Abstract
Background
The non-typhoidal salmonellosis (NTS) is a pathogenic bacterial zoonosis with substantial but often under-appreciated public health impacts. The NTS is prevalent in poultry and humans in Nigeria, yet its economic and social burden have not been determined through any empirical study. To bridge the gap, we evaluated the impact of NTS in social and economic terms.
Methods
Relevant population, economic and epidemiological data were retrieved from peer-reviewed publications, open sources and relevant authorities. Additional data were obtained through experts' opinions and field surveys. Using a customized and validated Microsoft Excel® tool, economic analysis was conducted.
Results
Using the year 2020 reference point, the burden of NTS was 325,731 cases and a total of 1043 human deaths, at a disability-adjusted life year (DALYs) of 37,321. The cost associated with infection in humans was US$ 473,982,068. A total loss of US$ 456,905,311 was estimated in poultry including 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.
Interpretation
The outcomes of this important work provide empirical evidence to support informed decisions and investments in the control and eradication of human and poultry salmonellosis (NTS) in Nigeria.
Keywords: Economic burden, Social burden, Non-typhoidal salmonella, Disability-adjusted life years, Years of life lost, Years lost due to disability
1. Introduction
Salmonellosis is a pathogenic bacterial zoonosis with substantial public health impacts [1,2]. With over 2600 different serovars identified to date, Salmonella spp. are broadly divided into typhoidal and non-typhoidal Salmonella (NTS) serovars [3,4]. The NTS is one of the widespread causes of food-borne diarrhoeal diseases, while the invasive NTS (iNTS) is responsible for major bloodstream infections universally [1,3,5]. Humans are infected with NTS through contamination from poultry products (egg fragments, hatching eggs, chick boxes, fluff and faeces), partially cooked meat and raw eggs [2,3]. The global estimates of burden of NTS varied widely, including an estimates of over 27 million human cases and 200,000 deaths per annum [6,7]; approximately 79 million human cases and over 59,000 deaths annually [2]; and 93.8 million human infections and 155,000 fatalities annually [8]. Furthermore, in a recent ranked study in the USA, Salmonella spp. was the first-ranked foodborne pathogens, with the most significant cost of illness and the quality-adjusted life-year (QALY) losses [9].
The iNTS was estimated to cause 177–388 cases per 100,000 children under 5 years in Africa, but may reach up to 2000–7500 cases per 100,000 humans in immunocompromised HIV-infected adults, and a case fatality ranging between 20 and 25% [10]. In Nigeria, the poultry farm level prevalence of NTS range from 41.6 to 47.9% and the risk factors for NTS infection of poultry farms in Nigeria have been fully explored [4,11,12]. Based on a recent meta-analytic study, Nigeria has a burden of prevalence (in humans) of 1.9% (2732/143,756) Salmonella bacteremia and 16.3% (1967/12,081) Salmonella-associated gastroenteritis [13]. In addition, a total of 53 Salmonella serotypes have been identified in humans in the country including 39 associated with Salmonella-bacteremia and 31 associated with Salmonella-gastroenteritis [13].
The country has an estimated human population of approximately 219 million as of 2022 and has the largest market in sub-Saharan Africa, with a GDP PPP in excess of US$ 1 trillion for the year 2020 [11,14,15]. The agriculture sector contributes 24.1% of the country's GDP in the year 2020, with the poultry sector contributing approximately 25% of the agriculture GDP, and 6–8% to real GDP annually [16,17]. The 2020 poultry population in Nigeria was approximately 224 million [18], and is a major source of readily available and affordable animal protein (11). In 2019, the consumption of poultry products was approximately US$ 2 billion while the industry was worth US$ 4.2 billion [19].
Previous workers have made efforts to estimate the cost of animal health challenges globally and in Nigeria, including for multiple pathogens [2,20,21], Salmonella [1,8], avian influenza [22], and African swine fever [23], among others. Animal diseases cause significant, often undervalued economic losses through morbi-mortality, treatment and intervention cost, effects on production and productivity, and human health components (livelihoods, psychosocial and zoonotic impacts). It is therefore important to continue to estimate the burden of animal disease and relative microbiological hazards that may originate through animal-sourced food system to prioritise interventions aimed at mitigating these impacts. The aim of this work was to determine the economic and social costs and consequences of NTS in human and poultry in Nigeria, using the year 2020 as a reference point. The outcome should provide empirical information to guide informed decision, investment, and adequate planning for human and animal health interventions against poultry salmonellosis (NTS) in Nigeria.
2. Materials and method
This work is a follow-up on the previous one where Salmonella isolates were obtained and characterized from samples collected from poultry farms in North central Nigeria where Salmonella enterica, S. arizonae, S. paratyphi and S typhi were recovered at prevalences of 41.6%, 0.2%, 1.9% and 2.3% respectively [4].
2.1. Data sources and evaluation tool
We used the semi-automated Microsoft Excel® costing tool developed as part of the disease estimation process under the Food and Agriculture Organization of the United Nations' (FAO) Africa Sustainable Livestock 2050 [21, Supplementary materials S1 – S7]. Extensive economic, population and poultry sector data were obtained from various sources including: 1). The United Nations' Department of Economic and Social Affairs, Population Division, 2). The World Bank, 3). The Nigerian Federal Ministry of Agriculture and Rural Development (FMARD), 4). The Federal Ministry of Finance, Nigeria, 5). The National Agricultural Extension and Research Liaison Services (NAERLS), 6). Peer reviewed literatures, 7). Field surveys, 8). Experts' opinions and calculations made from these various sources (Table 1; Supplementary Tables S1 – S7).
Table 1.
Input data for the computation of economic and social costs of non-typhoidal salmonellosis for the year 2020 in Nigeria.
Poultry | Intensive (large-scale) | Intensive (small and medium-scale) | Free-range/Semi-intensive (indigenous) | Total | Source | |
---|---|---|---|---|---|---|
Year 2020 poultry population | 33,968,841 | 118,377,487 | 72,168,465 | 224,514,793 | [18]. | |
Price per carcass yield (Naira) | 2240 | 2002 | 2000 | Carcass weight (1.4–1.6 kg) [28,29]. | ||
Price of poultry meat (kg) (Naira) | 1400 | 1400 | 850 | [29]. | ||
Price of eggs (Naira) | 37 | 37 | 30 | [29] | ||
No of eggs laid per hen/year | 250 | 180 | 40 | Experts' opinions, [21]. | ||
Price of culled animal (or % decrease in price due to culling) (Naira) | 1340 | 741 | 739 | Experts' opinions, [21,30]. | ||
Price reduction for culled bird (Naira) | 40% | 63% | 63% | Experts' opinions, [21]. | ||
Number of cases | 6,793,768 | 26,043,047 | 10,825,270 | 43,662,085 | Experts' opinions, field survey, [18]. | |
Number of deaths | 2,717,507 | 10,417,219 | 2,706,317 | 15,841,044 | Experts' opinions, field survey, [18]. | |
Number of salvage slaughter | 2,038,130 | 10,417,219 | 8,118,952 | 20,574,302 | Experts' opinions, field survey, [18]. | |
Number of culls | 1,698,442 | 3,906,457 | 108,253 | 5,713,152 | Experts' opinions, field survey, [18]. | |
Number (eggs lost in survivor hen per year) | 38 | 27 | 3 | Experts' opinions, field survey, [18]. | ||
Humans | Livestock keepers | Consumers | ||||
Number of humans involved in the poultry value chain | 9,627,904 | 33,552,135 | 20,454,954 | 63,634,993 | 27,407,441 | [21]. |
Number of cases | 1155 | 40,263 | 147,276 | 188,694 | 137,037 | FMoH, Experts' opinions. |
Number of deaths | 4 | 129 | 471 | 604 | 439 | FMoH, Experts' opinions. |
Duration of disease in days | 6 | 6 | 3 | 3 | FMoH, Experts' opinions. | |
Average age of infection | 20 | 16 | 16 | 25 | FMoH, Experts' opinions. | |
Year 2020 human population | 208,327,405 | [14]. | ||||
Exchange rate (Naira to US$) (2020) | 380.26 | [31]. | ||||
Exchange rate (US$ PPP) (2020) | 144 | [32]. | ||||
DALYs weight (Salmonella) | 0.21 | |||||
Average life expectancy | 55 years | [33]. | ||||
VSLY (US$) | 11,353 | [26]. | ||||
GDP, US$ PPP 2020 (Naira) | N406,878,200,000,000 | (US$ 1.07 trillion) [34]. | ||||
Percentage Livestock VA (2020) | 1.39% | [16,19]. | ||||
Livestock VA, US$ PPP (Naira) (2020) | N5,655,606,980,000 | US$14,873,000,000) [35], | ||||
Animal production losses (2020) | N128,886,753,387 | [21]. | ||||
GDP in 2020 (Naira) | N164,382,595,400,000 | (US$432,290,000,000), [34]. | ||||
AG GDP % | 24.1% | [17]. | ||||
Loss as a % of GDP | 0.08% | Calculation using [–,17,19,21,26,32,34]. | ||||
Loss as a % of AG GDP | 0.33% | Calculation using [–,17,19,21,26,32,34]. |
Federal Ministry of Health = FMoH; GDP = Gross domestic product; PPP = Purchasing power parity; DALYs = Disability-adjusted life years; VSLY = Value of statistical life year; VA = Value added; N = Naira, AG GDP = Agriculture Value Added GDP. Additional data inputs are available in the Supplementary Tables S1 – S7.
2.2. Additional data and expert elicitation protocol for assembling information on zoonoses and AMR
Currently, in Nigeria, the information system may not always provide the government with sufficient and robust information on the incidence, prevalence and impact of zoonoses on society. It is therefore challenging to have a single source of comprehensive dataset for measuring economic evaluations, and return on investment aimed at prevention, management and control of animal diseases and zoonoses. We utilised the Google form (https://docs.google.com/forms/d/e/1FAIpQLSefH1i8YASvewU1y1x-OS0sgyuvWJnOuaECXKH9ReLV4YaYZw/viewform?vc=0&c=0&w=1&flr=0) to collect data briefs on humans and poultry from key informant, experienced stakeholders and value chain actors in the poultry industry. We also utilised the Africa Sustainable Livestock 2050 (ASL2050) expert elicitation protocol to assemble information on selected zoonoses and antimicrobial resistance using consensus of judgements of carefully selected experts [21]. It should be noted that experts were drawn using the snowballing sampling approach through which 30 animal health and 11 human health experts were obtained [21. These tools provided additional sources of data needed to measure the impact of zoonoses on society in monetary terms especially where industry, population and economic data were insufficient, unreliable or physically impossible to gather such data from current datasets. Data obtained through Google forms were evaluated for measure of central tendencies (absolute counts, minimum, median, average, maximum and mode) and those from experts' opinions were triangulated with field surveys, literature search and official statistics [2,21,24].
2.3. Estimation of burdens of non-typhoidal salmonellosis
We estimated the losses in humans (social cost) and poultry (economic cost) using the input data described above and the excel spreadsheet developed by the Africa Sustainable Livestock project [21].
To estimate the social cost of the disease, the Disability-Adjusted Life Years (DALYs) method was used as proposed by the World Health Organization (WHO) in quantifying the burden of disease from mortality and morbidity [2,25]. One DALY represents a one year of healthy life lost (a health gap measure that combines both time lost due to premature mortality and the time spent in illness). Following the methodology of Herrera et al. [26], the “cost” of one DALY has been defined as the willingness to pay for a DALY, which was determined based on the Value of Statistical Life (VSL). The VSL available for the United States was discounted to a yearly value and transferred into the Nigerian context using the benefit transfer methodology described in Hammit and Robinson [27].
The loss of production was calculated by estimating the value of animals lost and the value of forgone production (including losses from decrease in egg production, culling and salvage slaughter) as presented in the detailed study of FAO [21]. Input data and sources are detailed in Table 1.
3. Results
The results are presented in three sections as described below.
3.1. Losses in humans (social costs)
Overall, the total economic losses associated with NTS in Nigeria for the year 2020 was US$ 930,887,379 with approximate losses in humans (social costs) and animals (poultry sector) being 50.9% (US$ 473,982,068) and 49.1% (US$ 456,905,311) respectively (Table 2). The losses in the human population were further disaggregated into losses in workers in the poultry value chain (livestock keepers, 64.1%; US$303,911,990), and the general populace (consumers, 35.9%; US$170,070,078) (Table 2). Among the livestock keepers, a significant percentage of the social costs (77.9%) was borne by the value chain stakeholders in the free-range and semi-intensive (indigenous) poultry stock (Sector 4). Approximately 21.6% and 0.6% of the social costs were borne by the value chain stakeholders (humans) in the commercial intensive (small and medium-scale) (Sector 3), and intensive large scale and commercial operations (Sectors 1 and 2) (Table 3). In total, 188,694 and 137,037 cases were estimated among poultry keepers and consumers respectively; with 1043 deaths and 324,689 survivors predicted to be directly associated with NTS in the year 2020 in Nigeria. The estimated DALYs was 13,391, which translated to the social cost above (US$ 473,982,068.00; Table 3).
Table 2.
Overall economic and social costs of non-typhoidal salmonellosis in poultry and humans for the year 2020 in Nigeria.
Poultry | Intensive (large-scale) | Intensive (small & medium-scale) | Free-range/Semi-intensive (indigenous) | Total | ||
---|---|---|---|---|---|---|
Value of animals lost (US$) | 42,187,375 | 144,537,197 | 37,512,197 | 224,236,769 | ||
Value of forgone production (US$) | 26,573,102 | 134,195,062 | 71,900,378 | 232,668,542 | ||
Total loss in animals (US$) | 68,760,477 | 278,732,259 | 109,412,575 | 456,905,311 | ||
Loss as a % of livestock GDP | 0.00% | 0.00% | 0.00% | 0.01% | ||
Loss as a % of national GDP | 0.00% | 0.00% | 0.00% | 0.00% | ||
Loss per case (US$) | 10 | 11 | 10 | 10 | ||
Loss per case, as percentage of healthy animal | 65% | 77% | 73% | |||
Human (social) | Losses in Livestock keepers | Total for livestock keepers | Total for consumers | Total human loss | ||
Value of mortality (US$) | 1,643,368 | 63,814,550 | 233,426,044 | 298,883,961 | 167,075,760 | |
Value of morbidity (US$) | 50,490 | 1,759,506 | 3,218,033 | 5,028,029 | 2,994,318 | |
Total social cost (US$) | 1,693,857 | 65,574,056 | 236,644,077 | 303,911,990 | 170,070,078 | 473,982,068 |
Social cost as % of GDP | 0.00% | 0.00% | 0.00% | 0.00% | 0.00% | 0.00% |
Overall losses in poultry and humans (US$) | 930,887,379 |
All calculations were conducted at an exchange rate of Naira 380.26 to US$ 1.00.
Table 3.
Economic and social costs of non-typhoidal salmonellosis in humans for the year 2020 in Nigeria.
Salmonellosis parameters |
Poultry keepers |
Total Poultry keepers | Total Poultry consumers | ||
---|---|---|---|---|---|
Intensive (large-scale) | Intensive (small & medium-scale) | Free-range/Semi-intensive (indigenous) | |||
Ref. year | 2020 | 2020 | 2020 | 2020 | 2020 |
DALY Weight | 0.21 | 0.21 | 0.21 | 0.21 | 0.21 |
Number of cases in humans | 1155 | 40,263 | 147,276 | 188,694 | 137,037 |
Number of deaths in humans | 4 | 129 | 471 | 604 | 439 |
Number of survivors | 1152 | 40,134 | 146,804 | 188,090 | 136,599 |
Disease duration in years | 0.02 | 0.02 | 0.01 | 0.01 | |
Average age of infection | 20 | 16 | 16 | 25 | |
YLL | 129 | 5025 | 18,380 | 23,534 | 13,156 |
YLD | 4 | 139 | 253 | 396 | 236 |
DALY=YLL + YLD | 133 | 5163 | 18,633 | 23,930 | 13,391 |
Social cost(DALY*VSLY) (US$) | 1,693,857 | 65,574,056 | 236,644,077 | 303,911,990 | 170,070,078 |
Total social costs in humans (US$) | 473,982,068 |
DALYs = Disability-adjusted life years; YLL = years of life lost; YLD = years lost due to disability; VSLY = Value of statistical life year. All calculations were conducted at an exchange rate of Naira 380.26 to US$ 1.00.
3.2. Losses in poultry (economic costs)
Approximately 61% (US$278,732,259) of the total losses in poultry (chickens) originated from the intensive small and medium scale farms, while 23.95% (US$109,412,575) was from the free-range and semi-intensive (indigenous) poultry (Table 4). The direct values of poultry lost were 61.4% (US$42,187,375), 51.9% (US$144,537,197) and 34.3% (US$37,512,197) of the total losses in each evaluated sector (Intensive large-scale; Intensive small and medium-scale; and free-range and semi-intensive (indigenous) poultry) (Table 4). Specifically, the total value of animals lost, the value of loss from salvage slaughter and culling, and the total value of forgone production were US$224,236,769 (49.1%), US$220,386,556 (48.2%) and US$ 12,281,987 (2.7%) respectively (Table 4).
Table 4.
Economic costs of non-typhoidal salmonellosis in poultry for the year 2020 in Nigeria.
Salmonellosis parameters | Intensive (large-scale) | Intensive (small & medium-scale) | Free-range/Semi-intensive (indigenous) | Total |
---|---|---|---|---|
Number of cases in poultry | 6,793,768 | 26,043,047 | 10,825,270 | 43,662,085 |
I. Value of animals Lost (US$) | ||||
Number of deaths | 2,717,507 | 10,417,219 | 2,706,317 | 15,841,044 |
Value of animals lost (US$) | 42,187,375 | 144,537,197 | 37,512,197 | 224,236,769 |
II. Loss from salvage slaughter and culling | ||||
Number of salvage slaughter* | 2,038,130 | 10,417,219 | 8,118,952 | 20,574,302 |
Number of culls* | 1,698,442 | 3,906,457 | 108,253 | 5,713,152 |
*this number may exceed the number of cases if the whole flock is culled / slaughtered | ||||
Value of loss from salvage slaughter and culling (US$) | 23,306,641 | 125,179,537 | 71,900,378 | 220,386,556 |
II. Value of foregone production | ||||
Number of survivors | 339,688 | 1,302,152 | – | 1,641,841 |
Number of eggs lost per year in survivors | 38 | 27 | 3 | |
Total value of forgone production (US$) | 3,266,461 | 9,015,526 | – | 12,281,987 |
Total losses in poultry (US$) | 456,905,311 |
All calculations were conducted at an exchange rate of Naira 380.26 to US$ 1.00.
3.3. Pattern of antimicrobial use in the different sectors of the poultry industry
Based on the consensus of experts' opinions, the intensive small and medium-scale poultry farms as well as the intensive large poultry farms significantly access and used antimicrobials (92.5%), with only 62% of getting antimicrobials through recognised means (formal sources from veterinary drug stores or from veterinarians [[36], [37], [38]]) compared with the free-range and semi-intensive indigenous farms' access and use (49.2%), and access through the recognised means (13%) respectively (Fig. 1a). Similarly, 90.9% of the intensive small and medium-scale poultry farms as well as the intensive large farms have observed significant increase in the use of antimicrobials in the last decade compared with just 20% in the free-range and semi-intensive indigenous poultry farms (Fig. 1b). While 92% of the stakeholders in the intensive small and medium-scale poultry farms and the intensive large farms were seriously concerned with the observed trends in antimicrobial usage in poultry farms, it was shown that only 60% of the free-range and semi-intensive indigenous poultry farms stakeholders were seriously concerned (Fig. 1c). Among the human experts, 100% of them confirmed to have observed a significant increase in antimicrobial use in humans in the last decade. Only 20% and 80% were moderately and highly concerned about the trend respectively.
Fig. 1.
Experts' opinions elicitation on a. Antimicrobial use practice in poultry; b. Degree of increased use of antimicrobial in poultry; c. Degree of concern on increased use of antimicrobial in poultry.
Note that 100% of the human health experts observed increased antimicrobial use in humans in the last decade, and only 20% and 80% were moderately and highly concerned about the trend respectively. It should be noted that the most common antimicrobials used in poultry are: Tetracycline, Streptomycin, Penicillin, Nalidixic acid, Metronidazole, Gentamycin, Furazolidone, Furaltadone, Erythromycin, Enrofloxacin, Chloramphenicol and Ampicillin [38].
4. Discussion
We have estimated the overall economic burden of NTS in Nigeria for the year 2020, which came to US$ 930,887,379 (3.19% of the national budget). This represented a significant proportion in a country, which revised national budget for 2020 stood at 10.51 trillion naira ($29.19 billion) (https://www.reuters.com/article/nigeria-budget-idUSL8N2DA6Q9). Considering that the poultry sector contributed between 6 and 8% to real GDP for the year 2020, and approximately 25% of the agriculture GDP [16,17], the significance of these losses becomes more glaring. There is however lack of documentary evidence that the national government has taken account of this point, in planning and intensifying efforts to mitigate the impacts of NTS in humans and poultry. The only earlier estimates made in the past was conducted as part of the Africa Sustainable Livestock 2050 project in Nigeria [21]. The NTS typically presents as an acute onset of fever, abdominal pain, diarrhoea, nausea and sometimes vomiting, while the illness may last for 2–7 days [2]. In response to such acute self-limiting gastrointestinal illnesses, the households, particularly the poor in the rural and peri-urban households, and where healthcare services are hard to reach, primarily resort to habitual use of antibiotics and herbal medication, with high levels of self-prescription compared to antibiotic prescriptions that originate through the pharmacists [39]. In particular, metronidazole, tetracycline, amoxicillin, ampicillin or the Amplicox (a combination of ampicillin and cloxacillin) have been reported to be regularly abused [39]. In view of these observation, cases of NTS at the healthcare facilities may have been grossly underreported as only more serious cases may get to the hospital.
Comparing the case of NTS to other zoonotic diseases, which have occurred in Nigeria in recent times: 1). The highly pathogenic avian influenza subtype H5N1 (HPAI H5N1), which is a rapidly fatal disease in poultry and humans that occurred in 2006–2008, and has continued to date, and somewhat become endemic in Nigeria. This virus may presents in different subtypes. HPAI H5N1, may cause 70,000–145,000 household members to fall into poverty through loss of livelihoods associated with poultry, whereas, NTS is more insidious but will affect a lot more people through morbidity (≤ 325,731 humans) but much lower mortality (≤ 1043) [40]. In comparison, COVID-19, a largely public health issue, will produce much larger loss (up to 34.1%) loss in the country's GDP, amounting to US$ 16 billion, primarily from the services sector and within a short period [41]. The burden of NTS is also lower than the associated burden in malaria, an endemic human disease, which burden of illness in Nigeria may be in excess of 25% of the GDP [42].
We estimated a disability-adjusted life years (DALYs) associated with NTS in 2020 to be 37,321; and more specifically, a total of 325,731 cases and a total of 1043 human deaths was linked to NTS, with 64.1% of the social costs associated with the poultry keepers than the general populace which accounted for only 35.9%. This observation calls for systematic surveillance for NTS in humans, particularly the poultry keepers, and the need to intensify eradication of poultry salmonellosis in farmed poultry stock [13]. Two particular results were interesting. First, a significant percentage of the social costs (77.9%) originated from the free-range and semi-intensive (indigenous) poultry stock (Sectors 3 and 4). It should be understood that most of these category of farmers reside in the rural and peri-urban often unplanned areas, and public health facilities may be inadequate or hard to access, there are imbalanced ratio of health workers to patients at such facilities, and the direct and indirect costs to patients may be relatively higher [43]. These may be directly linked to findings in the study of Adeyemi et al. [39] where households regularly self-medicate using antibiotics and herbal medication, based on options of patients and household to adopt alternative cheaper healthcare measures due to impoverishment, with consequent contribution to underreporting and underestimation of cases of NTS in Nigeria [13,43]. Secondly, although NTS is perceived as a disease of livestock, especially poultry, in view of the different serotypes of Salmonella enterica subsp. Enterica present in poultry [11,12], the larger proportion of the total losses (50.9%) directly related to losses in humans (social costs), pointing to the fact that human costs of salmonellosis may have been underestimated highly in the past.
It is unsurprising that the significant proportion of the losses in poultry (chickens) originated from the intensive small and medium scale farms and the free-range and semi-intensive (indigenous) poultry. These poultry sectors (3 and 4) contribute approximately 85% of the total poultry population in Nigeria, mainly in the small town, peri-urban shanties and unplanned rural areas, operate with low biosecurity and sources of day-old chicks that feed the system which may not always be standardised [30]. The aforementioned issues are significant risk factors for infection of poultry farms with Salmonella organism in Nigeria [4,12,30]. The total value of forgone production accounted for only 2.7% of the total losses in the poultry sector, an indication that poultry farmers hardly destroy and clean out the farms completely post infection, which is the standard recommended practice. The aforementioned factor can be a precursor to maintenance of infection in poultry farms and re-infection of new stock as emphasised in earlier study by [4].
It is noteworthy to indicate that despite the efforts made by the national and subnational government in Nigeria, the experts still observed significant usage of antimicrobials in both human and animal health, especially in the intensive small and medium-scale poultry farms, the intensive large poultry farms, and the human health facilities. There is a need for more stringent measure to control dispensing and access to antimicrobials if efforts put in to date will yield any measurable progress.
4.1. Limitations of the study
Our work is subject to a number of limitations. First, while we have made effort to evaluate the comprehensive economic and social costs of Non-Typhoidal Salmonella infections in Nigeria, we are aware that it is generally impossible to measure everything necessary for a comprehensive analysis. Even when measurements are available, they may not adequately represent values appropriate for the analysis at hand [44]. Secondly, we assumed linear costs for lost units without considering the cost corresponding to discounted values, the costs of treatment and prevention. Hence, our evaluation may therefore be partially attributable to the overall costs. In a data-scarce environment like Nigeria, wherein comprehensive costs of prevention and control are not well detailed, especially in the sectors 1–3 of the poultry industry, this may serve a major limitation to conduct a comprehensive cost evaluation. Furthermore, our estimate does not take into account the cost of reducing the loss and an incompressible limit of loss inherent in the socio-economic and behavioural context from Nigeria. It was difficult to estimate these items during the evaluation.
Fourthly, we use computational model to estimate some costs and disease simulation rather than a direct clinical trial with control group, using data from the line ministry, the stakeholders and experts. We are aware that this may be subject to a degree of bias of experts submitting the data, and all outputs/outcomes are as meaningful as the input values [44,45]. While we advocate for a disease-specific collation of economic dataset informing future analysis, it becomes difficult to conduct a nationwide clinical trials for an insidious but impactful disease like NTS due to regulations and time, and using data from other country may introduce geographical context and bias. Finally, the time factor may be a limitation to this type of economic evaluation carried out in this work as the industry is very dynamic in growth, disease contexts change, and many variables of interventions (prevention, management, treatment and controls) may demand regular remodelling using datasets available for the industry.
5. Conclusions
Our work has highlighted the burden of non-typhoidal salmonellosis in Nigeria, and the level of under-appreciation of its impact in the human population. Importantly, we have demonstrated that in developing countries like Nigeria, where there are constraints in public and animal health infrastructures, the overall ramifications of NTS have consequences that are detrimental to patients (human and animal), the economy and the country as a whole. It is believed that findings from this study should stimulate discussions on the effort at control and eradication of poultry salmonellosis, and by extension the reduction in the burden of NTS and iNTS in humans in Nigeria.
Author contributions
Conceptualization, A.O.S. and F.O.F.; methodology, A.O.S., J.O., A.U., U.P., A.F.R., O.M. and F.O.F.; software, U.P., A.F.R., O.M. and F.O.F.; validation, U.P., A.F.R., O.M. and F.O.F.; formal analysis, A.O.S., J.O., A.U., and F.O.F.; investigation, A.O.S., A.U. and F.O.F.; resources, A.O.S. and F.O.F.; data curation, A.O.S., A.U., and F.O.F.; writing—original draft preparation, A.O.S., and F.O.F.; writing—review and editing, all authors; visualization, U.P., A.F.R., O.M. and F.O.F.; supervision, U.P. and F.O.F.; project administration, F.O.F.; funding acquisition, A.O.S. and F.O.F. All authors have read and agreed to the published version of the manuscript.
Funding
This research received no external funding and The APC was funded by AOS and FOF.
Institutional Review Board
The study was conducted in accordance with the Declaration of Helsinki, and approved by the Institutional Review Board (or Ethics Committee) of Federal University of Technology, Minna (Ethical Review Committee approval number: 000030, May 2022). It also got ethical approval of the Research Ethics Committee of the Faculty of Veterinary Science, University of Pretoria, with ethical approval number REC 142–22 (April 2023).
Informed consent
All respondents to the data brief independently filled the consent form (Attached as appendix 1).
Declaration of Competing Interest
The authors declare no conflict of interest.
Acknowledgments
We thank Dr. Abdulkadir Usman (Department of animal production Faculty of Agriculture Federal University of Technology, Minna) for his technical guidance, Dr. Mustapha Muhammad (Federal Ministry of Agriculture, Veterinary Department) for provision of poultry-related data, Mrs. Ajoge Kuriyetu (National Primary Health Care Development Agency, Nigeria) for support and provision of human-related data, and for their various contributions and pieces of advice on this manuscript. The semi-automated Microsoft Excel® costing tool used in this study was developed as part of the disease estimation process under the Food and Agriculture Organization of the United Nations' (FAO) project, The Africa Sustainable Livestock 2050.
Footnotes
Supplementary data to this article can be found online at https://doi.org/10.1016/j.onehlt.2023.100546.
Appendix A. Supplementary data
Supplementary material 1. The following supporting information are available as supplementary materials:Table S1. Number by cases data; Table S2. Basic Check on data; Table S3. Total Loss; Table S4. Loss (Humans); Table S5. Salmonellosis Loss (Poultry); Table S6. Poultry population (2020 estimates); and Table S7. Human populations estimates for the year 2006, 2020 and 2022.
Supplementary material 2
Data availability
All data utilised in this work are open sourced in the various institutions' websites (Table 1) or on request from the Federal Ministries of Health, Agriculture or other mentioned Federal Agencies in Nigeria.
References
- 1.Ao T.T., et al. Global burden of invasive nontyphoidal Salmonella disease, 2010. Emerg. Infect. Dis. 2015;21(6):941–949. doi: 10.3201/eid2106.140999. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2.World Health Organization (WHO) WHO; 2015. WHO estimates of the global burden of foodborne diseases: Foodborne Disease Burden Epidemiology Reference Group 2007–2015.https://apps.who.int/iris/handle/10665/199350 255p. Available at: accessed 21 September 2022. [Google Scholar]
- 3.Gal-Mor O., Boyle E.C., Grassl G.A. Same species, different diseases: how and why typhoidal and non-typhoidal Salmonella enterica serovars differ. Front. Microbiol. 2014;5:391. doi: 10.3389/fmicb.2014.00391. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.Sanni A.O., et al. Risk factors for persistent infection of non-Typhoidal Salmonella in poultry farms, North Central Nigeria. Antibiotics. 2022;11(8):1121. doi: 10.3390/antibiotics11081121. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Batz M.B., Hoffmann S., Glenn Morris J., Jr. Ranking the disease burden of 14 pathogens in food sources in the United States using attribution data from outbreak investigations and expert elicitation. J. Food Prot. 2012;75(7):1278–1291. doi: 10.4315/0362-028X.JFP-11-418. [DOI] [PubMed] [Google Scholar]
- 6.Crump J.A., Luby S.P., Mintz E.D. The global burden of typhoid fever. Bull. World Health Organ. 2004;82(82):346–353. [PMC free article] [PubMed] [Google Scholar]
- 7.Buckle G.C., Walker C.L., Black R.E. Typhoid fever and paratyphoid fever: systematic review to estimate global morbidity and mortality for 2010. J. Glob. Health. 2012;2 doi: 10.7189/jogh.02.010401. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.Majowicz S.E., et al. The global burden of non-typhoidal Salmonella gastroenteritis. Clin. Infect. Dis. 2010;50(6):882–889. doi: 10.1086/650733. [DOI] [PubMed] [Google Scholar]
- 9.Batz M.B., Hoffmann S., Glenn Morris J., Jr. Emerging Pathogens Institute, University of Florida; 2011. Ranking the Risks: The 10 Pathogen-Food Combinations with the Greatest Burden on Public Health.https://www.epi.ufl.edu/media/epiufledu/Ranking-the-Risks-REPORT.pdf Available at: accessed 21 September 2022. [Google Scholar]
- 10.Feasey N.A., et al. Invasive non-typhoidal salmonella disease: an emerging and neglected tropical disease in Africa. Lancet. 2012;379(9835):2489–2499. doi: 10.1016/S0140-6736(11)61752-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Fagbamila I.O., et al. Salmonella serovars and their distribution in Nigerian commercial chicken layer farms. PLoS One. 2017;12(3) doi: 10.1371/journal.pone.0173097. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Jibril A.H. Prevalence and risk factors of Salmonella in commercial poultry farms in Nigeria. PLoS One. 2020;15(9) doi: 10.1371/journal.pone.0238190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Akinyemi K.O., Ajoseh S.O., Fakorede C.O. A systemic review of literatures on human Salmonella enterica serovars in Nigeria (1999-2018) J. Infect. Dev. Ctries. 2021;15(9):1222–1235. doi: 10.3855/jidc.12186. [DOI] [PubMed] [Google Scholar]
- 14.United Nations, Department of Economic and Social Affairs, Population Division World Population Prospects 2022. 2022. https://population.un.org/wpp/Download/Files/1_Indicators%20(Standard)/EXCEL_FILES/1_General/WPP2022_GEN_F01_DEMOGRAPHIC_INDICATORS_REV1.xlsx Online Edition. Available at: accessed 23 September 2022.
- 15.The World Bank GNI, GDP PPP (constant 2017 international $) – Nigeria. 2022. https://data.worldbank.org/indicator/NY.GNP.MKTP.PP.KD?end=2021&locations=NG&start=2009 Available at: accessed 15 September 2022.
- 16.Anon Poultry Sector Study Nigeria. 2020. https://www.rvo.nl/sites/default/files/2020/10/Poultry-Sector-Study-Nigeria.pdf Available at: accessed on 22 September 2022.
- 17.The World Bank Agriculture, forestry, and fishing, value added (% of GDP) – Nigeria. 2022. https://data.worldbank.org/indicator/NV.AGR.TOTL.ZS?locations=NG Available at: accessed 15 September 2022.
- 18.Federal Ministry of Agriculture and Rural Development, Nigeria . 2020. Poultry population estimates; p. 2020. Internal report. [Google Scholar]
- 19.Anon Nigeria Sector: Agriculture – Poultry. 2020. https://www.agroberichtenbuitenland.nl/binaries/agroberichtenbuitenland/documenten/brieven/2020/10/20/kansenkaarten-nigeria-pluimvee/Kansenkaart+Nigeria-Poultry.pdf Available at: accessed 22 September 2022.
- 20.Fadiga M., Jost C., Ihedioha J. ILRI; Nairobi, Kenya: 2013. Financial costs of disease burden, morbidity and mortality from priority livestock diseases in Nigeria. Disease burden and cost–benefit analysis of targeted interventions. ILRI Research Report 33. [Google Scholar]
- 21.Food and Agriculture Organization of the United Nations (FAO) Africa Sustainable Livestock (ASL) 2050. The monetary impact of zoonotic diseases on society - Nigeria. Rome. 2018. https://www.fao.org/documents/card/en/c/CA2146EN/ Available at: accessed 22 September 2022.
- 22.Fasanmi O.G., et al. National surveillance and control costs for highly pathogenic avian influenza H5N1 in poultry: a benefit-cost assessment for a developing economy, Nigeria. Res. Vet. Sci. 2018;119:127–133. doi: 10.1016/j.rvsc.2018.06.006. [DOI] [PubMed] [Google Scholar]
- 23.Fasina F.O., et al. Cost implications of African swine fever in smallholder farrow-to-finish units: economic benefits of disease prevention through biosecurity. Transbound. Emerg. Dis. 2011;59(3):244–255. doi: 10.1111/j.1865-1682.2011.01261.x. [DOI] [PubMed] [Google Scholar]
- 24.Morgan M.G. Use (and abuse) of expert elicitation in support of decision making for public policy. PNAS USA. 2014;111(20):7176–7184. doi: 10.1073/pnas.1319946111. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Murray C.J., et al. Disability-adjusted life years (DALYs) for 291 diseases and injuries in 21 regions, 1990–2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet. 2012;380:2197–2223. doi: 10.1016/S0140-6736(12)61689-4. [DOI] [PubMed] [Google Scholar]
- 26.Herrera-Araujo D., Mikecz O., Pica-Ciamarra U. Placing a monetary value on the human health component of zoonotic diseases: a methodological note with an application to cysticercosis in Africa. Prev. Vet. Med. 2020;175 doi: 10.1016/j.prevetmed.2019.104862. [DOI] [PubMed] [Google Scholar]
- 27.Hammitt J.K., Robinson L.A. The income elasticity of the value per statistical life: transferring estimates between high and low-income populations. J. Benefit Cost Analysis. 2011;2(1):1–29. doi: 10.2202/2152-2812.1009. [DOI] [Google Scholar]
- 28.Obun C.O., et al. Growth, carcass and organ weights of finisher broilers fed differently processed Detarium microcarpum (Guill and Sperr) seed meal. Livest. Res. Rural. Dev. 2008;20 http://www.lrrd.org/lrrd20/8/obun20126.htm Article #126. [Google Scholar]
- 29.National Agricultural Extension and Research Liaison Services (NAERLS) and Federal Ministry of Agriculture and Rural Development (FMARD) National Report of Wet Season Agricultural Performance in Nigeria, 2021. https://fscluster.org/nigeria/document/2020-wet-season-agricultural-performance Available at: accessed 23 September 2022.
- 30.Adene D.F., Oguntade A.E. Food and Agriculture Organization of the UN (FAO), Animal Production and Health Division; 2006. Poultry sector country review – Nigeria.https://www.fao.org/3/ai352e/ai352e.pdf Available at: accessed 23 September 2022. [Google Scholar]
- 31.Exchange Rates UK US Dollar to Nigerian Naira Spot Exchange Rates for 2020. https://www.exchangerates.org.uk/USD-NGN-spot-exchange-rates-history-2020.html Available at: accessed 20 September 2022.
- 32.The World Bank PPP conversion factor, GDP (LCU per international $) – Nigeria. 2022. https://data.worldbank.org/indicator/PA.NUS.PPP?locations=NG Available at: accessed 21 September 2022.
- 33.The World Bank Life expectancy at birth, total (years) – Nigeria. 2022. https://data.worldbank.org/indicator/SP.DYN.LE00.IN?locations=NG Available at: accessed 21 September 2022.
- 34.The World Bank GDP (current US$) – Nigeria. 2022. https://data.worldbank.org/indicator/NY.GDP.MKTP.CD?locations=NG&start=2010 Available at: accessed 21 September 2022.
- 35.Sasu D.D. Share of Gross Domestic Production (GDP) generated by the agricultural sector in Nigeria as of. 2020. https://www.statista.com/statistics/1207940/share-of-gdp-by-agricultural-sector-in-nigeria/ Available at:
- 36.Bamidele O., et al. Antimicrobial Usage in Smallholder Poultry Production in Nigeria. Vet. Med. Intl. 2022 doi: 10.1155/2022/7746144. Article ID 7746144. 12p. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Om C., McLaws M.L. Antibiotics: practice and opinions of Cambodian commercial farmers, animal feed retailers and veterinarians. Antimicrob. Resist. Infect. Control. 2016;5:42. doi: 10.1186/s13756-016-0147-y. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 38.Adebowale O., et al. Multi-drug resistant Escherichia coli, biosecurity and anti-microbial use in live bird markets, Abeokuta, Nigeria. Antibiotics. 2022;11(2):253. doi: 10.3390/antibiotics11020253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 39.Adeyemi O.O., et al. Acute gastroenteritis and the usage pattern of antibiotics and traditional herbal medications for its management in a Nigerian community. PLoS One. 2021;16(10) doi: 10.1371/journal.pone.0257837. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 40.Diao X., Alpuerto V., Nwafor N. IFPRI, ILRI and RVC; Washington DC: 2009. Economy-wide impact of avian flu in Nigeria: a dynamic CGE model analysis. HPAI Research Brief 15.http://orcid.org/0000-0003-4843-1670 Available at: accessed 27 February 2023. [Google Scholar]
- 41.Andam K.S., et al. International Food Policy Research Institute (IFPRI); Washington, DC: 2020. Estimating the economic costs of COVID-19 in Nigeria. NSSP Working Paper 63. accessed 27 February 2023. [DOI] [Google Scholar]
- 42.Jimoh A. In: Handbook of Disease Burdens and Quality of Life Measures. Preedy V.R., Watson R.R., editors. Springer; New York, NY: 2010. The economic burden of malaria in Nigeria and willingness to pay. [DOI] [Google Scholar]
- 43.Breman J.G., Alilio M.S., Mills A. In: The Intolerable Burden of Malaria II: What’s New, What’s Needed: Supplement to Volume 71(2) of the am J Trop Med Hyg. Breman J.G., Alilio M.S., Mills A., editors. American Society of Tropical Medicine and Hygiene; Northbrook (IL): 2004. The intolerable burden of malaria: what’s new, what’s needed. [Google Scholar]
- 44.Weintraub W.S., Cohen D.J. Limits of cost-effectiveness analysis. Circ. Cardiovasc. Quality Outcomes. 2009;2:55–58. doi: 10.1161/CIRCOUTCOMES.108.812321. [DOI] [PubMed] [Google Scholar]
- 45.Drummond M.F., et al. Oxford University Press; Oxford, England: 2015. Methods for the Economic Evaluation of Health Care Programmes. [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Supplementary Materials
Supplementary material 1. The following supporting information are available as supplementary materials:Table S1. Number by cases data; Table S2. Basic Check on data; Table S3. Total Loss; Table S4. Loss (Humans); Table S5. Salmonellosis Loss (Poultry); Table S6. Poultry population (2020 estimates); and Table S7. Human populations estimates for the year 2006, 2020 and 2022.
Supplementary material 2
Data Availability Statement
All data utilised in this work are open sourced in the various institutions' websites (Table 1) or on request from the Federal Ministries of Health, Agriculture or other mentioned Federal Agencies in Nigeria.