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Campylobacter positivity and public health risks in live bird markets in Busia, Kenya: A value chain analysis

Abstract Live bird markets (LBMs) provide integral hubs for 95% of poultry produced for food. Surveillance systems in LBMs serving smallholder farmers in sub‐saharan Africa are often non‐functional, and data about public health risks and emerging pathogens are lacking. Studies in Kenya have reported 29–44% Campylobacter prevalence in poultry. We analysed such LBMs in Kenya for likely transmission of Campylobacter from poultry to humans. We conducted a cross‐sectional survey among 186 live poultry traders (LPTs) in 14 LBMs in a region with widespread backyard poultry systems. A pretested structured questionnaire was administered to all LPTs having regular contacts with poultry to gather market data and risk information on campylobacteriosis. Campylobacter was detected in individual cloacal cultures and identified through PCR. The median score obtained from the outcome of risk assessment dichotomized respondents into high and low risk categories. We performed logistic regression at 95% confidence interval (CI) to compare market characteristics and Campylobacter positivity to risk categories to identify LBM‐associated public health risks. Markets had a median of 13 traders, and mean age of 46.3 ± 13.7 years. Majority 162/186 (87.1%) were males. Market behavioural processes by LPTs varied: Only 58.6% LPTs held bird species separate; onsite slaughter (38.7%); encountered sick‐bird (93%) and dead‐bird (83%) amidst limited health inspection (31.2%). Campylobacter positivity in live birds was 43/112 (38.4%, 95% CI: 29.4–48.1). Risk information on campylobacteriosis was low 41/114 (36%, 95% CI: 27.2–45.5). Sanitary risks were related to accumulation of litter (adjusted prevalence odds ratio [aPOR]: 19.67, 95% CI: 3.01–128.52). Accessing hand‐wash facilities (aPOR: .32, 95% CI: .13–.78) and access to information (aPOR: .24, 95% CI: .09–.61) were protective. Sanitary risks were related to poor hygiene. LBMs could be central surveillance sites for Campylobacter. Public health authorities/actors should consider appropriate targeting to improve sanitary measures and Campylobacter control strategies.


INTRODUCTION
Poultry farming is an important component of the agricultural sector worldwide, providing food, nutrition and income (Mottet et al., 2017).
The global poultry sector is projected to grow substantially at 24% to reach 131,255 metric tons by 2025 (Carron et al., 2017;Mottet et al., 2017). This growth is catalysed by urbanization, increasing populations and consumer taste (Food and Agriculture Organization [FAO], 2011; Okello et al., 2010). Poultry production is of vital importance in improving livelihoods of rural populations, but without a policy framework, it is likely the poorest smallholders who make up a large proportion of producers in many low-and middle-income countries (LMIC) will be outclassed by the well-resourced commercial operations from overall economic growth and transformation of market structures (Aklilu et al., 2007;Chaiban et al., 2020;Okello et al., 2010).
The poultry sector in Kenya contributes about 30% of agricultural gross domestic product (GDP) (Abubakar et al., 2019;Okeno et al., 2012). The consumption of poultry in Kenya is predicted to reach 164.6 metric tonnes by 2030 (Chaiban et al., 2020). Kenya's poultry population is estimated at 37 million birds at any given time, of which about 74−80% are raised in backyard settings (Abubakar et al., 2019;MOLFD, 2012;Okello et al., 2010). Backyard systems are unspecialized, raising on average 13-50 birds on low inputs and outputs to provide for home consumption and possibly raise cash without targeting specific markets. The sale of most backyard poultry occurs in either general food markets or stalls. In urban centres, the live poultry traders (LPTs) may confine birds in cages and stalls, while in rural areas the birds may be tied on open ground (McCarron et al., 2015;Molia et al., 2016).
Poultry value chain studies in Kenya have examined productivity and challenges within poultry systems to improve on performance and profitability (Okello et al., 2010;Okeno et al., 2012). Value chains analysis involves the mapping and description of the production-supply, commercial and institutional environment in which businesses operate to supply goods to consumers (Carron et al., 2017;Okello et al., 2010;Rushton, 2011). Studies of trading networks may markedly recognize markets involved in the perpetuation of infection and be focus of control measures, seasonal fluctuations in volumes traded consistent with risk of transmission (Van Kerkhove et al., 2009) and the role of traders in potential transmission from village to village during collection and spread through market network (Tiensin et al., 2009).
Poultry are recognized asymptomatic carriers of several important human pathogens including Campylobacter, Salmonella, Escherichia coli and highly pathogenic avian influenza (HPAI) (Magalhães et al., 2010).
In many LMICs, up to 95% of birds produced for food are marketed live or as freshly slaughtered in live bird markets (LBMs) (Cardona et al., 2009;Sayeed et al., 2017;Van Kerkhove et al., 2009). Several LBM-based surveillance studies in Egypt, Bangladesh, Cambodia and China concluded the collective topographies of diverse ecological origins, close contact of various bird species, keeping birds on floors and inadequate hygiene measures from cleaning and disinfection, lack of an allin, all-out management and longer than a day stay in LBMs promoted local transmission and genetic reassortment of pathogens (Abdelwhab et al., 2010;Fasina et al., 2016;Kayali et al., 2014;Martin et al., 2011).
The detailed comprehension of interactions, interdependence of traderelated structures and patterns of mobility in LBM can explain disease emergence and spread (Jones et al., 2016). Such an understanding of epidemiological and market behavioural processes is necessary to manage the diseases under such circumstances by developing appropriate mitigation on identified risk pathways and public health risks.
In many LMICs, surveillance for Campylobacter seldom exists in humans and poultry, and data pertaining the organism's presence, risk factors and impacts are rare (Asuming-Bediako et al., 2019;Carron et al., 2018;World Health Organization, 2013). Large disparities ranging from 2 to 100% in prevalence of Campylobacter in chicken across different countries are reported (Meunier et al., 2016), and when amalgamated at a global level, leave global assessments of Campylobacter burden severely lacking in data from sub Saharan Africa. The European Food Safety Authority reports a mean Campylobacter prevalence of 70% in primary broiler production (Meunier et al., 2016), while a prevalence study for Campylobacter from 171 poultry premises and 53 retail traders in Nairobi, Kenya, reported a range of 33-44% for broiler and indigenous chicken farms, respectively, 60 and 64% for retailers (Carron et al., 2018). Poultry markets are constituent of the food chain, but the public health risks and emerging pathogens have not been fully elaborated in much of East Africa. These markets also lack policy guidelines to support the market development and food safety measures.

Study area
This study was conducted in Busia county, western Kenya in the Lake Victoria basin region on the border with Uganda ( Figure 1). Busia county lies between latitude 0 • 45 north and longitude 34 • 25 east.
Busia county is a site with a trading network for the supply of live birds mainly from backyard settings to the rest of Kenya (McCarron et al., 2015). Poultry production is typically extensive, estimated at 1.4 million birds and characterized by dualism of local and improved breeds.
The majority of villages have a certain day each week for selling foodstuffs such as cereals, legumes and live birds in community markets.

Study design
We conducted a LBM-based cross-sectional survey from July to October 2018.

Study population
This study consisted of all LPTs having regular contacts with poultry.
An LPT was defined as a trader with occupation requiring transporta-tion of live poultry, selling live poultry or slaughtering of poultry for customers and comprised of sellers and middlemen. A seller would have a stall/cage at the market, while the middleman had none. In instances where the middleman also doubled as market seller, the respondent was asked which role they identified with most closely. We included LPT who had worked in the selected LBMs for at least six months prior to the survey, aged above 18 years old and willing to participate in the study. Eligible poultry species for obtaining Campylobacter faecal samples included chickens, ducks, geese, guinea fowl and turkeys. Those who bought poultry for home consumption and non-designated LBM sites with less than three poultry stalls were excluded.

Sampling strategy
A minimum sample size of 170 LPTs was determined using 95% confidence level and 5% margin of error with a considered proportion of 87.3% LPTs who never separated birds by species (Kirunda et al., 2015). The formula of Thrusfield (2005)

Data collection
Using an interviewer-administered pretested structured questionnaire, market survey data were collected (Conceptual framework,  (Table 1).

2.5.1
Bacteriological testing for estimation of live bird Campylobacter positivity One bird per poultry held by each LPT was randomly selected, restrained and cleaned for any obvious dirt around the outside of the cloaca with disposable wipes. A sterile swab moistened by dipping in Preston enrichment medium was placed inside the cloacal opening against the internal surface of the mucosa and rotated two to three times before being withdrawn. Using scissors dipped in 70% alcohol, the stem was cut at the brim of the bottle to allow tight closure. The media vial was then labelled with a unique epidemiological identifier, placed in an insulated chilled cool box packed with ice packs (5 • C) and transported immediately within 5 hours of collection to the International Livestock Research Institute (ILRI) Busia laboratory for immediate processing. The procedure was repeated for the next poultry held and every participating LPT for every market The primers Jej-3 and Jej-4 were used to screen for C. jejuni as previously described (Rosenquist et al., 2007).

Ethical considerations
We obtained ethical approval to conduct the study from Institutional we organized market visits and held discussions with LPTs to explain the study objectives, participants' rights and obtain informed written consent. Names of respondents were not recorded on specimen labels.

Respondent demographic characteristics
We enrolled and interviewed all 186 eligible poultry sellers. Five LPTs declined interviews because they felt they had participated in similar surveys in the past.

Poultry information and sources
Only 16.1% of LPTs reported a lack of capacity building. Among the 83.9% who reported having benefited from capacity building around their LPT role, when asked the source of information, slightly less than a half (48.1%) had received information from fellow traders, 32.1% from animal health professionals, 25.6% from workshops and seminars, 25% through radio and television, 8.3% school curriculum, 3.2% from public health officers and 1.3% from information, education and communication (IEC) materials.

Risk characterization
The risk assessment measure was related to poultry sellers' knowledge on campylobacteriosis based on seven-item statements (Table 1).
Seventy-two respondents recorded a 'no comment' to one or more of the risk statements and were excluded from analysis (n = 114

Market structure and operations
Markets that operated on weekly market days had lesser odds of public health risks than daily markets (POR = .47, 95% CI: .14-1.44), while non-association members showed a higher risk compared to poultry association members (POR = 1.5, 95% CI: .45-5.82).

Multivariable analysis for public health risks in LBMs
In the final model, accumulation of litter (adjusted POR, 19.67, 95% CI: 3.01-128.52) independently increased exposure to public health risks.

DISCUSSION
This study examined LBMs in a region typical of smallholder poultry farming for public health risks associated with likely transmission of

Market demographics
The dominance of males in these LBMs contrasts Egyptian traditional markets, which are largely operated by women vendors (Abdelwhab et al., 2010). Socio-cultural factors have been reported to influence gender participation in markets in other livestock production systems (Aklilu et al., 2007). The higher male participation could be associated with access to financial resources, ability to take risks and access to market information (Aklilu et al., 2007). The understanding of the gender differences in Busia could contribute to identifying opportunities for women to participate and bargain power in the overall economic growth of these markets. The mean age of 46 ± 13.7 years implied that the energetic, enterprising and active productive age were major participants in LBMs. A risk management study of 84 poultry farmers in Imo, Nigeria reported this age category was likely to enjoy enduring capacity for innovations and risk bearing (Iheke et al., 2016). A contextual understanding why participation of this age group increases could contribute to realization of opportunities to improve market access and benefits. The LBMs were largely driven by LPTs (75%) with a primary level of education. Parallel proportion of LPTs' educational levels 74-84% in Uganda (Kirunda et al., 2015) and 79% in Bangladesh (Sayeed et al., 2017) has been reported. The learning attainment may depict traders' literacy and numerical skills and possible entrepreneurship skills gained over the years. This could impact positively for decision making, since the practical knowledge acquired over time could be useful in overcoming certain inherent deficits and customer tastes in the market environment (Aklilu et al., 2007;Elelu, 2017). An Egyptian study by Kayali et al. (2014) also reported that the educational status limits their options for gainful engagement. He understandably argues that any interventions being made in the LBMs should be appraised for implications that seem to threaten their economic activity (Kayali et al., 2014).

Mechanisms for supply and retention of birds
Poultry trade was largely an individual undertaking without formal marketing linkages. This contrasts organized retail poultry shops in Egypt (Abdelwhab et al., 2010) and well-structured retail and wholesale bird markets in Chittagong metropolis of Bangladesh offering both live and dressed poultry (Sayeed et al., 2017). The informal and low marketing allows them to exert their independence and control over their own sales but exposes them to possible economic instabilities of inadequate finances, ravages of poultry diseases and make access to agribusiness services difficult (Aklilu et al., 2007).
The LBMs connected backyard production systems and commercial producers to traders and consumers. Even though the region's agriculture is intensifying, backyard poultry farming dominates in western Kenya (Chaiban et al., 2020, Okeno et al., 2012. These poultry systems are characteristic of inadequate maintenance of biosecurity and have been associated with outbreaks of poultry diseases such as salmonellosis, Newcastle and HPAI (Okello et al., 2010;Okeno et al., 2012), which are likely to compromise biosecurity of LBMs and health of consumers (Carron et al., 2017). Increase in volume of poultry deliveries to LBMs mirrors Egypt and Ethiopian poultry markets which coincided with secular and religious festivals (Abdelwhab et al., 2010;Aklilu et al., 2007;ElMasry et al., 2017). The bidirectional movement of birds in and out of markets and farms reported has previously been described in Kenya and Cambodia poultry movement networks (Carron et al., 2017;Van Kerkhove et al., 2009). Similarly, Kayali et al. (2014)

Value chain actor relationships
Poultry market associations were present in the LBMs. Membershipto-market associations promote equity, are source of credit, structure the marketing of products and likely reduce transaction costs for obtaining market information (Carron et al., 2017;Okello et al., 2010). The challenges reported had implications on LBM performance, and similar constraints have been identified in other livestock production systems (Mutua et al., 2017;Okello et al., 2010). Our study agrees with other studies recommendations for formulation of policies to improve traders' use and access to agribusiness services to alleviate impacts of these challenges (Carron et al., 2017;Okello et al., 2010 in Busia is within the 33-44% prevalence for broiler and indigenous poultry, respectively, but lower than 66% prevalence at retail markets of chicken meat system in Nairobi, Kenya (Carron et al., 2018). It

Public health risks
Consistent with risk factors for infection with Campylobacter, public health risks were related to poor hygiene practices and missing food safety inspections. Onsite slaughtering of poultry with limited access to water supplies poses a risk of contamination of carcasses with intestinal bacteria and subsequently human infections (Figure 4).
These biosecurity shortfalls may have been occasioned by limited access to information on LBM-associated public health risks from reliable sources (Table 3). In such market settings, Elelu (2017)

Limitations
Selection bias could have emanated from failure to contact some of the LPTs during our visits to LBMs. The return visits to enlist all LPTs ensured sample representativeness, high response rate and minimized selection bias. Asking traders to recollect their trading practices with scanty record keeping might have introduced recall bias to the data collected. Pretesting carefully structured questionnaire and training of interviewers served to reduce this bias. The modest sample size for cloacal faecal samples arose from constraints of time and resources and may have introduced bias in some descriptive measures, but all samples remained randomly allocated. It is likely the estimated positivity captured diversities in live birds from diverse production systems, hygiene and biosecurity status, factors previously described to be associated with Campylobacter-positive flocks. The positivity data and sample distribution are LBM based, which limit wider implications of the study to poultry systems with different dynamics. Nonetheless, the study results present a useful foundation for sanitary risk management in LBMs.

Conclusions and recommendations
This study generates an understanding of informal LBMs in smallholder farming environments to reveal Campylobacter positivity in live birds and associated public health risks in East Africa where data are scarce.
The LBMs were unstructured, displaying multi-species from different poultry production systems. Campylobacter-positive flocks may con-