Foodborne diseases are a significant global health issue, leading to considerable morbidity and mortality (WHO, 2015). These illnesses can arise at any point along the food production, distribution, or consumption chain and persist in both high- and low-income countries (Grace, 2023). In Low- and Middle-Income Countries (LMICs), food safety challenges are exacerbated by the inherent structure of the food sector. These systems are typically fragmented and diverse, characterized by a vast network of small-scale operators and a dominant informal sector that operates with minimal organizational cohesion (Grace, 2015). Contamination may result from multiple sources, including water, air, and soil, and is often aggravated by unsafe handling, improper storage, and inadequate processing. Globally, about 10% of the population suffers from foodborne illnesses annually, leading to over 420,000 deaths (WHO, 2015). In 2010, contaminated food caused approximately 600 million cases and 33 million disability-adjusted life years (DALYs), affecting nearly one in ten people worldwide (Havelaar et al., 2015).

Foods of animal origin, particularly meat, milk, eggs, and their products, are major contributors to foodborne infections. In India, meat production has steadily increased, reaching 9.77 million tons in 2022–23 (Department of Animal Husbandry and Dairying, 2023), with poultry meat constituting about 51.14% of total output. Affordability and widespread acceptance among all communities are the key factors driving the increased consumption of eggs and poultry meat (Mohanapriya et al., 2023). It is preferred for its high protein content, low fat, affordability, and short rearing cycles (Karabasanavar et al., 2020). The rise in per capita meat consumption, from 6.15 kg in 2018–19 to 7.39 kg in 2023–24, is primarily driven by the expansion of the poultry sector. As poultry meat already accounts for a significant share of the country’s total meat output, its increased production—combined with a growing public awareness of protein-rich diets—has directly fueled this (Department of Animal Husbandry and Dairying, 2025). However, the poultry sector faces major food safety and hygiene challenges, as most meat is sold through informal wet markets lacking proper infrastructure and cold chain systems (Gulati and Juneja, 2023). Such deficiencies may increase the likelihood of contamination by microorganisms, including bacteria, viruses, fungi, and parasites, that can cause food poisoning.

Globally, about two-thirds of foodborne disease outbreaks occur in homes and catering establishments (Hedberg et al., 2006), which are particularly vulnerable due to large meal volumes and extensive handling. Foodborne pathogens may be introduced at multiple stages, from raw material production, storage to processing and distribution, with key sources including animals, the environment, and human handlers (Bridier et al., 2015). Common risk factors include unsafe food sources, inadequate cooking, improper holding temperatures, and contaminated equipment (WHO, 2023). Slaughtering transfers bacteria from the animal and equipment onto the meat. This contamination can persist, and sometimes even grow, on the final cuts during processing and storage (Rouger et al., 2017). Although a healthy bird’s muscle tissue is sterile, its skin, feathers, and internal tracts naturally carry diverse microbes. The slaughterhouse itself—including its surfaces, air, and water—also contains bacteria. During processing, these two sources combine, leading to the contamination of carcasses and meat cuts by microbes from both the animal and the environment (Rouger et al., 2017).

Salmonella spp., Campylobacter spp., and Listeria monocytogenes are three critical foodborne pathogens associated with poultry. Non-typhoidal Salmonella (NTS) is a major cause of illness, resulting in 93.8 million cases and 155,000 deaths annually (Majowicz et al., 2010), with Salmonella Enteritidis and Salmonella Typhimurium being predominant globally (Galanis et al., 2006; Reddy et al., 2010). Recent surveillance across India highlights a significant, albeit geographically fragmented, burden of foodborne pathogens within the poultry value chain. The prevalence of Salmonella spp. in retail chicken meat demonstrates extreme regional heterogeneity, ranging from hyper-endemic levels of 74% in Mumbai (Shashidhar et al., 2011) and 47% in the Delhi-Haryana belt (Bhardwaj et al., 2022) to a comparatively low 4.83% in Karnataka (Karabasanavar et al., 2020). Among foodborne transmission routes, the consumption of raw or undercooked chicken meat is recognized as the single largest potential source of human Campylobacter infection (Popa et al., 2022). Campylobacteriosis, primarily from Campylobacter jejuni and Campylobacter coli, is a high-burden disease strongly linked to poultry (Abebe et al., 2020), which carries high intestinal loads (10⁶–10⁸ CFU/g) (Oh et al., 2018), and can infect humans at low doses, sometimes leading to severe complications like Guillain-Barré syndrome (Poropatich et al., 2010). Campylobacter spp. isolation rates vary across the Indian subcontinent, with high prevalence reported in West Bengal (72%) (Sharma et al., 2016) and Northern India (38.6%) (Khan et al., 2018), in sharp contrast to the 2.3% incidence observed in broiler meat samples (Kumar et al., 2023). L. monocytogenes, while less prevalent, is highly severe, with 20–30% mortality and 91% hospitalization (Jemmi and Stephan, 2006; Dhama et al., 2015). In India its distribution is notably erratic; isolation rates vary from 16% in Chhattisgarh (Beigh et al., 2019) and 8.5% in North East India (Shakuntala et al., 2019) to 1.7% in Punjab (Kaur et al., 2018), with complete absence (0%) reported in Kerala (Latha et al., 2017). It poses a unique threat in the poultry value chain due to its ability to survive refrigeration and form biofilms in processing environments (Colagiorgi et al., 2017), leading to severe outcomes like meningitis in vulnerable populations (Mateus et al., 2013; Jamshidi and Zeinali, 2019). A recent PRISMA-based systematic review (2010–2023, 90 studies) highlighted that Indian retail poultry meat frequently carries major foodborne pathogens, with Campylobacter spp. and Salmonella spp. each showing a pooled prevalence of 18% each (95% CI, 11–27% and 11–26%, respectively), while L. monocytogenes was also detected at 13% (95% CI, 1–33%). The review further underscored that Campylobacter and Salmonella isolates exhibited high resistance to critically important antimicrobials, including erythromycin, tetracycline, ciprofloxacin, and colistin, posing a substantial public-health concern (Ayoub et al., 2025). Despite this burden, studies from India that examine upstream or downstream risk factors in poultry production, retail, or consumer handling remain scarce. These findings reinforce the importance of formal surveillance of Indian poultry systems, to better understand contamination patterns and associated risk factors for the priority pathogens.

The present study was conducted to identify the risk factor associated with the microbiological quality of chicken meat at chicken meat value chain with a specific focus on pathogen indicators such as Salmonella spp., Campylobacter spp., and L. monocytogenes. Identification of the risk factors associated with the pathogen indicators in the chicken meat value chain may give insight to take necessary steps to reduce microbial contamination.

The combined prevalence of the pathogen indicator was 30.0% (108/360) in raw chicken meat at the retailer level, 6.7% (12/180) in consumer-cooked meat, and 6.6% (16/242) in restaurant-cooked meat (Table 3). Among the chicken meat samples examined, Salmonella spp. was the most prevalent, being isolated from 23.3% (84/360) of raw meat samples at the retailer level, 6.7% (12/180) of consumer-cooked meat samples, and 6.2% (15/242) of restaurant-cooked meat samples. Campylobacter spp. was detected in 9.4% (34/360) of raw meat samples collected from retailers, whereas only 0.6% (1/180) of consumer-level cooked meat samples and 0.4% (1/242) of restaurant-cooked meat samples tested positive. L. monocytogenes was detected in 0.6% (2/360) of retailer-level raw meat samples, while none of the consumer or restaurant-cooked meat samples showed its presence.

The present study was conducted to identify the risk factor associated with the microbiological quality of chicken meat at chicken meat value chain with a specific focus on Salmonella spp., Campylobacter spp., and L. monocytogenes. However, we have combined the results together into a ‘Pathogen indicator’. The decision to use a composite ‘Pathogen indicator’ was driven strictly by statistical constraints due to low prevalence of individual organism. Attempting to model these individually resulted in quasi-complete separation and unstable odds ratios due to the sparsity of positive events. Therefore, we conceptualized the dependent variable not as a specific biological outcome, but as a ‘Pathogen indicator’. Since all three pathogens are vegetative bacteria that should be eliminated by adequate hygiene and cooking, their presence, regardless of species, serves as a robust indicator for a breakdown in the safety control system. Also, from a public health and consumer safety perspective, the presence of any of these major foodborne pathogens renders the product unsafe. By grouping them, we created an indicator that evaluates the efficacy of current intervention strategies against a set of major biological hazards.

The study identified the retail outlet as a critical hotspot for pathogen presence. Although the slaughter process inevitably introduces the initial microbial load via exposure to gut and respiratory flora (Rouger et al., 2017), it is the retail environment that facilitates amplification. Unlike the standardized conditions of industrial processing or the immediate thermal intervention in restaurants or home, retail meat is frequently subjected to handling lapses, extended display periods, and cold chain interruptions. These time–temperature fluctuations act as critical drivers for microbial proliferation (Nychas et al., 2008). Retail level has been implicated as the primary determinant of human infection risk and it can be effectively neutralized at the consumer node through rigorous hygiene and proper cooking practices (Akil and Ahmad, 2019). The public health implication is significant, as reducing contamination loads at this specific stage correlates directly with declines in foodborne illness incidence, supporting the prioritization of post-slaughter interventions (Rosenquist et al., 2003; Williams et al., 2021).

The univariate analysis initially indicated that extended pre-slaughter holding (>24 h) significantly reduced contamination odds. However, after adjusting for confounders in the multivariable model, this protective effect was most robustly defined within the 6.1–12 h window (AOR = 0.232). This refinement aligns perfectly with international best practices; the Codex Alimentarius Commission (CAC, 2011) explicitly recommends an 8–12 h feed withdrawal period to minimize the contamination of carcasses by fecal material and ingesta. This regulatory standard is supported by a previous work that have explicitly shown that a 6 to 10-h fasting period significantly reduces the likelihood of carcass contamination (Xue et al., 2020). In our study most samples were collected within 60 min of slaughter. The significant association of pathogen presence in relation to a period of 31–60 min, as opposed to longer durations, is likely due to sample distribution, where the low frequency of extended storage times limited the statistical power of the Chi-square analysis. The elevated risk associated with cotton cloth covers, compared to fly nets, is likely attributable to the physical properties of the materials. Fly nets serve as essential physical barriers, preventing the introduction of pathogens by mechanical vectors known to transport bacteria from external fecal sources (Hald et al., 2004). In contrast, porous cloths absorb moisture and organic residues, creating a damp microenvironment that facilitates microbial survival and acts as a persistent source for contamination (Todd et al., 2009). Wooden surfaces exhibited the highest frequency of pathogen presence, followed by plastic, even though the association was not statistically significant (p > 0.05). This trend likely reflects the inherent physical vulnerabilities of the cutting media. The porous nature of wood entraps moisture and microbes, whereas plastic surfaces eventually develop micro-fissures that facilitate bacterial adherence (Cliver, 2006). However, higher retention rates in wood do not necessarily correlate with increased transmission risk (Cliver, 2006). These physical characteristics significantly affect effective disinfection, as wooden boards and worn plastic surfaces have been shown to remain contaminated even after cleaning, supporting the recommendation for their exclusion from critical meat handling areas (Tebbutt, 1991). Work attire becomes easily contaminated during the handling of unprocessed ingredients, particularly raw meat, and serves as a source for pathogen transfer to food products if not changed at appropriate intervals (Todd et al., 2010a). In practice, this rule is often neglected, as many workers keep wearing soiled clothes instead of changing (Gemeda et al., 2024). The area beneath the fingernails traps significantly more bacteria than the fingertips or palms. And these long or untrimmed nails pose a serious risk, as these hidden germs are easily spread to meat during handling (Todd et al., 2010b). The best practices dictate that fingernails be kept short and mechanically scrubbed with a nailbrush during washing to prevent the transfer of pathogens to food products (Todd et al., 2010b). This risk associated with hand hygiene is heightened in this study, where it was observed that no butcher wore gloves during slaughtering, resulting in direct contact between hands and meat. Similarly, the presence of jewelry on hands is associated with higher pathogen retention. While this risk is frequently documented in clinical environments (Trick et al., 2003; Fagernes and Lingaas, 2011), it is equally critical in food handling settings. Accessories such as rings impede thorough washing and create protected areas for microbial survival, making the removal of hand ornaments a necessary precaution for preventing cross-contamination (Todd et al., 2010b). Higher contamination levels were observed in settings lacking glass covers or involving open-air sales, reflecting increased exposure to dust and vectors. The strong association between fly density and infectious illness confirms their role as effective mechanical vectors for spreading enteric pathogens (Collinet-Adler et al., 2015). This finding underscores the necessity of physical barriers; interventions such as installing glass covers could effectively prevent contamination by simultaneously excluding flies and reducing the deposition of airborne dust, thereby mitigating the overall microbial load in the retail environment. Pathogenic microorganisms can survive on various surfaces for extended periods, ranging from hours to days. Key foodborne bacteria, including L. monocytogenes and Salmonella spp. are notably capable of forming protective biofilms on these surfaces (Martinon et al., 2012). These biofilms, once formed within different food industry settings, become a sustained source of food contamination (Srey et al., 2013). Therefore, proper disinfection and frequent thorough cleaning are essential to eliminate microbial reservoirs and minimize the risk of contamination. Multivariable logistic regression confirmed that pre-slaughter holding periods, slaughter-to-sale intervals, outlet washing frequency, and fingernail hygiene act as independent determinants of contamination. Shorter slaughter-to-sale intervals and longer pre-slaughter holding periods emerged as significant protective factors, reflecting the critical necessity of minimizing exponential bacterial growth and ensuring effective gut clearance prior to evisceration Specifically, the finding that frequent shop cleaning and trimmed nails significantly reduced risk highlights the critical need for basic hygiene. These routine practices are essential for preventing bacterial biofilms on surfaces and thereby eliminating cross-contamination risks (Chmielewski and Frank, 2003).

At the restaurant level, the use of separate cutting boards and knives for raw and cooked meat was identified as a significant protective factor against pathogen presence. Microorganisms transfer efficiently from raw to cooked products via shared surfaces (Goh et al., 2014), while organic residues on cutting boards facilitate pathogen persistence (Kusumaningrum et al., 2004). These findings underscore the necessity of strict utensil segregation to disrupt cross-contamination pathways. Regarding temperature management, bulk cooking and hot holding showed distinct associations with contamination risk. Failure to maintain adequate hot-holding temperatures significantly increased the odds of pathogen presence, consistent with observations that inadequate thermal maintenance allows surviving microorganisms like L. monocytogenes to proliferate (Sun et al., 2019). Conversely, products cooked in bulk showed lower contamination risk. Large-scale cooking operations are generally forced to use more organized steps and strict rules. This organized system leads to better process control and fewer mistakes compared to small, uncontrolled batch handling (Hartantyo et al., 2023). Cross-contamination risks were evident in storage and plating practices. The use of raw vegetable garnish was associated with higher pathogen presence, corroborating studies identifying raw produce as a source for transferring pathogens to cooked meat (Omurtag et al., 2013). Furthermore, storing raw and cooked items together significantly increased contamination odds. Poor segregation and unsatisfactory storage conditions are recognized as primary contributors to microbial hazards in restaurant environments (Sani and Siow, 2014). The protective effect observed in restaurants preparing multiple chicken dishes simultaneously (AOR = 0.177) likely reflects the operational discipline inherent to high-volume kitchens. Unlike ad-hoc preparation, simultaneous multi-dish cooking typically requires structured workflows and task segregation to maintain efficiency. This organized approach minimizes the chaotic mixing of raw and cooked handling steps, thereby reducing opportunities for cross-contamination. This interpretation is reinforced by the multivariable model, which identified equipment segregation (using separate cutting boards/knives) and bulk cooking as independent protective factors. Together, these findings suggest that the rigor of organized cooking workflows and consistent utensil separation are the primary drivers of pathogen control in restaurant settings, acting as effective barriers against contamination regardless of the kitchen’s physical layout.

At the consumer level, understanding of food safety is often broad, yet many lack awareness of the specific procedures necessary to prevent contamination. This procedural gap is significant, as many fail to use separate or adequately clean utensils for raw ingredients and cooked foods, creating a high risk of cross-contamination (Redmond and Griffith, 2003). Furthermore, casual handwashing is often insufficient because pathogens stay in hard-to-clean areas, such as beneath the fingernails, thereby requiring systematic and thorough cleaning of both hands and utensils to break the contamination cycle (Todd et al., 2010b). The odds of pathogen presence were significantly lower when vegetables were added during cooking compared to when they were added post-cooking. This suggests that heat exposure during cooking may inactivate potential contaminants. Similar observations were noted indicating that mixing raw vegetables with cooked meat can promote cross-contamination (Omurtag et al., 2013). Furthermore, the odds of pathogen presence were markedly lower when separate cutting boards or knives were used for raw meat and vegetables. Comparable findings have been observed in studies, which described the use of shared boards and knives as an important contributor to microbial transfer (Kusumaningrum et al., 2004; Goh et al., 2014). Bacterial multiplication during inadequate storage (at warm ambient temperatures or slow refrigeration) significantly increases contamination risk in leftovers compared to freshly served food (Bryan, 1980). This risk is compounded when accumulated microbial growth is followed by uneven reheating, which fails to eliminate surviving pathogens. Therefore, effective process control must strictly govern all post-cooking phases, including rapid chilling and thorough reheating (Bryan, 1980). The multivariable model identified hand hygiene and utensil use as the primary determinants of contamination at the consumer level. Washing hands ‘only before handling raw meat’ was associated with significantly higher risk, whereas using separate cutting boards and knives markedly reduced it. These statistical associations confirm that preventing cross-contamination requires both strict utensil segregation and comprehensive handwashing (before and after handling) to ensure safety.

The findings from our study integrate seamlessly into existing food safety frameworks, reinforcing the model that contamination risk is not static; rather, it accumulates through a complex mix of behavioral, infrastructural, and environmental factors, most of which are indeed modifiable. The retail sector clearly emerges as the critical hotspot for microbial amplification. While the slaughter process introduces the initial microbial load, subsequent exponential growth is primarily driven by lapses in time–temperature management and insufficient environmental sanitation. Effective mitigation requires disciplined action across the entire chain. Simple, achievable interventions like, improving cleaning frequency, enforcing strict personal hygiene (including utensil segregation), and maintaining physical barriers to control vectors would substantially cut contamination loads. Ultimately, these findings underscore the necessity of strict adherence to prerequisite programs and confirm that focusing on modest, feasible interventions applied systematically yields significant and lasting improvements in microbiological safety. Achieving a reduction in foodborne illness incidence demands disciplined process control from post-slaughter handling all the way to the final consumer preparation stage.