bieneusi and Cryptosporidium spp. in farmed wild boars (Sus scrofa) in Beijing, China. Infection Genetics and Evolution 80, 104231.10.1016/j.meegid.2020.104231CrossRefGoogle ScholarPubMed
Fiuza, VR, Gallo, SS, Frazão-Teixeira, E, Santín, M, Fayer, R and Oliveira, FC (2011) Cryptosporidium pig genotype II diagnosed in pigs from the state of Rio De Janeiro, Brazil. Journal of Parasitology 97, 146147.10.1645/GE-2479.1CrossRefGoogle ScholarPubMed
Fleta, J, Sánchez-Acedo, C, Clavel, A and Quílez, J (1995) Detection of Cryptosporidium oocysts in extra-intestinal tissues of sheep and pigs. Veterinary Parasitology 59, 201205.10.1016/0304-4017(94)00758-5CrossRefGoogle ScholarPubMed
García-Presedo, I, Pedraza-Díaz, S, González-Warleta, M, Mezo, M, Gómez-Bautista, M, Ortega-Mora, LM and Castro-Hermida, JA (2013) Presence of Cryptosporidium scrofarum, C. suis and C. parvum subtypes IIaA16G2R1 and IIaA13G1R1 in Eurasian wild boars (Sus scrofa). Veterinary Parasitology 196, 497502.10.1016/j.vetpar.2013.04.017CrossRefGoogle Scholar
Gorospe, E (2005) Updates on the environmental risks and control of cryptosporidiosis. International Journal of Infectious Diseases 5, 15.Google Scholar
Guyatt, GH, Oxman, AD, Vist, GE, Kunz, R, Falck-Ytter, Y, Alonso-Coello, P and Group, GW (2008) GRADE: an emerging consensus on rating quality of evidence and strength of recommendations. British Medical Journal 336, 924926.10.1136/bmj.39489.470347.ADCrossRefGoogle ScholarPubMed
Han, JQ, Shi, LQ, Wu, J, Li, C, Zhu, XQ, Zou, FC and Luo, ML (2018) Molecular epidemiological investigation and species identification of Cryptosporidium on Yunnan pig farm. Chinese Journal of Veterinary Science 48, 311315 (In Chinese).Google Scholar
Hatam-Nahavandi, K, Ahmadpour, E, Carmena, D, Spotin, A, Bangoura, B and Xiao, L (2019) Cryptosporidium infections in terrestrial ungulates with focus on livestock: a systematic review and meta-analysis. Parasites & Vectors, 14 12, 453.10.1186/s13071-019-3704-4CrossRefGoogle ScholarPubMed
Iwashita, H, Takemura, T, Tokizawa, A, Sugamoto, T, Thiem, VD, Nguyen, TH and Yamashiro, T (2021) Molecular epidemiology of Cryptosporidium spp. in an agricultural area of northern Vietnam: a community survey. Parasitology International 83, 102341.10.1016/j.parint.2021.102341CrossRefGoogle Scholar
Jagai, JS, Castronovo, DA, Monchak, J and Naumova, EN (2009) Seasonality of cryptosporidiosis: a meta-analysis approach. Environmental Research 109, 465478.10.1016/j.envres.2009.02.008CrossRefGoogle ScholarPubMed
Johnson, J, Buddle, R, Reid, S, Armson, A and Ryan, UM (2008) Prevalence of Cryptosporidium genotypes in pre and post-weaned pigs in Australia. Experimental Parasitology 119, 418421.10.1016/j.exppara.2008.04.009CrossRefGoogle ScholarPubMed
Katsuda, K, Kohmoto, M, Kawashima, K and Tsunemitsu, H (2006) Frequency of enteropathogen detection in suckling and weaned pigs with diarrhea in Japan. Journal of Veterinary Diagnostic Investigation 18, 350354.10.1177/104063870601800405CrossRefGoogle ScholarPubMed
Kennedy, GA, Kreitner, GL and Strafuss, AC (1977) Cryptosporidiosis in three pigs. Journal of the American Veterinary Medical Association, 1 170, 348350.Google ScholarPubMed
Kotloff, KL (2017) The burden and etiology of diarrheal illness in developing countries. Pediatric Clinics of North America 64, 799814.10.1016/j.pcl.2017.03.006CrossRefGoogle ScholarPubMed
Kvác, M, Sak, B, Hanzlíková, D, Kotilová, J and Kvetonová, D (2009a) Molecular characterization of Cryptosporidium isolates from pigs at slaughterhouses in South Bohemia, Czech Republic. Parasitology Research 104, 425428.10.1007/s00436-008-1215-xCrossRefGoogle ScholarPubMed
Kvác, M, Hanzlíková, D, Sak, B and Kvetonová, D (2009b) Prevalence and age-related infection of Cryptosporidium suis, C. muris and Cryptosporidium pig genotype II in pigs on a farm complex in the Czech Republic. Veterinary Parasitology 160, 319322.10.1016/j.vetpar.2008.11.007CrossRefGoogle Scholar
Kvác, M, Kvetonová, D, Sak, B and Ditrich, O (2009c) Cryptosporidium pig genotype II in immunocompetent man. Emerging Infectious Diseases 15, 982983.10.3201/eid1506.071621CrossRefGoogle Scholar
Lam, HYP, Tseng, YC, Wu, WJ, Yu, YH, Cheng, PC and Peng, SY (2022) Prevalence and genotypes of Cryptosporidium in livestock in Hualien Country, Eastern Taiwan. Parasitology International 88, 102553.10.1016/j.parint.2022.102553CrossRefGoogle ScholarPubMed
Langkjaer, RB, Vigre, H, Enemark, HL and Maddox-Hyttel, C (2007) Molecular and phylogenetic characterization of Cryptosporidium and Giardia from pigs and cattle in Denmark. Parasitology 134, 339350.10.1017/S0031182006001533CrossRefGoogle ScholarPubMed
Li, W, Yu, XM, Zhong, ZJ, Wang, Q, Liu, XH, Yu, JQ and Peng, GN (2016) Isolation and identification of Giardia and Cryptosporidium from wild boar source and small fragrant pig source in Sichuan province. China Veterinary Science 46, 11661169 (In Chinese).Google Scholar
Li, W, Deng, L, Wu, K, Huang, X, Song, Y, Su, H and Peng, G (2017) Presence of zoonotic Cryptosporidium scrofarum, Giardia duodenalis assemblage A and Enterocytozoon bieneusi genotypes in captive Eurasian wild boars (Sus scrofa) in China: potential for zoonotic transmission. Parasites & Vectors 10, 10.10.1186/s13071-016-1942-2CrossRefGoogle Scholar
Li, WC, Yang, HH, Kan, ZZ, Yang, YL, Sun, YY, Gu, YF and Chen, HL (2018a) Investigation on the status of Cryptosporidium infection in large-scale pig farms in Jiangbei area, Anhui Province. Chinese Journal of Schistosomiasis Control 30, 420423, 464. (In Chinese).Google Scholar
Li, Y, Guo, Y, Wen, Z, Jiang, X, Ma, X and Han, X (2018b) Weaning stress perturbs gut microbiome and its metabolic profile in piglets. Scientific Reports, 24 8, 18068.10.1038/s41598-018-33649-8CrossRefGoogle ScholarPubMed
Li, D, Deng, H, Zheng, Y, Zhang, H, Wang, S, He, L and Zhao, J (2022) First characterization and zoonotic potential of Cryptosporidium spp. and Giardia duodenalis in pigs in Hubei Province of China. Frontiers in Cellular and Infection Microbiology 12, 949773.10.3389/fcimb.2022.949773CrossRefGoogle ScholarPubMed
Lin, Q, Wang, XY, Chen, JW, Ding, L and Zhao, GH (2015) Cryptosporidium suis infection in post-weaned and adult pigs in Shaanxi province, northwestern China. Korean Journal of Parasitology 53, 113117.10.3347/kjp.2015.53.1.113CrossRefGoogle ScholarPubMed
Liu, H, Ni, H, Xu, J, Wang, R, Li, Y, Shen, Y and Yin, J (2021) Genotyping and zoonotic potential of Cryptosporidium and Enterocytozoon bieneusi in pigs transported across regions in China. Microbial Pathogenesis 154, 104823.10.1016/j.micpath.2021.104823CrossRefGoogle ScholarPubMed
Maddox-Hyttel, C, Langkjaer, RB, Enemark, HL and Vigre, H (2006) Cryptosporidium and Giardia in different age groups of Danish cattle and pigs – occurrence and management associated risk factors. Veterinary Parasitology, 10 141, 4859.10.1016/j.vetpar.2006.04.032CrossRefGoogle ScholarPubMed
Moore, CE, Elwin, K, Phot, N, Seng, C, Mao, S, Suy, K, Kumar, V, Nader, J, Bousfield, R, Perera, S, Bailey, JW, Beeching, NJ, Day, NP, Parry, CM and Chalmers, RM (2016) Molecular characterization of Cryptosporidium species and Giardia duodenalis from symptomatic Cambodian children. PLoS Neglected Tropical Diseases, 7 10, e0004822.10.1371/journal.pntd.0004822CrossRefGoogle ScholarPubMed
Němejc, K, Sak, B, Květoňová, D, Hanzal, V, Jeníková, M and Kváč, M (2012) The first report on Cryptosporidium suis and Cryptosporidium pig genotype II in Eurasian wild boars (Sus scrofa) (Czech Republic). Veterinary Parasitology 184, 122125.10.1016/j.vetpar.2011.08.029CrossRefGoogle Scholar
Němejc, K, Sak, B, Květoňová, D, Kernerová, N, Rost, M, Cama, VA and Kváč, M (2013a) Occurrence of Cryptosporidium suis and Cryptosporidium scrofarum on commercial swine farms in the Czech Republic and its associations with age and husbandry practices. Parasitology Research 112, 11431154.10.1007/s00436-012-3244-8CrossRefGoogle ScholarPubMed
Němejc, K, Sak, B, Květoňová, D, Hanzal, V, Janiszewski, P, Forejtek, P and Kváč, M (2013b) Cryptosporidium suis and Cryptosporidium scrofarum in Eurasian wild boars (Sus scrofa) in Central Europe. Veterinary Parasitology 197, 504508.10.1016/j.vetpar.2013.07.003CrossRefGoogle ScholarPubMed
Ng, J, Yang, R, Whiffin, V, Cox, P and Ryan, U (2011) Identification of zoonotic Cryptosporidium and Giardia genotypes infecting animals in Sydney's water catchments. Experimental Parasitology 128, 138144.10.1016/j.exppara.2011.02.013CrossRefGoogle ScholarPubMed
Nguyen, ST, Honma, H, Geurden, T, Ikarash, M, Fukuda, Y, Huynh, VV, Nguyen, DT and Nakai, Y (2012) Prevalence and risk factors associated with Cryptosporidium oocysts shedding in pigs in Central Vietnam. Research in Veterinary Science 93, 848852.10.1016/j.rvsc.2012.01.007CrossRefGoogle ScholarPubMed
Patz, JA, Graczyk, TK, Geller, N and Vittor, AY (2000) Effects of environmental change on emerging parasitic diseases. International Journal for Parasitology 30, 13951405.10.1016/S0020-7519(00)00141-7CrossRefGoogle ScholarPubMed
Petersen, HH, Jianmin, W, Katakam, KK, Mejer, H, Thamsborg, SM, Dalsgaard, A and Enemark, HL (2015) Cryptosporidium and Giardia in Danish organic pig farms: seasonal and age-related variation in prevalence, infection intensity and species/genotypes. Veterinary Parasitology 214, 2939.10.1016/j.vetpar.2015.09.020CrossRefGoogle ScholarPubMed
Pettersson, E, Ahola, H, Frössling, J, Wallgren, P and Troell, K (2020) Detection and molecular characterisation of Cryptosporidium spp. in Swedish pigs. Acta Veterinaria Scandinavica 62, 40.10.1186/s13028-020-00537-zCrossRefGoogle ScholarPubMed
Pumipuntu, N and Piratae, S (2018) Cryptosporidiosis: a zoonotic disease concern. Veterinary World 11, 681686.10.14202/vetworld.2018.681-686CrossRefGoogle ScholarPubMed
Qi, M, Zhang, Q, Xu, C, Zhang, Y, Xing, J, Tao, D and Zhang, L (2020) Prevalence and molecular characterization of Cryptosporidium spp. in pigs in Xinjiang, China. Acta Tropica 209, 105551.10.1016/j.actatropica.2020.105551CrossRefGoogle ScholarPubMed
Quílez, J, Sánchez-Acedo, C, Clavel, A, del Cacho, E and López-Bernad, F (1996) Prevalence of Cryptosporidium infections in pigs in Aragón (northeastern Spain). Veterinary Parasitology 67, 8388.10.1016/S0304-4017(96)01026-6CrossRefGoogle ScholarPubMed
Ramirez, NE, Ward, LA and Sreevatsan, S (2004) A review of the biology and epidemiology of cryptosporidiosis in humans and animals. Microbes and Infection 6, 773785.10.1016/j.micinf.2004.02.021CrossRefGoogle ScholarPubMed
Resnhaleksmana, E, Wijayanti, MA and Artama, WT (2021) A potential zoonotic parasite: Cryptosporidium parvum transmission in rats, pigs and humans in West Lombok, Indonesia. African Journal of Infectious Diseases 15, 4451.10.21010/ajid.v15i2.8CrossRefGoogle ScholarPubMed
Rivero-Juarez, A, Dashti, A, López-López, P, Muadica, AS, Risalde, MLA, Köster, PC and Carmena, D (2020) Protist enteroparasites in wild boar (Sus scrofa ferus) and black Iberian pig (Sus scrofa domesticus) in southern Spain: a protective effect on hepatitis E acquisition? Parasites & Vectors 13, 281.10.1186/s13071-020-04152-9CrossRefGoogle Scholar
Rodriguez-Rivera, LD, Cummings, KJ, McNeely, I, Suchodolski, JS, Scorza, AV, Lappin, MR and Bodenchuk, MJ (2016) Prevalence and diversity of Cryptosporidium and Giardia identified among feral pigs in Texas. Vector Borne and Zoonotic Diseases 16, 765768.10.1089/vbz.2016.2015CrossRefGoogle ScholarPubMed
Rose, JB, Huffman, DE and Gennaccaro, A (2002) Risk and control of waterborne cryptosporidiosis. FEMS Microbiology Reviews 26, 113123.10.1111/j.1574-6976.2002.tb00604.xCrossRefGoogle ScholarPubMed
Ryan, UM, Samarasinghe, B, Read, C, Buddle, JR, Robertson, ID and Thompson, RC (2003) Identification of a novel Cryptosporidium genotype in pigs. Applied and Environmental Microbiology 69, 39703974.10.1128/AEM.69.7.3970-3974.2003CrossRefGoogle ScholarPubMed
Ryan, UM, Feng, Y, Fayer, R and Xiao, L (2021) Taxonomy and molecular epidemiology of Cryptosporidium and Giardia – a 50 year perspective (1971–2021). International Journal for Parasitology 51, 10991119.10.1016/j.ijpara.2021.08.007CrossRefGoogle ScholarPubMed
Rzeżutka, A, Kaupke, A, Kozyra, I and Pejsak, Z (2014) Molecular studies on pig cryptosporidiosis in Poland. Polish Journal of Veterinary Sciences 17, 577582.10.2478/pjvs-2014-0086CrossRefGoogle ScholarPubMed
Sannella, AR, Suputtamongkol, Y, Wongsawat, E and Cacciò, SM (2019) A retrospective molecular study of Cryptosporidium species and genotypes in HIV-infected patients from Thailand. Parasites & Vectors 12, 91.10.1186/s13071-019-3348-4CrossRefGoogle ScholarPubMed
Schubnell, F, von Ah, S, Graage, R, Sydler, T, Sidler, X, Hadorn, D and Basso, W (2016) Occurrence, clinical involvement and zoonotic potential of endoparasites infecting Swiss pigs. Parasitology International 65, 618624.10.1016/j.parint.2016.09.005CrossRefGoogle ScholarPubMed
Suárez-Luengas, L, Clavel, A, Quílez, J, Goñi-Cepero, MP, Torres, E, Sánchez-Acedo, C and del Cacho, E (2007) Molecular characterization of Cryptosporidium isolates from pigs in Zaragoza (northeastern Spain). Veterinary Parasitology 148, 231235.10.1016/j.vetpar.2007.06.022CrossRefGoogle ScholarPubMed
Thathaisong, U, Siripattanapipong, S, Inpankaew, T, Leelayoova, S and Mungthin, M (2020) High prevalence of Cryptosporidium infection caused by C. scrofarum and C. suis among pigs in Thailand. Parasitology International 77, 102122.10.1016/j.parint.2020.102122CrossRefGoogle Scholar
Vítovec, J and Koudela, B (1992) Pathogenesis of intestinal cryptosporidiosis in conventional and gnotobiotic piglets. Veterinary Parasitology 43, 2536.10.1016/0304-4017(92)90045-BCrossRefGoogle ScholarPubMed
Vítovec, J, Hamadejová, K, Landová, L, Kvác, M, Kvetonová, D and Sak, B (2006) Prevalence and pathogenicity of Cryptosporidium suis in pre- and post-weaned pigs. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 53, 239243.10.1111/j.1439-0450.2006.00950.xCrossRefGoogle ScholarPubMed
Wang, R, Qiu, S, Jian, F, Zhang, S, Shen, Y, Zhang, L and Xiao, L (2010) Prevalence and molecular identification of Cryptosporidium spp. in pigs in Henan, China. Parasitology Research 107, 14891494.10.1007/s00436-010-2024-6CrossRefGoogle ScholarPubMed
Wang, H, Zhang, Y, Wu, Y, Li, J, Qi, M, Li, T and Zhang, L (2018a) Occurrence, molecular characterization, and assessment of zoonotic risk of Cryptosporidium spp., Giardia duodenalis, and Enterocytozoon bieneusi in pigs in Henan, Central China. Journal of Eukaryotic Microbiology 65, 893901.10.1111/jeu.12634CrossRefGoogle ScholarPubMed
Wang, ZD, Liu, Q, Liu, HH, Li, S, Zhang, L, Zhao, YK and Zhu, XQ (2018b) Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: a global systematic review and meta-analysis. Parasites &Vectors 11, 28.10.1186/s13071-017-2558-xCrossRefGoogle ScholarPubMed
Wang, FY, Shi, WQ, Hou, ZF, Zhao, ZX, Feng, J, Xu, JJ, Tao, JP and Liu, DD (2019) Investigation of Cryptosporidium infection in a large-scale pig farm in Yancheng, Jiangsu Province. Animal Husbandry & Veterinary Medicine 51, 7882 (In Chinese).Google Scholar
Wang, W, Gong, QL, Zeng, A, Li, MH, Zhao, Q and Ni, HB (2021) Prevalence of Cryptosporidium in pigs in China: a systematic review and meta-analysis. Transboundary and Emerging Diseases 68, 14001413.10.1111/tbed.13806CrossRefGoogle Scholar
Wang, P, Li, S, Zou, Y, Du, ZC, Song, DP, Wang, P and Chen, XQ (2022) The infection and molecular characterization of Cryptosporidium spp. in diarrheic pigs in southern China. Microbial Pathogenesis 165, 105459.10.1016/j.micpath.2022.105459CrossRefGoogle ScholarPubMed
Wieler, LH, Ilieff, A, Herbst, W, Bauer, C, Vieler, E, Bauerfeind, R and Zahner, H (2001) Prevalence of enteropathogens in suckling and weaned piglets with diarrhoea in southern Germany. Journal of Veterinary Medicine. B, Infectious Diseases and Veterinary Public Health 48, 151159.10.1046/j.1439-0450.2001.00431.xCrossRefGoogle ScholarPubMed
Xiao, L, Moore, JE, Ukoh, U, Gatei, W, Lowery, CJ, Murphy, TM and Rao, JR (2006) Prevalence and identity of Cryptosporidium spp. in pig slurry. Applied and Environmental Microbiology 72, 44614463.10.1128/AEM.00370-06CrossRefGoogle ScholarPubMed
Yang, MT, Zhang, HJ, Li, YH, Lin, Q, Song, JK and Zhao, GH (2020) Study on Cryptosporidium infection of Tibetan fragrant pigs in Northwest China. Progress in Veterinary Medicine 41, 130134 (In Chinese).Google Scholar
Yao, Q, Wang, JW, Wang, SS, Li, YH, Zhao, SS, Song, JK and Zhao, GH (2020) Analysis on the infection status of Cryptosporidium in piglets from large-scale pig farms in Shaanxi Province. Chinese Journal of Veterinary Science 40, 23482352 (In Chinese).Google Scholar
Yin, J, Shen, Y, Yuan, Z, Lu, W, Xu, Y and Cao, J (2011) Prevalence of the Cryptosporidium pig genotype II in pigs from the Yangtze River Delta, China. PLoS ONE 6, e20738.10.1371/journal.pone.0020738CrossRefGoogle Scholar
Yin, JH, Yuan, ZY, Cai, HX, Shen, YJ, Jiang, YY, Zhang, J and Cao, JP (2013) Age-related infection with Cryptosporidium species and genotype in pigs in China. Biomedical and Environmental Sciences 26, 492495.Google ScholarPubMed
Yui, T, Shibahara, T, Kon, M, Yamamoto, N, Kameda, M and Taniyama, H (2014a) Epidemiological studies on intestinal protozoa in pigs in Saitama. Japanese Jarq-japan Agricultural Research Quarterly 48, 8793.10.6090/jarq.48.87CrossRefGoogle Scholar
Yui, T, Nakajima, T, Yamamoto, N, Kon, M, Abe, N, Matsubayashi, M and Shibahara, T (2014b) Age-related detection and molecular characterization of Cryptosporidium suis and Cryptosporidium scrofarum in pre- and post-weaned piglets and adult pigs in Japan. Parasitology Research 113, 359365.10.1007/s00436-013-3662-2CrossRefGoogle ScholarPubMed
Zhang, W, Yang, F, Liu, A, Wang, R, Zhang, L, Shen, Y and Ling, H (2013) Prevalence and genetic characterizations of Cryptosporidium spp. in pre-weaned and post-weaned piglets in Heilongjiang Province, China. PLoS ONE 8, e67564.10.1371/journal.pone.0067564CrossRefGoogle ScholarPubMed
Zhang, Y, Xu, CY, Xing, JM, Ao, WP, Qi, M and Jing, B (2020) Detection of Cryptosporidium and Giardia duodenalis by PCR in a pig farm in Aksu. Progress in Veterinary Medicine 41, 6871 (In Chinese).Google Scholar
Zheng, S, Li, D, Zhou, C, Zhang, S, Wu, Y, Chang, Y and Zhang, L (2019) Molecular identification and epidemiological comparison of Cryptosporidium spp. among different pig breeds in Tibet and Henan, China. BMC Veterinary Research 15, 101.10.1186/s12917-019-1847-3CrossRefGoogle ScholarPubMed
Zintl, A, Neville, D, Maguire, D, Fanning, S, Mulcahy, G, Smith, HV and De Waal, T (2007) Prevalence of Cryptosporidium species in intensively farmed pigs in Ireland. Parasitology 134, 15751582.10.1017/S0031182007002983CrossRefGoogle ScholarPubMed
Zou, Y, Ma, JG, Yue, DM, Zheng, WB, Zhang, XX, Zhao, Q and Zhu, XQ (2017) Prevalence and risk factors of Cryptosporidium infection in farmed pigs in Zhejiang, Guangdong, and Yunnan provinces, China. Tropical Animal Health and Production 49, 653657.10.1007/s11250-017-1230-yCrossRefGoogle ScholarPubMed
Figure 0

Fig. 1. Flow diagram of the selection of eligible studies.

Figure 1

Fig. 2. Map of Cryptosporidium infection in pigs across the world. Prevalence ranges are shown in different colours. [The figure was designed using Arcgis 10.2, and the original vector diagram imported in Arcgis was adapted from Natural Earth (http://www.naturalearthdata.com).]

Figure 2

Table 1. Estimated pooled prevalence of Cryptosporidium infection by country/region

Figure 3

Table 2. Pooled prevalence of Cryptosporidium infection in pigs across the world

Figure 4

Table 3. Extracted data from included studies for molecular methods of Cryptosporidium species

Figure 5

Fig. 3. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Asia.

Figure 6

Fig. 4. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Europe.

Figure 7

Fig. 5. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Africa.

Figure 8

Fig. 6. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in North America.

Figure 9

Fig. 7. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in South America.

Figure 10

Fig. 8. Forest plot of the prevalence estimates of Cryptosporidium infection in pigs in Oceania.

Figure 11

Fig. 9. Funnel plot for examination of publication bias of the prevalence estimates of Cryptosporidium infection in pigs across the world.

Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material 1

Download Chen et al. supplementary material(File)
File 17.1 KB
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material 2

Download Chen et al. supplementary material(File)
File 69.1 KB
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material 3

Download Chen et al. supplementary material(File)
File 66.3 KB
Supplementary material: File

Chen et al. supplementary material

Chen et al. supplementary material 4

Download Chen et al. supplementary material(File)
File 32.4 KB