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Citation of this paper

Prevalence and risk factors associated with porcine cysticercosis transmission in Babati district, Tanzania

Michael D B Kavishe, Ernatus M Mkupasi1, Erick V G Komba1 and Helena A Ngowi1

Livestock Training Institute Tengeru, P.O. Box 3101, Arusha, Tanzania.
emkupasi@yahoo.com
1 Department of Veterinary Medicine and Public Health, Sokoine University of Agriculture, P.O. Box 3021, Morogoro, Tanzania.

Abstract

Porcine cysticercosis (PC) caused by T. solium larvae is regarded as one of the most important zoonotic parasites causing great economic losses and affecting many people worldwide. A cross-sectional study was conducted to determine the prevalence of PC and risk factors for its transmission in Babati District, Tanzania. For assessment of potential risk factors, a structured questionnaire was administered to individuals in 150 pig keeping households from 15 randomly selected villages. For prevalence estimation, a total of 442 pigs were subjected to lingual examination and Ag-ELISA test. In addition, postmortem inspection was conducted in nine slaughter slabs involving 1039 pig carcasses.

Results of lingual examination revealed the overall PC prevalence of 13%, with individual village prevalence ranging from 0 to 25%. Ag-ELISA test detected infections in 25% of sampled pigs, individual village prevalence ranging from 0 to 63%. Abattoir survey found a PC prevalence of 8.2% in slaughter pigs. Questionnaire results indicated free ranging of pigs to be a significant (p = 0.0002) risk factor for PC in the area. In conclusion, this study indicates PC to be highly prevalent in Babati District.

Key words: Ag ELISA, free ranging pigs, lingual examination, T. solium, slaughter slabs


Introduction

Pig production plays a crucial role in the livelihood of many rural communities in Tanzania and other developing countries (Phiri et al 2003; Karimuribo et al 2011). The sector is also important in ensuring food and nutrition security in rural communities as well as urban areas where most pigs are transported to and consumed (WHO 2009; Mkupasi et al 2011). Pig production became an attractive investment to many rural smallholder farmers due to high prolificacy, rapid growth rate, relatively small space requirement and ultimately fast economic returns (Lekule and Kyvsgard 2002; Ngowi et al 2004a). Nevertheless, the pig sector in developing countries is facing a number of limitations such as poor housing, poor nutrition, poor genetic potential and parasite and diseases (Petrus et al 2011; Muhanguzi et al 2012). Porcine cysticercosis caused by a zoonotic parasite T. solium is amoung the most important health constraints preventing farmers’ access to formal market and posing high public health risk (Lekule and Kyvsgaard 2003: Phiri et al 2003; Zoli et al 2003; Ngowi et al 2004a ; Pawlowski et al 2005; Ngowi et al 2013).

Taenia solium life cycle is maintained between humans and pigs, however, human can also acquire cysticercosis becoming a dead end host (Pawlowski 2002). Humans acquire the infection through consumption of raw or undercooked infected pork leading to taeniosis (Pawlowski 2002; Del Brutto 2012). Although a number of animal species including dogs and cats can be infected with T. solium larvae, domesticated pigs play a major role in perpetuating the life cycle of the parasite (Ngowi et al 2013). Pigs develop larval stage of the parasite (cysts) in different parts of the body tissues and organs following ingestion of viable T. solium eggs excreted from human carrier of T. solium (Pawlowski 2002). When cysts lodge in the central nervous system (CNS) (neurocysticercosis) they cause severe and sometimes fatal neurologic symptoms in humans (Garcia et al 2003). Epidemiological studies have revealed that PC is widespread in sub-Saharan Africa, Asia and Latin American countries (Phiri et al 2003; Zoli et al 2003; WHO/FAO/OIE 2005).

The impact of the parasite in the affected societies is huge (Zoli et al 2003; Rajshekhar et al 2003). The infection is strongly associated with poverty, pig marketing system and cultural factors (Boa et al 2001; Juyal et al 2008; Willingham III et al 2010); being most prevalent in rural settings, with poor sanitation, free ranging pigs and inadequate pig inspection and pork control (Phiri et al 2003; Assana et al 2012).

In Tanzania, porcine cysticercosis is reported to be highly endemic in many pig producing areas (Ngowi et al 2004a). It has been reported in the northern highlands with prevalence ranging from 0.3 - 17.4% (Nsengwa 1995; Nsengwa and Mbise 1995; Boa et al 1995; Ngowi et al 2004b; Ngowi et al 2004c) and in southern highlands of the country with prevalence ranging from 5.5 - 16.9% (Boa et al 2001; Boa et al 2006). It is also reported to be prevalent in Dodoma, the central part of the country; however, the extent of the problem has not been established (Mkupasi et al 2011). Human infections have also been reported in some studies conducted in the country (Mwang’onde et al 2012; Mwanjali et al 2013), suggesting the parasite to be of serious public health concern prompting immediate control measures to be taken.

Different control strategies have been proposed for control of PC (Schantz et al 1992; Juyal et al 2008). However, the control of the condition in the country has been passive due to limited evidence based information about the extent of T. solium cysticercosis to stakeholders; the information needed to influence them to develop sustainable control programs (Anonymous 2003; WHO 2013). Therefore more epidemiological information is still needed to influence the community at all levels to actively participate in parasite control interventions (Anonymous 2003; Ngowi et al 2004a). Despite the existence of traditional pig production system among small scale pig producers in Babati District, information on the prevalence of porcine cysticercosis and the associated risk factors were lacking. This study was thus carried out to determine the prevalence and potential risk factors for porcine cysticercosis transmission in the area, the information will be useful in planning appropriate control strategies.


Materials and methods

Study Area

This study was conducted in Babati District, Manyara region, northern Tanzania, located between latitudes 4 13S and 4 12 S and longitudes 35 45E and 35 44E during the period of October 2010 to February 2011. The altitude ranges from 950 to 2450 meters above sea level. The area receives rainfall of about 500 - 1200 mm annually with an average temperature range of 22 to 25C. Total population of Babati District was estimated to be 19587 (Anonymous 2012).  Majority of them practice mixed farming, keeping pigs as an important source of household income and animal protein. The study area was selected due to the observed free range pig keeping and the fact that no previous studies on porcine cysticercosis were conducted. When crops are in farms the pigs are confined, while after crops harvest pigs are allowed to freely scavenge. Pig population in Babati District was approximated at 19,587 (Anonymous). Apart from pig keeping, other livestock kept by farmers were cattle, sheep, goats, donkeys and poultry.

Study design and sample size determination for prevalence estimation

This study adopted a cross-sectional design. The sample size for porcine cysticercosis prevalence determination was estimated using the formula n =Z2P (1-P)/L2 (Thrusfield 1995), where: n is required sample size; Z is the multiplier from the normal distribution, P is the expected prevalence and L is the desired absolute precision. Setting p = 0.174 (Ngowi et al 2004b), with Z value of 1.96 at 95% confidence interval (CI) and desired precision (L) of 0.05, the calculated sample size (n) was 221. The obtained sample size was doubled to adjust for the multi-stage sampling (Martin et al 1987). Therefore, a total of 442 pigs were recruited and examined. Six wards were omitted from the study because they had very few pig keeping households. From each of the fifteen wards a list of villages with households keeping pigs was prepared with the help of livestock field officers and local administration and then one village was randomly selected from each ward. In the villages, households keeping pigs were identified using snowball sampling technique where the first household located on one end of the village was identified with guidance of local administration who recruits the next until the whole village was covered. Households with two or more pigs meeting the criteria were included. In households with more than two pigs, a maximum of five pigs were randomly sampled. Piglets younger than two months old and suckling sows were excluded from the study. Piglets younger than two months were left because cysts require about two months to develop after ingestion of eggs; pregnant and suckling sows were excluded to avoid inflicting unnecessary stress.

Survey for porcine cysticercosis and blood sampling

In each household a maximum of five pigs that met our selection criteria were examined for the presence of T. solium cysts by tongue inspection following a procedure described by Gonzalez et al (1990). Briefly, the pig was firmly restrained in lateral recumbence, a pig snare was used to stabilize the head and a wooden stick was used to open the mouth. Using a piece of cotton cloth, the tongue was griped and pulled out, examined and palpated along its ventral side for the presence of cysts. A pig was considered positive for porcine cysticercosis if cyst-like nodule(s) were seen or felt. Subsequently, 5 ml of blood were obtained from the cranial vena cava using plain vacutainer tubes from all tongue examined pigs regardless of their infection status. The blood was transported in a cool box to the nearest Health Centre laboratory. To obtain serum, within eight hours of collection, the clotted blood was separated by centrifugation and serum was dispensed into 2 ml labeled aliquots and stored at -20C until use.

Detection of T. solium cysts circulating antigens

The Ag-ELISA for detection of circulating T. solium cysts antigens was performed as described by Brandt and others (1992) and modified by Dorny and others (2004). Briefly, the serum samples were pre-treated using trichloroacetic acid (TCA) and used in ELISA at a final dilution of 1/4. Two monoclonal antibodies (MoAb) were used in a sandwich ELISA. MoAb B158C11A10 was diluted at 5 mg/ml in carbonate buffer (0.06M/pH 9.6) for coating and a biotinylated MoAb B60H8A4 (1.25 mg/ml in PBS-Tween20 + 1%NBCS) was included as detector antibody. The incubation was carried out at 37C on a shaker for 30 min for the coating of the first MoAb and for 15 min for all subsequent steps. The substrate solution consisting of ortho phenylenediamine (OPD) and H 2O2 was added and incubated without shaking at 37C for 15 min. To stop the reaction, 50 ml of H2SO4 (4N) was added to each well. The plates were read using an ELISA reader at 492 nm. Sera from two known positive pigs were used as positive controls. To determine the cut-off, the optical density (OD) of each serum sample was compared with a series of 8 reference negative serum samples at a probability level of 0.1% using a modified Student’s t-test (Sokal and Rohlf 1981).

Slaughter slab survey for porcine cysticercosis

Retrospective and prospective surveys were also conducted in study villages with slaughter slabs to determine prevalence of porcine cysticercosis in slaughtered pigs. In the prospective study, pigs slaughtered during the study period in villages with slaughter slabs were thoroughly inspected for presence of T. solium larvae. The meat inspection procedures as per government guidelines for routine meat inspection were adopted (Boa et al 2002). Visual inspection and palpation of organs and muscles was followed by incisions. Previous records of PC in the slaughter slabs were also reviewed.

Assessment of risk factors associated with T. solium cysticercosis transmission

A structured questionnaire in Swahili was administered to the head or representative of each household where pigs were sampled. The information concerning general pig production, knowledge about T. solium cysticercosis and the possible risk factors for its transmission reported in endemic areas such as free ranging of pigs, absence of toilets, home slaughter, lack of pork inspection and ignorance about life cycle of the parasite were collected. In cases where the respondent couldn’t speak Swahili the questionnaire was translated and administered in native language (Iraqw). The information on hygiene and sanitary practices was supplemented with direct observation.

Statistical data analysis

Collected data in this study were analysed using Epi Info statistical software version 7. For prevalence data descriptive statistics were computed to determine proportions. The Chi-square test was used to determine the significance of differences in proportions at p≤0.05. Agreement between tongue examination and Ag-ELISA tests was determined using Kappa statistic. Risk factor data were analyzed in two steps; 1) Univariate logistic regression was used to screen all potential risk factors for statistical significance at a p-value of ≤0.20, 2); statistically significant variables in univariate logistic regression were included in a multivariable logistic regression analysis based on a forward variable selection approach utilising the likelihood ratio statistic at a p-value ≤0.05. The Mantel-Haenszel method was used to identify confounding factors. A factor was considered to have potential confounding effect if its magnitude of change was ≥25% in the coefficient estimates of other predictors. Goodness of fit of the final model was assessed by using the Hosmer and Lemeshow test (Hosmer and Lemeshow, 2002). The final model was assessed for discrimination ability using receiver operating characteristic curves (ROC), based on area under the curve (AUC) (Balk et al., 2006).


Results

Descriptive statistics

In this study a total of 442 pigs aged 2 months to 5 years were examined from 150 households. Ninety seven percent of the sampled pigs were of indigenous breeds, the rest were crosses between local and Large White and 64.3% were female.

A total of 87 males and 63 females, members from the sampled households were interviewed, their age ranged from 20 - 90 years. The possible risk factors of T. solium cysticercosis transmission were as presented in Table 1.

Table 1. Household’s characteristics on potential risk factors for T. solium transmission

Risk factors

Yes (%)

No (%)

Pig confinement

31

69

Pork consumption

97

3

Home slaughter

86.7

23.3

Pig inspection

1

99

Presence of latrine

30

70

Awareness on porcine cysticercosis

93

7

Knowledge on how pig acquire the infection

12.7

87.3

Knowledge on the link between pig and human infections

4.7

95.3

Prevalence of porcine cysticercosis in sampled pigs

The overall prevalence of PC in the sampled pigs was 12.9% (95% CI: 8.98% - 18.05%) and 25% (95% CI: 19.6% - 31.3%) based on tongue examination and Ag-ELISA tests, respectively. The individual village prevalence ranged from 0% to 25% by tongue examination, with 40% of the villages being infected. On the other hand, Ag-ELISA test detected PC in 73.3% of the villages involved in the study with the individual village prevalence ranging from 0% to 63.6%. Furthermore, there was a good agreement between the ante-mortem tongue examination method and the Ag-ELISA test in detecting PCC (kappa = 0.61).

Prevalence of porcine cysticercosis by meat inspection

During the study period a total of 1039 pigs were slaughtered and inspected in nine slaughter slabs, an average of 115 pigs per slab (37-184). Meat inspection revealed a prevalence of PC of 8.2% with a range of 5.8 % to 24 % for individual slaughter slab.

T. solium cysticercosis transmission risk factors

Considering other factors in the multivariate logistic regression model, Free-range husbandry system was significantly associated with PC transmission (OR = 5.17; 95% CI = 2.20 to 12.1).

Table 2. Multivariate analysis of factors associated with positive Ag-ELISA test result in pigs in Babati District, Tanzania

Risk factor

Level

%

Prevalence

Odds ratio

p-value

Pork consumption

Yes

93

20

1

No

7

40

0.375(0.101 – 1.39

0.141

 

Home slaughter of pigs

Yes

86.7

30

1

No

23.3

42.3

0.584(0.211-1.62)

0.300

 

Free ranging of pigs

Yes

31

17

1

No

69

51.5

5.17(2.20-12.1)

<0.001

 

Awareness on cysticercosis

Yes

83

47.4

1

No

17

39.7

0.731(0.278-1.92)

0.526

 

Presence of toilet/latrine

Yes

30

44.4

1

NO

70

39

1.25(0.61-2.53)

0.537


Discussion

From this study we report a high prevalence of PC in the area, and that free range of pigs is important risk factor responsible for the observed infection rate in the study area (Table 2). The observed high prevalence of T. solium cysticercosis in pigs diagnosed by tongue examination in smallholder farmers in the area is similar to what was reported from Mbulu (Ngowi et al 2004b) and southern highlands of the country (Boa et al 2006). The meat inspection results are also comparable to those obtained in other studies conducted elsewhere in the country (Boa et al 1995; Ngowi et al 2004c; Boa et al 2006; Komba et al 2013). However, Mkupasi et al (2011) reported a lower prevalence in pigs slaughtered in Dar es Salaam possibly because of mixed pig origins. As expected, the Ag-ELISA test was more sensitive than the other two techniques, detecting almost twice as much of the infected pigs (Nguekam et al 2003; Sikasunge et al 2008). These results indicate that the condition is highly prevalent in the area implying the existence of the risk factors for T. solium cysticercosis transmission allowing complete cycle of the parasite to occur. Although tongue examination is known to be quick and inexpensive, being a useful tool in screening purposes in endemic areas for PC, it is continuously being proven to be of low sensitivity, grossly under reporting the infection (Gonzalez et al 1990; Gonzalez et al 2001; Ito et al 2003; Dorny et al 2004; Phiri et al 2006).

Understanding the risk factors for the parasite transmission is crucial for planning effective control strategies. Most smallholder pig farmers in the study area practice free range husbandry system (Tab. 1); pigs get access to T. solium eggs if outdoor defecation is practiced. Similar observation has been previously reported by other researchers in the country and elsewhere (Sarti et al 1992; Pouedet et al 2002; Phiri et al 2003; Zoli et al 2003; Ngowi et al 2004a; Sikasunge et al 2007).

Questionnaire results indicated general lack of knowledge about epidemiological link existing between T. solium infections in humans and pigs in the studied community (Tab. 1), making them difficulty to adopt control measures. The lack of knowledge about the parasite life cycle and the way socio-economic conditions influence the transmission has been found to fuel transmission of T. solium cysticercosis in different rural communities (Krecek et al 2012). In this study the prevalence of PC didn’t show significant difference among households with and without knowledge about the parasite (p=0.526). Pondja et al (2010) had a similar observation in a study conducted in a rural community in Mozambique. May be there are some factors which mask its effect. However, health education campaigns have been reported to be effective in reducing the transmission rates of T. solium infections in humans and pigs (Sarti and Rajshekhar 2003; Ngowi et al., 2008). It has been postulated that health education increases awareness and knowledge for the infection is important for a control program to be successful (Maridadi et al 2011; Krecek et al 2012; WHO 2013).

Pigs must get access to human faeces to sustain T. solium life cycle (Schantz et al 1992). In spite of that, in this study the occurrence of PC did not differ significantly between households with and without latrines (P = 0.5378). Our observation differs from some researchers who found positive association between occurrence of PC and lack of toilet/latrine in the households (Ngowi et al 2004b; Sikasunge et al 2007; Krecek et al 2012). However, some studies similarly reported lack of association between presence of toilet/latrine and PC occurrence (Sarti et al 1992; Pouedet et al 2002; Pondja et al 2010). The observation in this study could be due to the fact that when members of families with no access to latrines practice outdoor defecation, they contaminate the environment. Free roaming pigs from households with and without latrines accesses the faeces. Another possible explanation is that, some households may have toilets/latrines but still members practice open air defecation. In most communities the children are discouraged to use the toilet/latrine due to danger of falling into a pit or drowning (Phaswana – Mafuya 2006).

In explaining the same finding in Burkina Faso, Ganaba et al (2011) pointed out that in some village communities; a risk associated with lifestyle in one family is shared by other families nearby. Also most of the toilets/latrines were observed to lack closing doors and always had human faeces on the floor; allowing roaming pigs to get access to the faeces. Furthermore, in some communities people refrain themselves from using toilet/latrines due to cultural beliefs or presence of foul smell, flies and lack of privacy (Rajshekhar et al 2003; Phaswana – Mafuya 2006). This suggests more work to be done to promote the individuals not only to have toilets/latrines, but also properly use them. Local by laws should be formulated and enforced to ensure compliance.

To our surprise, no case was found in the retrospective data which indicate that either the pigs were not inspected or the findings were not recorded. Most pigs in the area were reported to be slaughtered at home and consumed without official inspection (Tab. 1). This may endanger the health of the community as infected pigs enter the food chain and perpetuate the infection. With the aim to reduce the problem, the government of Tanzania has increased recruitment of livestock field officers; however, they should be updated about the problem and the need to excise active pig inspection and control. Close monitoring of their day to day activities at all levels is required.


Conclusions


Acknowledgement

We are thankful to Danish International Development Agency (DANIDA) for financing this work through Securing Livelihood through Improve Pig Production (SLIPP) project, under Grant number 09-07-LIFE. We also thank the farmers and meat inspectors for accepting to participate in this study.


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Received 19 May 2015; Accepted 24 November 2016; Published 1 January 2017

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