Pig Farming Systems and Cysticercosis in Northern Uganda

Pig farming systems and cysticercosis in Northern Uganda

Joseph Morison Kungu1 Charles Masembe2 Michael Apamaku3 Joyce Akol4 Winfred Christine Amia4 Michel Dione4*

Keywords Summary Swine, livestock management, Rudimentary non-market-oriented pig rearing systems have been implicated in Taenia spp., cysticercosis, the persistence of Taenia solium cysticercosis, an endemic disease of high public seroprevalence, risk factors, Uganda health concern in Uganda. We investigated the seroprevalence and key predis- posing factors of the disease in Moyo and Lira, two pig-producing districts in Submitted: 14 July 2017 Northern Uganda. Cross-sectional serosurveys were conducted in 428 pig farms Accepted: 5 September 2019 (Moyo, 262; Lira, 166). Farmers kept on average two adult pigs per herd. Tether- Published: 30 September 2019

ing was a common practice in rural areas; free-ranging less so. Confinement of ANIMALE ET ÉPIDÉMIOLOGIE ■ SANTÉ DOI: 10.19182/remvt.31254 pigs in pens was characteristic of periurban farming systems. Pigs were mainly fed crop residues and forages in the rainy season, and swill and crop residues in the dry season. The majority of farmers of the survey were women (55%) above 45 years old, and 51% of farmers had attained primary school education. A total of 723 pig serum samples were collected, 403 in Moyo, and 320 in Lira. They were analyzed for Taenia spp. antigens using B158C11A10/B60H8A4 Antigen-ELISA. The overall animal seroprevalence of Taenia spp. serum antigen was 10.4% (95% confidence interval [CI]: 4.9–17.6), with 13.2% (95% CI: 7.1– 21.2) the highest in Moyo vs 6.9% (95% CI: 2.9–13.9) in Lira. The herd-level seroprevalence was estimated at 13.7% (95% CI: 9.8–18.5) in Moyo and 11.4% (95% CI: 7.0–17.2) in Lira. Out of 12 explanatory variables assessed for association with the observed seroprevalence, only the district of origin was significant (p = 0.01). Pigs originating from Lira were a protective factor against Taenia spp. cysticercosis (odds ratio: 0.54). These findings highlight the urgent need for an awareness campaign with prevention and control measures to minimize the risk of transmission to pork consumers in these districts.

■ How to quote this article: Kungu J.M., Masembe C., Apamaku M., Akol J., Amia W.C., Dione M., 2019. Pig farming systems and cysticercosis in Northern Uganda. Rev. Elev. Med. Vet. Pays Trop., 72 (3): 115-121, doi: 10.19182/remvt.31254

■ INTRODUCTION Uganda, free-ranging, tethering and housing management systems are common farming systems for rearing pigs. These management systems In recent years the rural poor, and middle income urban communi- tend to be used interchangeably depending on seasonal patterns (Dione ties in Uganda have come to appreciate pig production systems as an et al., 2014; Muhanguzi et al., 2012). The increase in pig production important source of income and financial security (Ouma, et al., 2014). in response to the increasing urban pork consumption in Uganda rep- Pork production has been promoted as a fairly inexpensive option to resents a market opportunity for rural producers if they can guarantee address protein deficiency, given the limited consumption of animal the production of disease-free pork. However, good biosecurity prac- source foods in Uganda (FAOSTAT, 2014). In Central and Eastern tices are not uniformly applied along the pig value chain (Dione et al., 2017). The authors of these studies observed that practices where 1. College of Veterinary Medicine, Animal Resources and Biosecurity, Makerere University, Kampala, Uganda. biosecurity and hygiene are poor have a high potential for disease 2. College of Natural Sciences, Department of Zoology, Entomology and Fisheries transmission, and this risk is greater when the pathogen is zoonotic. Sciences, Makerere University, Kampala, Uganda. In free-ranging, tethering pig-rearing systems if hygiene and sanitation 3. National Agricultural Research Organization, Abi Zonal Agricultural Research are poor, they are key drivers of transmission of pig diseases such as and Development Institute, Arua, Uganda. Taenia solium cysticercosis, a condition of high public health concern. 4. International Livestock Research Institute, C/O Bioversity International, PO Box 24384, Kampala, Uganda. In pig-keeping systems in Uganda, some socio-cultural practices may undermine good hygiene and sanitation; scarcity of feed and water in * Corresponding author Email: [email protected] the dry season may encourage free-range management, compromising the implementation of strategies to control and prevent cysticercosis

https://creativecommons.org/licenses/by/4.0/ (Adenuga et al., 2018; Krecek et al., 2012; Kungu et al., 2017b). tropicaux, 2019, 72 (3) : 1 15-121 des pays et de médecine vétérinaire Revue d’élevage 115 116 Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2019, 72 (3) : 115-121 ■ SANTÉ ANIMALE ET ÉPIDÉMIOLOGIE Porcine cysticercosis inUganda population using the formulapopulation using n =[Z the infinite pig an The population considering sample was size calculated Sample sizecalculation Adekokwok domains. were rural as classified and whereas Barr domains, divisionsLira were periurban as classified Adyel, District, Lira In domain. production and Ojwina rural the in viously (Ouma used et al., 2015), Moyo subcounties classified were all study. classification was pig on Based that pre the domain value chain (Ojwina,Lira Barr,Adyel Lira, Adekokwok) and were for selected the subcounties.target Two Moyo subcounties in (Moyo, Metu) five and in on pig were perceptions the in populations about consulted their areas the validation, DVOs in For the data operating para-veterinarians and for indicator additional pigwere an high as population used density. fever swine surveys.current reports (ASF) African outbreak disease est pig population densities, subcounties were these and included the in high subcounties with the the identify to assisted personnel veterinary (DVOs) officers veterinary MoyoIn district subcounty the and Lira, and Site selection 9,034and pigs Moyo in 2009). MAAIF, and (UBOS Uganda with 28,631 pig Northern population in of total the pigs Lira in population,of respectively. this Together have two districts these 11% of 137,439. subcounties surveyed target 47% The constituted 39% and 1). (Figure population of 410,516districts ahuman has Lira Moyo and surveysCross-sectional were July in conducted 2015 Moyo and Lira in Study area ■ MATERIALSMETHODS AND Moyo. and of Lira districts for factors risk cysticercosis Northern the in prevalence the and pig the production systems determine describe and to study aimed thus This area. pig Northern production systems the in in of infection magnitude done the assess to been has research limited document to cysticercosis studies Uganda, in undertake to efforts been of country. the have there Although parts geographical larger ation in provide will more insight situ on increasing the production is steadily Uganda where pig of Northern settings remote rural condition the in et al., factors (Kungu risk 2017a,b).potential investigation An of this Uganda, discussed and Eastern and Central in settings urban and rural of condition pigs, the in both Uganda occurrence in have ahigh reported et al., Sciutto et al., 2006; 2003; Sreedevi et al., 2012). Recent in studies sis problem (Adenuga et al., 2018; et al., Rodriguez-Hidalgo Praet 2009; solium Uganda,In available emerging T. an indicate studies Africa. and developing various tion in America Asia, in Latin countries of condi the Previous prevalence occurrence have the studies reported 2015). et (Carabin al., Mwape with taeniasis feces ofthe 2009; humans et al., with T. eggs by contaminated shed in solium ingesting food or fluids leptic even cysticercosis seizures, pigs and acquire death. humans Both become stages of parasite the larval the hosts.diate Under circumstances these result interme health when become effects human humans to terious development and implicationshas on growth More children. dele in cycle, life the with development of (taeniasis), tapeworms pork which solium stagesof of encysted T. larval by infection consumptionprognosis humans. Human of in infection outcome stage of and/or with the T. The infection determines solium mum sample size to detect a seroprevalence samplemum detect to size of cysticercosis with an Uganda et al., (Kungu 2017a). Eastern and Central in mini The cysticercosis estimated seroprevalence an ofand 12.3%, reported larval cysts in the human brain or neurocysticercosis may brain epi result in human cysts the in larval

encysted in the brain and muscles and of brain encysted humans. Development the in of 2 in undercooked pork completes pork undercooked in P (1-P)] /d 2 (Thrusfield, 2007), 2007), (Thrusfield, cysticerco ------

-20°C serological pending analysis. whole the from at stored cryovials blood and 2-ml by into pipetting was harvested coagulation. Serum facilitate to at temperature room kept and overnight cold laboratories in boxes district the to ported using 20-gauge needles. vacutainers Bloodplain - samples were trans vena anterior cava the bledusing from and apig 10-ml into snare For blood characteristics. collection, pigs werefarming restrained ness, level of income, source education, of etc.) formal main pig and (gender, information demographic farmers’ age, of pig busi nature pigs individual on the (age, information collect to sex breed), and A pig biological a household were and form used data questionnaire Collection ofhouseholdinformationandpigserum pigs allowsampled. to be to their and study the in signed aconsentA508). participate to form farmers All for Ugandan Nationalthe Council Science Technology and (Ref. No. sciences University of Makerere (Ref. No. SBLS/REC/15/128) by and Bio and Resources of College the Medicine, of Animal Veterinary Committee Ethics by approval and Research the wasEthical granted Ethical considerations months old, sows, pregnant three than piglets. weak and selection exclusion random with the were under enrolled of pigs less for generated ers each subcounty. each household, pigs In up three to of alist survey farm from were the selected in randomly enrolled ever, we pigs 403 Moyo. and sampled 320 in pigs Lira in Households How pigs district. per at 200 adjustedthe sample was size estimated for usingsize correlation acoefficient of intra-cluster 0.2. aresult, As was 166 interval 80%–95% confidence pigs. We adjusted sample the ered to support findings. findings. support to ered mation on pig Such was production constraints. consid information more infor gain to order in of respectiveproduction officers districts out with DVOs interviewsKey were carried informant district and Key informantinterviews Figure 1: showing MapofUganda districtsofthe study. thetwo ------Cysticercose porcine en Ouganda

Table I Serological analysis Pig farmers’ demographic characteristics Serological analysis for Taenia spp. cysticercosis was carried out in two districts of Northern Uganda at the Molecular Biology Laboratory of the College of Natural Sci- ences, Department of Zoology, Entomology and Fisheries Sciences in Characteristic Lira District Moyo District Total (%) Makerere University. Analyses were performed using B158C11A10/ B60H8A4 Antigen-ELISA (apDia In Vitro Diagnostic Kit, Belgium) Num. of Num. of following the manufacturer’s instructions. The optical density (OD) farmers farmers of the samples was measured by reading the test plate at 450-nm Sex wavelength (Multiscan Ex, ThermoScientific). For the interpreta- Male 81 112 193 (45.0) tion of results, the cut-off of the antigen index (Ag Index) for porcine Female 85 150 235 (55.0) specimens was calculated. The mean OD of the negative control was used to calculate the cut-off by multiplying its value by 3.5. The Ag Age (years) Index of each sample was calculated by dividing the OD value of 15–24 16 36 52 (12.0) the sample by the cut-off value. A positive reaction corresponded to 25–34 45 69 114 (27.0) an Ag Index greater than or equal to 1.3. A negative reaction cor- 35–44 56 65 121 (28.0) responded to an Ag Index less than or equal to 0.8. When the Ag ≥ 45 49 92 140 (33.0) Index was between 0.8 and 1.3, it was considered as a gray zone and samples were retested. They were considered as doubtful if the results Nature of pig business remained the same and were excluded from the analysis. Positive and Producer 164 256 420 (98.0) negative controls were provided by the manufacturer. Village boar keeper 2 6 8 (2.0) Level of education Statistical analysis Primary 92 127 219 (51.0) Secondary 36 50 86 (20.0) Individual pig biological data was entered in SPSS 16 for analysis. Samples that did not have biological information associated to them Tertiary 38 85 123 (29.0) were removed from the analysis (n = 18). Descriptive statistics were Main source of income for the household used to analyze data on farmers’ demographic characteristics as well Pig keeping 28 19 47 (11.0) as pig keeping and feeding systems. A logistic regression was con- Crop farming 110 218 328 (76.6) ducted to determine associations between cysticercosis seropreva- Other 28 25 53 (12.4) lence and potential risk factors. At first, a univariable analysis using a logistic regression was performed. Factors with p ≤ 0.2 were expected to be included in a model for multivariable logistic stepwise regres- Table II sion analysis. Since the seroprevalence of cysticercosis was significantly different in the two districts, the logistic regression analysis of Demographic characteristics of pigs sampled the explanatory variables was also independently done. Multivariable in two districts of Northern Uganda analysis was not conducted in any case because none of the variables were significant at univariable analysis. Lira District Moyo District

Characteristic Num. of pigs Num. of pigs Total (%) ■ RESULTS Sex Farmers’ demographic characteristics Male 130 150 280 (38.7) Female 190 253 443 (61.3) A total of 428 pig-keeping households were visited. Female respon- Breed type dents predominated (55%) and most farmers were more than 45 years old. Almost all pig farmers characterized their livelihood as Local 194 223 416 (58.0) a pig-keeping business (98%), as opposed to communal village boar Cross 96 180 276 (38.0) keeping (2%). Up to 51% of household heads had received primary Exotic 30 0 30 (4.0) level education only (Table I). Category Weaner 52 3 55 (7.6) Pig demographic characteristics Gilt 108 95 203 (28.1) Grower 15 20 35 (4.8) Demographic data are presented in Table II. Sizes of the pig herds were very small with an average of two adult pigs per farm. The pigs Communal boar 47 34 81 (11.2) sampled in Lira and Moyo were predominantly local breed (58%) Castrate 30 109 139 (19.2) females (61.3%). However, a number of farmers had improved pig Sow 68 142 210 (29.1) breeds (mainly crossbreeds). Age (months) 4–6 179 39 218 (30.2) Pig management practices 7–12 55 159 214 (29.6) > 12 86 205 291 (40.2) Tethering (Figure 2) was the most prevalent practice in both districts compared to free-ranging. Highly significant variations in the three management systems were observed between the rainy and the dry seasons (χ2 = 6.2, p = 0.00). The proportion of farmers who practiced one (4%). Likewise, the number of pigs tethered was lower in the dry free-ranging was higher in the dry season (16%) than in the rainy season (66%) than in the rainy one (78%). tropicaux, 2019, 72 (3) : 1 15-121 des pays et de médecine vétérinaire Revue d’élevage 117 118 Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2019, 72 (3) : 115-121 ■ SANTÉ ANIMALE ET ÉPIDÉMIOLOGIE Porcine cysticercosis inUganda 4.9–17.6). Moyo pigs (95% more affected had CI: 13.2%; 7.1–21.2) overallthe prevalence was 10.4% (95% [CI]: interval confidence Out of 723 samples, pig only serum 75 were positive, implying that Seroprevalence andriskfactor analysis of animals. dead level of farmers’ processing knowledge and safe handling regarding low about awareness v) zoonotic diseases, and of community the low control,enabling exchange easy iv) of sanitary livestock with limited porosity Moyo of high and iii) South Sudan districts, border District movement of livestock outside livestock and and the within products office, ii) uncontrolled veterinary district the to outbreaks pig disease report to included by i) community practitioners the health failure extension officers, inspectors, meat workersnary private animal and by veteri reported allowing Major inspection. meat easy constraints pig slaughter,slaughter centralize order to slab in built been thus had not did frequently occur. Moyo inspection pork In and acommunity slaughter slaughter backyard was districts, in conducted slabs both in was not well humans to Pig impact understood. and of transmission was relatively butchers, and but its mode traders known by farmers, zoonoses was generally very poor. However, cysticercosis porcine out majorwere as pointed Farmers’ also concerns. knowledge of pig lack of and feeds of piglet rate high affections. mortality The skin problems, weightratory and appetite loss, shivering (fever sign), and respi were diarrheas, pigs, most their reported the commonly in and could onlyis signs known mention by names, clinical local farmers pig to systems. constraint health Besides ASF,most important which the as was key perceived and informants byseason. farmers ASF dry the during especially frequently occurred outbreaks and tricts - dis ASF both was in endemic ticks). and lice (worms, parasites challengesPig health included ASF, external and internal and Pig healthconstraints (χ seasons dry and rainy the in used types feed the in variation was significant There Pig feedingstrategies and dry seasons. dry and rainy the both during was less practiced supplementation but diets, were supplement to used blood fishmeal bran, and rice maize, (39%)swill including residues crop and (38%).feeds Commercial (25%). season, fed they were household dry mainly the kitchen In husk) rice and peelings, forages sweetand vine, and pumpkin potato fedwere residues on crop mainly (63%) (raw cassava or boiled leaf Figure 2: Tethered Uganda. ofNorthern piginaruralarea 2

4.01, p

0.00). season, rainy pigs the During - - of a typical smallholder pig farming system, in pig which smallholder farming is predominant of a typical were practices characteristic pig observed The farming children. and forPigs numbers were subsistence kept small in mostly by women ■ DISCUSSION (95% Lira than CI: 6.9%; 2.9–13.9) (Table CI: 95%confidence interval; R:ruralpigproduction;U:periurban pigproduction CI: 95%confidenceinterval;R:ruralpigproduction;U:periurbanproduction with the age increase of pigs age Moyowith the increase in (p (Table V). Results significantly showed increased infection the that condition was with the shown associated district significantly be to logistica univariable regression analysis (Table V). However, only the were for assessed association with cysticercosis seroprevalence using (95% CI: 7.0–17.2) (Table Lira in IV). Eleven factors risk potential at 13.7%lence was estimated (95% CI: 9.8–18.5) for Moyo, 11.4% and significant factors observed. factors significant Univariable with no independentlyLira. by analyses were district run age between association observed pig and in no infection significant Overall total Overall total Moyo Moyo Lira Lira District District Pig seroprevalence ofcysticercosis accordingtothe to thelocationintwo districtsofNorthernUganda Herd seroprevalence ofcysticercosis according location intwo districts ofNorthernUganda Adekokwok (R) Adekokwok (R) Ojwina (U) Ojwina (U) Subcounty Subcounty Adyel (U) Adyel (U) Moyo (R) Moyo (R) Metu (R) Metu (R) Barr (R) Lira (U) Barr (R) Lira (U) Total Total Total Total

Table III Table IV Num. of Num. 428 262 166 166 herds 96 32 20 14 77 23 pigs 723 403 215 188 320 143 of 60 42 29 46 = positive positive 0.014; F Num. Num. (%) III). The herd seropreva The III). 55 36 11 25 19 10 (%) 75 53 32 21 22 12 4 2 1 2 4 2 1 3

= 14.9(8.7–23.50 12.8 (9.8–16.4) 13.7 (9.8–18.5) 11.4 (5.9–19.6) 15.0 (9.9–21.4) 11.4 (7.0–17.2) 10.4 (4.9–17.6) 13.2 (7.1–21.2) 11.2 (5.6–18.8) 6.9(2.9–13.9) 6.7(2.9–13.9) 4.8(1.6–11.3) 8.4(3.5–15.2) 6.5(2.9–13.9) 6.09). was There 1.2 (0.4–2.9) 0.7 (0.1–3.2) 0.6 (0.1–3.4) 1.3 (0.6–2.2) 0.4 (0.1–2.2) 3.4 (0.6–8.5) % Positive % Positive (CI) (CI)

- Cysticercose porcine en Ouganda

Table V Uganda, where up to 80% of pig farmers hold a small stock ranging Univariable regression of risk factors of cysticercosis from one to five pigs (Ouma et al., 2015). In this study, the majority in two districts of Northern Uganda of the pig farmers interviewed were female. The proportion of female- headed households owning pigs in Uganda has increased significantly Variable Num. of pigs Num. P in the last 10 years, from 15% to 32%. Regardless of who heads the positives (%) household, it is widely agreed that women and children actively participate in managing pigs and other animals reared in homesteads (Uganda District Bureau of Statistics, 2014). Lira 320 22 (6.9) 0.01 The pig management practices reported in this study (free-ranging, Moyo 403 53 (13.2) tethering and housing) were similar to those reported in Central and Eastern Uganda, and in Gulu District in the North (Chenais et al., 2017; Pig sex Dione et al., 2014). Although tethering was predominantly practiced in Male 280 27 (9.6) 0.61 both districts, highly significant variations were noted in the three sys- Female 443 48 (10.8) tems of management during the rainy and dry seasons. The number of free-ranging pigs was higher in the dry season than in the rainy one, a Pig breed finding which concurs with previous studies in Uganda and the Demo- Local 416 42 (10.1) 0.83 cratic Republic of Congo (Dione et al., 2014; Lekule and Kyvsgaard, Cross 275 30 (10.9) 2003). These changes in management systems with seasonal patterns Exotic 30 3 (10.0) have mainly been associated with limited feed resources and minimal crops during the dry season (Lekule and Kyvsgaard, 2003). Most far- Pig category mers favored tethering as an alternative to roaming, as they could not Weaner 55 4 (7.3) 0.24 afford building proper housing for pigs. In comparison with the housing Gilt 203 17 (8.4) system, it is considered to be less labor intensive (Dione et al., 2014). Grower 35 5 (14.3) A significant variation in feed types given to the pigs was noted in this Entire boar 81 5 (6.2) study, whereby crop residues and forages were mainly used in the rainy Castrate 139 14 (10.1) season, whereas swill and crop residues predominated during the dry Sow 210 30 (14.3) season. During the rainy season, there was an increased availability of Rainy season, day management forage and crop residues such as cassava leaf and sweet potato vine. During the dry season, feeds became scarce, resulting in farmers tethe- Free-ranging 29 2 (6.9) 0.56 ring their pigs in grazing fields with scanty pastures and supplementing Tethering 567 63 (11.0) them with swill (Braae et al., 2015). Limited use of commercial feed Housed 127 10 (7.9) (concentrate) was reported probably because of their high cost (Lekule Rainy season, night management and Kyvsgaard, 2003). Free-ranging 27 4 (14.8) 0.16 The rearing systems reported here faced many challenges such as expo- Tethering 539 61 (11.2) sure of pigs to diseases, theft and predation, environmental stressors, Housed 157 10 (6.4) poor nutrition, as reported elsewhere (Lekule and Kyvsgaard, 2003). Pig farmers also faced other challenges such as a high disease prevalence Dry season, day management (especially ASF), feed scarcity and limited access to markets, which are Free-ranging 114 14 (12.3) 0.62 the same challenges reported in other districts of Uganda (Dione et al., Tethering 477 50 (10.5) 2014; Muhanguzi et al., 2012). Housed 130 11 (8.5) The overall cysticercosis prevalence (10.4%) was within the range of Dry season, night management that reported elsewhere in the country (Kungu et al., 2016; Nsadha et al., 2014; Waiswa et al., 2009). The higher odds of disease occurrence in Free-ranging 105 13 (12.4) 0.23 Moyo could be attributed to a greater exposure of pigs to the infection Tethering 465 52 (11.2) given that Moyo had a more extensive pig system than Lira. Tethering Housed 150 10 (6.7) and free-ranging represented risks that could not be underestimated. Feed in rainy season Traditional rearing systems increase the likelihood of pigs accessing Crop residues 454 47 (10.4) 0.17 human fecal matter contaminated with tapeworm eggs, facilitating the Forage 178 24 (13.5) completion and maintenance of the transmission cycle of pork tape- Concentrate 54 2 (3.7) worms and cysticercosis (Carabin et al., 2015; Mwanjali et al., 2013; Swill 37 2 (5.4) Thys, 2016; Braae et al., 2015). In Uganda, the occurrence of cysticercosis is a major public health concern given that farmers who are also Feed in dry season consumers have little awareness of the condition and how to prevent and Crop residues 276 28 (10.1) 0.16 control it (Kungu et al., 2017b). Therefore, there is a need to raise aware- Forage 87 8 (9.2) ness among pig value chain actors and stakeholders about the risks of Concentrate 79 3 (3.8) infection with Taenia spp. through community advocacy campaigns with relevant authorities. Improved prevention and mitigation measures Swill 281 36 (12.8) are highly needed to minimize transmission of the disease to people, Dewormer used in pigs with apparent benefits to the pig sector in terms of incomes and human Levamizole 368 37 (10.1) 0.98 health. Further studies should focus on the assessment of the roles of Ivermectin 35 4 (11.4) pig value chain actors in the management of cysticercosis and to inves- tigate the effectiveness of approaches that promote the participation of Albendazole 5 0 (0.0) farmers and other actors and stakeholders in the control of the disease. tropicaux, 2019, 72 (3) : 1 15-121 des pays et de médecine vétérinaire Revue d’élevage 119 120 Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2019, 72 (3) : 115-121 ■ SANTÉ ANIMALE ET ÉPIDÉMIOLOGIE Porcine cysticercosis inUganda Krecek R.C.,MohammedH.,Michael L.M.,Schantz P.M., NtanjanaL.,Morey Dione M.M., Akol J., Roesel K., Kungu J., Ouma E.A., Wieland B., Pezo Carabin H.,Millogo A., Praet N.,HountonS., Tarnagda Z.,GanabaR.,Dorny Chenais E.,BoqvistS.,Sternberg-LewerinEmanuelsonU.,OumaDione Carabin H.,Millogo A., Cissé A., GabriëlS.,SahluI.,Dorny P., BauerC.,et Braae U.C.,Harrison W., LekuleF., MagnussenP., Johansen M.V., 2015.Feed Adenuga A., Mateus A., Ty, C.,BorinK.,HollD., SanS.,Duggan V., etal., REFERENCES manuscript. the wrote MD analysis; and statistical the JMK performed analysis; laboratory the JMK JAhold and CM information; performed study;the JA, MA, house samples and the WCA collected JMK and coordinated designed and MA study; and the MD conceptualized MD Author contributionsstatement support. logistical and technical cooperation, for and extension their pig and farmers staffs veterinary (Dr. W.Lira Okwir) Moyo and (Dr. R. 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Résumé Resumen Kungu J.M., Masembe C., Apamaku M., Akol J., Amia W.C., Kungu J.M., Masembe C., Apamaku M., Akol J., Amia W.C., Dione M. Systèmes d’élevage porcin et cysticercose au nord Dione M. Sistemas de crianza porcina y cisticercosis en el de l’Ouganda norte de Uganda

Les systèmes rudimentaires d’élevage de porcs, non orientés Los sistemas más rudimentarios de cría de cerdos, no orien- vers le marché, ont été impliqués dans la persistance de la tados al mercado, se han visto implicados en la persistencia cysticercose à Taenia spp., maladie endémique présentant un de la cisticercosis de Taenia spp., enfermedad endémica que grave problème de santé publique en Ouganda. Nous avons representa un grave problema de salud pública en Uganda. La étudié la séroprévalence et les principaux facteurs prédispo- seroprevalencia y los principales factores predisponentes de sant de la maladie à Moyo et à Lira, deux districts producteurs dicha enfermedad fueron estudiados en Moyo y Lira, dos dis- de porcs au nord du pays. Des enquêtes sérologiques transver- tritos productores de carne de cerdo en el norte del país. Para sales ont été menées dans 428 élevages porcins (Moyo, 262 ; ello se realizaron encuestas serológicas transversales en 428 Lira, 166). Deux porcs adultes étaient gardés en moyenne granjas porcinas (Moyo, 262; Lira, 166). Se contabilizó una par troupeau. En milieu rural ils étaient souvent attachés, la media de dos cerdos adultos por rebaño. En las zonas rura- divagation étant occasionnelle. Le confinement en enclos les, los animales se encontraban principalmente atados, con était observé en milieu périurbain. Les animaux étaient prin- desplazamientos libres ocasionales. En las zonas periurbanas cipalement alimentés avec des résidus de culture et des four- sin embargo se observó un predominio del sistema de estabu- rages pendant la saison des pluies, et des restes d’aliment des lación. También se observó que la alimentación se basa prin- ménages et les résidus de culture en saison sèche. La majo- cipalmente en los residuos de cultivos y los forrajes durante la rité des éleveurs de l’enquête étaient des femmes (55 %) âgées época lluviosa, mientras que en la época seca se distribuyen de plus de 45 ans ; 51 % des éleveurs avaient le niveau de residuos de cocina (domésticos) y otros residuos de cultivo. l’école primaire. Au total 723 échantillons sériques porcins En la encuesta, la mayoría de los productores fueron mujeres ont été prélevés (Moyo, 403 ; Lira, 320). Ils ont été analysés (55%) mayores de 45 años y el 51% contaban con el nivel pour la détection des antigènes de Taenia spp. en utilisant le de escolaridad primario. Se recogieron en total 723 muestras test B158C11A10/B60H8A4 Elisa-antigène. La séroprévalence de suero porcino (Moyo, 403; Lira, 320). Para la detección de animale totale de l’antigène sérique de Taenia spp. était de antígenos de Taenia spp., las mismas fueron analizadas utili- 10,4 % (intervalle de confiance [IC] à 95 % : 4,9–17,6). Elle a zando el test Elisa B158C11A10/B60H8A4. La seroprevalen- été la plus élevée à Moyo avec 13,2 % (IC à 95 % : 7,1–21,2) cia animal total de antígeno sérico de Taenia spp. resultó ser vs 6,9 % (IC à 95 % : 2,9–13,9) à Lira. La séroprévalence au del 10,4% (intervalo de confianza [IC] del 95%: 4,9–17,6). niveau du troupeau a été estimée à 13,7 % (CI 95 % : 9,8– Los valores más altos se encontraron en Moyo (13,2%; IC 18,5) à Moyo vs 11,4 % (CI 95 % : 7,0–17,2) à Lira. Parmi les 95%: 7,1–21,2) vs 6,9% (IC 95%: 2,9–13,9) en Lira. La sero- 12 variables explicatives évaluées pour l’association avec la prevalencia a nivel del rebaño se estimó a la altura del 13,7% séroprévalence observée, seul le district d’origine était signifi- (IC 95%: 9,8–18,5) en Moyo y al 11,4% (IC 95%: 7,0–17,2) catif (p = 0,01). Les porcs originaires de Lira étaient un facteur en Lira. Entre las 12 variables predictivas evaluadas para la protecteur contre la cysticercose à Taenia spp. (odds ratio : asociación con la seroprevalencia observada, solo el distrito 0,54). Ces résultats ont souligné le besoin urgent de mettre en de origen resultó ser significativo (p = 0,01). Los cerdos proce- place des mesures de lutte pour minimiser le risque de trans- dentes de Lira fueron un factor protector contra la cisticercosis mission aux consommateurs de porc dans ces districts. provocada por Taenia spp. (odds ratio: 0,54). Estos resultados indican la necesidad urgente de establecer medidas de control Mots-clés : porcin, conduite d’élevage, Taenia spp., cysticer- para minimizar el riesgo de transmisión a los consumidores de cose, séroprévalence, facteur de risque, Ouganda carne de cerdo en estos distritos.

Ganado bovino: cerdo, manejo del ganado, Taenia spp., cisticercosis, seroprevalencia, factores de riesgo, Uganda Revue d’élevage et de médecine vétérinaire des pays tropicaux, 2019, 72 (3) : 1 15-121 des pays et de médecine vétérinaire Revue d’élevage 121