Meta-Analysis of the Prevalence of Porcine Zoonotic Bacterial Pathogens in India: A 13-Year (2010–2023) Study

The presence of bacterial pathogens such as Brucella spp., Clostridium spp., E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., and Streptococcus suis not only hampers pig production but also carries significant zoonotic implications. The present study aims to conduct a comprehensive meta-analysis spanning over 13 years (2010–2023) to ascertain the prevalence of these zoonotic bacterial pathogens in Indian pig populations. The study seeks to synthesize data from diverse geographic regions within India and underscores the relevance of the One Health framework. A systematic search of electronic databases was meticulously performed. Inclusion criteria encompassed studies detailing zoonotic bacterial pathogen prevalence in pigs within India during the specified timeframe. Pertinent information including authors, publication year, geographical location, sampling techniques, sample sizes, and pathogen-positive case counts were meticulously extracted. The meta-analysis of zoonotic bacterial pathogens in Indian pig populations (2010–2023) unveiled varying prevalence rates: 9% Brucella spp., 22% Clostridium spp., 19% E. coli, 12% Listeria monocytogenes, 10% Salmonella spp. and Streptococcus suis, and 24% Staphylococcus spp. The application of random effects further revealed additional variability: 6% Brucella spp., 23% Clostridium spp., 24% E. coli, 14% Listeria monocytogenes, 10% Salmonella spp. and Streptococcus suis, and 35% Staphylococcus spp. Notably, the observed heterogeneity (I2) varied significantly from 87% to 99%. The meta-analysis findings underscore the pervasive nature of these diseases throughout India’s pig populations, accentuating the substantial impact of these pathogens on pig health and the potential for zoonotic transmission. The present study reinforces the importance of the adoption of a comprehensive One Health approach that acknowledges the intricate interplay between animal, human and environmental health.


Introduction
The prevalence of zoonotic bacterial pathogens in animal populations poses substantial challenges to both animal and human health, calling for comprehensive assessments to inform effective management strategies.It is of particular concern for a country like India where pig husbandry plays a pivotal role in uplifting the socio-economic status of the people, especially the tribal masses for whom pig rearing is a way of life.Pork is a high-risk source of foodborne diseases worldwide.Zoonotic bacterial pathogens, such as Brucella spp., Clostridium spp., E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., Mycobacterium spp., Campylobacter spp., and Streptococcus suis have been identified as detrimental to both pig health and public health due to their potential for zoonotic transmission.Individuals closely involved in pig farming, including pig handlers and those who consume pork products under unhygienic conditions, are highly susceptible to infections by these zoonotic bacterial pathogens.These pathogens utilize a range of mechanisms to cause diseases, such as releasing toxins, possessing virulence factors, evading the host's immune system and establishing chronic infections within the host.In clostridial infection, Clostridium perfringens releases alpha toxin [1], while Clostridium difficile produces toxins A (TcdA, enterotoxin A) and B (TcdB, cytotoxin B), which target the colon's lining, causing colitis and severe diarrhoea [2].Enterohemorrhagic E. coli (EHEC) produces Shiga toxins, specifically Shiga toxin 1 (Stx1) and Shiga toxin 2 (Stx2), leading to severe foodborne illnesses [3], while Extended Spectrum Beta-Lactamase (ESBL) E. coli resists many antibiotics due to enzyme production, posing treatment challenges [4,5].Listeria monocytogenes produces listeriolysin O, causing listeriosis [6].Salmonella spp.exhibit resilience to gastric acidity, enabling colonization of the gastrointestinal tract and subsequent invasion of the intestinal mucosa; they produce endotoxins, such as lipid A which can trigger inflammatory responses, and exotoxins, including cytotoxins and enterotoxins like stn, which can damage host cells, disrupt intestinal function, and stimulate cytokine release, contributing to gastrointestinal infections [7].While Staphylococcus spp.are known to produce a wide range of toxins, including staphylococcal enterotoxins, Toxic Shock Syndrome Toxin-1 (TSST-1), exfoliative toxins (ETA and ETB), haemolysins (alpha, beta, and delta), Panton-Valentine Leukocidin (PVL), and superantigens (such as TSST-1 and various staphylococcal enterotoxins) [8,9].The pathogenicity of Staphylococcal toxins is associated with various clinical conditions, from food poisoning to severe skin and systemic infections.Streptococcus suis produces a range of virulence factors, including extracellular enzymes for tissue damage and immune evasion, adhesins for host cell attachment and streptolysins, like suilysin, which induce cell lysis and tissue damage, collectively enhancing its pathogenicity [10,11].Streptococcus pyogenes, on the other hand, produces toxins like streptolysins (SLO, SLG, and SLS haemolysins), pyrogenic exotoxins, streptococcal superantigens (SAgs), streptokinase, and hyaluronidase, which collectively contribute to tissue damage, immune system overstimulation, and clinical symptoms like strep throat and necrotizing fasciitis [12][13][14].In contrast, Brucella spp.primarily cause brucellosis with toxin production playing a minor role [15].The major virulence factors of Brucella are lipopolysaccharide (LPS), the Type IV Secretion System (T4SS), and the BvrR/BvrS system, to interact with host cells, create specialized vacuoles (Brucella Containing Vacuole (BVC)), and establish connections with the endoplasmic reticulum, enhancing their ability to cause chronic infection within host cells [16,17].
It is known that almost two-thirds of the pathogens that cause diseases in humans are of animal origin.Brucellosis is one of the most common, widespread zoonoses throughout the world, mainly caused by Brucella abortus, Brucella melitensis or Brucella suis and is transmitted to people from various animal species [18].All Shiga-toxin-producing E. coli (STEC) strains are pathogenic in humans, capable of causing at least diarrhoea.Depending on the presence of certain stx subtypes and the presence/absence of the eae gene, all STEC subtypes may be associated with severe outcomes, i.e., haemolytic uraemic syndrome (HUS), bloody diarrhoea (BD), kidney failures, hospitalizations, and deaths [19].Pigs are important reservoirs of STEC.The entrance of these strains into the food chain implies a risk to consumers because of the severity of haemolytic uremic syndrome [20].Clostridium difficile is a well-established pathogen of both humans and animals that contaminates foods and the environment.To manage Clostridium difficile infections (CDI), a One Health approach with the collaboration of clinicians, veterinarians, environmentalists, and policymakers is paramount.Listeriosis, a zoonotic disease caused by Listeria monocytogenes, is a major public health problem and one of the most common notifiable foodborne diseases [21].It has also been observed that pigs are an important reservoir for L. monocytogenes and in particular, younger animals are at risk for asymptomatic carriage [22].Salmonellosis is one of the most serious zoonotic diseases in the world and pigs are one of the most common sources of Salmonella infections in humans [23].Streptococcus suis is considered one of the most important pathogens affecting pig production worldwide and is also an emerging zoonotic agent in humans [24].Methicillin-resistant Staphylococcus aureus (MRSA) infections can occur in both humans and pigs, leading to a range of illnesses, from skin and soft tissue infections to more severe systemic infections [25].ESBL E. coli and MRSA's resistance to multiple antibiotics complicates treatment, and it poses a public health concern due to its potential for community-and hospital-acquired infections [26,27].The emergence of multidrug-resistant pathogens in pig populations, driven by genetic mutations and selective pressures from antimicrobial use, threatens both animal health and public safety.Resistant bacteria of pig origin can be transmitted to humans through direct contact, environmental contamination, and the consumption of pork and its products, raising significant concerns about the spread of antimicrobial resistance.Addressing this issue requires judicious use of antibiotics in pig farming, improved biosecurity measures, and a One Health approach that recognises the interconnectedness of animal, environmental, and human health.
In this context, conducting a meta-analysis to determine the prevalence of various zoonotic bacterial pathogens in Indian pig populations is very much essential.Metaanalysis offers a powerful approach to synthesise data from various studies, providing a comprehensive overview of the prevalence landscape.By collating and analysing prevalence data from different geographic regions within India, this study aims to establish a clear understanding of the extent of prevalence of these pathogens in the pig population.This analysis not only aids in quantifying the extent of the issue but also contributes to the identification of potential trends and patterns that can guide targeted interventions and preventive measures.By exploring the prevalence rates of Brucella spp., Clostridium, spp., E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., and Streptococcus suis within the Indian pig population, this meta-analysis seeks to provide valuable insights into the distribution and potential impacts of these pathogens.

Literature Retrieval and Data Compilation
The process encompassed the accumulation of published studies, facilitating a methodical evaluation of the prevalence and associated risk factors of zoonotic bacterial pathogens in pigs, spanning the years 2010 to 2023.These published works were sourced from a diverse array of online search engines, such as NCBI-PubMed, Science Direct, Google Scholar, Research Gate, etc. Subsequently, an extensive review of these studies was conducted, ensuring both their quality and relevance.This review adhered to the guidelines outlined in the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA) and the Meta-analysis of Observational Studies in Epidemiology (MOOSE) protocols.The procedural flow is depicted in Figure 1, delineating the meticulous steps taken throughout this systematic review process.
The criteria guiding the incorporation and exclusion of studies were devised in accordance with the specifications outlined in Table 1.The relevant details within the published studies, including author details, year of publication, study location (regional designation), sample dimension, sample types, and instances of positive occurrences, were methodically extracted to facilitate the meta-analytical process.The determination of the collective prevalence of zoonotic bacterial pathogens in pigs within India was carried out distinctly for each distinct pathogen.

Methods Used for Meta-Analysis
Utilizing R-software, the prevalence of zoonotic bacterial pathogens in pigs was computed through the application of meta-analysis tools.This encompassed the systematic analysis of 73 published studies conducted across India, spanning the timeline from 2010 to 2023.A funnel plot generated using the 'dplyr' package in R was employed to visually assess publication bias and the potential influence of small-study effects.This plot aids in identifying any asymmetry in the distribution of effect sizes and offers insights into the presence of bias within the included studies.The presentation of a funnel plot involves the plotting of the logit proportion against the standard error.The emergence of signs suggesting publication bias implies the appropriateness of employing the random effects model for the analysis of this dataset (Figure 2).
plot, an effective visual tool for presenting the effect sizes and corresponding confidence intervals of individual studies.Two distinct models were employed to estimate the proportion of positive samples in relation to the sample size using Forest plots: the common effect model was used to estimate the overall prevalence of zoonotic bacterial pathogens across all studies, assuming homogeneity among the studies; the random effects model, accounting for potential heterogeneity, provided a more conservative estimate.Heterogeneity among the studies was assessed using the I 2 statistic, which quantifies the proportion of variability attributable to true heterogeneity rather than chance.The presence of heterogeneity was considered significant at I 2 values greater than 50%.The τ 2 (tau-square) value was calculated to estimate the extent of true differences contributing to the observed heterogeneity.The analysis was subdivided pathogen-wise, such as Brucella spp., Clostridium spp., E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., and Streptococcus suis separately.The list of studies included in the meta-analysis of zoonotic bacterial pathogens in pigs is given in Table 2.The 'meta' package in R was employed to generate a forest plot, an effective visual tool for presenting the effect sizes and corresponding confidence intervals of individual studies.Two distinct models were employed to estimate the proportion of positive samples in relation to the sample size using Forest plots: the common effect model was used to estimate the overall prevalence of zoonotic bacterial pathogens across all studies, assuming homogeneity among the studies; the random effects model, accounting for potential heterogeneity, provided a more conservative estimate.Heterogeneity among the studies was assessed using the I 2 statistic, which quantifies the proportion of variability attributable to true heterogeneity rather than chance.The presence of heterogeneity was considered significant at I 2 values greater than 50%.The τ 2 (tausquare) value was calculated to estimate the extent of true differences contributing to the observed heterogeneity.

Meta-Analysis
The prevalence of Brucella spp., Clostridium, E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., and Streptococcus suis were calculated separately for pigs.The meta-analysis for these organisms was carried out using 73 published studies from India, which included 23 studies on Brucella spp., 7 studies on Clostridium spp., 23 studies on E. coli, 8 studies on Listeria monocytogenes, 14 studies on Salmonella spp., 11 studies on Staphylococcus spp., and 10 studies on Streptococcus suis on pig from India (Figure 3).

Meta-Analysis
The prevalence of Brucella spp., Clostridium, E. coli, Listeria monocytogenes, Salmonella spp., Staphylococcus spp., and Streptococcus suis were calculated separately for pigs.The meta-analysis for these organisms was carried out using 73 published studies from India, which included 23 studies on Brucella spp., 7 studies on Clostridium spp., 23 studies on E. coli, 8 studies on Listeria monocytogenes, 14 studies on Salmonella spp., 11 studies on Staphylococcus spp., and 10 studies on Streptococcus suis on pig from India (Figure 3).

Meta-Analysis of the Prevalence of Brucellosis in Pigs
In this meta-analysis of the prevalence of Brucella spp. in pigs across India (2010-2023), a total of 22,846 events were included (Figure 4).The common effect model yielded an estimated overall prevalence proportion of nine percent (95% CI: [8%; 9%]), suggesting that approximately 9 out of every 100 pigs were infected with Brucella spp. in India.On the other hand, the random effects model, which accounts for potential heterogeneity among the studies, yielded an estimated proportion of six percent (95% CI: [3%; 13%]).The considerable heterogeneity observed in the random effects model, indicated by an I² value of 99%, underscores the diversity in the study outcomes beyond what could be attributed to chance.This indicates the presence of factors influencing Brucella prevalence differences across the studies, such as variations in sample collection methods, geograph-

Meta-Analysis of the Prevalence of Brucellosis in Pigs
In this meta-analysis of the prevalence of Brucella spp. in pigs across India (2010-2023), a total of 22,846 events were included (Figure 4).The common effect model yielded an estimated overall prevalence proportion of nine percent (95% CI: [8%; 9%]), suggesting that approximately 9 out of every 100 pigs were infected with Brucella spp. in India.On the other hand, the random effects model, which accounts for potential heterogeneity among the studies, yielded an estimated proportion of six percent (95% CI: [3%; 13%]).
The considerable heterogeneity observed in the random effects model, indicated by an I 2 value of 99%, underscores the diversity in the study outcomes beyond what could be attributed to chance.This indicates the presence of factors influencing Brucella prevalence differences across the studies, such as variations in sample collection methods, geographical regions, management practices and testing protocols.The associated p-value of zero further confirms the statistical significance of this heterogeneity.The calculated τ 2 value of 3.4092 highlights the extent to which true differences in Brucella prevalence rates among the studies contribute to the observed heterogeneity.

Meta-Analysis of the Prevalence of Clostridium spp. in Pigs
The meta-analysis of the prevalence of Clostridium spp. in Indian pigs (2010-2023) based on 698 events revealed an estimated overall proportion of 22% (95% CI: [0.19; 0.25]) using the common effect model and 23% (95% CI: [0.11; 0.41]) using the random effects model (Figure 5).Heterogeneity was substantial (I 2 = 90%, p < 0.01), suggesting diverse factors contributing to the observed variation.The τ² value of 1.0815 highlighted the degree of true differences between studies.

Meta-Analysis of the Prevalence of Clostridium spp. in Pigs
The meta-analysis of the prevalence of Clostridium spp. in Indian pigs (2010-2023) based on 698 events revealed an estimated overall proportion of 22% (95% CI: [0.19; 0.25]) using the common effect model and 23% (95% CI: [0.11; 0.41]) using the random effects model (Figure 5).Heterogeneity was substantial (I 2 = 90%, p < 0.01), suggesting diverse factors contributing to the observed variation.The τ 2 value of 1.0815 highlighted the degree of true differences between studies.

Meta-Analysis of the Prevalence of Clostridium spp. in Pigs
The meta-analysis of the prevalence of Clostridium spp. in Indian pigs (2010-2023) based on 698 events revealed an estimated overall proportion of 22% (95% CI: [0.19; 0.25]) using the common effect model and 23% (95% CI: [0.11; 0.41]) using the random effects model (Figure 5).Heterogeneity was substantial (I 2 = 90%, p < 0.01), suggesting diverse factors contributing to the observed variation.The τ² value of 1.0815 highlighted the degree of true differences between studies.

Meta-Analysis of the Prevalence of E. coli in Pigs
In the present study, the meta-analysis of the prevalence of E. coli in pigs in India between 2010 and 2023 employed two distinct models to estimate the proportion of positive cases (Figure 6).The common effect model yielded an estimated prevalence of 19% (95% CI: [18%; 19%]), suggesting that about 19% of cases were associated with E. coli infection in the pig population during this period.The random effects model, which considers study variability, provided a slightly higher estimate of 24% (95% CI: [13%; 40%]), reflecting potential differences across studies.Heterogeneity was pronounced, with an I 2 value of 98%, signifying significant variation beyond chance.The τ 2 value of 3.1956 further quantified true differences contributing to heterogeneity.

Meta-Analysis of the Prevalence of E. coli in Pigs
In the present study, the meta-analysis of the prevalence of E. coli in pigs in India between 2010 and 2023 employed two distinct models to estimate the proportion of positive cases (Figure 6).The common effect model yielded an estimated prevalence of 19% (95% CI: [18%; 19%]), suggesting that about 19% of cases were associated with E. coli infection in the pig population during this period.The random effects model, which considers study variability, provided a slightly higher estimate of 24% (95% CI: [13%; 40%]), reflecting potential differences across studies.Heterogeneity was pronounced, with an I² value of 98%, signifying significant variation beyond chance.The τ 2 value of 3.1956 further quantified true differences contributing to heterogeneity.

Meta-Analysis of the Prevalence of Listeria monocytogenes in Pigs
The results of the meta-analysis of the prevalence of Listeria monocytogenes in Indian pigs from 2010 to 2023 are shown in Figure 7.With a total of 1146 events, the common effect model estimated a prevalence of 12% (95% CI: [10%; 14%]), suggesting that approximately 12% of pigs were affected.The random effects model estimated a prevalence of 14% (95% CI: [8%; 22%]), indicating potential study variations.Heterogeneity was significant (I 2 = 91%), denoting substantial variation beyond chance.The p-value below 0.01 affirmed this heterogeneity's statistical significance.A τ 2 value of 0.5654 quantified genuine differences contributing to the variation.

Meta-Analysis of the Prevalence of Listeria monocytogenes in Pigs
The results of the meta-analysis of the prevalence of Listeria monocytogenes in Indian pigs from 2010 to 2023 are shown in Figure 7.With a total of 1146 events, the common effect model estimated a prevalence of 12% (95% CI: [10%; 14%]), suggesting that approximately 12% of pigs were affected.The random effects model estimated a prevalence of 14% (95% CI: [8%; 22%]), indicating potential study variations.Heterogeneity was significant (I 2 = 91%), denoting substantial variation beyond chance.The p-value below 0.01 affirmed this heterogeneity's statistical significance.A τ 2 value of 0.5654 quantified genuine differences contributing to the variation.

Meta-Analysis of the Prevalence of Salmonella spp. in Pigs
The results of the meta-analysis of the prevalence of Salmonella spp. in Indian pigs spanning 2010 to 2023 are shown in Figure 8.With a total of 3542 events, the common effect model estimated a prevalence of ten percent (95% CI: [9%; 11%]), implying that approximately ten percent of pigs were infected.Interestingly, the random effects model produced a comparable estimate of ten percent (95% CI: [6%; 16%]), accommodating potential variations in study approaches.Substantial heterogeneity was observed (I 2 = 87%), implying significant variation beyond chance.This heterogeneity's statistical significance was reaffirmed by the p-value less than 0.01.A τ 2 value of 1.1165 quantified the extent of authentic differences contributing to this observed variation.

Meta-Analysis of the Prevalence of Salmonella spp. in Pigs
The results of the meta-analysis of the prevalence of Salmonella spp. in Indian pigs spanning 2010 to 2023 are shown in Figure 8.With a total of 3542 events, the common effect model estimated a prevalence of ten percent (95% CI: [9%; 11%]), implying that approximately ten percent of pigs were infected.Interestingly, the random effects model produced a comparable estimate of ten percent (95% CI: [6%; 16%]), accommodating potential variations in study approaches.Substantial heterogeneity was observed (I 2 = 87%), implying significant variation beyond chance.This heterogeneity's statistical significance was reaffirmed by the p-value less than 0.01.A τ 2 value of 1.1165 quantified the extent of authentic differences contributing to this observed variation.

Meta-Analysis of the Prevalence of Salmonella spp. in Pigs
The results of the meta-analysis of the prevalence of Salmonella spp. in Indian pigs spanning 2010 to 2023 are shown in Figure 8.With a total of 3542 events, the common effect model estimated a prevalence of ten percent (95% CI: [9%; 11%]), implying that approximately ten percent of pigs were infected.Interestingly, the random effects model produced a comparable estimate of ten percent (95% CI: [6%; 16%]), accommodating potential variations in study approaches.Substantial heterogeneity was observed (I 2 = 87%), implying significant variation beyond chance.This heterogeneity's statistical significance was reaffirmed by the p-value less than 0.01.A τ 2 value of 1.1165 quantified the extent of authentic differences contributing to this observed variation.

Meta-Analysis of the Prevalence of Staphylococcus spp. in Pigs
In the current study, a meta-analysis was conducted to explore the prevalence of Staphylococcus spp. in Indian pigs between 2010 and 2023 (Figure 9).The dataset encompassed a total of 1865 events.The common effect model estimated a prevalence of 24% (95% CI: 22% to 26%), indicating that approximately 24% of pigs were affected by Staphylococcus spp.during this period.Contrastingly, the random effects model, accounting for potential study variations, presented a higher estimated prevalence of 35% (95% CI: 21% to 52%).Heterogeneity was pronounced, with an I 2 value of 97%, indicating substantial variation beyond chance.The associated p-value of less than 0.01 confirmed the statistical significance of this heterogeneity.The τ 2 value of 1.3396 quantified the extent to which genuine differences in Staphylococcus spp.prevalence rates contributed to the observed heterogeneity.

Meta-Analysis of the Prevalence of Staphylococcus spp. in Pigs
In the current study, a meta-analysis was conducted to explore the prevalence of Staphylococcus spp. in Indian pigs between 2010 and 2023 (Figure 9).The dataset encompassed a total of 1865 events.The common effect model estimated a prevalence of 24% (95% CI: 22% to 26%), indicating that approximately 24% of pigs were affected by Staphylococcus spp.during this period.Contrastingly, the random effects model, accounting for potential study variations, presented a higher estimated prevalence of 35% (95% CI: 21% to 52%).Heterogeneity was pronounced, with an I² value of 97%, indicating substantial variation beyond chance.The associated p-value of less than 0.01 confirmed the statistical significance of this heterogeneity.The τ² value of 1.3396 quantified the extent to which genuine differences in Staphylococcus spp.prevalence rates contributed to the observed heterogeneity.

Meta-Analysis of the Prevalence of Streptococcus suis in Pigs
The comprehensive meta-analysis investigating the prevalence of Streptococcus suis in Indian pigs from 2010 to 2023 analysed a total of 3205 events (Figure 10).The common effect model estimated a prevalence of 13% (95% CI: [12%; 15%]), suggesting that roughly 13% of pigs were affected by Streptococcus suis during this period.The random effects model, designed to account for potential variations between studies, yielded a similar estimated prevalence of 13% (95% CI: [6%; 27%]).Heterogeneity emerged with an I 2 value of 97%, signifying significant variation beyond chance.The associated p-value of less than 0.01 confirmed the statistical significance of this heterogeneity.The τ 2 value of 1.9289 provided insight into the extent to which genuine differences in Streptococcus suis prevalence rates contributed to the observed heterogeneity.
Table 3 shows the overall meta-analysis of the prevalence patterns of various zoonotic bacterial pathogens in pig populations in India from 2010 to 2023.

Meta-Analysis of the Prevalence of Streptococcus suis in Pigs
The comprehensive meta-analysis investigating the prevalence of Streptococcus suis in Indian pigs from 2010 to 2023 analysed a total of 3205 events (Figure 10).The common effect model estimated a prevalence of 13% (95% CI: [12%; 15%]), suggesting that roughly 13% of pigs were affected by Streptococcus suis during this period.The random effects model, designed to account for potential variations between studies, yielded a similar estimated prevalence of 13% (95% CI: [6%; 27%]).Heterogeneity emerged with an I 2 value of 97%, signifying significant variation beyond chance.The associated p-value of less than 0.01 confirmed the statistical significance of this heterogeneity.The τ 2 value of 1.9289 provided insight into the extent to which genuine differences in Streptococcus suis prevalence rates contributed to the observed heterogeneity.

Discussion
Zoonotic bacterial pathogens within the pig production system represent a significant public health concern due to their potential to transmit diseases to humans.In this study, we performed a systematic meta-analysis of 73 published studies conducted across India, spanning between 2010 to 2023 to assess the prevalence patterns of various zoonotic bacterial pathogens in pigs.The findings have provided some valuable insights into the distribution and prevalence of these pathogens, along with their potential implications for public health and veterinary interventions.Table 3 shows the overall meta-analysis of the prevalence patterns of various zoonotic bacterial pathogens in pig populations in India from 2010 to 2023.

Discussion
Zoonotic bacterial pathogens within the pig production system represent a significant public health concern due to their potential to transmit diseases to humans.In this study, we performed a systematic meta-analysis of 73 published studies conducted across India, spanning between 2010 to 2023 to assess the prevalence patterns of various zoonotic bacterial pathogens in pigs.The findings have provided some valuable insights into the distribution and prevalence of these pathogens, along with their potential implications for public health and veterinary interventions.
The present analysis revealed distinct patterns of prevalence across different bacterial pathogens, which have zoonotic importance.Staphylococcus spp.exhibited the highest estimated prevalence with a random effects proportion of 0.35 (95% CI: [0.21; 0.52]), followed by Clostridium spp. with a random effects proportion of 0.  [64,65,67].In the present study, it was also observed that the prevalence of Streptococcus suis was on par with the findings of several researchers [90,94,96].
The study also revealed that heterogeneity was a common feature among the studies, with I 2 values exceeding 50% for all of the pathogens.This indicated substantial variability among the included studies.Furthermore, funnel plots were used to assess publication bias, and in some cases, asymmetry was observed, suggesting the potential influence of small-study effects or publication bias.
The higher prevalence of zoonotic bacterial pathogens as observed in the present study, such as Staphylococcus spp.and Clostridium spp.underscores the need for continued surveillance, targeted interventions and control measures both at the farm and processing levels to reduce the risk of zoonotic disease transmission from pigs to humans.Serological and molecular epidemiological studies can help in elucidating the genetic diversity and evolution of these pathogens [99].It has also been observed that the studies included in the present meta-analysis commonly used techniques like biochemical tests and PCR [44,56,97] followed by ELISA [34,37,64] and lateral flow assays [33] for the detection of bacterial pathogens.It is very much desired that longitudinal studies are needed to monitor the changes in prevalence over time and to assess the effectiveness of control measures.

Conclusions
The meta-analysis covering 2010 to 2023 revealed a significant prevalence of zoonotic bacterial pathogens among the pig population in India.The study elucidated the prevalence patterns of zoonotic bacterial pathogens in the Indian pig population, with Staphylococcus spp.emerging as the most prevalent bacterial pathogen in pigs, closely followed by E. coli and Clostridium spp., while Brucella spp.and Salmonella spp.exhibited lower prevalence rates.Additionally, Listeria monocytogenes and Streptococcus suis demonstrated moderate prevalence among zoonotic bacterial pathogens in the Indian pig population.These findings underscore the urgent need for adopting a One Health approach, which recognizes the interconnectedness of animal and human health to effectively mitigate economic losses and mitigate zoonotic risks.

Figure 1 .
Figure 1.Schematic depiction of the literature selection procedure for the systematic review of the prevalence of zoonotic bacteria pathogens in swine of India from 2010 to 2023

Figure 1 .
Figure 1.Schematic depiction of the literature selection procedure for the systematic review of the prevalence of zoonotic bacterial pathogens in swine of India from 2010 to 2023.

Figure 2 .Table 2 .
Figure 2. Funnel plot that elucidates potential publication bias in prevalence of zoonotic bacterial pathogens in India from 2010 to 2023 Table 2. List of published research articles and details of studies included in the meta-analysis of zoonotic bacterial pathogens of pigs in India from 2010-2023.

Figure 2 .
Figure 2. Funnel plot that elucidates potential publication bias in prevalence of zoonotic bacterial pathogens in India from 2010 to 2023.

Figure 3 .
Figure 3. Representation of a scatter plot, depicting the positive percentage trends in the prevalence of different zoonotic bacterial pathogens among Indian swine.The data spans the years from 2010 to 2023 and includes samples from different regions across India.

Figure 3 .
Figure 3. Representation of a scatter plot, depicting the positive percentage trends in the prevalence of different zoonotic bacterial pathogens among Indian swine.The data spans the years from 2010 to 2023 and includes samples from different regions across India.

Figure 4 .
Figure 4. Forest plot showing the result of 23 studies reporting the prevalence of brucellosis in pigs in India from 2010 to 2023.

Figure 5 .
Figure 5. Forest plot showing the result of 7 studies reporting the prevalence of Clostridium spp. in pigs in India from 2010 to 2023

Figure 4 .
Figure 4. Forest plot showing the result of 23 studies reporting the prevalence of brucellosis in pigs in India from 2010 to 2023.

Figure 4 .
Figure 4. Forest plot showing the result of 23 studies reporting the prevalence of brucellosis in pigs in India from 2010 to 2023.

Figure 5 .
Figure 5. Forest plot showing the result of 7 studies reporting the prevalence of Clostridium spp. in pigs in India from 2010 to 2023

Figure 5 .
Figure 5. Forest plot showing the result of 7 studies reporting the prevalence of Clostridium spp. in pigs in India from 2010 to 2023.

Figure 6 .
Figure 6.Forest plot showing the result of 23 studies reporting the prevalence of E. coli in pigs in India from 2010 to 2023

Figure 6 .
Figure 6.Forest plot showing the result of 23 studies reporting the prevalence of E. coli in pigs in India from 2010 to 2023.

Figure 7 .
Figure 7. Forest plot showing the result of 8 studies reporting the prevalence of Listeria monocytogenes in pigs in India from 2010 to 2023

Figure 8 .Figure 7 .
Figure 8. Forest plot showing the result of 14 studies reporting the prevalence of Salmonella spp. in pigs in India from 2010 to 2023

Pathogens 2023 , 19 Figure 7 .
Figure 7. Forest plot showing the result of 8 studies reporting the prevalence of Listeria monocytogenes in pigs in India from 2010 to 2023

Figure 8 .Figure 8 .
Figure 8. Forest plot showing the result of 14 studies reporting the prevalence of Salmonella spp. in pigs in India from 2010 to 2023 Figure 8. Forest plot showing the result of 14 studies reporting the prevalence of Salmonella spp. in pigs in India from 2010 to 2023.

Figure 9 .
Figure 9. Forest plot showing the result of 11 studies reporting the prevalence of Staphylococcus spp. in pigs in India from 2010 to 2023

Figure 9 .
Figure 9. Forest plot showing the result of 11 studies reporting the prevalence of Staphylococcus spp. in pigs in India from 2010 to 2023.

Figure 10 .
Figure 10.Forest plot showing the result of 10 studies reporting the prevalence of Streptococcus suis in pigs in India from 2010 to 2023

Figure 10 .
Figure 10.Forest plot showing the result of 10 studies reporting the prevalence of Streptococcus suis in pigs in India from 2010 to 2023.

Table 1 .
Details of inclusion and exclusion criteria used in the study.

Table 1 .
Details of inclusion and exclusion criteria used in the study.

Table 2 .
List of published research articles and details of studies included in the meta-analysis of zoonotic bacterial pathogens of pigs in India from 2010-2023.

Table 3 .
Meta-analysis of the prevalence patterns of various zoonotic bacterial pathogens in pig populations in India from 2010 to 2023.

Table 3 .
Meta-analysis of the prevalence patterns of various zoonotic bacterial pathogens in pig populations in India from 2010 to 2023.