Economic Implications of Porcine Cysticercosis Based on Meta-Analysis Estimates of its Prevalence in India

A meta-analysis of 27 studies systematically obtained from online free databases spanned over period from 2000 to 2019 from different parts of India was done. The pooled estimate of porcine cysticercosis prevalence using random effect model was found 5.21% with 95% CI as 4.04% to 6.52% and 95% PI 1.62%–15.46%. A wide variation in the prevalence estimates among studies under this analysis was observed which is confirmed through Q statistics =1322.38 (P=0.000). Substantial heterogeneity was observed between studies which is significant (I 2 =96.52; p =<0.0001 and Tau squared value =0.0341) considering the diversity of populations reported in recruited studies. The sub-group analysis showed significantly higher prevalence in South region followed by North, North-east and West region of India. As regards the methods employed for detection of cysticerci from pigs, it was found that serological method showed higher rate of prevalence. A prevalence of 10.66% (95% CI=5.63% to 15.95%) is reported from those studies which used serological methods whereas carcass examination which is the frequently adopted method detected only 3.71% prevalence (95% CI =2.77% to 4.78%) and other methods such as molecular and histo-pathological studies for prevalence detected cysticercosis in 4.19% (95% CI=2.61% to 5.99%) carcasses over the study period under this meta-analysis. Considering its zoonotic significance as well as economic losses to pork industry, control strategies for PCC need to be devised with regards to health monitoring, hygienic meat practices coupled with education to both the producers and consumers through one health approach. ABSTRACT


INTRODUCTION
L ivestock parasitism constitutes one of major biotic stress factors in reducing the productivity of animals and deterioration of health (Radostits et al., 2000). Amongst them, zoonotic parasites has a distinct perspective as they exert risks both to livestock as well as human along with the state of persistent contamination of environment (Reinhard et al., 2013;Laranjo-Gonzalez et al., 2017). Taenia solium cysticercosis is known to be one of the most important parasitic zoonoses in tropical countries and porcine cysticercosis results in significant losses to pork industry worldwide (Rashid et al., 2018;Devleesschauwer et al., 2017). In human, the disease shows variable clinical entities if present in vital organs and remains sub-clinical if the cysts are present in striated muscles (Coral-Almeida et al., 2015, Mendlovic et al., 2021. Depending on the location, cysticercosis in human is manifested as ocular cysticercosis when eyes are involved or neurocysticercosis when nervous system is involved (Wardrop et al., 2016;Rajshekhar, 2016). The tapeworm is disseminated in the environment through pigs which are predominantly reared under scavenging type of management (Basanez et al., 2012). Due to lack of proper sanitation and un-hygienic conditions, human settlements in the proximity of such rearing systems are at higher risk of contracting the cysticercosis (Bizhani et al., 2020). In addition the lack of awareness coupled with unhygienic surroundings for a living make the populations at risk more prone to contracting such diseases (Kungu et al., 2017;Alarakol et al., 2021). The association between the prevalence of PCC with societies with poor sanitary conditions, inadequate hygiene, open defecation, presence of free roaming pigs and poverty have been reported through several earlier studies (Macpherson, 2005, Quet et al., 2010Assana et al., 2012). With more prevalence in downtrodden societies, the impact of PCC is enormous (Ito et al., 2019).
Even after several control programs have been suggested and implemented in India, the situation in the country remain passive due to partial evidence based information about the extent of PCC to the stakeholders (Anonymous, 2013). The immunological control option though available in limited locations in India, its adoption in pigs is low and similar possibility in human seems obscure (Kabululu et al., 2020;Kaur et al., 2021). This warrants more information need to be generated with substantial accuracy as regards to the extent of PCC, validation of different detection methods as well as regarding awareness of common public on PCC apt practices (Wardrop et al., 2015).
Due to its zoonotic significance, as per the meat regulatory guidelines in most of the countries, the cysticercosis infected pork needs to be condemned and termed as unfit for human consumption (Girotra et al., 2014;Gabriel et al., 2015). Such meat condemnation although implies pork industry loss of a huge amount of revenue which would have added unless the safe pork is sold (Pathak and Chhabra, 2012). The economic impact of porcine cysticercosis due to the rejection of meat and edible offal has been reported throughout the globe (Rashid et al., 2018). In India, perhaps very few primary studies were attempted to estimate the losses suffered to pork industry due to porcine cysticercosis , Barua et al., 2019. The present study is an estimation of approximate losses to Indian meat industry due to porcine cysticercosis however it relies on data obtained from the meta-analysis of published prevalence reports.

Meta-analysis
The primary studies reporting the prevalence of porcine cysticercosis in pig carcasses and published between 2000 and 2019 obtained through systematic search of online free databases viz. GoogleScholar, PubMed, J-GatePlus were subjected to meta-analysis of its prevalence. PRISMA guidelines were followed for selection of studies for metaanalysis (Moher et al., 2009). Prevalence data from such selected studies were then systematically tabulated in Ms-Excel with respect to name of authors and year of publication, year of abattoir survey / sampling, place of work, method of detection, organs detected, number of carcasses/ animals detected and number of carcasses / samples found positive for harbouring Taenia solium cysts.
Meta-analysis was done to obtain pooled prevalence of PCC by employing random effects meta-analysis because of significant heterogeneity between studies for which Meta-XL addon is used as described in earlier studies (Bhangale, 2020). The effect size i.e. pooled prevalence and standard error of the effect size was calculated and then pooled with a 95% confidence interval. The between study variance was measured by Cochran's Q and Higgin's I 2 statistics. The heterogeneity was considered low, moderate and high if I 2 values were 25%, 50%, and 75% respectively (Higgins and Thompson, 2002). Funnel plot visualization and LFK Index was used for assessment of publication bias (Kanamori et al., 2018). Subgroup meta-analysis was also analyzed by grouping variables by regions of studies and methods of detection of cysts. All the analyses were done with the help of MetaXL add-in (EpiGear International Pty Ltd, Queensland, Australia).

Economic losses
The economic loss accruing to organ condemnation and body weight loss due to cysticercosis was estimated on the basis of estimate given by Vaidya et al. (2014). The average economic loss reported in the study was calculated as ` 1726.31 per cysticercosis affected pig carcass which Bhangale, 2022 was adjusted to the value of Rupees during in 2019 as per dynamics of Consumer price Index (RBI). Assuming that 50% of total pig population is slaughtered annually for meat purpose, total number of pigs slaughtered was calculated based on National Livestock Census report 2019 (DAHD, 2019). Consequently, number of cysticercosis infected pigs was then calculated by multiplying the pooled prevalence obtained through this meta-analysis with the total number of animals slaughtered in 2019.

Characteristics of studies under meta-analysis
Systematic search of the databases yielded 27 studies encompassing the prevalence of PCC from all over the country ( Figure 1, Table 1). More number of studies were from Southern region (10) followed by Northern (09), North-eastern and Western region (04 each). Studies recruited showed that multiple methods were employed in same study for detection of cysts. Post mortem inspection (26 reports from 23 studies) was the most adopted method of detection of PCC while serological detection (18 reports from 07 studies) and molecular diagnosis were also followed for its detection. for post slaughter detection of PCC in pig carcasses shoulder muscle, thigh muscle, masseter muscle, neck, diaphragm and heart were most preferred sites while tongue, greater omentum, mesentery, other visceral organs including liver were also searched for presence of cysticerci. Serological detection was also found on rising trend of utility and adoption wherein ELISA, IFAT, CIEP, Western Blot were the preferred tests. One study revealed PCC prevalence by employing molecular diagnostic method while one other study reported prevalence from histo-pathological screening of pigs' brains.

Meta-analysis
The pooled estimate of porcine cysticercosis prevalence using random effect model was found 5.21% with 95% CI as 4.04% to 6.52%. Proportion forest plot of pooled prevalence is presented in Figure 2. A wide variation in the prevalence estimates among studies under this analysis was observed which is confirmed through Q statistics =1322.38 with DF =29 and P=0.000. Substantial heterogeneity was observed between studies which is significant (I 2 =96.52; p=<0.0001 and Tau squared value =0.0341) considering the diversity of populations reported in recruited studies.
Current review revealed pooled prevalence of porcine cysticercosis to the tune of 5.21% in pork samples/ pig carcasses. These results corroborate with Atawalna and Mensah (2015) from Ghana where they reported 4.59% prevalence of PCC in sows. Adesokan and Adeoye (2019) also reported 4.4% prevalence of PCC from Nigeria. Similarly, Rajshekhar (2004) in a review reported its prevalence in the range of 7−26% from India and 14−32% from Nepal. Mwabonimana et al. (2020) found porcine cysticercosis detected visually in 3.7% carcasses while with serological methods they detected PCC in 5.3% carcasses. Systematic review coupled with meta-analysis provide comprehensive overview on the dynamics of diseases or pathogens in a particular setup even if the outcomes may not be precise yet their applicability in planning surveillance and monitoring cannot be overlooked ( Zammarchi et al., 2013;Laranjo-Gonzalez et al., 2017). None of the studies under the current meta-analysis reported organ wise prevalence. Yet it is established that lingual palpation is the best suited method for accurate diagnosis of cysticercosis in pig carcasses (Shonyela et al., 2018). As far as diagnostic approach with serological or molecular methods are concerned, it is not widely adopted evidenced by the reports under this meta-analysis.

Sub-group analysis
The sub-group analysis of the prevalence of cysticercosis among pig in India has shown that more prevalence was noted in South (9.09% CI=6.08% to 12.40%) region followed by North (4.88% 95% CI=2.34% to 7.85%), North-east (3.67%, CI =1.54% to 6.22%) and West (2.46% CI=1.55% to 3.53%) which was significant ( Table 2). As regards the methods employed for detection of cysticerci from pigs, it was found that serological method had shown precision in detecting the cysts in porcine hosts. Overall prevalence of 10.66% (95% CI=5.63% to 15.95%) is reported from those studies which used serological methods whereas carcass examination which most followed method detected  The sub group analysis according to detection methods suggests that due to higher prevalence values in seroprevalence studies, overall pooled prevalence is higher which would not be actual prevalence as detected by direct detection of cysts through carcass examination or histo-pathological investigation. Yet their utility in ante-mortem screening followed by treatment must be encouraged for assuring the food safety standards (Phiri et al., 2006). In recent times the developments in imaging techniques such as ultrasonography may yield precision in the detection of cysticercosis (Flecker et al., 2017). The need of development of newer diagnostic approaches synergistically with immunological and molecular tools have been advocated by several studies mostly due to unsatisfactory reports on the part of specificity and sensitivity issues of existing methods (Jayashi et al., 2012, McKarthy et al., 2012Goussanou et al., 2014).
Sub-group analysis according to the sample size of studies shows no major deviation in heterogeneity and indicates that as the sample size increases prevalence rates decreases. The studies under this meta-analysis mostly cover the urban or city areas where slaughtering is practiced under the aegis of regulations of municipal corporations (Prasad et al., 2008, Sarma et al., 2000Prasad et al., 2002Hafeez et al., 2004An Hafeez et al., 2004An a Hafeez et al., 2004An b Hafeez et al., 2004KI Hafeez et al., 2004KI a Hafeez et al., 2004KI b Hafeez et al., 2004Kn Hafeez et al., 2004Kn a Hafeez et al., 2004Kn b Hafeez et al., 2004TN Hafeez et al., 2004TN a Hafeez et al., 2004TN b Selvam et al., 2004Sharma et al., 2005a Sharma et al., 2005Prakash et al., 2007Borkataki et al., 2012Mohan et al., 2013Sreedevi et al., 2012Rout and Saikumar 2012Kalai et al., 2012Saravanan et al., 2014Bhadrige et al., 2014Koushik and Islam 2014Vaidya et al., 2014Pg Chawhan et al., 2015Sahoo et al., 2016Sreedevi et al., 2016Sharma et al., 2017Shende et al., 2016Abirami et al., 2018Satyaprakash et al., 2018Singh et al., 2018Vaidya et al., 2018ELISA Vaidya et al., 2018Ml Vaidya et al., 2018PCR Vaidya et al., 2018Visual Vaidya et al., 2018 Barua et al., 2021). Yet the data on swine diseases including PCC from pigs slaughtered in rural settings has not been recorded or documented (Prasad et al., 2007, Haldar et al., 2017. This might reveal presence of the disease at relatively greater extent. The rationale for geographically uneven distribution of PCC may be attributed to the social and culinary preferences of various regions for swine husbandry in general and pork as a food in particular as compared to other regions of the country (Barua et al., 2021).
In India, pigs' husbandry in urban areas is mostly under scavenging system of rearing. Usually pigs are marked for identification and let free for roaming in town and city areas in open public places and sewage streams or tanks (Chouhan et al., 2016). Roaming of pigs around and proximity of slaughter facility to localities contribute significantly in risks of NCC in human (Assana et al., 2010, Akoko et al., 2019. Although no correlation reported between consumption of meat type and occurrence of NCC in human (Girotra et al., 2014).

Publication bias
For publication bias assessment, the funnel plot was used and it showed presence of bias to the right side which could be attributed to more studies with relatively higher prevalence estimates. This was also supported by the Doi plot and LFK index (4.63) showing major asymmetry and thereby a substantial publication bias (Figure 3 and 4).   It was also to be noted that these estimates are based only on the organ condemnation, however losses due to reduction in carcass weight are not dealt with in this study. In recent times, monetary losses associated with porcine cysticercosis were estimated at USD 19507171 in 2015 in Mexico, a South American country which considered the prevalence in the range of 0.05 to 0.33% in pigs slaughtered in various municipal abattoirs of the country (Bhattarai et al., 2019). Although the economic losses due to PCC may appear apprehensively lower as compared to the economic anatomy of the country to justify the steps to be taken for its control; its public health considerations undeniably needs significant attentions.

CONCLUSION
T he prevalence of porcine cysticercosis in Indian pig is 5.21% and it has considerable bearing on the swine industry through meat condemnation and reduced production. Therefore special attention shall be given to concerted epidemiological monitoring of porcine cysticercosis and hygienic meat production and consumption practices should be popularized for its effective control. Diagnostics with enhanced specificity and sensitivity shall be developed for accurate surveillance in both human and pig hosts.

ACKNOWLEDGEMENT
T he author expresses sincere gratitude to the authorities of College of Veterinary and Animal Sciences, Parbhani, MAFSU, Nagpur for providing the necessary facilities required for this research.