Skip to main content
Erschienen in: BMC Infectious Diseases 1/2017

Open Access 01.12.2017 | Research article

Risk factors, perceptions and practices associated with Taenia solium cysticercosis and its control in the smallholder pig production systems in Uganda: a cross-sectional survey

verfasst von: Joseph M. Kungu, Michel M. Dione, Francis Ejobi, Michael Ocaido, Delia Grace

Erschienen in: BMC Infectious Diseases | Ausgabe 1/2017

Abstract

Background

Prevalence studies report Taenia solium cysticercosis in pig and human populations in Uganda. However, the factors influencing occurrence in smallholder pig production systems are not well documented and little is known about farmers’ perceptions of T. solium cysticercosis or farmer practices that could reduce transmission.

Methods

To determine the risk factors, perceptions and practices regarding T. solium cysticercosis, a household survey using a semi-structured questionnaire was conducted in 1185 households in the rural and urban pig production systems in Masaka, Mukono and Kamuli Districts. Logistic regression was used to measure associations of risk factors with infection. Performance scores were calculated to summarise perceptions and practices of farmers regarding taeniosis, human cysticercosis and porcine cysticercosis as well as farmer behavior related to control or breaking transmission.

Results

Pig breed type, farmers’ knowledge about transmission, sources of water used, and pig keeping homes where family members were unable to use the latrine were all significantly associated with T. solium cysticercosis in pigs. Performance scores indicated that farmers were more aware of taeniosis (63.0%; 95% Confidence Interval 60.0-65.8) than human or porcine cysticercosis; only three farmers (0.3%, 95% CI = 0.1–0.8) had knowledge on all three conditions. More farmers reported that they dewormed pigs (94.1%) than reported deworming themselves and their family members (62.0%). Albendazole was the most commonly used drug for deworming both pigs and humans (85.0 and 81.5% respectively). Just over half (54.6%) of the farmers interviewed had clean water near the latrines for washing hands. Of these, only 41.9% used water with soap to wash hands after latrine use.

Conclusion

Factors that significantly influenced occurrence of T. solium cysticercosis in pigs were identified. Farmers had some knowledge about the disease but did not link taeniosis, human cysticercosis, and porcine cysticercosis. Therefore, there is need to employ strategies that raise awareness and interrupt transmission.
Abkürzungen
CI
Confidence interval

Background

Uganda is a developing country known to be endemic for Taenia solium cysticercosis, a public health challenge associated with poor pig-keeping practices and sanitation. The condition has a two-stage development cycle: the intermediate (larval) and the definitive (adult) stages. The intermediate stage occurs in pigs as the primary hosts causing porcine cysticercosis and in humans as accidental hosts resulting in human cysticercosis/neurocysticercosis [1, 2]. Humans harbor the final stage, a condition called taeniosis. Cases of pigs as secondary final hosts of this tapeworm infection have been described [3]. Neurocysticercosis, a life threatening form of human cysticercosis that occurs following invasion of the brain with metacestodes, has been reported to be the chief known cause of epilepsy in human populations in pig-keeping communities in the developing countries [4]. A recent study in Zambia indicated that up to 57% of epilepsy cases reported were attributed to neurocysticercosis [5, 6]. Although no such study has been done in Uganda to estimate prevalence of human cysticercosis/neurocysticercosis, presence of T. solium infection in pigs is a key indicator of the occurrence of the infection in the human population. Recent serological studies in Uganda have indicated that prevalence of porcine cysticercosis in pigs ranges between 8 and 12% [7, 8].
Various factors influencing the occurrence and spatial distribution of this condition in pigs and humans have been identified [9, 10]. Such factors include: poor hygiene and sanitation practices in humans, free-range pig rearing and tethering, lack of awareness about the disease and its transmission, poor or non-inspection of pigs before or following slaughter, use of contaminated water for pigs and people, and, eating under-cooked pork [11, 12].
Specifically, poor hygiene practices such as not washing hands with soap following visits to the latrines and before eating food, eating unwashed fruits and vegetables, and, drinking un-boiled or untreated water can lead to humans ingesting the eggs of T. solium [13]. Poor sanitation practices, such as open air defecation and latrines in poor conditions can allow pigs access to human feces [14]. Feces deposited in the open environment can be washed into unprotected springs and wells posing a risk to both pigs and humans [12, 15].
There are 3 main pig-rearing systems practiced in Uganda: free-range, tethered, and intensive confinement where pigs are kept in corrals with or without raised floors. The extensive production systems (free-range and tethered) are usually practiced during dry season when there is a scarcity of feed and agricultural activities, which pigs might disturb, are minimal [16, 17]. Extensive systems allow pigs access to human fecal material, thereby enabling the continuity of the T. solium lifecycle [13]. In northern Cameroon, where the free range pig management was estimated to be 90.7%, prevalence of the condition was high (26.6%) [10]. In Zambia, it was also reported that free-range management significantly influenced occurrence of the condition [18].
The disease has been shown to be prevalent in areas where inadequate or no inspection of pork is practiced [1, 18, 19]. This is the case in most communities in Uganda where pigs are slaughtered in un-gazetted areas and uninspected pork is then sold locally or transported to urban centres for marketing [20]. This poses a serious risk to pork consumers especially when they eat undercooked pork [14].
Community awareness of a disease is crucial for control and eventual eradication. Lack of knowledge about the pork tapeworm transmission cycle by farmers, consumers and non-consumers of pork, medical and veterinary personnel, policy makers and implementers in developing countries has made control of the potentially eradicable condition difficult [21]. Limited knowledge has been linked to increasing incidence among rural poor pig-keeping communities [12, 2224].
Stakeholders in endemic areas may know about tapeworm infections in humans but may not relate it to porcine cysticercosis and neuro-cysticercosis [12]. In Uganda, misleading reports by the media which allege that “eating pork directly causes epilepsy” could complicate the control of T. solium infection [25]. Although change of behavior in communities is not automatic after acquisition of knowledge, it could be a key step in prevention of T. solium cysticercosis [12, 15, 23, 24].
Given the importance of pig rearing in Uganda and the high risk that consumption of poorly cooked pork represent for the communities, this study aimed to investigate risk factors, perceptions and practices of farmers regarding taeniosis and T. solium cysticercosis in order to inform future control initiatives of the disease.

Methods

Study design

The study was conducted from April to August 2013 in 22 villages of Masaka, Mukono and Kamuli districts in Uganda. Full details of selection criteria of study sites have been reported by Ouma et al. [26]. Description of study area, sample size calculation and sampling strategy were reported by Kungu et al. [7]. In short, districts were selected as being of high potential for smallholder pig systems. Power calculation indicated a minimum sample size of 384 pigs in each district. In each village, households were randomly selected from all pig-keeping households in each village. In selected households, one pig was randomly picked and blood collected. Serum harvested was then analyzed using the HP10Ag-ELISA [27] and B158C11A10/ B60H8A4 Ag-ELISA (apDIA Cysticercosis) [28]. Every sample that tested positive in either assays contributed to the overall estimated apparent sero-prevalence of the condition.

Household questionnaire

A questionnaire was administered to the owner of each pig that had been included in the survey to assess the risk factors for T. solium cysticercosis in the study sites. This questionnaire was adapted and modified from the Cysticercosis Working Group of East and Southern Africa (CWGESA) tool [29]. It was pre-tested by the first author on pig farmers in a non-study village (Mukono Municipality). It captured data on demographic characteristics, pig production and management, hygiene practices, knowledge and perceptions, as well as treatment of the condition in pigs and humans. Considering that many respondents were not fluent in English, four veterinary officers fluent in the commonly spoken indigenous language (Luganda in Masaka and Mukono, Lusoga in Kamuli) were used in each district as research assistants. Bleeding of pigs was concurrently done as already described by Kungu et al. [7]. Prior to the questionnaire administration, the study protocol was explained to the farmer and signed consent obtained.

Statistical analysis

Data from serology, household questionnaire was entered in Microsoft excel (2010) and exported to the STATA 11 software for analysis.

Analysis of risk factors

Descriptive statistics for the respondents and pig characteristics were determined. A univariable analysis using logistic regression was performed to determine associations between the risk factors and sero-prevalence of T. solium cysticercosis (Table 1). Factors with P-values ≤ 0.1 were included in a model for multivariable logistic step-wise regression analysis. A backward elimination procedure was used to exclude the factors one at a time, using P >0.05 as the criterion. Clustering was accounted for at two levels with district as a fixed variable and village as a random effect in the multivariable models. Model diagnostics were carried out by checking for normality of residuals at village level, as well as heteroscedasticity of residuals [30]. There was minimal variation between villages considering that village level residuals were all quite small (between −1 and +1). This was also shown by the small value for the village level variance in the final model. Therefore, the fixed effects had very little effect on the size of this variance, implying that even when they were removed from the model, variation between villages still remained limited. Tests for significance of associations and odds ratios were performed at Confidence Interval of 95% and significance level of 0.05.
Table 1
Characteristics of respondents in the three districts
Characteristics
Category
Frequency
Percent (%)
Respondent age-group
<20 years
17
1.6
20–40years
405
37
41–60year
507
46.3
>60 years
167
15.2
Sex
Female
351
32
Male
745
68
Religion
Christian
1065
97.2
Muslim
4
0.4
SDA
10
0.9
Traditional beliefs
17
1.6
Ethnic grouping
Baganda
670
61.1
Basoga
339
30.9
Banyankole
15
1.4
Others
72
6.6
Level of education
Never been
114
10.4
Primary
550
50.2
Secondary
349
31.8
Tertiary
83
7.6
Primary activity
Livestock
198
18.1
Crop farming
747
68.2
Civil service
38
3.47
Business
59
5.38
Others
54
4.93

Analysis of perceptions and practices

Performance scores were calculated for each of the five different variables used to assess knowledge on taeniosis, porcine cysticercosis, and human cysticercosis as described by Dohoo [30]. Briefly, weights of 0–10 points were subjectively assigned as overall scores to the responses on questions assessing each knowledge variable. A respondent was considered to have knowledge on a variable when his/her responses scored 8–10 points and these were then recoded into dichotomous variables (has adequate knowledge versus does not have adequate knowledge). Descriptive statistics was used to generate proportions of responses on practices associated with control of T. solium cysticercosis.

Results

We sampled 375, 408, and 402 pigs in Masaka, Kamuli and Mukono, respectively. Only 1096 farmers of the 1185 whose pigs had been bled were interviewed. The remainder claimed to have commitments and left home immediately their pigs had been bled. Out of the 1185 pigs tested, 144 (12.2%) were positive by serology. Most respondents ranged from 20 to 60 years, and most were male (67.97%) and Christian by religion (97.2%). Details of the socio-demographic characteristics of the respondents are in Table 1.

Determination of risk factors of T. solium cysticercosis

Several factors at the animal and household level were analyzed for their association with T. solium cysticercosis sero-prevalence in pigs. At animal level, six variables were assessed using univariable analysis. Only breed type had p-value ≤ 0.1 as indicated in Table 2. At the household level, 10 variables were assessed by univariable analysis. Level of education, knowledge of transmission cycle, water sources, and homes where people were unable to use latrine facilities had p-values ≤0.1 as shown in Table 3.
Table 2
Univariable analysis of risk factors for T. solium cysticercosis in pigs at animal level
Factor
Number of pigs
Seropositive pigs (%)
p-value
Odds (95% CI)
Pig category
 Weanera
455
60(13.2)
-
-
 Gilt
25
2(8)
0.457
0.572 (0.132–2.490)
 Castrate
178
28(15.7)
0.406
1.229 (0.756–1.999)
 Boar
177
17(9.6)
0.218
0.699 (0.396–1.236)
 Sow
350
37(10.6)
0.259
0.778 (0.503–1.203)
At least grazed on pasture
 Yes
786
101(12.8)
0.611
0.899 (0.597–1.355)
 Noa
299
35(11.7)
-
-
Husbandry systems
 Intensivea
501
59(11.8)
-
-
 Free range
13
1(7.7)
0.354
0.709 (0.342–1.469)
 Tethering
577
75(13)
0.544
0.893 (0.621–1.286)
Breed type
 Locala
195
26(13.3)
-
-
 Cross
733
104(14.2)
0.005
2.659 (1.349–5.243)
 Exotic
256
14(5.5)
0.000
2.858 (1.604–5.091)
Deworm pigs
 Yesa
797
102(12.8)
-
-
 No
388
42(10.9)
0.337
0.829 (0.566–1.215)
Source of pig
 Born on farma
326
42(13.2)
-
-
 Trader
758
89(11.7)
0.746
0.810 (0.227–2.898)
 NGO/NAADS
15
2(12.5)
0.782
0.821 (0.119–5.675)
 Gift
62
7(11.3)
0.591
0.710 (0.119–5.670)
 Boar pay
19
3(15.8)
0.604
0.679 (0.157–2.930)
aReference variable
Table 3
Univariable analysis of risk factors for T. solium cysticercosis at household level
Factor
Number of pigs
Seropositive pigs (%)
p-value
Odds (95% CI)
Level of education
 None
114
11(9.7)
0.073
0.449(0.187–1.079)
 Primary
548
68(12.4)
0.06
0.452(0.197–1.033)
 Secondary
348
40(11.5)
0.089
0.593(0.325–1.083)
 Tertiarya
83
16(19.3)
-
-
Training in pig management
 Yesa
488
62(12.7)
-
-
 No
603
73(12.1)
0.397
0.728(0.348–1.52)
Water sources
 Unprotecteda
419
37(8.8)
-
-
 Protected
677
98(14.5)
0.008
0.583(0.391–0.870)
Boil water
 Alwaysa
638
79(12.4)
-
-
 Never
453
56(12.4)
0.992
1.002(0.695–1.444)
Eating pork
 At least once a month
640
81(12.7)
0.281
0.653(0.3–1.418)
 After a month
204
20(9.8)
0.644
0.904(0.587–1.39)
 Nevera
246
34(13.8)
-
-
Slaughter at home
 Once a year
101
8(16.5)
0.200
0.629(0.31–1.278)
 After a year
21
4(19)
0.157
0.583(0.276–1.231)
 Nevera
957
123(12.9)
-
-
Inspection on slaughter
 Alwaysa
11
0
-
-
 Sometimes
20
3(15)
0.59
0.687(0.175–2.692)
 Never
111
12(10.8)
0.999
0.000
Presence of latrine
 No
133
3(6)
0.384
0.729(0.358–1.484)
 Yesa
1041
132(12.7)
-
-
Unable to use latrine
 Yes
595
90(15.1)
0.006
0.581(0.395–0.855)
 Noa
458
43(9.4)
-
-
Know transmission cycle
 Yes
121
26(21.5)
0.002
0.463(0.287–0.746)
 Noa
975
109(11.2)
-
-
aReference variable
A multivariable logistic regression was performed to ascertain the effects of breed type, level of education, knowledge of transmission cycle, water sources, and being unable to use a latrine on the likelihood of pigs having T. solium cysticercosis (Table 4). Crossbred and exotic pigs were more likely to be positive than local pigs. Knowledge of the transmission cycle by farmers significantly was associated with a reduced likelihood of disease (0.476 times). Pigs from households that used water from protected sources (borehole, tap, tanks) were 0.525 times less likely to have the condition than those who used unprotected sources. Pigs in homes where all family members were able to use latrines were 0.576 times less likely to have disease.
Table 4
Multivariable analysis of animal and household level risk factors for T. solium cysticercosis
Variable
B coefficient
P-value
Odds ratio (95% CI)
Breed type
   
 Local
Reference
  
 Cross
1.17
0.001
3.221 (1.599–6.488)
 Exotic
1.135
0.000
3.110 (1.733–5.580)
Level of education
   
 None
Reference
  
 Primary
−0.687
0.111
0.503 (0.216–1.172)
 Secondary
−0.443
0.161
0.642 (0.345–1.194)
 Tertiary
−0.542
0.104
0.582 (0.303–1.118)
Know transmission cycle
   
 Yes
−0.743
0.003
0.476 (0.291–0.779)
 No
Reference
  
Water source
   
 Unprotected
Reference
  
 Protected
−0.644
0.020
0.525 (0.350–0.787)
 Unable to use latrine
   
 Yes
Reference
  
 No
−0.551
0.006
0.576 (0.389–0.853)

Determination of perceptions and practices of farmers

Farmers’ perceptions of the three conditions

A knowledge performance score was conducted on the 1096 farmers’ responses related to taeniosis, human cysticercosis (HC) and porcine cysticercosis (PC) (Table 5). The proportions of the five different knowledge variables were calculated. Generally, farmers had highest knowledge on taeniosis (63.0%, 95% CI = 60.0-65.8) compared to other conditions. Only 3/1096 (0.3%, 95%CI = 0.1–0.8) respondents had knowledge about all three conditions as described in Fig. 1.
Table 5
Proportions of the different variables used to assess level of knowledge on the infection
Knowledge variable
Taeniosis, n (%)
Human cysticercosis, n (%)
Porcine cysticercosis, n (%)
How condition clinically manifests
782 (71.4)
56 (5.1)
319 (29.1)
How condition is acquired
780 (71.2)
22 (2.0)
127 (11.6)
Organs affected
683 (62.4)
32 (2.9)
127 (11.6)
Effects of condition
683 (62.4)
56 (5.1)
11 (1.0)
How to control condition
658 (60)
22 (2.0)
38 (3.5)
Male farmers had more knowledge about the three conditions than females. Farmers of Kamuli district, the most rural area of the study sites, had less knowledge about T. solium cysticercosis than Masaka and Mukono districts which are more urbanized. Table 6 shows the details of these findings.
Table 6
Average proportions of knowledge of the condition by gender, level of education and districts
Categories
Taeniosis (%)
Porcine cysticercosis (%)
Human cysticercosis (%)
Gender
 Male
495/745 (66.4)
107/745 (14.4)
29/745 (3.9)
 Female
223/351 (63.5)
18/351 (5.1)
8/351 (2.2)
Level of education
 None
71/114 (62.3)
18/114 (15.8)
4/114 (3.5)
 Primary
344/550 (62.6)
71/550 (12.9)
19/550 (3.5)
 Secondary
224/349 (64.2)
18/349 (5.2)
12/349 (3.4)
 Tertiary
79/83 (95.2)
18/83 (21.7)
2/83 (2.4)
District
 Kamuli
160/400 (40.0)
40/400 (10.0)
6/400 (1.5)
 Masaka
259/324 (79.9)
67/324 (20.7)
16/324 (4.9)
 Mukono
293/372 (78.8)
18/372 (4.8)
15/372 (4.0)

Control practices

Practices such as deworming of pigs and humans, as well as hand washing were assessed. More farmers reported that they dewormed pigs (94.1%) than reported deworming themselves and their family members (62.0%). Albendazole was the most commonly used drug for deworming both pigs and humans (85 and 81.5% respectively). Deworming practices varied significantly among the districts of Kamuli, Masaka and Mukono (Table 7). Just over half (54.6%) of the farmers interviewed had clean water near the latrines for washing hands. Of these, only 41.9% used water with soap to wash hands after latrine use. Availability of both water and soap varied significantly among the three districts (X2 = 16.944, P < 0.05) (Table 8).
Table 7
Proportions of responses on deworming practices associated with control of T. solium cysticercosis
Deworming practice
Kamuli
Masaka
Mukono
Total, n (%)
X 2
P-value
Deworming pigs
    
4.295
0.000
 Yes
303
357
371
1031 (94.1)
  
 No
39
18
8
65 (6.3)
  
Deworm pigs how often
    
3.495
0.000
 3 months interval
94
178
216
488 (44.5)
  
 Once a month
131
110
93
334 (30.5)
  
  > 3 months interval
84
64
61
209 (25.0)
  
Drugs used
      
 Albendazole
122
229
209
932 (85.0)
  
 Ivermectin
33
23
108
164 (15.0)
  
Deworming self and family
    
4.97
0.000
 Yes
143
244
293
680 (62.0)
  
 No
197
129
90
416 (38.0)
  
How often
    
2.338
0.000
 Once a month
44
50
20
114 (16.8)
  
 3 months interval
42
117
167
326 (47.9)
  
  > 3 months
57
77
106
240 (35.3)
  
Drugs used
    
2.492
0.000
 Albendazole
122
228
204
554 (81.5)
  
 Ivermectin
0
1
0
1 (0.15)
  
 Praziquantel
0
0
5
5 (0.74)
  
 Others
23
13
84
120 (17.7)
  
Table 8
Proportions of responses on hand washing practices associated with control of taeniosis-T. solium cysticercosis
Practice
Masaka
Mukono
Kamuli
Total, n (%)
X 2
P-value
Practice hand washing
    
0.698
0.706
 Yes
203
201
194
598 (54.6)
  
 No
185
163
150
498 (45.4)
  
Presence of clean water and soap
    
16.944
0.00
 Both present
172
174
113
459 (76.8)
  
 Only water present
217
200
220
139 (23.2)
  

Discussion

Although various factors expected to influence the transmission pattern of T. solium cysticercosis were assessed, only breed type, knowledge of the transmission cycle, use of water from protected sources, households with members unable to use latrines were found to be significant. We found that the odds of exotic and crossed pigs having T. solium cysticercosis infection were significantly higher than local ones. Similarly, Krecek et al. in South Africa reported a significantly higher sero-prevalence among crossbred pigs [31]. The pig breed types referred to here as ‘local’ have been reared for decades in the communities and are characterized by slow growth but they have adapted to the harsh conditions over time and are considered more resilient to diseases than recently introduced breeds or their crosses [32]. Also, there are some systematic differences in the way local pigs are kept and this may have influenced exposure or susceptibility. Sero-prevalence of T. solium cysticercosis in pigs was significantly less in homes that used protected water sources. A study in Mexico found that use of stagnant water in pigs significantly increased the prevalence in pigs [33]. Likewise, studies in Tanzania and Rwanda reported use of water from unprotected sources as an etiological factor for the condition [14, 34]. When contamination of the environment with T. solium eggs occurs, then the possibility for pigs and humans ingesting them is high when water from open sources such as rivers, streams, wells, and lakes is used in the homes without boiling or using decontaminating chemicals like chlorine [33]. Again confounding is possible, as households not using protected water sources are likely to differ consistently from those that do, and some of these differences could also affect pig exposure or susceptibility.
In our study, some household had latrines which some family members were not able to use. This was associated with a significant increase in porcine cysticercosis sero-prevalence. Children under age of 5 years, and weak, less mobile people (the old and sick) tend to carelessly defecate thereby increasing the risk of environmental contamination with the T. solium eggs. Thys et al. [12] reported that latrine use was influenced by taboos and socio-cultural beliefs thereby encouraging open-air defecation and eventual contamination of the environment with the T. solium eggs.
Community awareness about a disease is important for its control [35]. Our study associated knowledge of the transmission cycle by farmers with reduced likelihood of T. solium cysticercosis in pigs. Likewise, a study in Tanzania demonstrated that sensitization of pig keeping communities resulted in a significant reduction of the condition in pigs [21]. This study indicated that awareness of taeniosis was high among farmers compared to knowledge of human cysticercosis and porcine cysticercosis. Lack of knowledge of the latter conditions could hinder efforts of controlling the most preventable cause of epilepsy in the sub-Saharan African region [36]. Male farmers had more knowledge about the three conditions compared to female. This could be attributed to the more exposure men have at social gatherings than the women who are mostly involved in domestic work [20].
Many farmers routinely dewormed themselves and their pigs using albendazole. This practice would help limit transmission. According to the farmers, the practice was being implemented not because of their awareness about the specific dangers of T. solium cysticercosis but as a way of controlling worm infestations that were believed to hinder growth of the pigs and cause humans to get hungry shortly after a meal [37].
In our survey, just over half the farmers reported hand washing, similar to a nationwide survey which reports around one third of people practice hand washing (32.7%) [38]. Moreover, effectiveness of hand washing would be reduced by the low use of soap. Hand washing with soap, latrine use, and safe water use are considered by the World Health Organization as the key hygiene behaviors that limit the burden of infectious conditions like taeniosis-T. solium cysticercosis [39].

Conclusion

This study indicates that a number of factors associated with etiology and persistence of T. solium cysticercosis exist in pig production systems in Uganda. Special considerations should be giving to making latrines accessible to children, old people and people with disabilities. Use of water from protected sources should be encouraged. Programs of sensitization about the pig tapeworm and its public health importance could raise awareness. Appropriate health education of local communities on the transmission cycle of this condition might enhance good practices such as proper hygiene and sanitation, use of water from protected sources, boiling of drinking water.
A holistic approach drawing together veterinary, medical, and public health professionals involved in activities to control taeniosis-T. solium conditions should be envisaged to make such efforts cheaper yet more effective.

Acknowledgements

We thank the Smallholder Pig Value Chain Development (SPVCD) project funded by International Fund for Agricultural Development (IFAD) to the CGIAR CRP3.7 Livestock and Fish through the International Livestock Research Institute (ILRI), and the German Academic Exchange Services (DAAD) for their financial support. We also thank pig farmers for Masaka, Mukono and Kamuli districts who willingly offered their valuable time to participate in this study, as well as all stakeholders and partners including District Veterinary Officers and Volunteer Efforts for Development Concerns (VEDCO) in Kamuli.

Availability of data and materials

Data has been submitted to this journal as additional supporting file.

Authors’ contributions

JMK: Conception and design of study, collection, analysis and interpretation of data; drafting and critical review of manuscript, gave final approval for submission of manuscript. MMD: Design of study, collection, analysis and interpretation of data; drafting and critical review of manuscript, gave final approval for submission of manuscript. FE: Conception and design of study, drafting and critical review of manuscript, gave final approval for submission of manuscript. MO: Conception and design of study, drafting and critical review of manuscript, gave final approval for submission of manuscript. DG: Conception of study, drafting and critical review of manuscript, gave final approval for submission of manuscript.

Authors’ information

JMK: Holds a PhD in Veterinary Epidemiology and works as a researcher of Animal Health at the National Livestock Resources Research Institute, Tororo, Uganda.
MMD: Holds a PhD in Veterinary Epidemiology and works as an Animal Health Scientist at International Livestock Research Institute, Kampala Uganda.
FE: Holds a PhD in Food safety and heads the Department of Veterinary Medicine Ecosystems and Biosecurity, College of Veterinary Medicine Animal Resources and Biosecurity Makerere University.
MO: Holds a PhD in Veterinary Medicine and heads the Department of Wildlife Animal Resources Management, College of Veterinary Medicine Animal Resources and Biosecurity Makerere University.
DG: Holds a PhD and heads the Food safety and Zoonoses program at International Livestock Resources Research Institute, Nairobi Kenya.

Competing interests

The authors declare that they have no competing interests.
Not applicable in this study.
Approval of study was sought from the Research and Ethics Committee of the College of Veterinary Medicine and Biosciences of Makerere University (Reference number: VAB/REC/13/104) and the Ugandan National Council for Science and Technology (Reference number: HS1477). Prior to the interview, the objectives of the study were explained to each respondent and signed consent was obtained.
Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://​creativecommons.​org/​licenses/​by/​4.​0/​), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://​creativecommons.​org/​publicdomain/​zero/​1.​0/​) applies to the data made available in this article, unless otherwise stated.
Literatur
1.
Zurück zum Zitat Sikasunge C, Siziya S, Vercruysse J, Phiri IK, Dorny P, Gabriel S, Willingham AL. Assessment of routine inspection methods for porcine cysticercosis in Zambian village pigs. J Helminthol. 2006;80(1):69–72.CrossRefPubMed Sikasunge C, Siziya S, Vercruysse J, Phiri IK, Dorny P, Gabriel S, Willingham AL. Assessment of routine inspection methods for porcine cysticercosis in Zambian village pigs. J Helminthol. 2006;80(1):69–72.CrossRefPubMed
3.
Zurück zum Zitat Nakaya K, Craig PS, Margono SS. Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. J Helminthol. 2002;76:311–4.CrossRefPubMed Nakaya K, Craig PS, Margono SS. Dogs as alternative intermediate hosts of Taenia solium in Papua (Irian Jaya), Indonesia confirmed by highly specific ELISA and immunoblot using native and recombinant antigens and mitochondrial DNA analysis. J Helminthol. 2002;76:311–4.CrossRefPubMed
4.
Zurück zum Zitat Pondja A, Neves L, Mlangwa J, Afonso S, Fafetine J, Willingham AL, et al. Prevalence and risk factors of porcine cysticercosis in Angónia District, Mozambique. Flisser A, editor. PLoS Negl Trop Dis. 2010;4(2):5.CrossRef Pondja A, Neves L, Mlangwa J, Afonso S, Fafetine J, Willingham AL, et al. Prevalence and risk factors of porcine cysticercosis in Angónia District, Mozambique. Flisser A, editor. PLoS Negl Trop Dis. 2010;4(2):5.CrossRef
5.
Zurück zum Zitat Mwape KE, Phiri IK, Praet N, Speybroeck N, Muma JB, Dorny P, et al. The incidence of human cysticercosis in a Rural Community of Eastern Zambia. PLoS Negl Trop Dis. 2013;7:3.CrossRef Mwape KE, Phiri IK, Praet N, Speybroeck N, Muma JB, Dorny P, et al. The incidence of human cysticercosis in a Rural Community of Eastern Zambia. PLoS Negl Trop Dis. 2013;7:3.CrossRef
6.
Zurück zum Zitat Mwape KE, Blocher J, Wiefek J, Schmidt K, Dorny P, Praet N, et al. Prevalence of neurocysticercosis in people with epilepsy in the Eastern province of Zambia. PLoS Negl Trop Dis. 2015;9(8):1–15.CrossRef Mwape KE, Blocher J, Wiefek J, Schmidt K, Dorny P, Praet N, et al. Prevalence of neurocysticercosis in people with epilepsy in the Eastern province of Zambia. PLoS Negl Trop Dis. 2015;9(8):1–15.CrossRef
8.
Zurück zum Zitat Nsadha Z, Thomas LF, Fèvre EM, Nasinyama G, Ojok L. Prevalence of porcine cysticercosis in the Lake Kyoga Basin, Uganda. BMC Vet Res. 2014;10:239. doi:10.1186/s12917-014-0239-y. Nsadha Z, Thomas LF, Fèvre EM, Nasinyama G, Ojok L. Prevalence of porcine cysticercosis in the Lake Kyoga Basin, Uganda. BMC Vet Res. 2014;10:239. doi:10.​1186/​s12917-014-0239-y.
9.
Zurück zum Zitat Venkata RM, Jayaraman T, Muliyila J, Oommenb A, Dorny P, Vercruysse J, Rajshekhar V. Prevalence of porcine cysticercosis in Vellore, South India. Trans R Soc Trop Med Hyg. 2012;107:67–8. Venkata RM, Jayaraman T, Muliyila J, Oommenb A, Dorny P, Vercruysse J, Rajshekhar V. Prevalence of porcine cysticercosis in Vellore, South India. Trans R Soc Trop Med Hyg. 2012;107:67–8.
10.
Zurück zum Zitat Assana E, Amadou F, Thys E, Lightowlers MW, Zoli AP, Dorny P, et al. Pig-farming systems and porcine cysticercosis in the north of Cameroon. J Helminthol. 2010;84(4):441–6.CrossRefPubMedPubMedCentral Assana E, Amadou F, Thys E, Lightowlers MW, Zoli AP, Dorny P, et al. Pig-farming systems and porcine cysticercosis in the north of Cameroon. J Helminthol. 2010;84(4):441–6.CrossRefPubMedPubMedCentral
11.
Zurück zum Zitat Sikasunge CS, Phiri IK, Phiri AM, Dorny P, Siziya S, Willingham AL. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet Parasitol. 2007;143(1):59–66.CrossRefPubMed Sikasunge CS, Phiri IK, Phiri AM, Dorny P, Siziya S, Willingham AL. Risk factors associated with porcine cysticercosis in selected districts of Eastern and Southern provinces of Zambia. Vet Parasitol. 2007;143(1):59–66.CrossRefPubMed
12.
Zurück zum Zitat Thys S, Mwape KE, Lefèvre P, Dorny P, Marcotty T, Phiri AM, et al. Why latrines are not used: communities??? Perceptions and practices regarding latrines in a Taenia solium endemic rural area in Eastern Zambia. PLoS Negl Trop Dis. 2015;9(3):1–20.CrossRef Thys S, Mwape KE, Lefèvre P, Dorny P, Marcotty T, Phiri AM, et al. Why latrines are not used: communities??? Perceptions and practices regarding latrines in a Taenia solium endemic rural area in Eastern Zambia. PLoS Negl Trop Dis. 2015;9(3):1–20.CrossRef
13.
Zurück zum Zitat Mwape KE, Phiri IK, Praet N, Muma JB, Zulu G, van den Bossche P, et al. Taenia solium infections in a rural area of Eastern Zambia-A community based study. PLoS Negl Trop Dis. 2012;6:3.CrossRef Mwape KE, Phiri IK, Praet N, Muma JB, Zulu G, van den Bossche P, et al. Taenia solium infections in a rural area of Eastern Zambia-A community based study. PLoS Negl Trop Dis. 2012;6:3.CrossRef
14.
Zurück zum Zitat Mwanjali G, Kihamia C, Kakoko DVC, Lekule F, Ngowi H, Johansen MV, et al. Prevalence and risk factors associated with human Taenia solium infections in Mbozi District, Mbeya Region, Tanzania. PLoS Negl Trop Dis [Internet]. 2013;7(3):e2102.CrossRef Mwanjali G, Kihamia C, Kakoko DVC, Lekule F, Ngowi H, Johansen MV, et al. Prevalence and risk factors associated with human Taenia solium infections in Mbozi District, Mbeya Region, Tanzania. PLoS Negl Trop Dis [Internet]. 2013;7(3):e2102.CrossRef
15.
Zurück zum Zitat Bulaya C, Mwape KE, Michelo C, Sikasunge CS, Makungu C, Gabriel S, et al. Preliminary evaluation of community-led total sanitation for the control of Taenia solium cysticercosis in Katete District of Zambia. Vet Parasitol. 2015;207(3–4):241–8.CrossRefPubMed Bulaya C, Mwape KE, Michelo C, Sikasunge CS, Makungu C, Gabriel S, et al. Preliminary evaluation of community-led total sanitation for the control of Taenia solium cysticercosis in Katete District of Zambia. Vet Parasitol. 2015;207(3–4):241–8.CrossRefPubMed
16.
Zurück zum Zitat Dione MM, Ouma EA, Roesel K, Kungu J, Lule P, Pezo D. Participatory assessment of animal health and husbandry practices in smallholder pig production systems in three high poverty districts in Uganda. Prev Vet Med. 2014;117(3–4):565–76.CrossRefPubMed Dione MM, Ouma EA, Roesel K, Kungu J, Lule P, Pezo D. Participatory assessment of animal health and husbandry practices in smallholder pig production systems in three high poverty districts in Uganda. Prev Vet Med. 2014;117(3–4):565–76.CrossRefPubMed
17.
Zurück zum Zitat Muhanguzi D, Lutwama V, Mwiine FN. Factors that influence pig production in Central Uganda - Case study of Nangabo Sub-County, Wakiso district. Vet World. 2012;5(6):346–51.CrossRef Muhanguzi D, Lutwama V, Mwiine FN. Factors that influence pig production in Central Uganda - Case study of Nangabo Sub-County, Wakiso district. Vet World. 2012;5(6):346–51.CrossRef
18.
Zurück zum Zitat Sikasunge CS, Johansen MV, Willingham AL, Leifsson PS, Phiri IK. Taenia solium porcine cysticercosis: viability of cysticerci and persistency of antibodies and cysticercal antigens after treatment with oxfendazole. Vet Parasitol. 2008;158(1–2):57–66.CrossRefPubMed Sikasunge CS, Johansen MV, Willingham AL, Leifsson PS, Phiri IK. Taenia solium porcine cysticercosis: viability of cysticerci and persistency of antibodies and cysticercal antigens after treatment with oxfendazole. Vet Parasitol. 2008;158(1–2):57–66.CrossRefPubMed
19.
Zurück zum Zitat Phiri IK, Dorny P, Gabriel S, Willingham AL, Speybroeck N, Vercruysse J. The prevalence of porcine cysticercosis in Eastern and Southern provinces of Zambia. Vet Parasitol. 2002;108(1):31–9.CrossRefPubMed Phiri IK, Dorny P, Gabriel S, Willingham AL, Speybroeck N, Vercruysse J. The prevalence of porcine cysticercosis in Eastern and Southern provinces of Zambia. Vet Parasitol. 2002;108(1):31–9.CrossRefPubMed
20.
Zurück zum Zitat Ouma E, Dione M, Lule P, Roesel K, Pezo D. Characterization of smallholder pig production systems in Uganda: constraints and opportunities for engaging with market systems. Livest Res Rural Dev. 2014;26:3. Ouma E, Dione M, Lule P, Roesel K, Pezo D. Characterization of smallholder pig production systems in Uganda: constraints and opportunities for engaging with market systems. Livest Res Rural Dev. 2014;26:3.
21.
Zurück zum Zitat Ngowi HA, Carabin H, Kassuku AA, Mlozi MRS, Mlangwa JED, Willingham AL. A health-education intervention trial to reduce porcine cysticercosis in Mbulu District, Tanzania. Prev Vet Med. 2008;85(1–2):52–67.CrossRefPubMed Ngowi HA, Carabin H, Kassuku AA, Mlozi MRS, Mlangwa JED, Willingham AL. A health-education intervention trial to reduce porcine cysticercosis in Mbulu District, Tanzania. Prev Vet Med. 2008;85(1–2):52–67.CrossRefPubMed
22.
Zurück zum Zitat Pawlowski Z. Taeniosis/Neurocysticercosis control as a medical problem—A discussion paper. World J Neurosci. 2016;6(6):165–70.CrossRef Pawlowski Z. Taeniosis/Neurocysticercosis control as a medical problem—A discussion paper. World J Neurosci. 2016;6(6):165–70.CrossRef
24.
Zurück zum Zitat Thys S, Mwape KE, Lefèvre P, Dorny P, Phiri AM, Marcotty T, Phiri IK, Gabriël S. Why pigs are free-roaming: Communities’ perceptions, knowledge and practices regarding pig management and taeniosis/cysticercosis in a Taenia solium endemic rural area in Eastern Zambiatle. Vet Parasitol. 2016;225:33–42.CrossRefPubMed Thys S, Mwape KE, Lefèvre P, Dorny P, Phiri AM, Marcotty T, Phiri IK, Gabriël S. Why pigs are free-roaming: Communities’ perceptions, knowledge and practices regarding pig management and taeniosis/cysticercosis in a Taenia solium endemic rural area in Eastern Zambiatle. Vet Parasitol. 2016;225:33–42.CrossRefPubMed
26.
Zurück zum Zitat Ouma E, Dione M, Lule P, Pezo D, Marshall K, Roesel K, Mayega L, Kiryabwire D, Nadiope G, Jagwe J. Smallholder pig value chain assessment in Uganda : results from producer focus group discussions and key informant interviews. In: ILRI (Research Report). Nairobi: ILRI; 2014. Ouma E, Dione M, Lule P, Pezo D, Marshall K, Roesel K, Mayega L, Kiryabwire D, Nadiope G, Jagwe J. Smallholder pig value chain assessment in Uganda : results from producer focus group discussions and key informant interviews. In: ILRI (Research Report). Nairobi: ILRI; 2014.
27.
Zurück zum Zitat Leslie HJ, Joshua GW, Wright SH, Parkhouse R. Specific detection of circulating surface/secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis. Parasite Immunol. 1989;11:351–70.CrossRef Leslie HJ, Joshua GW, Wright SH, Parkhouse R. Specific detection of circulating surface/secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis. Parasite Immunol. 1989;11:351–70.CrossRef
28.
Zurück zum Zitat ApDia n.v. In vitro diagnostic kit Cysticercosis Ag ELISA. 2004. p. 5–6. ApDia n.v. In vitro diagnostic kit Cysticercosis Ag ELISA. 2004. p. 5–6.
30.
Zurück zum Zitat Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. 2009. p. 102–3. Dohoo I, Martin W, Stryhn H. Veterinary epidemiologic research. 2nd ed. 2009. p. 102–3.
31.
Zurück zum Zitat Krecek RC, Mohammed H, Michael LM, Schantz PM, Ntanjana L, Morey L, et al. Risk factors of porcine cysticercosis in the Eastern Cape Province, South Africa. PLoS One. 2012;7(5):e37718.CrossRefPubMedPubMedCentral Krecek RC, Mohammed H, Michael LM, Schantz PM, Ntanjana L, Morey L, et al. Risk factors of porcine cysticercosis in the Eastern Cape Province, South Africa. PLoS One. 2012;7(5):e37718.CrossRefPubMedPubMedCentral
32.
Zurück zum Zitat FAO. Pig Sector Kenya. FAO Animal Production and Health Livestock Country Reviews. No.3. Rome. 2012. FAO. Pig Sector Kenya. FAO Animal Production and Health Livestock Country Reviews. No.3. Rome. 2012.
33.
Zurück zum Zitat Morales J, Martínez JJ, Rosetti M, Fleury A, Maza V, Hernandez M, Villalobos N, Fragoso G, Aluja A, Larralde C, Sciutto E. Spatial Distribution of Taenia solium Porcine Cysticercosis within a Rural Area of Mexico. Seto E, editor. PLoS Negl Trop Dis. 2008;2(9):7.CrossRef Morales J, Martínez JJ, Rosetti M, Fleury A, Maza V, Hernandez M, Villalobos N, Fragoso G, Aluja A, Larralde C, Sciutto E. Spatial Distribution of Taenia solium Porcine Cysticercosis within a Rural Area of Mexico. Seto E, editor. PLoS Negl Trop Dis. 2008;2(9):7.CrossRef
34.
Zurück zum Zitat Rottbeck R, Nshimiyimana JF, Tugirimana P, Düll UE, Sattler J, Hategekimana J-C, et al. High prevalence of cysticercosis in people with epilepsy in southern Rwanda. PLoS Negl Trop Dis. 2013;7(11):e2558.CrossRefPubMedPubMedCentral Rottbeck R, Nshimiyimana JF, Tugirimana P, Düll UE, Sattler J, Hategekimana J-C, et al. High prevalence of cysticercosis in people with epilepsy in southern Rwanda. PLoS Negl Trop Dis. 2013;7(11):e2558.CrossRefPubMedPubMedCentral
35.
Zurück zum Zitat Murrell KD, Dorny P, Flisser A, Geerts S, Kyvsgaard NC, Mcmanus DP, et al. WHO / FAO / OIE Guidelines for the surveillance, prevention and control of taeniosis / cysticercosis. 2005. Murrell KD, Dorny P, Flisser A, Geerts S, Kyvsgaard NC, Mcmanus DP, et al. WHO / FAO / OIE Guidelines for the surveillance, prevention and control of taeniosis / cysticercosis. 2005.
36.
Zurück zum Zitat Willingham AL, Mugarura A. Taenia solium tapeworms and epilepsy in Uganda. Int Epilepsy News. 2008. p. 10–2. Willingham AL, Mugarura A. Taenia solium tapeworms and epilepsy in Uganda. Int Epilepsy News. 2008. p. 10–2.
37.
Zurück zum Zitat Kolaczinski JH, Onapa AW, Ndyomugyenyi R, Brooker S. Neglected tropical diseases and their control in Uganda. Uganda: Situational analysis and needs assessment for the Malaria Consortium; 2006. Kolaczinski JH, Onapa AW, Ndyomugyenyi R, Brooker S. Neglected tropical diseases and their control in Uganda. Uganda: Situational analysis and needs assessment for the Malaria Consortium; 2006.
38.
39.
Zurück zum Zitat Aiello AE, Larson EL. What is the evidence for a causal link between hygiene and infections? Lancet Infect Dis. 2002;2:103–10.CrossRefPubMed Aiello AE, Larson EL. What is the evidence for a causal link between hygiene and infections? Lancet Infect Dis. 2002;2:103–10.CrossRefPubMed
Metadaten
Titel
Risk factors, perceptions and practices associated with Taenia solium cysticercosis and its control in the smallholder pig production systems in Uganda: a cross-sectional survey
verfasst von
Joseph M. Kungu
Michel M. Dione
Francis Ejobi
Michael Ocaido
Delia Grace
Publikationsdatum
01.12.2017
Verlag
BioMed Central
Erschienen in
BMC Infectious Diseases / Ausgabe 1/2017
Elektronische ISSN: 1471-2334
DOI
https://doi.org/10.1186/s12879-016-2122-x

Weitere Artikel der Ausgabe 1/2017

BMC Infectious Diseases 1/2017 Zur Ausgabe

Leitlinien kompakt für die Innere Medizin

Mit medbee Pocketcards sicher entscheiden.

Seit 2022 gehört die medbee GmbH zum Springer Medizin Verlag

Notfall-TEP der Hüfte ist auch bei 90-Jährigen machbar

26.04.2024 Hüft-TEP Nachrichten

Ob bei einer Notfalloperation nach Schenkelhalsfraktur eine Hemiarthroplastik oder eine totale Endoprothese (TEP) eingebaut wird, sollte nicht allein vom Alter der Patientinnen und Patienten abhängen. Auch über 90-Jährige können von der TEP profitieren.

Niedriger diastolischer Blutdruck erhöht Risiko für schwere kardiovaskuläre Komplikationen

25.04.2024 Hypotonie Nachrichten

Wenn unter einer medikamentösen Hochdrucktherapie der diastolische Blutdruck in den Keller geht, steigt das Risiko für schwere kardiovaskuläre Ereignisse: Darauf deutet eine Sekundäranalyse der SPRINT-Studie hin.

Bei schweren Reaktionen auf Insektenstiche empfiehlt sich eine spezifische Immuntherapie

Insektenstiche sind bei Erwachsenen die häufigsten Auslöser einer Anaphylaxie. Einen wirksamen Schutz vor schweren anaphylaktischen Reaktionen bietet die allergenspezifische Immuntherapie. Jedoch kommt sie noch viel zu selten zum Einsatz.

Therapiestart mit Blutdrucksenkern erhöht Frakturrisiko

25.04.2024 Hypertonie Nachrichten

Beginnen ältere Männer im Pflegeheim eine Antihypertensiva-Therapie, dann ist die Frakturrate in den folgenden 30 Tagen mehr als verdoppelt. Besonders häufig stürzen Demenzkranke und Männer, die erstmals Blutdrucksenker nehmen. Dafür spricht eine Analyse unter US-Veteranen.

Update Innere Medizin

Bestellen Sie unseren Fach-Newsletter und bleiben Sie gut informiert.