Preventive Veterinary Medicine 215 (2023) 105919 Contents lists available at ScienceDirect Preventive Veterinary Medicine journal homepage: www.elsevier.com/locate/prevetmed Access to vaccination services for priority ruminant livestock diseases in Ghana: Barriers and determinants of service utilization by farmers Francis Sena Nuvey a,b,*, Günther Fink a,c, Jan Hattendorf a,c, Gloria Ivy Mensah d, Kennedy Kwasi Addo d, Bassirou Bonfoh e, Jakob Zinsstag a,d a Swiss Tropical and Public Health Institute, Kreuzstrasse 2, 4123 Allschwil, Switzerland b Faculty of Medicine, University of Basel, Klingelbergstrasse 61, 4056 Basel, Switzerland c Faculty of Science, University of Basel, Klingelbergstrasse 50, 4056 Basel, Switzerland d Department of Bacteriology, Noguchi Memorial Institute for Medical Research, University of Ghana, Accra, P.O. Box LG 581, Ghana e Centre Suisse de Recherches Scientifiques en Côte d′Ivo ire, Abidjan BP 1303, Côte d′Ivoire A R T I C L E I N F O A B S T R A C T Keywords: Introduction: Livestock diseases are a major constraint to agricultural productivity, frequently causing significant Livestock livelihood losses for farmers, and negatively affecting public food safety and security. Vaccines provide an Livestock diseases effective and profitable means for controlling most infectious livestock diseases, but remain underutilized. This Livestock farmers study sought to assess the barriers and determinants of vaccination utilization for priority livestock diseases in Vaccination access Ghana. Methods: We conducted a mixed-method study involving a quantitative survey with ruminant livestock farmers (N = 350) and seven focus group discussions (FGD) involving 65 ruminant livestock farmers. The survey data were analyzed, and distribution of barriers to vaccination access described. We evaluated the determinants of vaccination utilization (any use of vaccination against contagious-bovine-pleuropneumonia (CBPP) and peste- des-petits-ruminants (PPR) in 2021) using logistic regression analyses at the 0.05 significance level. FGD tran- scripts were analyzed deductively. We used triangulation to achieve convergence across the different datasets and analyses. Results: The farmers kept an average (median) of 5 tropical livestock units (TLUs) of ruminant livestock (IQR=2.6–12.0) that were on average 8 kilometers (IQR=1.9–12.4) away from veterinary officers (VOs). Only 16% (56/350) of herds were vaccinated against the diseases. Most farmers (274/350) had limited knowledge on vaccines against CBPP and PPR infections, 63% (222/350) perceived low risk of these diseases to their herds. About half of farmers reported experiencing outbreaks of either disease in the study year (2021). Farmers scored on average 80.5 out of 98 (IQR=74–85) on the RS-14 resilience scale. After adjusting for farmers’ livestock rearing experience, herd size, sex, wealth status, distance to VOs, previous disease outbreaks, and perceived risk of the diseases, vaccination utilization was negatively associated with limited knowledge (aOR=0.19, 95% CI=0.08–0.43), and positively associated with personal exposure to outbreaks in the study year (aOR=5.26, 95% CI=2.01–13.7) and increasing resilience (aOR=1.13, 95%CI=1.07–1.19). FGDs revealed farmer misconceptions about vaccines, costs of vaccines, and timely access to vaccines from VOs as additional barriers. Conclusions: Acceptability, affordability, accessibility, and availability of vaccine services represent the main barriers to vaccines utilization by ruminant livestock farmers in Ghana. Given that limited knowledge regarding the value of vaccination and shortfalls in veterinary service supply are of central importance for both the demand and supply side, more collaboration between the different stakeholders in a transdisciplinary manner to effec- tively address the low vaccination utilization problem is needed. * Corresponding author at: Swiss Tropical and Public Health Institute, Kreuzstrasse 2, 4123 Allschwil, Switzerland. E-mail address: francis.nuvey@swisstph.ch (F.S. Nuvey). https://doi.org/10.1016/j.prevetmed.2023.105919 Received 16 February 2023; Received in revised form 3 April 2023; Accepted 9 April 2023 Available online 11 April 2023 0167-5877/© 2023 The Author(s). Published by Elsevier B.V. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 1. Introduction and PPR and Mange in sheep and goats based on previous research in Ghana (Nuvey et al., 2023), only CBPP in cattle and PPR in sheep and The production in the livestock sector accounts for about 40% of the goats have approved vaccines by the veterinary system in Ghana for agriculture sector’s gross domestic product in West Africa; the main their control (Diop et al., 2011). We therefore sought in this study to species reared being ruminants (cattle, sheep, and goats) and poultry identify ways to improve the utilization of these vaccines by farmers to (OECD and ECOWAS, 2008). Ruminants are mostly domesticated mitigate the occurrence and impact of these priority diseases. Identi- mammals with digestive systems that depend on pre-gastric retention of fying the barriers and determinants of farmers’ utilization of vaccination digesta associated with fermentation of plant materials by symbiotic services in the Ghanaian context is needed, to inform policy actions microorganisms (Stover et al., 2016). Mobility in search for optimal towards achieving this goal. grazing resources for the animals, known as transhumance, is an essential part of livestock farming, particularly for cattle farmers. 2. Materials and methods Although these animal movements can be predicted due to their sea- sonality, the national borders have not been able to adequately prevent 2.1. Description of study area unapproved animal movements in the region. Thus, there is a high level of interaction between the transhumance and local herds, leading to the The study was conducted in the Mion, Pru East and Kwahu Afram frequent introduction and spread of pathogens across borders (Motta Plains South (KAPS) Districts, which are representative of the northern, et al., 2017; Apolloni et al., 2019). middle and southern farming belts of Ghana. The three districts lie in the Livestock diseases impose significant costs on the livestock sector Guinea Savannah, Transition and Deciduous forest Vegetation zones through animal deaths, disease control costs, and restrictions on animal respectively that are the main livestock production zones in Ghana (GSS, trade (Grace et al., 2015; Nuvey et al., 2022a). At the individual farmer 2014a; b, c) (Fig. 1). Ghana has a population of 31 million people; with a level, the diseases cause significant livelihood losses for households sex ratio of 97 males for every 100 females, of which about 60% are (Pradère, 2014; Huntington et al., 2021), affecting their domestic food economically active. A higher share of males (64%) than females (53%) security (Dominguez-Salas et al., 2019; Nuvey et al., 2022b), and psy- engage in economic activity in the country. Unemployment rate is 13% chosocial wellbeing (Mort et al., 2005; Nuvey et al., 2020). While the among the economically active population (GSS, 2021). The annual public is affected potentially unsafe food, due to misuse of antimicro- average household per capita income is GHC 11,694 (USD 1949) [GHC bials in livestock production entering the food chain (Kimera et al., is Ghanaian Cedis: USD 1 ≈ GHC 6 at the time of the survey (Bank of 2020; Mshana et al., 2021), and heightened food insecurity from a Ghana, 2021)]; with significantly higher per capita income for urban reduction in the productivity of diseased animals (Herrero et al., 2013). dwellers [GHC 16,373 (USD 2729)] compared to rural dwellers [GHC For the most part, the livestock diseases with the most severe impact are 5880 (USD 980)] (GSS, 2019). The agricultural sector contributes about transboundary in nature (Islam et al., 2013; Clemmons et al., 2021). 20% to the country’s gross domestic product. For most households, These transboundary diseases are highly contagious animal diseases, agricultural activity mainly entail the cultivation of crops and livestock whose epidemiology may differ across countries; they occur mainly as rearing (GSS, 2020b). epidemics, but could also become endemic in the ecosystems of affected The selected districts are mainly rural and agrarian, with about one- countries (Otte et al., 2004). In the West African region, the diseases third of the livestock holdings of households being ruminant species. with the highest impact on countries includes Newcastle disease (ND) in The primary ruminant livestock species reared by farmers are cattle, poultry, peste-des-petits-ruminants (PPR) in sheep and goats, contagious sheep, and goats. The primary non-ruminant livestock species reared are bovine pleuropneumonia (CBPP) in cattle, and African swine fever (ASF) poultry, pigs, and rabbits. The majority of the livestock rearing (53%) is in pigs (Otte et al., 2004; Fadiga et al., 2013). for income generation – the rest is directly consumed by the household. In Ghana, the livestock sector provides employment for about 10% of The livestock production system is largely extensive and dominated by the country’s population, with about 20% of livestock holders being small-scale farmers (GSS, 2020a). In Ghana, vaccination services for women. About 80% of livestock farmers are rural dwellers, who keep livestock are provided mainly by government employed veterinary of- 60% of the 18 million heads of livestock (GSS, 2021). Livestock pro- ficers (VOs), and is usually done from farm to farm. The VOs providing duction is dominated by smallholder farmers practicing the extensive veterinary services including vaccination in rural areas, where livestock system of rearing. Aside from poultry (74%), ruminant livestock rearing are usually reared, are mainly veterinary paraprofessionals with a constitute the other significant proportion (21%) of livestock holdings of diploma degree (equivalent to three years of training) in animal health households engaged in livestock production (GSS, 2020a). The livestock as a minimum qualification. The VOs work under the direct supervision sector in Ghana similar to other countries in the West African region, of district or regional veterinarians (usually with a doctor of veterinary faces challenges with transboundary animal diseases. In a previous medicine qualification) (Diop et al., 2011). study, the livestock farmers and veterinary service providers identified FMD and CBPP in cattle, and PPR and Mange in sheep and goats as priority diseases affecting ruminant livestock productivity, causing an 2.2. Study design average of 10% (and up to 70%) of herd losses per year. The farmers mainly use treatment services for managing diseases, most of which This was a cross-sectional study which employed a convergent par- service is provided by informal persons who are not supervised by the allel mixed-method research approach. This study design enabled us to veterinary system or the treatment is done by farmers themselves. In conduct both quantitative and qualitative elements of the research addition, the medicines applied by the farmers are not useful for the project during the same phase of the research process. Although the conditions treated in most cases (Nuvey et al., 2023). An effective con- analysis of data is conducted separately for each method, the results trol of these priority livestock diseases is therefore critical to sustaining have equal weighting and are interpreted jointly (Creswell and Clark, the livelihoods and wellbeing of farmers on one hand, and the food 2018). We conducted a cross-sectional survey involving 350 ruminant safety and security of the population on the other hand. livestock farming households, as well as seven focus group discussions Preventive veterinary services particularly vaccination have been (FGDs) involving 65 ruminant livestock farmers purposively selected shown to be both effective and profitable in controlling livestock dis- within the study area. A household refers to a person or group of persons eases (Charlier et al., 2022; Nuvey et al., 2022a). However, vaccines who normally live together and are catered for as one unit; members supply and utilization rates by farmers in many sub-Saharan African may or may not be related. Any member of the household who takes countries including Ghana remain very low (Donadeu et al., 2019; OIE, responsibility for the upkeep of the livestock kept by the household was 2019). Among the reported priority diseases; FMD and CBPP in cattle, eligible to participate in the study. 2 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 Fig. 1. Administrative map of Ghana showing the agro-ecological zones and study districts. (The figure shows the district-level administrative and ago-ecological map of Ghana. It presents the distinct locations of the study districts (shaded areas to which arrows point) within the main agro-ecological zones. MION, PRU EAST, and KAPS denote the Mion, Pru East and Kwahu Afram Plains South Districts respectively.) 2.3. Study population and Pru East Districts respectively, with an average of about 10 holdings per household. We randomly drew 15 villages in the KAPS District, and In the survey, we firstly obtained district maps and created a sam- 10 villages each in the Pru East and Mion Districts, proportional to the pling frame of villages within the study area to be sampled for data number of livestock farming households per district (GSS, 2014a; b, c). collection. Based on the population and housing census data available From the selected villages, at least two persons were approached per prior to the study, there were about 80880, 54694, 47230 tropical village to participate in FGDs organized after the surveys in each study livestock units (TLUs) of ruminant livestock species in the KAPS, Mion district. Seven FGDs were conducted involving 65 participants in the 3 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 study area. between 1 and 7, and higher scores indicative of higher resilience. We used the median split approach to categorize knowledge and perception 2.4. Sample size and sampling technique scale scores (Iacobucci et al., 2015), with scores above the median corresponding to good knowledge and good perception respectively, and The sample size was determined using Epi Info version 7 (Dean et al., lower scores otherwise. We adapted the access framework proposed by 2011) with the following assumptions: Expected vaccination utilization (Obrist et al., 2007), for each of the reported barriers to vaccination rate of 10% was estimated based on previously reported vaccination utilization, to determine the applicable dimension of access they fit. utilization rates in the West African region (Dione et al., 2017; ElArbi Based on the observed distribution in each dimension, we could deter- et al., 2019). The acceptable margin of error was 5%, at a 95% confi- mine the access dimension(s) to be prioritized for interventions to dence level. With an assumed average of eight subjects per cluster (m) improve vaccination utilization by ruminant livestock farmers. We and an intra-cluster correlation coefficient (ICC) of 0.2, the design effect compared the access dimension distribution among the households by of the study was 2.4 To reach a margin of error of 5%, a sample size of study district. 350 livestock farmers was required. We recruited 350 livestock farmers In a pre-specified model, we evaluated the relationship between from 38 villages using random segmentation. In villages where sufficient vaccination use (any use of vaccination in the past 12 months) to protect households were not realized, the adjoining village was selected for livestock against contagious bovine pleuropneumonia (CBPP) and peste- sampling of the remainder of households missed. For the FGDs, we used des-petits-ruminants (PPR), and farmers’ sex, herd size, wealth status, a purposive sampling approach to recruit farmers during the survey in resilience level, experience with livestock rearing, distance to VOs, each district. The farmers who consented to participate in FGDs in the perception of the diseases risk to herds, previous and current history of three districts were 65. outbreaks of the diseases in herds, and knowledge level of vaccination against the diseases, adjusting for clustering at the village level, at the 2.5. Data collection and data management 95% confidence level in a logistic regression model. We presented crude (cOR) and adjusted odds ratios (aOR) with their respective 95% confi- The enumeration team visited the households rearing ruminant dence intervals (CI) for univariable and multivariable analyses livestock in their homes to conduct the survey between November 2021 respectively. and January 2022. The survey questionnaires were administered to the The analysis of FGD transcripts was performed from a social respondents’ face-to-face using tablets with Open Data Kit (ODK) constructivism viewpoint, as we understood agricultural (livestock) application. The survey instruments collected data on farmers’ previous production to entail the social and cultural creations of those involved. and current history of experiencing outbreaks of the priority diseases We sought to find convergence on farmers’ perception of the risk of the (CBPP and PPR) in herds, perception of the risk of the diseases to herds, priority diseases to their herds, level of knowledge on vaccination utilization of vaccination services, barriers to service utilization, against the diseases, the challenges that farmers face in accessing knowledge of vaccines to protect herds against the diseases, and other vaccination services, and to identify ways to address these challenges to socio-demographic characteristics of the participating farmers. Knowl- improve vaccination uptake. We conducted thematic analysis of the edge level was assessed based on farmers’ responses to questions on the transcripts deductively, by generating codes and categories from the raw vaccines’ functions and effectiveness, required frequency of use, pro- transcript texts, based on the study objectives. We present the results as tection offered to animals, and places to acquire the vaccines when narratives supported by verbatim quotes with clarification phrases needed. Correct responses yielded a score of 1 while wrong responses where required for quotes, placed in square brackets. yielded a score of zero (0). Perception of the diseases risk to herds was assessed on a five-item Likert scale with responses ranging from 1 to 5; 3. Results higher scores denote higher risk perception of the diseases to a herd, one item’s score (Q4) is reversed to achieve a similar direction of perception 3.1. Characteristics of the study respondents score (Additional file 1). The FGDs were conducted during the same period at designated Table 1 presents a summary of the obtained household survey data in venues in the study districts using a paper-based interview guide, and the study area. On average (median), farmers participating in the survey the FGD sessions were recorded using an audiotape. The farmers dis- (N = 350) were 45 years old (IQR = 35–54). The farmers reported cussed in the FGDs their experiences with the outbreaks of the priority rearing livestock for an average 9 years (IQR = 6–15), with households diseases, awareness of vaccines for protecting herds against the priority keeping on average of 5 TLUs of ruminant livestock (IQR = 2.6–12); diseases, vaccine utilization and effectiveness in protecting livestock, including cattle, goats, and sheep in their herds. More than two-thirds main constraints of vaccination access and utilization, and the potential (71%) of the farmers were male. The farmer households were 8 kilo- measures to improve vaccine uptake. meters (IQR = 1.9–12.4) away from their veterinary service providers The survey data were downloaded in Microsoft Excel format from (VOs) on average. Households’ wealth index differed significantly be- ODK and imported into Stata version 16 (StataCorp, 2019) for analyses. tween study districts (p < 0.001), with Mion (59%) and Pru East (69%) The interview audio recordings from the FGDs were transcribed Districts having the highest proportion of the poorest and least poor verbatim, and the transcripts were imported into NVivo software version households respectively. Furthermore, the farmers scored an average 12 (QSR International Pty Ltd, 2018) for analysis. resilience score of 80.5 out of 98 (IQR = 74–85), with the average resilience scores highest in the Mion District (82.5), and lowest in the 2.6. Data analyses KAPS District (78.0). Table 1 also shows that the farmers scored an average of 19 out of 25 We performed descriptive analyses of the survey data, comparing the (IQR = 17–21) on the perception scale, and 3 out of 5 (IQR = 2–3) on the distribution of farmers’ responses by study district. The farmers’ herd knowledge scale. Only 22% (76/350) of the farmers had good knowl- sizes were converted to tropical livestock units (TLU) to standardize edge of vaccines (score above the median knowledge score) to protect livestock holdings as follows: 1 TLU corresponds to 1 cattle or 5 small their herds against contagious bovine pleuropneumonia (CBPP) and/ or ruminants (sheep and goats) (Njuki et al., 2011). We determined the peste-des-petits-ruminants (PPR) infections. Also, only 37% (128/350) relative wealth of households using an index of a household’s ownership of the farmers perceived a high risk of CBPP and/or PPR infections to of selected assets, such as televisions, refrigerators and bicycles (ICF, their herds. About 47% (164/350) of households experienced either 2019). Resilience was assessed using the Resilience scale (RS-14) CBPP (49%, 43/87) or PPR (46%, 155/338) outbreaks in the study year. (Wagnild, 2009). The RS-14 is a 14 item Likert-scale with scores ranging The farmers participating in the focus group discussions (FGDs) 4 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 Table 1 3.2. Utilization of vaccination services against priority diseases Summary of data collected from household survey by study district (N = 350). Characteristic KAPS MION PRU EAST We found that only 18% (65/350) of households had ever vaccinated Socio-demographic n Median Median Median their herds against CBPP and/or PPR before the study year. In the study characteristics (IQR) (IQR) (IQR) year (2021), only 16% (56/350) of farmers had vaccinated their herds Livestock farming 9 (5.0 – 10 (6.0 – 9 (5.0 – against these priority diseases (Table 1). The previous and present experience (years) 16.0) 17.0) 15.0) vaccination utilization rates were significantly different between the Distance to veterinary 12.0 (8.0 – 6.9 (1.6 – 1.9 (0.6 – study districts (p < 0.001). service (km) 14.4) 12.7) 5.6) Resilience level 78 (73.0 – 82.5 (78.0 – 81 (75.0 – We present the determinants of current vaccination utilization by the 84.0) 87.0) 86.0) farmers in Table 2. In our pre-specified univariable models, we found Knowledge of CBPP and/or 3 (2.0 – 3 (3.0 – 3.0) 3 (3.0 – positive associations between farmers utilizing vaccination and years of PPR vaccines 4.0) 4.0) experience with livestock rearing (cOR = 1.04, 95% CI = 1.01 – 1.08, Perception of CBPP and/or 19 (17.0 – 18 (17 – 20) 18 (16.0 – p = 0.02), farmers’ resilience (cOR = 1.12, 95% CI = 1.06 – 1.18, PPR disease risk 21.0) 21.0) % (n/N) % (n/N) % (n/N) p < 0.001), herd size (cOR = 2.34, 95% CI = 1.59 – 3.44, p < 0.001), Sex male sex (cOR = 2.10, 95% CI = 1.01 – 4.33, p = 0.04), wealth status Female 102 38% (57/ 16% (16/ 28% (29/ 149) 98) 103) Male 248 62% (92/ 84% (82/ 72% (74/ Table 2 149) 98) 103) Determinants of livestock farmers’ utilization of vaccination services against Wealth status quintiles priority ruminant livestock diseases in Ghana (N = 350). Poorest 70 14% (21/ 42% (41/ 8% (8/ 149) 98) 103) Unadjusted model Adjusted model Below average 74 28% (41/ 26% (25/ 8% (8/ Variables cOR (95% P-value aOR (95% P-value 149) 98) 103) CI) CI) Average 66 24% (36/ 14% (14/ 15% (16/ 149) 98) 103) Livestock farming 1.04 (1.01, 0.02 1.02 (0.97, 0.40 Above average 70 25% (37/ 10% (10/ 22% (23/ experience (years) 1.08) 1.08) 149) 98) 103) Distance to veterinary 0.90 (0.86, < 0.001 0.93 (0.85, 0.08 Least poor 70 9% (14/ 8% (8/98) 47% (48/ service (km) 0.95) 1.01) 149) 103) Resilience level 1.12 (1.06, < 0.001 1.13 (1.07, < 0.001 Herd size (Tropical 1.18) 1.19) Livestock Units) Herd size (TLU) Small (1st tertile: 0.6 – 3.2 127 42% (62/ 43% (42/ 23% (24/ Small (1st tertile) ref ref TLUs) 149) 98) 103) Medium (2nd tertile) 2.01 (0.83, 0.12 0.94 (0.35, 0.90 Medium (2nd tertile: 3.4 – 107 31% (46/ 25% (25/ 34% (35/ 4.85) 2.52) 8.2 TLUs) 149) 98) 103) Large (3rd tertile) 5.26 (2.39, < 0.001 1.34 (0.45, 0.60 Large (3rd tertile: 8.4 – 116 27% (41/ 32% (31/ 43% (44/ 11.6) 3.99) 249.8 TLUs) 149) 98) 103) Sex Utilization of CBPP and Female ref ref PPR vaccinationa Male 2.10 (1.01, 0.04 1.43 (0.63, 0.39 Past herd vaccination against 65 29% (43/ 13% (13/ 9% (9/ 4.33) 3.24) CBPP and/or PPR 149) 98) 103) Wealth status Current herd vaccination 56 4% (6/149) 14% (14/ 35% (36/ Poorest ref ref against CBPP and/or PPR 98) 103) Below average 0.94 (0.31, 0.91 1.61 (0.47, 0.45 History of CBPP and/or PPR 2.83) 5.77) outbreak in herdsb Average 1.07 (0.35, 0.91 1.26 (0.35, 0.73 Previous history of CBPP 159 35% (52/ 48% (47/ 58% (60/ 3.23) 4.53) and/or PPR outbreak 149) 98) 103) Above average 1.33 (0.47, 0.60 1.03 (0.27, 0.96 Present history of CBPP and/ 164 31% (46/ 41% (40/ 76% (78/ 3.79) 3.94) or PPR outbreak 149) 98) 103) Least poor 5.32 (2.12, < 0.001 2.51 (0.84, 0.10 13.3) 7.51) Percentages (%) are the proportion of ruminant livestock farmers within each Herd history of CBPP/PPR characteristic explored per study district sub-sample (N). Numbers (n) of outbreak* households, falling into each sub-category of assessed characteristics within the History of CBPP/PPR 3.68 (1.96, < 0.001 1.16 (0.48, 0.74 study districts; KAPS: households from the Kwahu Afram Plains South District, outbreak in herd 6.87) 2.81) MION: households from the Mion District and PRU EAST: households from the Present (2021) CBPP/PPR 5.32 (2.70, < 0.001 5.17 (1.96, 0.001 outbreak in herd 10.5) 13.7) Pru East District in Ghana. For continuous variables, the median with corre- Knowledge of CBPP and/or sponding lower and upper quartile values are reported in parentheses. CBPP PPR vaccines denotes contagious bovine pleuropneumonia infection in cattle, and PPR de- Good ref ref notes peste-des-petits-ruminants infection in sheep and/ or goats. aFor the uti- Limited 0.18 (0.10, < 0.001 0.18 (0.07, < 0.001 lization of CBPP/PPR vaccinations, non-use of the vaccines by a household in the 0.33) 0.42) past years (before 2021) and non-use of the vaccines in the study year (2021) Perception of CBPP and/or were the reference categories respectively in each case. bFor the herd history of PPR disease risk CBPP/PPR outbreak, non-experience of an outbreak in herd in the previous years High ref ref (before 2021) and non-experience of an outbreak in the study year (2021) were Low 0.47 (0.27, 0.01 1.76 (0.95, 0.07 0.84) 3.24) the reference categories respectively. Variables included as predictors of the current utilization of professional vet- (N 65) reared on average 5.2 TLUs (IQR 32.4 TLUs) of ruminant erinary services by livestock farmers in Ghana. Crude odds ratio (cOR) with 95% = = livestock per herd. Most of the participating farmers were male (85%), Confidence Intervals (CI) and the associated p-values for the unadjusted model and adjusted odds ratio (aOR) with 95% CI and the associated p-values for the and about (60%) of the farmers had at least some basic formal adjusted model, accounting for clustering during sampling of respondents. ‘ref’ education. denotes the reference category. * For the herd history of CBPP/PPR outbreak, non-experience of an outbreak in a household’s herd in the past years (before 2021) and non-experience of an outbreak in the study year (2021) were the reference categories respectively in each case. 5 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 (cOR = 1.58, 95% CI = 1.27 – 1.98, p < 0.001), and previous (cOR = honest, even if the animal is infected, it won’t die. And the phlegm 3.68, 95% CI = 1.96 – 6.87, p < 0.001) and current history (cOR = 5.32, [mucous discharge] that comes out of their head [via nostrils], is 95% CI = 2.70 – 10.5, p < 0.001) of disease (CBPP and/or PPR) reduced. At times, when the disease comes, it often doesn’t affect outbreak in a herd. There was a negative association between vaccina- them. And even if they get infected by it, it takes only about two to tion use and distance between the livestock farming households and VOs three days and then it resolves. So, it [vaccine] protects them [sheep (cOR = 0.90, 95% CI = 0.86 – 0.95, p < 0.001), perception of low risk of and goats] against the different kinds of diseases that we mentioned. CBPP and/or PPR infection to herds (cOR = 0.47, 95% CI = 0.27 – 0.84, So, as for the vaccination, it is very very important, ahaa.” (Female p = 0.01), and limited knowledge of CBPP and/or PPR vaccines (cOR = farmer, 46 years old, KAPS District) 0.18, 95% CI = 0.10 – 0.33, p < 0.001). After adjusting for the covariates described above, we found positive “Vaccinations are usually very helpful; they protect the animals very associations between vaccination use and farmers’ resilience (aOR well against those diseases [CBPP and PPR]. Even when you’re = 1.13, 95% CI = 1.07 – 1.19, p < 0.001), and personal experience of an doubtful whether there is an outbreak among your animals or not, outbreak of the diseases (CBPP and/or PPR) in the study year (aoR and you call for vaccination, only those animals which have already = 5.17, 95% CI 1.96 – 13.7, p 0.001). While vaccination use was contracted the disease are badly affected, and those vaccinated = < negatively associated with farmers’ limited knowledge of vaccines to before contracting the disease are usually safe.” (Male farmer, 41 protect their livestock herds against diseases (aOR 0.18, 95% CI years old, Mion District). = = 0.07 – 0.42, p < 0.001). “What I observed is that the older ones [bucks, does, ewes, and rams] In the FGDs we similarly found that farmer knowledge of vaccination that I vaccinated were not affected by the disease [PPR] when it against these priority diseases and self-conviction or willingness to came. But the young ones [kids and lambs] that were given birth to protect assets (resilience), influences greatly the utilization of vaccina- afterwards, it was not yet time for them to be vaccinated, so they tion services. Thus, mere provision of information about vaccination were the ones that the disease normally infected.” (Male farmer, 32 availability to the farmers is not sufficient. There are also significant years old, Pru East District) misconceptions about vaccine effectiveness, particularly during an active disease outbreak. Thus, farmers generally only seek to protect their animals when they hear about or experienced the disease 3.3. Barriers to the utilization of vaccination services outbreaks. “For me I have only heard about the vaccine that prevents CBPP. I We applied the access framework proposed by Obrist et al. (2007), to know that it will be good for us to take that CBPP vaccine, but if the identify the barriers to farmers accessing vaccination services against disease [CBPP] is already in the kraal [an enclosure or pen where the infectious livestock diseases in general. Our results showed that the main farmers’ animals or herd is kept] and you go ahead to vaccinate bottlenecks were in the acceptability (59%), affordability (53%), them, it would kill most of them. So, for me, I have stopped vacci- accessibility (42%), and availability (34%) dimensions of the access nating my cattle, because if they are already infected and you framework (Table 3). The barriers were somewhat district specific. The vaccinate [them], some may die.” (Male farmer, 46 years old, proportion of households reporting challenges for each dimension was KAPS District) highest in the KAPS district in all the dimensions except for affordability (Fig. 2). Affordability as a barrier was highest for farmers in the Pru East “Some time back, the veterinary officer reached out and explained to us about the vaccine that could protect our animals before the dis- ease [PPR] comes. During that time when he [veterinary officer] said Table 3 that, I also vaccinated my animals…, it protected them against the Barriers to households’ access to vaccination against ruminant livestock diseases. disease [PPR].” (Male farmer, 40 years old, Pru East District) Access Measure Prevalence “I also do similar as she [another farmer participant] said. If the dimension disease doesn’t infect your animals…, even if the veterinary officer is Acceptability Information on service is unaligned with values 59% (210/ talking about vaccinating them against the disease, you are not too and practices of users 350) worried about it. But when you see the infection with your own eyes Service is not perceived by users as valuable to [pauses]. For me, I don’t normally do it unless I see that the disease livestock farming has infected them… Even when he [veterinary officer] brings the Affordability Users had inadequate funds (money) to use the 53% (187/ service when provided 350) vaccines and asks us to vaccinate the animals, most of the farmers Users had inadequate time to participate when don’t take it seriously. We’ll hear the announcement that we should services were provided mobilize ourselves to come and vaccinate our animals, but we don’t Accessibility Service provider is distant (far) from the users 42% (148/ take it seriously… So, we the farmers; we do not have that spirit 350) Service provider is unreachable to users when [willingness] to vaccinate our animals.” (Male farmer, 59 years service was needed old, KAPS District) Availability Service is unavailable with the provider when 34% (119/ required by the user 350) Despite the low patronage of vaccination services, we found that Service offered by the provider is insufficient to many of the farmers that utilize the vaccination services mostly had meet the user’s needs positive outcomes of protection for their animals, comparing those with Adequacy Quality of service provided did not meet the 4% (17/350) and without vaccination use. Few farmers reported negative outcomes. user’s expectation User is dissatisfied with the attitude of service “With that medicine [vaccine], if you inject the animals before the provider disease [PPR] comes, it [vaccine] protects them from being infected Measures depict the indicators obtained in survey as barriers to service utiliza- by the disease, and also from dying from it. But now that we don’t tion. Service refers to vaccination against contagious bovine pleuropneumonia inject them with that medicine [vaccine] before it [PPR] comes, it (CBPP) in cattle, and/or peste-des-petits-ruminants (PPR) infection in sheep kills many of our animals.” (Male farmer, 54 years old, KAPS and/ or goats. Service providers are public employed veterinary officers deliv- District) ering veterinary services in study districts. Users are ruminant livestock farming households (rearing any of cattle, sheep and or goat) in the study districts. When he [veterinary officer] vaccinates them [sheep and goats] Prevalence denotes the proportion of households reporting at least one of the against the diarrheal disease [PPR], and there is an outbreak, to be indicators as barriers to their access to vaccination in any given farming year. 6 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 Fig. 2. Access dimensions influencing vaccination utilization by livestock farmers in Ghana by district. (The figure shows the access dimensions influencing farmers’ utilization of vaccination services against infectious diseases in livestock in Ghana. The color differences depict each study district. The point positions on the radar chart corresponds to the proportion of farmers reporting barriers that fall within each of the access dimensions.) District (63%), compared to the other districts. The Mion District had and the veterinary people [officers] talk about that [vaccination], it acceptability as the main barrier (64%). In the KAPS District, accessi- appears as though they [veterinary officers] are basically trying hard bility was the main barrier (69%), followed by acceptability (64%), to make money from us the farmers rather than the intended pro- availability (60%), and affordability (56%). Adequacy was not much of a tection the veterinary officers’ vaccination would offer against ani- barrier for the farmers. We also found the barriers to vaccination access mal losses. It’s a big challenge.” (Male farmer, 41 years old, Mion to be gendered; whereby the proportion of female farmers reporting District). barriers to access was higher in all dimensions compared to males. We did not find marked differences in barriers to access stratified by age “I remember that some time ago an announcement was made that we categories and marital status of the farmers (Additional file 2). should come together as livestock farmers for a vaccination exercise. The discussions with the farmers similarly affirm the demand side They said that, when a vial of vaccine is opened, unless he [veteri- barriers of acceptability and affordability. Farmers frequently do not nary officer] uses all [vaccine doses] in a day. We were told that for consider vaccination against infectious diseases as a part of livestock some of the medicine [vaccine], it must be used to inject hundred farming. Even when the farmers are informed and willing to utilize (100) animals [cattle] and for others, fifty (50) animals [goats and vaccination, the requirement by VOs to have sufficient animals per vial sheep]. So, as we were thinking about it, whether to participate, of vaccine [100 cattle for CBPP, and 50 sheep or goats for PPR] before someone [a farmer] was saying that the veterinary officer had gone vaccine vials are administered, is a disincentive for farmers whose herds to buy his medicines that he was planning to come and sell…, but are not sufficiently large, unless they can get other farmers to participate because they were about to expire; and he doesn’t know what to do or offer to pay for the unused doses of vaccines. There are also farmers with them, that was why he wanted to come and inject our animals. who nevertheless, do not consider vaccination a priority enough to It made some of us who were willing then to vaccinate our animals to spend their resources on it. In the study year, average vaccination cost have a change of mind. So that is part of the reasons why some were GHC 6 (USD 1) and GHC 5 (USD 0.83) for CBBP and PPR [farmers] don’t vaccinate their animals before the diseases come.” respectively. (Male farmer, 37 years old, KAPS District) “…If the animal is not sick, why should I spend my money to “Usually, the veterinary officers come to inform us about these vaccinate the animal? Myself sitting here, I’m sick, and I need money vaccines. But when you go to ask them [veterinary officers], they tell to treat myself [laughs], and to talk of the animal. If the animal gets you that after opening the vaccine vial, he needs to inject a lot of the infected by the disease [PPR] today, I don’t have money, so why animals at a go, from one animal to another until the vial is finished, should I use money to vaccinate an animal that is not ill [diseased]. so it doesn’t go to waste., It can be that on a date [scheduled] we all How about me myself?” (Male farmer, 40 years old, KAPS agreed to inject [vaccinate] our animals, maybe your friend [farmer] District). does not have the money to do it,…, so he [veterinary officer] would not be able to administer it [vaccine] to your animals” (Male famer, “Majority of us have no education on the importance of preventive 60 years old, Pru East District) veterinary services like vaccination… Some farmers do think their cattle are healthy and need no treatment. So, when the time comes Aside the demand side barriers, some farmers also reported supply 7 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 side barriers regarding the accessibility, availability, and adequacy of “Like he [another farmer participant] said, I think we those livestock the vaccination services offered. farmers living in one area [village], have to form a union or an as- “Sometimes, even if one [a farmer] gets the money today [for sociation. So that when we have this group, then we could say, all vaccination] but is not able to access the veterinary officers, you will those who have these kind of animals, we want to vaccinate the end up spending the money. Later when they [veterinary officers] animals this year so that they are not infected by these diseases… show up, what can you do? You will not be able to participate in the When the association meets and decides on a particular date, then we vaccination for the animals.” (Female famer, 46 years old, Mion can go and call the veterinary officer, for him to come and vaccinate District) our animals. When we join and there is understanding, it would help us all… Because when you leave your own animals and someone else “In times past, the veterinary officers would come around to vacci- vaccinates their own, the disease could infect your animals and could nate our animals yearly. But nowadays it is no longer so…, in fact spread to other animals in the area, or in some cases, it could affect because the veterinary officers are few, we don’t get them [animals] all of us.” (Female farmer, 62 years old, Pru East District) vaccinated regularly… Because we don’t get the vaccines on time… You need access to the vaccine every year to give them [animals], so “I also do support the suggestion that it should be made compulsory you can protect them. By the time the next vaccination period is that everyone undertakes the vaccination of their animals. I believe if approaching, the veterinary officer would say he is going to Accra we have a mandatory regulation that it is enforceable in the com- [360 km from district] to get the vaccines, so organize yourself and munity,… so that if you don’t vaccinate your animals, you would be get other people to also take the vaccine. But where am I going to get caught and sanctioned,…, you won’t be permitted to keep livestock, them? Maybe the other farmer is doing something on his own and I and your farm would be closed to serve as a deterrent.” (Male famer, also on my own. But if it was possible that if you have only 20 cattle, 48 years old, KAPS District) the veterinary officer can just vaccinate your animals and do similar for other farmers, then all the time we could vaccinate to protect 4. Discussion them [animals]. But we don’t get it that way.” (Male farmer, 46 years old, KAPS District) Infectious livestock diseases significantly reduce the productivity in “For me I have a veterinary man [officer] who usually treat my an- the livestock sector, which negatively affects farmers’ livelihoods and imals for me. So maybe on the day the veterinary officers come for a wellbeing, and public food safety and security. Although vaccination has vaccination exercise, I may have already spent the money on treating been shown to be effective and provide high returns on investment, the animals or the veterinary man who sees my animal is not part of farmers’ utilization of vaccination services for livestock diseases remain the exercise…, so therefore I would not be able to participate in the very low in many sub-Saharan African countries. In this study, we aimed vaccination.” (Male farmer, 53 years old, Mion District) to identity the barriers and determinants of farmers’ utilization of vaccination against priority diseases for the livestock sector in Ghana. The farmers argued that increased community engagements by VOs We implemented a convergent parallel mixed-method design to achieve on the value of vaccinations and discounting of vaccination costs, and this goal. Our results suggest that the utilization of vaccination services legislation by local authorities, as well as community mobilization by by farmers is mainly influenced by the service costs, and farmers’ farmers, would improve vaccination adoption and use. experience of disease outbreaks in herds, knowledge level of vaccines, “When there is a vaccination exercise, we only want to have the and resilience to adversity and motivation levels. information about the exercise in good time. The veterinary officers Previous studies among livestock farmers in East Africa made similar should give the scheduled times that they would always call on us for findings, where factors including cultural norms, farmers’ knowledge of education on the vaccination exercises. When veterinary officers disease and vaccines, history of disease occurrence in herds, vaccine organize it and get us involved, then we can spread the message costs, and distance to vaccine sources influenced households’ utilization among ourselves… I believe that if the education is done on media of vaccination services (Mutua et al., 2019; Mukamana et al., 2022; platforms like radio and television, it would be great. Because even if Williams et al., 2022). A study also showed that socio-cultural factors a farmer is not able to get the time to listen to the education, at least including age, sex, ethnicity, marital status, geographic location, phys- some people in the community who are fortunate to follow the dis- ical ability and education influence access to vaccination in Uganda cussion on the media platform, can share what they heard or learnt (Acosta et al., 2022). We found similar influences on vaccination access for others to benefit as well. If that is done, all the farmers who never of sex, farmers’ experience, wealth status, and distance to veterinary paid attention to vaccination would bring back their attention and services in our unadjusted model. Although the acceptability, afford- enhance the patronage…. Because for example, if I know the ability, accessibility, and availability of vaccines mainly constrain importance [of vaccination] and I have to vaccinate my animals farmers’ access, the increased engagement of veterinary personnel (VOs) against a disease and I have 3 animals, I can sell one to cater for with the farmers on the usefulness of vaccinations and discounting of [protect] the other two.” (Male farmer, 41 years old, Mion vaccination costs as well as community mobilization, have been pro- District) posed to have the potential to improve uptake and utilization of vacci- nation services. In addition to these, farmers proposed implementation “Nowadays you can’t get the medicine [vaccine] free [like in the of legislation to compel participation. This approach however is likely to past]. But they [veterinary officers] should give us a moderate price. be counterproductive if awareness and confidence in vaccines are not If the price is moderate, we can easily afford. So, if government can improved first (Brewer et al., 2017). help us so that the medicine [vaccine] will come; and if every year, Farmers’ decision to utilize vaccination could be treated as a discrete we are supposed to pay a certain amount of money to the govern- choice problem based on the random utility theory (Hensher et al., ment so that they [veterinary officers] will vaccinate our animal for 2005), whereby the utility a farmer derives from participating in a us, that is better. For you to pay money, for your animal to stay vaccination exercise would be the sum of the utility derived from the healthy, is better than when the diseases infects the animals, and you characteristics of the vaccination program. Thus, it is intuitive that all don’t get money to buy medicines to treat them, then they all die. things being equal, improving farmers’ awareness on vaccination as an That would mean that we are working in vain. If we are able to pay effective and profitable control measure against infectious diseases something small every year, for them to come to inject the animals could address most of the demand side barriers of access (acceptability for us, I think that would help us.” (Male famer, 54 years old, KAPS and affordability). More so, we found the limited knowledge of the District) effectiveness of vaccines, particularly during active disease outbreaks as 8 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 the main driver of farmers’ misconceptions about vaccines and unwill- 5. Conclusion ingness to invest resources in vaccinating their herds during the FGDs. The farmers showed in the survey and FGDs that they were more Our study shows that limited knowledge of the effectiveness and knowledgeable particularly on where the vaccines for protecting the profitability of vaccines, lack of timely access to vaccines and the cost of herds could be accessed and on the concept of herd immunity offered by vaccination services discourage farmers’ utilization of vaccination to vaccination. protect their livestock herds against priority infectious diseases, while Government subsidies are often used to incentivize adoption of increased resilience to adversity as well as the experience of diseases in vaccination in some contexts (Mongoh et al., 2008; China, 2017; herds are positively associated with vaccination use. Thus, acceptability, Greenville, 2020; Roch and Conrady, 2021; Parliament, 2022). How- affordability, accessibility, and availability of vaccine services represent ever, given the current resource constraints of the veterinary system in the main access dimensions constraining vaccination adoption and use. Ghana, we argue that public funding of such subsidies would not be Misconceptions about vaccines cannot be addressed by information possible currently to achieve optimal vaccination coverage. Moreover, provision of vaccine effectiveness alone. These strategies need to include previous research has showed that motivational risk communication thorough engagement with community members, and should be sensi- strategies that increase farmer awareness and willingness are equally tive to gender issues relating to vaccination access. Farmer proposals effective in increasing farmer vaccination uptake compared with the with potential to address the problem would include increased provision of financial compensation in the form of subsidies (Sok and engagement of communities by veterinary service providers on the value Fischer, 2020). Future studies in Ghana could address the costing issue and effectiveness of vaccines, discounting of vaccination costs, and by evaluating farmers’ valuation and willingness to pay for vaccines, to farmer community mobilization. Given that limited knowledge of the inform pricing policy that would incentivize use. effectiveness of vaccination and veterinary services supply shortfalls in The main supply side barriers were related to availability of vaccines the districts drive the observed demand and supply side challenges and accessibility of VOs to farmers when required, and could be respectively, greater collaboration between the different stakeholders in addressed by increasing budgetary allocation to veterinary services, a transdisciplinary manner to effectively address the low vaccination which would help reduce the human resource gap in the veterinary utilization problem is needed. sector. The recent review of the performance of veterinary services of African countries showed that funding for operationalizing veterinary Consent for publication services was very poor for 78% of countries (OIE, 2019). The public resource allocations to the veterinary system certainly has to be Not applicable. improved if the sector is able to attain its goals, particularly in disease control. In a recent review of the livestock vaccine supply chain, (Acosta Ethics approval et al., 2019) argued that addressing farmer willingness to vaccinate through increased awareness creation alone, without a commensurate The study was reviewed and approved by the Ghana Health Service effort to address the supply side challenges would be ineffective in Ethics Review Committee (approval number: GHS-ERC 006/09/20). In optimizing the vaccination coverage. This underscore the need for the study districts, permission was obtained from all the relevant au- increased collaborative and transdisciplinary approaches, involving thorities prior to field data collection. The study participants provided scientists, policy makers and communities, working together to address written informed consent and the data generated are kept as confidential the key challenges. records. All the methods in this study were carried out in accordance The access framework proposed by (Obrist et al., 2007) also enables with relevant guidelines and regulations (such as Declaration of the evaluation of the equitability of people’s access to health services. Helsinki). We found marked differences in the distribution of the barriers to access in the study districts. The Kwahu Afram Plains South (KAPS) District had Funding a higher proportion of farmers reporting challenges in almost all the access dimensions. This could be explained by the relatively large vet- This work was supported by the Royal Society of Tropical Medicine erinary workload in KAPS, more than two times that of the other dis- and Hygiene [GT21/14282/GB], and the Afrique One-African Science tricts. The veterinary livestock units, which is calculated by dividing the Partnership for Intervention Research Excellence [Afrique One-ASPIRE/ standardized total number of animal heads in tropical livestock units by DEL-15-008]. The funders had no role in the study. the number of VOs was about 30000 in KAPS compared to about 11500 and 9000 in Mion and Pru East Districts respectively. The Veterinary Author contributions Services Directorate in Ghana should thus endeavor to maintain an equitable distribution of the available staffing resources to districts. Conceptualization, all authors; methodology, all authors; valida- Our study had some limitations. Despite our best efforts to obtain a tion, G.F., J.H., G.I.M., K.K.A., B.B. and J.Z.; formal analysis, F.S.N.; representative sample of the different agro-ecological zones in Ghana, investigation, F.S.N.; resources, B.B., J.H., J.Z. and G.F.; data cura- this study did not account for the two other minority agro-ecological tion, F.S.N.; writing—original draft preparation, F.S.N.; wri- zones namely the Evergreen and Coastal Savannah zones. Even though ting—review and editing, all authors; visualization, F.S.N., and J.H.; these zones are not typical areas for livestock production in Ghana, supervision, G.F., G.I.M., K.K.A., B.B. and J.Z.; project administra- determining the barriers faced in their contexts would have improved tion, F.S.N. and B.B.; funding acquisition, K.K.A., B.B. and J.Z. All the representativeness of our findings. In spite of this omitted perspec- authors have read and agreed to the published version of the tive, we do not expect the parameters evaluated to be markedly different manuscript. in these agro-ecological zones. Additionally, even though we relied mainly on reported information in this study, we believe that the Declaration of Competing Interest triangulation of results from the different methods show validity of our instruments. Our study thus, has provided valuable information on the The authors declare that they have no competing interests. barriers and determinants of vaccination utilization in a developing country context, which would inform strategies to address low coverage Availability of data and materials of preventive vaccination in livestock. All data generated or analyzed during this study are included in this published article, and its supplementary files. 9 F.S. Nuvey et al. P r e v e n t i v e V e t e r i n a r y M e d i c i n e 215 (2023) 105919 Acknowledgements GSS, 2020a. 2017/18 Ghana Census of Agriculture: National report. Ghana Statistical Service, Accra, 〈https://statsghana.gov.gh/gssmain/fileUpload/pressrelease/Final% 20Report%2011%2011%202020%20printed%20version.pdf〉. We would like to acknowledge the livestock farmers and agricultural GSS, 2014c. GSS. District analytical report: Kwahu Afram Plains South district. Ghana department staff in all the study districts for their participation in this Statistical Service (GSS), Accra, Ghana, 〈https://www2.statsghana.gov.gh/docfiles/ study. The corresponding author is grateful to the State Secretariat for 2010_District_Report/Eastern/KWAHU%20AFRAM%20PLAINS%20SOUTH.pdf〉. GSS, 2020b. Rebased 2013–2019 Annual Gross Domestic Product. Ghana Statistical Education, Research, and Innovation (SERI) of Switzerland for the Service, Accra, Ghana, 〈https://statsghana.gov.gh/gssmain/storage/img/mar scholarship to fund his doctoral studies during which this study was queeupdater/Annual_2013_2019_GDP.pdf〉. conducted. GSS, 2014b. District analytical report: Pru district. Statistical Service (GSS), Accra, Ghana, 〈https://www2.statsghana.gov.gh/docfiles/2010_District_Report/Brong%20 Ahafo/Pru.pdf〉. Appendix A. Supporting information GSS, 2014a. District analytical report: Mion district. Statistical Service (GSS), Accra, Ghana 〈https://www2.statsghana.gov.gh/docfiles/2010_District_Report/North Supplementary data associated with this article can be found in the ern/Mion.pdf〉. GSS, 2019. Ghana Living Standards Survey. GLSS. Ghana Statistical Service, Accra, 〈https online version at doi:10.1016/j.prevetmed.2023.105919. ://www.statsghana.gov.gh/gssmain/fileUpload/pressrelease/GLSS7%20MAIN% 20REPORT_FINAL.pdf〉. 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