Eco-Epidemiology and Microbiological Evaluation of Poultry Salmonellosis in North Central Nigeria, and its Socioeconomics and Public Health Impacts

Abstract

Nigeria is a country with a mid-2020 human population of approximately 209 million, and the poultry industry in Nigeria has rapidly expanded in recent years despite many health and economic challenges. Poultry production in the different agro-ecological zones of Nigeria are characterized by generalized and specific production and health-related challenges principal among which are: 1) low level of production, 2) inadequate scaling up and specialization, 3) antimicrobial use and resistance, and 4) a poor level of biosecurity implementation. Hence, there are a number of poultry-related zoonoses can be found in humans and animals in Nigeria. The Salmonella spp. is a Gram-negative enteric pathogen (bacterium), with potentials to infect almost all animals including humans. Though, only two species have been identified in this genus, vis the enterica and bongori, almost 2,700 serotypes (serovars) have been listed with approximately 10% isolated from birds. Most serotypes of Salmonella can infect several animal species including

humans, such as Salmonella Typhimurium and Salmonella Enteritidis, which are primarily poultry- associated. Salmonellosis, as a bacterial zoonosis, causes an array of health conditions in humans

and animals, and the non-typhoidal salmonellosis (NTS) is prevalent with substantial under- appreciated public health impacts. This work was set out with the objectives of conducting

microbiological evaluation of NTS in North Central zone of Nigeria (NCN) using classical and molecular methods; conducting a comprehensive re-analysis of risk of introduction of NTS to poultry farms, determining the epidemiology of foodborne Salmonella among poultry farmers and consumers, determining the economic burden of food borne salmonellosis in humans and poultry, demonstrating the benefit of disease control measures against salmonellosis in poultry using validated tools, and map spatial heterogeneity of habitat suitability for salmonellosis in poultry farms in Nigeria to aid evidence-based support to decision makers. Using field sampling, laboratory methods and a semi-structured questionnaire (n = 1000) in poultry farms in NCN, the incidence and risk factors for the persistence of NTS infection in poultry were explored. Approximately 41.6% (95%CI: 38.58 to 44.68) of the farms had experienced NTS over the last 18 months and the awareness of salmonellosis was moderate. A number of risk factors for increased odds of NTS infection in poultry including increasing stock in smallholder farms, self-mixing of concentrate on the farm, usage of stream water, pen odour, non-adherence

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and partial adherence of farms to recommended poultry vaccination against pullorum and fowl typhoid and lack of and non-adherence to biosecurity were identified. Overall, 66 isolates including Salmonella enterica, Salmonella arizonae, S. paratyphi, and S. typhi, with 94.5% mixed infections with Klebsiella pneumoniae and Lactobacillus bulgarius, were obtained, and irrational antibiotic-use practice remains a major problem in the industry. Specifically, the study obtained a number of multi-drug resistant isolates, with likelihood of passing such resistant organisms through the human food chain. To evaluate the economic and social burden of NTS, poultry and human populations, economic and epidemiological data were retrieved from various sources and validated. A customized and validated Microsoft Excel® tool was utilized to conduct the economic analysis for the reference year 2020. The burden of NTS was 325,731 human cases and a total of 1,043 human deaths per year, at a disability-adjusted life year (DALYs) of 37,321. The cost associated with infection in humans was US$ 473,982,068, and for poultry, US$ 456,905,311 (the direct value of animal loss, US$ 224,236,769, loss from salvage slaughter and culling, US$ 220,386,556, and value of foregone production, US$ 12,281,987). Using Outbreak Costing Tool (OCT), the benefit-cost of multisectoral intervention against NTS was estimated. Approximately 4,835 technical officers and 3,700 non-technical staff (n = 8,535) with an annual investment of over 2.2 million work hours, and at a total cost of US$ 53,854,660.87 are needed for an annual NTS control programme in humans and animal. The non-labour-related cost was 89.21% of the total intervention costs, and major costs were incurred in medical countermeasures, travel and transports, and laboratory support. The overall intervention’s investment was 374.15% of the estimated national and subnational systems’ annual budget for diarrhoeal diseases, and the outbreak response period incurred the highest costs (53%) of the total intervention. The benefit– cost ratio (BCR) of intervention was 17.29. Through a cohort study, the cost-effectiveness of NTS

in humans in Nigeria for the year 2020 was determined. Specifically, an Excel-based cost- effectiveness analysis tool was developed to compare structured (One Health) and unstructured (episodic intervention against NTS), with input data from various sources. The non-complicated and complicated cases were 309,444 (95%) and 16,287 (5%) respectively, and the overall programme cost was US$ 31,375,434.38. The current non-systematic episodic intervention costed US$ 14,913,480.36, indicating an additional US$ 16,461,954 to introduce the proposed intervention. The intervention averted 4,036.98 NTS DALYs in a single year. The non-complicated NTS case was US$ 60/person with significant rise in complicated cases. The cumulative costs of NTS with and without complications far outweighed the program cost for One Health intervention with an incremental cost-effectiveness ratio (ICER) of -US$ 221.30). The suitability map for continued infection in humans and poultry indicated that the disease would remain prevalent unless significant behavioural change communication is undertaken and intense control for NTS challenges are implemented. The identified risk practices must be mitigated intentionally, and biosecurity and hygiene must be improved to reduce the burden of NTS. Since the utilization of One Health approach to intervention is cost-effective and cost-beneficial, and they carry additional mitigative benefits for other diseases, multisectoral investigation and response against NTS in Nigeria is advocated. The health system should re-focus and re-prioritize, with coordinated collaborations and through the utilization of a more decentralized approach. Anticipatory planning, adequate resource allocation and more intense outbreak investigations to reduce critical response time are warranted. Identified limitations in this study must be improved to optimize benefits associated and to facilitate policy discussions. The outcomes of this work provide empirical evidence to support informed decisions and investments in the control and eradication of human and poultry salmonellosis (NTS) in Nigeria.