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Article

The Prevalence of Trichinella spiralis in Domestic Pigs in China: A Systematic Review and Meta-Analysis

by
Huifang Bai
†,
Bin Tang
†,
Weidong Qiao
,
Xiaoxia Wu
,
Mingyuan Liu
* and
Xuelin Wang
*
State Key Laboratory for Zoonotic Diseases, Key Laboratory for Zoonosis Research, Ministry of Education, College of Veterinary Medicine, Jilin University, Changchun 130062, China
*
Authors to whom correspondence should be addressed.
†
These authors contributed equally to this work.
Animals 2022, 12(24), 3553; https://0-doi-org.brum.beds.ac.uk/10.3390/ani12243553
Submission received: 15 November 2022 / Revised: 10 December 2022 / Accepted: 11 December 2022 / Published: 15 December 2022
(This article belongs to the Special Issue Veterinary Parasitology: Epidemiology, Control and Prevention Strategies)
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Abstract

:

Simple Summary

As a pathogen of trichinellosis, Trichinella spiralis is a foodborne zoonotic nematode that can infect more than 100 species including mammals, birds, and reptiles. Pigs infected with T. spiralis are the primary host for disseminating it to humans. Therefore, a meta-analysis was performed here to assess the prevalence of T. spiralis in domestic pigs in China. After considering 43 different studies, including a total sample size of 551,097 pigs, these results indicated that T. spiralis were still prevalent in some areas in China and the highest prevalence region was Guangxi.

Abstract

The meta-analysis was performed to assess the prevalence of T. spiralis in domestic pigs in China. The potential studies from seven databases (Pubmed, Web of science, Scopus, Google Scholar, CNKI, Wanfang, CBM) were searched. I2, Cochran’s Q statistic and the funnel plot and Egger’s test were used to assess heterogeneity and publication bias, respectively. In this study, a total of 179 articles were captured in the initially screened. Of these, we finally obtained 39 significant articles (including 43 studies involving in 551,097 pigs) for the final analysis. We calculated using a random-effects model, and we found the overall infection rate was 0.04 (95% CI 0.03–0.06). The highest prevalence region was Guangxi. The funnel plot and Egger’s test showed no publication bias in our meta-analysis. In addition, this high heterogeneity index was suggestive of potential variations which could be due to regions, quality scores, detection methods, publication years, or samplings. These results indicated that T. spiralis were still prevalent in some areas in China. This highlights the need for an increased focus on implementing affordable, appropriate control programs to reduce economic losses and T. spiralis infection in domestic pigs in China.

1. Introduction

As a pathogen of trichinellosis, Trichinella spiralis (Owen, 1835) is a foodborne zoonotic nematode that can infect more than 100 species including mammals, birds and reptiles [1,2]. T. spiralis infection is fatal in humans infected with a large number of larvae [3,4]. The nematode of pork products can be thermally inactivated at 76.7 °C, a cooking internal temperature recommended by US Food and Drug Administration (USDA) [5]. Humans are infected by eating raw or undercooked pig meat and sausage containing the larvae of T. spiralis. The nematode has caused serious physical and financial burdens on public health [6]. T. spiralis infection have two phases in the human, the enteric or gastrointestinal phase and the systemic (parenteral) phase. Gastrointestinal symptoms are the first symptoms of trichinellosis. Symptoms include abdominal pain, diarrhea, nausea, and vomiting. Muscle pain is a common complaint, chiefly in the mid-abdomen, face (masseter), and chest (intercostal muscles). During the second phase, larvae enter the lymphatic circulation and then into the blood, reaching skeletal muscles, myocardium, and the brain which are high in oxygen content. This phase leads to systemic symptoms like fevers, myositis, myalgias, periorbital edema, and can even cause myocarditis and encephalitis [7]. According to the estimation of World Health Organization (WHO) based on data from 2010 to 2015, parasitic diseases resulted in 48.4 million cases and 59,724 deaths annually, resulting in 8.78 million disability-adjusted life years (DALYs), and it is further estimated that 48% of these parasitic diseases were foodborne [8]. According to Murrell and Pozio [9], from 1986 through 2009, there were 65,818 trichinellosis cases and 42 deaths reported from 41 countries. As the definitive hosts, pigs play an important role in the whole life cycle of T. spiralis [10]. According to preliminary statistics, the production and consumption of pig meat in China is the highest in the world [11]. As a result, it is estimated that approximately 400,000 people are at the risk of infection with T. spiralis in China [12,13].
The traditional current line of trichinellosis treatment commonly employs drugs belonging to benzimidazole derivatives [14]. Albendazole (ABZ) is considered the drug of choice in the treatment of trichinellosis [15]. However, in addition to the emerging resistance, ABZ have low water solubility resulting in reduced bioavailability [16]. Although the therapy methods of trichinellosis have been improved, the controlling key of this disease is still decreasing its definitive-host infection rate [17]. T. spiralis is slightly virulent to pigs and hardly causes obvious symptoms. Normally, the larvae parasitized in the striated muscles and intestines of pigs [18]. However, in the early stage of large dose infection, infected pigs may show symptoms such as loss of appetite, diarrhea, vomiting, and so on. In the middle and late stage, infected pigs may show symptoms such as pain or paralysis, temperature rise, emaciation, chewing and swallowing disorders, hoarseness, and so on [7,19].
Currently, as a result of drug-resistance escalation and immune failure [20,21,22,23], pig industries have to alter approaches to controlling the parasitic nematodes by developing new vaccines or drugs against T. spiralis infection in pigs. The lack of information on the epidemiology also lead to difficulty in the development of new vaccines, drugs, and the diagnosis technology of trichinellosis. Trichinellosis is not only fatal; there are severe debilitating morbidity associated with the detrimental effects of drug resistance which can lead to prolonged drug treatment, negative socioeconomic effects, and adversely impact normal daily productive activities [24,25]. As a result, based on numerous impacts of trichinellosis on animal welfare, the economy, and public health, further considerations and research are deemed to be a desideratum for epidemiological approaches and monitoring programs in China.
Until this study, no attempt has been made to integrate all published studies and reports to derive a robust prevalence estimate of T. spiralis. As a result of the estimation, the aim of this study was to estimate the prevalence and distribution of T. spiralis in domestic pigs in China. This review will also help to evaluate the suitable sample size of vaccine and drug experiments in the high prevalence regions and validate diagnostic tests and vaccine developments for the prevention and control of trichinellosis.

2. Methods

The protocol of this systematic review was defined in advance and registered with PROSPERO (International Prospective Register of Systematic Reviews) (ID: CRD42021270969). The systematic review and meta-analysis in the study was conducted according to the guidelines provided by PRISMA 2020 (Preferred Reporting Items for Systematic Reviews and Meta-analysis 2020) [26]. The PRISMA 2020 checklist (Text S1) was followed to ensure the inclusion of relevant information and maintain study standards.

2.1. Literature Search

To evaluate the prevalence of T. spiralis in domestic pigs in China, the potential studies from 7 databases (Pubmed, Web of science, Scopus, Google Scholar, CNKI, Wanfang, CBM) were searched. The modified searches were performed by various combinations of the following terms using Boolean operator “AND” and “OR”: (Trichinella spiralis OR Trichinella spp. OR Trichinella OR Trichinellosis) AND (prevalence OR distribution OR epidemic OR incidence OR frequency OR occurrence OR detection OR identification OR characterization OR investigation OR survey OR rate) AND (China OR Chinese OR Asia OR Asian). The reference lists of selected articles were also screened manually and appropriate articles were included. Full-text articles were downloaded or obtained through library resources. No attempt was made to identify unpublished reports.

2.2. Selection of Studies

All selected articles had to meet the following inclusion criteria: (i) cross-sectional, cohort, or case-control studies; (ii) the studies were published between January 1990 and December 2021; (iii) the language was limited to Chinese or English; (iv) full-text articles were published; (v) infection cases were from China; (vi) reported as animal level prevalence data, not laboratory infected animals; (vii) exact total numbers and positive cases numbers were given; (viii) animal numbers higher than 200; (ix) the animals must be domestic pigs or swine. Studies were excluded if they did not fulfill all of these criteria. Furthermore, if the same study data were published in both English and Chinese sources, the articles with less detailed information would be excluded from our study. When any authors found articles difficult to judge, the corresponding author was consulted, and differences were discussed until a consensus decision on whether to include or exclude the article was reached.

2.3. Quality of the Studies

The quality of the selected publications was accessed according to the criteria derived from the Grading of Recommendations Assessment, Development and Evaluation (GRADE) method [27]. The quality of the publications was graded using a scoring approach (Text S2). This action was performed by three independent authors. Any difference in opinion among authors or uncertainty was discussed with the corresponding author and all authors had to extract data according to the result of the discussion. A checklist including 8 items was considered for thorough reporting of observational studies. These items were related to the article’s title, abstract, introduction, materials and methods, results, and discussion sections. The score under 2 (≤2) was considered a low quality, between 2 and 5 (>2, ≤5) were middle, and >5 was high [28].

2.4. Data Analysis

The statistical software used in the analysis was R software version 3.6.3 (New Zealand, University of Auckland, Auckland, New Zealand). Before preforming the meta-analysis, we used four methods to convert the observed proportions: The logarithmic conversion (PLN), the logit transformation “PLOGIT”, arcsine transformation (PAS), and Freeman–Tukey double arcsine transformation (PFT). We performed a normal distribution test on the observed proportions and the transformation proportions. We first assumed that the overall data obeyed a normal distribution. The maximum value of the statistic W is 1, and the closer the value of W is to 1 indicates that the sample matches the normal distribution. If p < 0.05, the null hypothesis is rejected, and the dataset does not conform to the normal distribution. When W is close to 1 and p > 0.05, the null hypothesis cannot be rejected, and the dataset matches the normal distribution. After transforming the observed proportions, all analyses were conducted using the transformed proportion as the effect size statistic and the inverse of the variance of the transformed proportion as the study weight [29]. According to the above, in this analysis, estimated pooled prevalence and 95% confidence intervals (CI) were calculated with PFT. Heterogeneity testing was performed using the I2 and Cochran’s Q statistic methods (represented as χ2 and p value) [30,31]. A significant value (p < 0.05) in the analysis suggested a real effect difference. The I2 values of 25%, 50%, and 75% were considered as low, moderate, and high heterogeneity, respectively. The risk of study publication bias was assessed using the funnel plots, and the Egger’s regression test. We also used trim and fill analysis and sensitivity analysis to assess the stability of our study [32].
Furthermore, a significant value (p < 0.05) in the analysis suggested a real effect difference. The potential sources of heterogeneity (I2 > 50%) were further investigated by subgroup analysis and meta-regression analysis. Five potential sources of heterogeneity were examined: regions, detection methods, samplings, publication years, and quality scores. The Q and I2 statistics values were calculated for each subgroup to determine the effective factors on the prevalence T. spiralis and heterogeneity about all included studies [33].

3. Results

3.1. Search Results and Eligible Studies

A flow diagram depicted the study selection process in the flow chart (Figure 1). In this study, totally 179 articles were searched after retrieval from 7 databases, and 169 papers were identified after the removal of duplicates. After screening on title and abstract, 77 articles were further excluded, 2 papers from Japan, 1 paper from Thailand, and 74 articles have little association with our topic. Of these, 53 articles were further excluded due to the following reasons: 4 articles shared the same data, 13 articles were case reports, the animal numbers were less than 200 in 7 articles, 1 article was non-English and Chinese, and 26 articles, of which 8 were dogs, 2 were cats, 9 were rats, 7 were other animals, did not refer domestic pigs, 1 article was a review, and 1 article concerned aother parasite. Finally, a total of 39 articles, including 43 studies were used for meta-analysis. The complete list of included articles can be found in Table 1. Each study used a cross-sectional design. There were 6 studies from Qinghai, 1 from Gansu, 9 from Henan, 2 from Hubei, 10 from Guangxi, 1 from Guizhou, 1 from Tibet, 4 from Yunnan, 1 from Sichuan, 1 from Heilongjiang, 2 from Inner Mongolia, 1 from Shanxi, 1 from Beijing, 1 from Hebei, 1 from Jiangsu, and 1 from Shandong, respectively.

3.2. Pooling and Heterogeneity Analysis

The pooled prevalence estimates of T. spiralis infection in domestic pigs with individual studies were showed in a forest plot (Figure 2). A substantial heterogeneity was observed among studies (p < 0.05; I2 = 99.72%). The overall infection rate calculated using a random-effects model was 0.04 (95% CI 0.03–0.06; 36,439/551,097) and lower than 1.97% as reported by Wang et al. [73].
The estimates of infection rates for different subgroups and heterogeneity were presented in Table 2 and Figures S1–S5. All pooled infection rates for each subgroup were calculated using a random-effects model because of the observed high heterogeneity of subgroups among the studies. Infection rates varied across different geographical regions in China. In the region subgroups, the highest point estimate was in Central South (0.06, 95% CI 0.03–0.09; 35,072/484,584), especially in Guangxi (0.12, 95% CI 0.12–0.12; 111,335/97,196) (Figure 3). At the region level, there was no prevalence in Hebei as we described. Moreover, we further analyzed the studies by years. The different publication years showed a significantly different (p < 0.05) infection rate: the prevalence in 2000 to 2008 was the highest (0.08, 95% CI 0.05–0.13; 12,822/120,986), followed by before 2000 (0.02, 95% CI 0.01–0.04, 23,179/400,190), and the lowest was 2008 and later (0.02, 95% CI 0.01–0.03; 438/29,921). Based on study detection methods, P&E (parasitology and enzyme-linked immunosorbent assay) showed the highest detection rate (0.08, 95% CI 0.04–0.13; 12,087/128,475). We also conducted other subgroup analyses such as sampling. The result showed the B&S (biopsy and serology) sampling was highest (0.08, 95% CI 0.05–0.13; 12,124/127,689). Finally, in terms of quality levels, the estimate was highest in the middle score (0.05, 95% CI 0.02–0.08; 30,938/452,599). The univariate meta-regression showed that regions, publication years, samplings, detection methods, and quality scores may be major sources of heterogeneity (p < 0.05).

3.3. Publication Bias and Sensitivity Analysis

We used PFT to convert the raw rate to ensure the data were closer to a normal distribution (Table 3). As the funnel plot showed, the studies that we included might have publication bias or small-sample size bias (or small-study effects bias) (Figure S6). The result of Egger’s test revealed that there was no publication bias (p = 0.2374 > 0.05) (Figure 4). Therefore, the studies we included may not have publication bias, but a small sample size bias cannot be ruled out [74,75]. The result of the trim and fill test showed that there were nine studies which were added (the point estimate was 0%) and the pooled estimate was finally changed (Figure 5). The sensitivity analysis indicated that the pooled prevalence was not significantly affected by each study after omitting any one study at a time, so we believed that the stability of the results was reliable and rational (Figure S7).

4. Discussion

Trichinellosis is a seriously neglected foodborne zoonotic disease with a worldwide prevalence [76]. An overview of knowledge on the geographical distribution and burden of T. spiralis will offer a better understanding of its impacts on animal production and risk to public health [77,78,79]. We conducted a meta-analysis to estimate the prevalence of T. spiralis in domestic pigs in China and assess the potential factors. In this study, the overall infection rate was 0.04 (95% CI 0.03–0.06) but the highest prevalence region was 11.7% in Guangxi, which was higher than the prevalence region of China reported by Cui et al. [80]. The result was consistent with previous studies. Studies conducted in neighboring countries found the seroprevalence to be 2.5% in Rural Cambodia, 5.6% in Vietnam, and 2.1% and 14.4% in different provinces in Lao PDR [81,82,83,84]. The infection rate may vary significantly within and between countries. The pig international trade represents one of the largest livestock markets in the world [85]. The risk of trichinellosis linked to pig consumption is higher in China than in neighboring countries [86,87,88].
There was high heterogeneity in prevalence levels in domestic pigs across China mainland among the eligible studies, but no significant publication bias was found at cut off level of 0.05 by Egger’s test or trim and fill analysis. This high heterogeneity index was suggestive of potential variations, which could be influenced by regions, quality scores, detection methods, publication years, or samplings. To trace the source of heterogeneity, articles were first divided into six subgroups. There was a significantly higher prevalence in Central China (p < 0.05), although further meta regression analysis of the region subgroups did show no significant differences (p > 0.05). The epidemiology of trichinellosis are the results of many geographical, ecological, and social interactions which may explain some of these differences. The majority of outbreaks attributed to domestic pigs have been traced to pigs raised in small farms or backyards, often outdoors, where poor husbandry conditions place pigs at high risk [85]. However, the growing popularity of free-range pig production, because it involves varying degrees of outdoor exposure and even direct contacting with reservoir hosts such as foxes, raccoon dogs, or wild boars/feral pigs, has raised concerns that pastured pigs may have an increased risk of spillover of T. spiralis. Correspondingly, in Central China, pigs industry was especially widespread and more backyard or outdoor free-ranging pigs are maintained than in other regions of the country. In China, pig T. spiralis infection is still principally transmitted by garbage (i.e., feeding pigs with swills containing raw pork scraps). T. spiralis-infected pigs predominantly also came from small backyard farms where animals were raised under poor hygienic conditions and outdoor free-ranging pigs that were fed raw waste products or animal carcasses [89]. Prevention and controlling infection with T. spiralis should be seriously considered in these regions, and the traditional pig-rearing mode should be improved.
Most of studies in our analysis (n = 35) were of high and middle quality; therefore, this study can reflect the basic prevalence of T. spiralis among domestic pigs in China. The reason for losing points in some studies was a failure to distinguish the region. The results showed the difference of prevalence rates was significant between studies of different quality, and we found the estimate was highest in middle score (>2 to ≤5). In addition, results of the univariate regression analysis suggested that the quality of articles may be a source of heterogeneity in this study. The result was consistent with the report by Gong [90].
In the study, the infection rate of T. spiralis was identified by different methods with significant difference in the reported prevalence (p < 0.05). In 2016, the World Organization for Animal Health (OIE) reported that the digestion method is the best testing method for diagnosing trichinellosis [91]; however, detection rate was lowest in this method in our analysis. Although this method was simple and inexpensive, it was not sensitive; it was easy to confused T. spiralis with other microorganisms and increase the false positive rate. Moreover, compared to microscopic examination, the digestion method is the reliable method, but it is laborious, biohazardous, and could raise ethical issues [92,93]. We also found that the most common method (ELISA) was still lower; however, this method, without optimizing antibody concentration, is fast, reliable, sensitive, and suitable for large-scale testing. The test result of the method will largely depend on operation [94]. Additionally, the manufacturers, and cross-reaction between species of T. spiralis or other helminth antigens, can also lead to false positives [95]. The P&E methods were highest, which may improve the detection rate of T. spiralis. The classification of sampling types confirmed the infection rate used by B&S. As Eslahi et al. [96] stated, serology has been shown as a better and more efficient detection tool than biopsy. Serological techniques were the most frequently used methods for trichinellosis diagnosis. However, higher rates of infection were detected by the combination with biopsy [97]. Serology diagnostic tests was the most appropriate diagnostic method with a combination of serology, molecule, and biopsy approaches [11,74].
The study demonstrated that the estimated pooled prevalence of T. spiralis in domestic pigs in China between 2000 to 2008 was the highest. The infection rate was decreasing after 2008. The microscopy techniques used by different authors before 2000, the more sensitive methods such as LAMP, PCR-based, and ELISA detection methods were used in the 2000s. As a result, there was greater T. spiralis prevalence surveyed by government programs in China after 2000. The reasons led to the higher infection rate which is consistent with previous hypotheses. T. spiralis ranked first in the Food and Agriculture Organization of the United Nations (FAO) and WHO international trade list of 24 parasites according to nine global criteria in 2012 [98]. With the implementation of National Mid- and Long-Term Animal Disease Control Plan (2012–2020) and Biosecurity Law (2021) in China, the infection rate was decreasing and there was a positive contribution to changing dietary habits and environments and public awareness after 2008 [74].
Understanding the distribution and associated risk factors of T. spiralis was essential to improving public health. The potentially increasing risk of pig trichinellosis may influence the re-emergency occurrences of human infection in China. It should encourage government administration to implement more measures to control trichinellosis of domestic pigs. Overall, these results showed that special attention should be paid to public hygiene and animal care in order to prevent T. spiralis infection in China.

5. Limitations

There are some limitations to this study. First, the number of eligible studies was small for available analysis on T. spiralis prevalence. Some studies had a small sample size which may have affected the validity of the overall estimates. We also consider that more than 700 million pigs are produced annually in China. In this meta-analysis, the data we obtained was limited. In order to improve this search, we will continue to pay more attention to new reports on China in the future. Second, although the publication bias was not detected, the unreported articles might lead to an uneven coverage and confounding factors affecting differences in T. spiralis infection prevalence among different regions by the study. This highlights the need for improving disease surveillance and clearly identifying trichinellosis’s geographic heterogeneities by epidemiology nationwide. Third, overall heterogeneity for all pooled prevalence estimations was high, and should be interpreted with caution. Furthermore, heterogeneity remained high after stratification by regions, quality scores, detection methods, publication years, or samplings, suggesting that there were significant residual effects of unmeasured variables. Fourth, no more risk factors were analyzed. Further studies are required to exclude other influencing factors, such as rearing methods, farming scale, and sampling seasons, which might have been sources of high heterogeneity.

Supplementary Materials

The following supporting information can be downloaded at: https://0-www-mdpi-com.brum.beds.ac.uk/article/10.3390/ani12243553/s1, Text S1: PRISMA checklist 2020; Text S2: Quality assessment checklist; Figure S1: Forest plot diagram showing Trichinella spiralis infection in domestic pigs in China in different regions; Figure S2: Forest plot diagram showing Trichinella spiralis infection in domestic pigs in China in different publication year; Figure S3: Forest plot diagram showing Trichinella spiralis infection in domestic pigs in China in different detection methods; Figure S4: Forest plot diagram showing Trichinella spiralis infection in domestic pigs in China in different scores; Figure S5: Forest plot diagram showing Trichinella spiralis infection in domestic pigs in China in different samplings; Figure S6: Funnel plot displaying prevalence data for all included articles of Trichinella spiralis infection in domestic pigs in China; Figure S7: Sensitivity analysis of Trichinella spiralis infection in domestic pigs in China. Reference [99] is cited in the supplementary materials.

Author Contributions

Conceptualization, M.L. and X.W. (Xuelin Wang); Methodology, H.B. and B.T.; Software, H.B.; Formal Analysis, H.B., B.T. and W.Q.; Investigation, H.B., B.T. and X.W. (Xiaoxia Wu); Data Curation, H.B., B.T. and W.Q.; Writing—Original Draft Preparation, H.B., B.T. and X.W. (Xiaoxia Wu); Writing—Review and Editing, M.L. and X.W. (Xuelin Wang); Project Administration, M.L. and X.W. (Xuelin Wang). All authors have read and agreed to the published version of the manuscript.

Funding

This work was supported by grants from JiLin Province Key Research and Development Program of China (20210204211YY), National Natural Science Foundation of China (NSFC31902290, 31872467).

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

All datasets are included in the manuscript or as supplementary files.

Acknowledgments

We sincerely thank personnel from College of Veterinary Medicine, Jilin University.

Conflicts of Interest

The authors declare that they have no competing financial interests.

References

  1. Pozio, E. The broad spectrum of Trichinella hosts: From cold- to warm-blooded animals. Vet. Parasitol. 2005, 132, 3–11. [Google Scholar] [CrossRef] [PubMed]
  2. Gottstein, B.; Pozio, E.; Nöckler, K. Epidemiology, diagnosis, treatment, and control of trichinellosis. Clin. Microbiol. Rev. 2009, 22, 127–145. [Google Scholar] [CrossRef] [Green Version]
  3. Murrell, K.D. Zoonotic foodborne parasites and their surveillance. Rev. Sci. Et Tech. 2013, 32, 559–569. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  4. Bruschi, F.; Murrell, K.D. New aspects of human trichinellosis: The impact of new Trichinella species. Postgrad. Med. J. 2002, 78, 15–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  5. Bacon, R.T.; Sofos, J.N. Characteristics of Biological Hazards in Foods. In Food Safety Handbook; John Wiley & Sons: New York, NY, USA, 2003; pp. 157–195. [Google Scholar]
  6. Lloyd-Smith, J.O.; George, D.; Pepin, K.M.; Pitzer, V.E.; Pulliam, J.R.; Dobson, A.P.; Hudson, P.J.; Grenfell, B.T. Epidemic dynamics at the human-animal interface. Science 2009, 326, 1362–1367. [Google Scholar] [CrossRef] [Green Version]
  7. Rawla, P.; Sharma, S. Trichinella Spiralis; StatPearls Publishing LLC: Treasure Island, FL, USA, 2022. [Google Scholar]
  8. Torgerson, P.R.; Devleesschauwer, B.; Praet, N.; Speybroeck, N.; Willingham, A.L.; Kasuga, F.; Rokni, M.B.; Zhou, X.N.; Fèvre, E.M.; Sripa, B.; et al. World Health Organization Estimates of the Global and Regional Disease Burden of 11 Foodborne Parasitic Diseases, 2010: A Data Synthesis. PLoS Med. 2015, 12, e1001920. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  9. Murrell, K.D.; Pozio, E. Worldwide occurrence and impact of human trichinellosis, 1986-2009. Emerg. Infect. Dis. 2011, 17, 2194–2202. [Google Scholar] [CrossRef]
  10. Basso, W.; Marreros, N.; Hofmann, L.; Salvisberg, C.; Lundström-Stadelmann, B.; Frey, C.F. Evaluation of the PrioCHECK™ Trichinella AAD kit to detect Trichinella spiralis, T. britovi, and T. pseudospiralis larvae in pork using the automated digestion method Trichomatic-35. Parasitol. Int. 2022, 86, 102449. [Google Scholar] [CrossRef]
  11. Bai, X.; Hu, X.; Liu, X.; Tang, B.; Liu, M. Current Research of Trichinellosis in China. Front. Microbiol. 2017, 8, 1472. [Google Scholar] [CrossRef] [Green Version]
  12. Chávez-Ruvalcaba, F.; Chávez-Ruvalcaba, M.I.; Moran Santibañez, K.; Muñoz-Carrillo, J.L.; León Coria, A.; Reyna Martínez, R. Foodborne Parasitic Diseases in the Neotropics—A Review. Helminthologia 2021, 58, 119–133. [Google Scholar] [CrossRef]
  13. Dupouy-Camet, J. Trichinellosis: A worldwide zoonosis. Vet. Parasitol. 2000, 93, 191–200. [Google Scholar] [CrossRef] [PubMed]
  14. Codina, A.V.; García, A.; Leonardi, D.; Vasconi, M.D.; Di Masso, R.J.; Lamas, M.C.; Hinrichsen, L.I. Efficacy of albendazole:β-cyclodextrin citrate in the parenteral stage of Trichinella spiralis infection. Int. J. Biol. Macromol. 2015, 77, 203–206. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  15. Kalaiselvan, R.; Mohanta, G.P.; Madhusudan, S.; Manna, P.K.; Manavalan, R. Enhancement of bioavailability and anthelmintic efficacy of albendazole by solid dispersion and cyclodextrin complexation techniques. Pharmazie 2007, 62, 604–607. [Google Scholar] [CrossRef]
  16. Jung, H.; Medina, L.; García, L.; Fuentes, I.; Moreno-Esparza, R. Absorption studies of albendazole and some physicochemical properties of the drug and its metabolite albendazole sulphoxide. J. Pharm. Pharmacol. 1998, 50, 43–48. [Google Scholar] [CrossRef] [PubMed]
  17. Bilska-Zając, E.; Różycki, M.; Korpysa-Dzirba, W.; Bełcik, A.; Ziętek-Barszcz, A.; Włodarczyk-Ramus, M.; Gontarczyk, A.; Cencek, T. Trichinella Outbreaks on Pig Farms in Poland in 2012–2020. Pathogens 2021, 10, 1504. [Google Scholar] [CrossRef]
  18. Deng, Y. Diagnosis and treatment of trichinellosis in pigs. China Anim. Health 2022, 24, 15–16. [Google Scholar]
  19. Abuseir, S. Meat-borne parasites in the Arab world: A review in a One Health perspective. Parasitol. Res. 2021, 120, 4153–4166. [Google Scholar] [CrossRef]
  20. Dimunová, D.; Matoušková, P.; Navrátilová, M.; Nguyen, L.T.; Ambrož, M.; Vokřál, I.; Szotáková, B.; Skálová, L. Environmental circulation of the anthelmintic drug albendazole affects expression and activity of resistance-related genes in the parasitic nematode Haemonchus contortus. Sci. Total Environ. 2022, 822, 153527. [Google Scholar] [CrossRef]
  21. Matoušková, P.; Vokřál, I.; Lamka, J.; Skálová, L. The Role of Xenobiotic-Metabolizing Enzymes in Anthelmintic Deactivation and Resistance in Helminths. Trends Parasitol. 2016, 32, 481–491. [Google Scholar] [CrossRef]
  22. Xu, D.; Bai, X.; Xu, J.; Wang, X.; Dong, Z.; Shi, W.; Xu, F.; Li, Y.; Liu, M.; Liu, X. The immune protection induced by a serine protease from the Trichinella spiralis adult against Trichinella spiralis infection in pigs. PLoS Negl. Trop. Dis. 2021, 15, e0009408. [Google Scholar] [CrossRef]
  23. Zhang, N.; Li, W.; Fu, B. Vaccines against Trichinella spiralis: Progress, challenges and future prospects. Transbound. Emerg. Dis. 2018, 65, 1447–1458. [Google Scholar] [CrossRef] [PubMed]
  24. Johne, A.; Filter, M.; Gayda, J.; Buschulte, A.; Bandick, N.; Nöckler, K.; Mayer-Scholl, A. Survival of Trichinella spiralis in cured meat products. Vet. Parasitol. 2020, 287, 109260. [Google Scholar] [CrossRef] [PubMed]
  25. Wit, J.; Dilks, C.M.; Andersen, E.C. Complementary Approaches with Free-living and Parasitic Nematodes to Understanding Anthelmintic Resistance. Trends Parasitol. 2021, 37, 240–250. [Google Scholar] [CrossRef] [PubMed]
  26. Moher, D.; Shamseer, L.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015 statement. Syst. Rev. 2015, 4, 1. [Google Scholar] [CrossRef] [Green Version]
  27. Guyatt, G.H.; Oxman, A.D.; Vist, G.E.; Kunz, R.; Falck-Ytter, Y.; Alonso-Coello, P.; Schünemann, H.J. GRADE: An emerging consensus on rating quality of evidence and strength of recommendations. BMJ 2008, 336, 924–926. [Google Scholar] [CrossRef] [Green Version]
  28. Wei, X.Y.; Gao, Y.; Lv, C.; Wang, W.; Chen, Y.; Zhao, Q.; Gong, Q.L.; Zhang, X.X. The global prevalence and risk factors of Toxoplasma gondii among foxes: A systematic review and meta-analysis. Microb. Pathog. 2021, 150, 104699. [Google Scholar] [CrossRef]
  29. Wang, N. How to Conduct a Meta-Analysis of Proportions in R: A Comprehensive Tutorial. ResearchGate 2018. preprint. [Google Scholar] [CrossRef]
  30. Ding, H.; Gao, Y.M.; Deng, Y.; Lamberton, P.H.; Lu, D.B. A systematic review and meta-analysis of the seroprevalence of Toxoplasma gondii in cats in mainland China. Parasites Vectors 2017, 10, 27. [Google Scholar] [CrossRef] [Green Version]
  31. Gao, Y.; Wang, W.; Lyu, C.; Wei, X.Y.; Chen, Y.; Zhao, Q.; Ran, Z.G.; Xia, Y.Q. Meta-Analysis of the Prevalence of Echinococcus in Sheep in China From 1983 to 2020. Front. Cell Infect. Microbiol. 2021, 11, 711332. [Google Scholar] [CrossRef]
  32. Ni, H.B.; Gong, Q.L.; Zhao, Q.; Li, X.Y.; Zhang, X.X. Prevalence of Haemophilus parasuis”Glaesserella parasuis” in pigs in China: A systematic review and meta-analysis. Prev. Vet. Med. 2020, 182, 105083. [Google Scholar] [CrossRef]
  33. Han, F.; Wu, G.; Zhang, S.; Zhang, J.; Zhao, Y.; Xu, J. The association of Metabolic Syndrome and its Components with the Incidence and Survival of Colorectal Cancer: A Systematic Review and Meta-analysis. Int. J. Biol. Sci. 2021, 17, 487–497. [Google Scholar] [CrossRef]
  34. Chen, S.L.; Ye, J.J. Prevalence and control status of human Trichinella sprialis in Hubei Province from 1993 to 2004. Endem. Dis. Bull. 2006, 21, 11–13. [Google Scholar]
  35. Chen, X.P. Investigation on infection of Trichinella spiralis in Dali city. Yunnan J. Anim. Sci. Vet. Med. 1990, 1, 34. [Google Scholar]
  36. Guan, G. Investigation on infection of Trichinella spiralis in pigs in Golmud city. J. Qinghai Coll. Anim. Husb. Vet. Med. Coll. 1996, 13, 33–34. [Google Scholar]
  37. Wang, H.Y. Epidemic situation of Trichinosis in Guangxi. Chin. J. Vet. Sci. Technol. 1995, 11, 20. [Google Scholar]
  38. Li, Y.L. Investigation of Pork Thrichinella Spiralis Infection and Toxoplasma in Luohe Area. Master’s Thesis, Henan University of Technology, Luoyang, Henan, 2015. [Google Scholar]
  39. Sun, S.M.; Pang, J.D.; Mao, J.D. Prevalence survey on trichinellosis of swine and dog in eastern Inner Mongolia. Heilongjiang Animal Science and Veterinary Medicine 2017, 6, 103–105. [Google Scholar]
  40. Han, X.M.; Wu, X.H.; Liu, B.R.; Liu, P.Y.; Tang, X.Y. Inspection of zoonotic diseases in livestock in Xining city. Chin. J. Zoonoses 2001, 17, 123–124. [Google Scholar] [CrossRef]
  41. Xu, D.M. The Epidemiological Investigation of Swine Trichinellosis and Identification of Species in Some Areas of Qinghai and Henan Province. Master’s Thesis, Zhengzhou University, Zhengzhou, Henan, 2010. [Google Scholar]
  42. Wang, H.L.; Xiao, X.D. Study on Trichinosis test by using dipstick in Nanyang area. Chin. J. Vet. Parasitol. 2007, 15, 29–32. [Google Scholar]
  43. Jiang, M.S.; Jiang, X.Z. Investigation of Trichinosis spiralis epidemic spreading resources in Dali. J. Dali Med. Coll. 1994, 3, 33–34. [Google Scholar]
  44. Wang, Z.W.; Wang, Z.R.; Jiang, D.C.; Yang, S.M.; Huang, Z.R. Investigation on infection of Trichinella spiralis and Fluke hepatica in Congjiang porcine. NongJia ZhiFu GuWen 2016, 18, 23. [Google Scholar]
  45. Jin, H.H. Investigation and Prevention and Cure to Trichinosis in Swine in Liuzhou City, Guangxi. Master’s Thesis, NanJing Agriculture University, Nanjing, Jiangsu, 2006. [Google Scholar]
  46. Liu, J.B. Survey of Trichinella spiralis in Slaughtering Pigs in Hechi City, Guangxi Autonomous Region. China Anim. Health Insp. 2004, 21, 34. [Google Scholar] [CrossRef]
  47. Gai, W.Y.; Wang, J.W.; Wang, J.; Huang, X.M.; Qu, Z.N.; Hong, J. Swine Trichinosis Detection in Slaughterhouses in Some Areas of Shandong Province. China Anim. Health Insp. 2018, 35, 11–12. [Google Scholar]
  48. Jiang, P.; Ding, Y.X.; Yao, Y.H.; Liu, L.N.; Zhang, D.; Wu, X.L.; Cui, J.; Wang, Z.Q. Investigation on swine Trichinella infection in Shangqiu area of Henan Province. Chin. J. Zoonoses 2011, 27, 846–847. [Google Scholar] [CrossRef]
  49. Yang, Y.B.; Zhang, X.J.; Ye, C.H.; Xu, H.F.; Li, Z. Serological Investigation on Trichinella spiralis Infection in Slaughted Swine in Qinhai Province. Prog. Vet. Med. 2011, 32, 135–136. [Google Scholar]
  50. Zhang, Y.Q.; Zhong, H.J.; Jiang, Y.J. Seroepidemiological investigation of trichinosis in zoonotic diseases. Chin. Anim. Husb. Vet. Abstr. 2016, 32, 131. [Google Scholar]
  51. Jia, Q.S.; Lu, X.D.; Peng, Y.L.; Xiao, K.C.; Lu, X.H. A investigation on the Trichina infection condition of swine in Xichang. Sichuan Anim. Vet. Sci. 2004, 31, 27–29. [Google Scholar]
  52. Wang, J.Q. Investigation on infection of trichinella spiralis in pork and analysis of epidemic factors. Mod. Anim. Husb. Sci. Technol. 2008, 2, 108–109. [Google Scholar]
  53. Bai, M.Y.Z.; Li, J.K.; Da, W.Z.M.; Shang, P.; Yang, T.; Liu, J.F.; Qiang, B.Y.Z. Investigation to Trichinosis in Swine in LinZhi city, molecular identification of Trichinella isolate from Tibet. Mod. Anim. Husb. Sci. Technol. 2010, 8, 112–113. [Google Scholar]
  54. Jiang, P.; Zhang, X.; Wang, L.A.; Han, L.H.; Yang, M.; Duan, J.Y.; Sun, G.G.; Qi, X.; Liu, R.D.; Wang, Z.Q.; et al. Survey of Trichinella infection from domestic pigs in the historical endemic areas of Henan province, central China. Parasitol. Res. 2016, 115, 4707–4709. [Google Scholar] [CrossRef]
  55. Cui, J.; Jiang, P.; Liu, L.N.; Wang, Z.Q. Survey of Trichinella infections in domestic pigs from northern and eastern Henan, China. Vet. Parasitol. 2013, 194, 133–135. [Google Scholar] [CrossRef]
  56. Cao, J.P.; Li, J.R.; Chen, S.X.; Zhou, H.J.; Jiang, B.Q.; Ren, R.S.; Zhang, Z.X.; Qiu, L.S. Investigation on infection of cysticercus and Trichinella spiralis in pigs in Xuzhou area. Chin. J. Schistosomiasis Control. 1996, 08, 238–239. [Google Scholar]
  57. Cao, Y.J.; Chen, Y.C.; Qin, B.Y.; Guan, M.; Wei, M.P. Investigation of Trichinella infection in slaughtered pigs in Nanning city. Guangxi J. Anim. Husb. Vet. Med. 2002, 18, 13–14. [Google Scholar]
  58. Zhai, W.H.; Ma, F.C.; Zhang, Y.Y.; Zhong, W.B.; Fan, X.L. Investigation on infection of Trichinella spiralis in commercial pigs in Huangyuan County. Chin. Qinghai J. Anim. Vet. Sci. 1999, 29, 19. [Google Scholar]
  59. Luo, G.P.; Hu, T.Y.; Zhang, Y.Q.; Lin, M.L.; Jiang, S.Z.; Hu, Y.J.; Lu, X.Y.; Song, M.X.; Lu, Y.X.; Li, S.S.; et al. Serological investigation of pig trichinosis in Mudanjiang City. Meat Hyg. 1998, 3, 9–10. [Google Scholar]
  60. Teng, Y.D.; Xue, C.Y.; Li, J.Q. Serological investigation of Trichinella spiralis in slaughtered pigs. Pop. Sci. Technol. 2007, 4, 138–145. [Google Scholar]
  61. Wen, Z.B.; Zhang, H.Z.; Huang, M.; Wei, Z.X. Investigation on infection of Trichinella spiralis in slaughtered pigs in Qinzhou City. Guangxi J. Anim. Husb. Vet. Med. 2006, 4, 154–156. [Google Scholar]
  62. Yuang, Y.Z.; Cai, R.Z.M. Investigation on infection of Trichinella spiralis in pigs in Delingha city. Chin. Qinghai J. Anim. Vet. Sci. 2004, 34, 28. [Google Scholar]
  63. Zhang, Y.L.; Zhu, Y.K.; Chen, W.Q.; Xu, B.L.; Zhang, H.W.; Deng, Y. The prevalence of trichinellosis in Sheqi, Nanyang in 2016. J. Trop. Med. 2017, 17, 1541–1543. [Google Scholar]
  64. Ji, Y.; Cao, R.J.; Liu, J.Y.; Li, S.G.; Li, S.; Gan, S.B. Investigation of several parasitic infection in pig population in Beijing. J. Pathog. Biol. 1993, 3, 219. [Google Scholar]
  65. Wang, X.; Liu, J.S.; Luo, J.; Hao, X.J.; Chen, X.N.; Wang, F.; Sun, R.Q. Investigation of the caterpillar disease infection in Chengde City. J. Med. Pest Control. 2003, 12, 736–737. [Google Scholar]
  66. Yao, Y.F.; Guo, J.G.; Li, H.M.; Deng, C.Y. Investigation of slaughtered pigs in Guangxi. Chin. J. Anim. Infect. Dis. 2004, 12, 13–14. [Google Scholar]
  67. Liu, X.L.; Wang, L. Investigation and prevention and control mode of parasitic diseases in large-scale pig farms in Henan Province. Heilongjiang Anim. Sci. Vet. Med. 2013, 21, 124–126. [Google Scholar]
  68. Wang, P.R.; Zhang, D.; Yang, H.C.; Dong, G.F.; Chen, X.S. Investigation on infection of trichinella spiralis in pork in Henan Province. Chin. J. Zoonoses 1997, 13, 71–72. [Google Scholar]
  69. Dong, Y.J.; Xing, X.L.; Wang, R.J.; Li, J.M. Investigation of Trichinosis infection in pigs in Xining area. Chin. Qinghai J. Anim. Vet. Sci. 1995, 5, 31–36. [Google Scholar]
  70. Xu, Z.M.; Cao, Z.Y. Investigation on infection of Trichinella and Cysticercosis in Xiangfan city. Chin. J. Parasitol. Parasit. Dis. 1997, 15, 58. [Google Scholar]
  71. Luo, C.F.; Kong, Z.X.; Tang, Y.H.; Jin, W.H.; Dong, Y.; Liu, H.; Li, J.S. Investigation of Trichinosis in CuiyunDistrict, Simao City. J. Med. Pest Control. 2004, 20, 296–297. [Google Scholar]
  72. Li, W.Z.; Wang, J.M.; Zhang, B.; Qin, W.; Yang, Y.; Guo, H.P.; Pu, S.W.; Guo, J.C.; Li, J.J. Epidemiological investigation of Trichinella spiralis infection in human and animal in Jianshui County. Guide China Med. 2010, 8, 116–117. [Google Scholar] [CrossRef]
  73. Wang, L.; Zhao, G.; Zhao, J.M.; Gao, Y.B.; Yan, S.G.; Li, Y.H.; Liu, N.; Zhang, Q.Q.; Huang, X.M.; Liu, J.H.; et al. Detection of Trichinella spiralis and Toxoplasma gondii in Pigs for Slaughtering in Some Regions of China in 2019. China Anim. Health Insp. 2020, 37, 1–4. [Google Scholar]
  74. Gong, Q.L.; Ge, G.Y.; Wang, Q.; Tian, T.; Liu, F.; Diao, N.C.; Nie, L.B.; Zong, Y.; Li, J.M.; Shi, K.; et al. Meta-analysis of the prevalence of Echinococcus in dogs in China from 2010 to 2019. PLoS Negl. Trop. Dis. 2021, 15, e0009268. [Google Scholar] [CrossRef]
  75. Wei, X.Y.; Gong, Q.L.; Zeng, A.; Wang, W.; Wang, Q.; Zhang, X.X. Seroprevalence and risk factors of Toxoplasma gondii infection in goats in China from 2010 to 2020: A systematic review and meta-analysis. Prev. Vet. Med. 2021, 186, 105230. [Google Scholar] [CrossRef]
  76. Asundi, A.; Beliavsky, A.; Liu, X.J.; Akaberi, A.; Schwarzer, G.; Bisoffi, Z.; Requena-Méndez, A.; Shrier, I.; Greenaway, C. Prevalence of strongyloidiasis and schistosomiasis among migrants: A systematic review and meta-analysis. Lancet Glob Health 2019, 7, e236–e248. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  77. Pozio, E.; Rinaldi, L.; Marucci, G.; Musella, V.; Galati, F.; Cringoli, G.; Boireau, P.; La Rosa, G. Hosts and habitats of Trichinella spiralis and Trichinella britovi in Europe. Int. J. Parasitol. 2009, 39, 71–79. [Google Scholar] [CrossRef] [PubMed]
  78. Nicorescu, I.M.D.; Ionita, M.; Ciupescu, L.; Buzatu, C.V.; Tanasuica, R.; Mitrea, I.L. New insights into the molecular epidemiology of Trichinella infection in domestic pigs, wild boars, and bears in Romania. Vet. Parasitol. 2015, 212, 257–261. [Google Scholar] [CrossRef] [PubMed]
  79. Pozio, E.; Darwin Murrell, K. Systematics and epidemiology of trichinella. Adv. Parasitol. 2006, 63, 367–439. [Google Scholar] [CrossRef] [PubMed]
  80. Cui, J.; Wang, Z.Q. An epidemiological overview of swine trichinellosis in China. Vet. J. 2011, 190, 323–328. [Google Scholar] [CrossRef]
  81. Söderberg, R.; Lindahl, J.F.; Henriksson, E.; Kroesna, K.; Ly, S.; Sear, B.; Unger, F.; Tum, S.; Nguyen-Viet, H.; Ström Hallenberg, G. Low Prevalence of Cysticercosis and Trichinella Infection in Pigs in Rural Cambodia. Trop. Med. Infect. Dis. 2021, 6, 100. [Google Scholar] [CrossRef]
  82. Conlan, J.V.; Vongxay, K.; Khamlome, B.; Gomez-Morales, M.A.; Pozio, E.; Blacksell, S.D.; Fenwick, S.; Thompson, R.C. Patterns and risks of trichinella infection in humans and pigs in northern Laos. PLoS Negl. Trop. Dis. 2014, 8, e3034. [Google Scholar] [CrossRef]
  83. Holt, H.R.; Inthavong, P.; Khamlome, B.; Blaszak, K.; Keokamphe, C.; Somoulay, V.; Phongmany, A.; Durr, P.A.; Graham, K.; Allen, J.; et al. Endemicity of Zoonotic Diseases in Pigs and Humans in Lowland and Upland Lao PDR: Identification of Socio-cultural Risk Factors. PLoS Negl. Trop. Dis. 2016, 10, e0003913. [Google Scholar] [CrossRef] [Green Version]
  84. Thi, N.V.; De, N.V.; Praet, N.; Claes, L.; Gabriël, S.; Dorny, P. Seroprevalence of trichinellosis in domestic animals in northwestern Vietnam. Vet. Parasitol. 2013, 193, 200–205. [Google Scholar] [CrossRef]
  85. Pozio, E. Searching for Trichinella: Not all pigs are created equal. Trends Parasitol. 2014, 30, 4–11. [Google Scholar] [CrossRef]
  86. Pannwitz, G.; Mayer-Scholl, A.; Balicka-Ramisz, A.; Nöckler, K. Increased prevalence of Trichinella spp., northeastern Germany, 2008. Emerg. Infect. Dis. 2010, 16, 936–942. [Google Scholar] [CrossRef] [PubMed]
  87. Pozio, E. Trichinella spp. imported with live animals and meat. Vet. Parasitol. 2015, 213, 46–55. [Google Scholar] [CrossRef] [PubMed]
  88. Széll, Z.; Marucci, G.; Pozio, E.; Sréter, T. Echinococcus multilocularis and Trichinella spiralis in golden jackals (Canis aureus) of Hungary. Vet. Parasitol. 2013, 197, 393–396. [Google Scholar] [CrossRef] [PubMed]
  89. Zhang, X.Z.; Wang, Z.Q.; Cui, J. Epidemiology of trichinellosis in the People’s Republic of China during 2009–2020. Acta Trop. 2022, 229, 106388. [Google Scholar] [CrossRef] [PubMed]
  90. Gong, Q.L.; Li, J.; Li, D.; Tian, T.; Leng, X.; Li, J.M.; Shi, K.; Zhang, N.Z.; Du, R.; Zhao, Q. Seroprevalence of Toxoplasma gondii in cattle in China from 2010 to 2019: A systematic review and meta-analysis. Acta Trop 2020, 211, 105439. [Google Scholar] [CrossRef] [PubMed]
  91. OIE. OIE Terrestrial Manual. Part 2 OIE Listed Diseases and Other Diseases of Importance Section 2.1. Multiple Species (Chapter 2.1.20 TRICHINELLOSIS); OIE: Paris, Franch, 2016. [Google Scholar]
  92. Liu, Y.; Xu, N.; Li, Y.; Tang, B.; Yang, H.; Gao, W.; Liu, M.; Liu, X.; Zhou, Y. Recombinant cystatin-like protein-based competition ELISA for Trichinella spiralis antibody test in multihost sera. PLoS Negl. Trop. Dis. 2021, 15, e0009723. [Google Scholar] [CrossRef] [PubMed]
  93. Health, W.O.f.A. Trichinellosis (infection with Trichinella spp.). Man. Diagn. Tests Vaccines Terr. Anim. 2021, 2018, 649–659. [Google Scholar]
  94. Wang, W.; Gong, Q.L.; Zeng, A.; Li, M.H.; Zhao, Q.; Ni, H.B. Prevalence of Cryptosporidium in pigs in China: A systematic review and meta-analysis. Transbound. Emerg. Dis. 2021, 68, 1400–1413. [Google Scholar] [CrossRef]
  95. Jenkins, D.J. WHO/OIE manual on Echinococcosis in humans and animals: A public health problem of global concern. Int. J. Parasitol. 2001, 31, 1717–1718. [Google Scholar] [CrossRef]
  96. Eslahi, A.V.; Badri, M.; Khorshidi, A.; Majidiani, H.; Hooshmand, E.; Hosseini, H.; Taghipour, A.; Foroutan, M.; Pestehchian, N.; Firoozeh, F.; et al. Prevalence of Toxocara and Toxascaris infection among human and animals in Iran with meta-analysis approach. BMC Infect. Dis. 2020, 20, 20. [Google Scholar] [CrossRef] [Green Version]
  97. Weerakoon, K.G.; Gobert, G.N.; Cai, P.; McManus, D.P. Advances in the Diagnosis of Human Schistosomiasis. Clin. Microbiol. Rev. 2015, 28, 939–967. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  98. WHO. Multicriteria-Based Ranking for Risk Management of Food-Borne Parasites. Microbiological Risk Assessment Series No. 23. Report of a Joint FAO/WHO Expert Meeting Rome; WHO: Geneva, Switzerland, 2012. [Google Scholar]
  99. 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] [PubMed]
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Figure 1. The flow diagram of search and selection of relevant articles for a systematic review on the prevalence of Trichinella spiralis in domestic pigs in China.
Figure 1. The flow diagram of search and selection of relevant articles for a systematic review on the prevalence of Trichinella spiralis in domestic pigs in China.
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Figure 2. Forest plot showing the pooled prevalence of Trichinella spiralis in domestic pigs in China. The length of the horizontal line represents the 95% confidence interval and the diamond represents the summarized effect [34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72].
Figure 2. Forest plot showing the pooled prevalence of Trichinella spiralis in domestic pigs in China. The length of the horizontal line represents the 95% confidence interval and the diamond represents the summarized effect [34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72].
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Figure 3. Distribution map of Trichinella spiralis in domestic pigs in China.
Figure 3. Distribution map of Trichinella spiralis in domestic pigs in China.
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Figure 4. Egger’s test for publication bias in Trichinella spiralis infection in domestic pigs in China.
Figure 4. Egger’s test for publication bias in Trichinella spiralis infection in domestic pigs in China.
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Figure 5. Funnel plot with trim and fill analysis of the publication bias in Trichinella spiralis infection in domestic pigs in China.
Figure 5. Funnel plot with trim and fill analysis of the publication bias in Trichinella spiralis infection in domestic pigs in China.
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Table
Table 1. Baseline characteristics of included studies of Trichinella spiralis infection in domestic pigs in China.
Table 1. Baseline characteristics of included studies of Trichinella spiralis infection in domestic pigs in China.
IDStudyPeriodLocationPe (%)SamplingDetection MethodsScore
NTotalBSPME
1[34]1993~2004Hubei693 (5.60)12,373Y Y 7
2[35]1998Yunnan35 (0.27)12,763Y Y 5
3[36]1995.3~1995.7Qinghai14 (0.69)2026Y Y 4
4[37]NAGuangxi67 (1.43)4673 YY Y2
5[38]2013.9~2014.12Henan12 (0.54)2238Y YY 7
6[39]NAInner Mongolia100 (0.50)20,000YYY Y7
7[40]NAQinghai14 (4.86)288 Y Y2
8[41]NAHenan18 (6.47)278Y YY 7
9[42]2003.1~2005.12Henan104 (2.93)3887YYYY 7
10[43]1965Yunnan44 (2.58)1700Y Y 5
11[44]2014.9~2015.8Guizhou18 (5.66)318Y Y5
12[45]2002.6~2002.9Guangxi305 (2.99)10,191YYY Y6
13[46]2001.7~2003.11Guangxi1363 (7.49)18,199YYY Y7
14[47]2015~2017Shandong12 (1.58)758YYY Y7
15[48]2010~2011Henan9 (3.30)273Y Y 8
16[49]2010.12Qinghai19 (1.78)1065 Y Y4
17[50]2015.1~2015.7Inner Mongolia225 (11.25)2000 Y Y7
18[51]NASichuan638 (6.22)10,260YYY Y4
19[40]NAGansu11 (5.14)214 Y Y2
20[52]NAShanxi4 (0.58)684Y Y 2
21[53]2009.8~2010.1Tibet2 (0.77)261YYY Y6
22[54]2014–2015Henan5 (0.61)823Y Y 5
23[55]2010.2~2011.2Henan18 (3.79)475Y Y 6
24[56]1993.11Jiangsu33 (0.003)7261NA NA 3
25[57]2001.7~2002.6Guangxi840 (16.47)5101YYY Y4
26[58] 1997.5~1997.7Qinghai40 (15.87)252Y Y 3
27[59]NAHeilongjiang38 (10.41)365 Y Y2
28[60]2004.1~2005.12Guangxi293 (17.81)1645YYY Y7
29[61]2004.1~2004.12Guangxi499 (16.63)3000YYY Y6
30[61]2005.1~2005.10Guangxi359 (19.7)1821YYY Y6
31[62]2004.1~2004.3Qinghai115 (23)500Y Y 3
32[63]NAHenan0 (0)346Y Y 3
33[64]NABeijing1 (0.09)1062 Y Y2
34[65]2002–2003Hebei0 (0)259Y Y 6
35[66] 2001Guangxi1720 (115.21)11,310YYY Y5
36[66] 2002Guangxi4539 (14.07)32,253YYY Y5
37[67]2010.5–2011.5Henan0 (0)580 Y Y6
38[68]1995Henan3241 (4.27)75,821Y Y 4
39[69]1990.5–1990.7Qinghai4 (0.12)3471Y Y 2
40[70]1985–1993Hubei19,637 (6.76)290,294Y Y 3
41[71]NAYunnan0 (0)500Y Y 2
42[72]2003.8Yunnan0 (0)506Y Y 3
43[46]2001.7–2003.11Guangxi1350 (15)9003YYY Y7
NA: data not applicable; P: parasitology; E: enzyme-linked immunosorbent assay; M: molecular; B: biopsy; S: serology; Pe: positive rate, N/Total (%); Y: yes.
Table
Table 2. Pooled prevalence of risk factors in Trichinella spiralis infection in domestic pigs in China.
Table 2. Pooled prevalence of risk factors in Trichinella spiralis infection in domestic pigs in China.
VariableNo. of StudiesNo. of TestNo. of Positive Prevalence (%) 95%CIHeterogeneity (Q)Univariate
Meta-Regression
QI2 (%)pCoefficient (95% CI)p
Region 0.501 (0.242,0.760)<0.05
Northwest 0.03 (0.01, 0.10)360.6998.34<0.01−0.314 (−0.585, −0.043)<0.05
Qinghai67602206
Gansu121411
Central South 0.06 (0.03, 0.09)7119.8999.72<0.01−0.256 (−0.521, 0.009)>0.05
Henan984,7213407
Hubei2302,66720,330
Guangxi1097,19611,335
Southwest 0.01 (0.00, 0.04)1007.1099.40<0.01−0.404 (−0.681, −0.128)<0.05
Guizhou131818
Tibet12612
Yunnan415,46979
Sichuan110,260638
Northeast NANANANANANA
Heilongjiang136538
North China 0.01 (0.00, 0.05)561.5199.29<0.01−0.425 (−0.741, −0.109)<0.01
Inner Mongolia222,000325
Shanxi16844
Beijing110621
Hebei12590
East China NANANANA−0.269 (−0.586, 0.048)>0.05
Jiangsu1726133
Shandong175812
Score 0.209 (0.070, 0.348)<0.05
≤2 (low)811,2571390.02 (0.00, 0.04)211.7296.69<0.01
>2 to ≤5 (middle)17452,59930,9380.05 (0.02, 0.08)8287.3399.81<0.01
>5 to ≤8 (high)1887,24153620.05 (0.02, 0.08)4993.4599.66<0.01
Detection methods 0.176 (0.073, 0.278)<0.01
P17403,06623,8590.02 (0.01, 0.05)4255.2099.62<0.01
E858923260.04 (0.01, 0.08)421.9498.34<0.01
P&E14128,47512,0870.08 (0.04, 0.13)8124.9799.84<0.01
P&M364031340.03 (0.00, 0.07)64.0296.88<0.01
NA1726133NANANANA
Sampling 0.195 (0.131, 0.259)<0.01
B20405,90023,9070.02 (0.01, 0.04)4504.6899.58<0.01
S810,2473750.03 (0.01, 0.07)478.2098.54<0.01
B&S14127,68912,1240.08 (0.05, 0.13)7834.3499.83<0.01
NA1726133NANANANA
publication year 0.281 (0.217, 0.345)<0.05
≤200013400,19023,1790.02 (0.01, 0.04)1612.7499.26<0.01
>2000 to ≤200816120,98612,8220.08 (0.05, 0.13)3974.1199.62<0.01
>20081429,9214380.02 (0.01, 0.03)685.1898.10<0.01
Overall 551,09736,439
CI: Confidence interval; NA: data not applicable; P: parasitology; E: enzyme-linked immunosorbent assay; M: molecular; P&E: parasitology and enzyme-linked immunosorbent assay; P&M: parasitology and molecular; B: biopsy; S: serology; B&S: biopsy and serology; p < 0.05 is statistically significant.
Table
Table 3. Normal distribution test for the normal rate and the different conversion of the normal rate in Trichinella spiralis infection in domestic pigs in China.
Table 3. Normal distribution test for the normal rate and the different conversion of the normal rate in Trichinella spiralis infection in domestic pigs in China.
Conversion Form Wp
PRAW0.825741.352 × 10−5
PLNNaNNA
PLOGITNaNNA
PAS0.9350.01732
PFT0.936840.02009
“PRAW”: original rate; “PLN”: logarithmic conversion; “PLOGIT”: logit transformation; “PAS”: arcsine transformation; “PFT”: double-arcsine transformation; “NaN”: meaningless number. “NA”: missing data; W; wilcoxon value; p: p value.
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Bai, H.; Tang, B.; Qiao, W.; Wu, X.; Liu, M.; Wang, X. The Prevalence of Trichinella spiralis in Domestic Pigs in China: A Systematic Review and Meta-Analysis. Animals 2022, 12, 3553. https://0-doi-org.brum.beds.ac.uk/10.3390/ani12243553

AMA Style

Bai H, Tang B, Qiao W, Wu X, Liu M, Wang X. The Prevalence of Trichinella spiralis in Domestic Pigs in China: A Systematic Review and Meta-Analysis. Animals. 2022; 12(24):3553. https://0-doi-org.brum.beds.ac.uk/10.3390/ani12243553

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Bai, Huifang, Bin Tang, Weidong Qiao, Xiaoxia Wu, Mingyuan Liu, and Xuelin Wang. 2022. "The Prevalence of Trichinella spiralis in Domestic Pigs in China: A Systematic Review and Meta-Analysis" Animals 12, no. 24: 3553. https://0-doi-org.brum.beds.ac.uk/10.3390/ani12243553

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