cysticercosis in Africa: Risk factors, epidemiology and prospects for control using vaccination

Veterinary Parasitology 195 (2013) 14–23

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Review

Taenia solium taeniosis/cysticercosis in Africa: Risk factors, epidemiology and prospects for control using vaccination Emmanuel Assana a,c,∗ , Marshall W. Lightowlers b , André P. Zoli a , Stanny Geerts d a b c d

University of Ngaoundéré, School of Sciences and Veterinary Medicine, P.O. Box 454, Ngaoundéré, Cameroon Veterinary Clinical Centre, the University of Melbourne, 250 Princes Hwy, Werribee, Victoria 3030, Australia University Institute of the Diocese of Buea, School of Agriculture and Natural Resources, P.O. Box 563, Buea, Cameroon Institute of Tropical Medicine, Nationalestraat 155, B-2000 Antwerpen, Belgium

a r t i c l e

i n f o

Article history: Received 30 April 2012 Received in revised form 4 December 2012 Accepted 11 December 2012 Keywords: Taenia solium Cysticercosis Control Africa Treatment Vaccination

a b s t r a c t Poor sanitary conditions, free-roaming of domestic pigs and lack of awareness of the disease play an important role in the perpetuation of the Taenia solium taeniosis and cysticercosis in Africa. Traditional pig production systems known as the source of T. solium taeniosis/cysticercosis complex are predominant in the continent, representing 60–90% of pig production in rural areas. It has been reported that T. solium cysticercosis is the main cause of acquired epilepsy in human population and results in considerable public health problems and economic costs to the endemic countries. Although the socioeconomic impact and public health burden of cysticercosis have been demonstrated, up to now no large-scale control programme has been undertaken in Africa. Most disease control trials reported in the literature have been located in Latin America and Asia. This review discusses the risk factors and epidemiology of T. solium cysticercosis in Africa and critically analyzes the options available for implementing control of this zoonotic disease in the continent. © 2012 Elsevier B.V. All rights reserved.

Contents 1. 2.

3.

4. 5.

Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Factors favouring T. solium taeniosis/cysticercosis complex in Africa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Limited use or absence of latrines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Pig production systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Limited research interest and investments in pig production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.4. Low priority afforded to the control of cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Epidemiology and disease burden . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.1. Epidemiology of the taeniosis/cysticercosis complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Impact of T. solium cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Tools for the control of T. solium cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusions and prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

14 15 15 15 15 16 16 16 17 18 20 20

1. Introduction ∗ Corresponding author. Tel.: +237 79856332; fax: +237 33322829. E-mail addresses: [email protected], assana [email protected] (E. Assana). 0304-4017/$ – see front matter © 2012 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.vetpar.2012.12.022

The Taenia solium taeniosis/cysticercosis complex constitutes an important public health problem and a serious socioeconomic obstacle for pig breeders in many African

E. Assana et al. / Veterinary Parasitology 195 (2013) 14–23

countries (Zoli et al., 2003; Willingham and Engels, 2006; Carabin et al., 2006). During the 1990s there was optimistic opinion on the control of cysticercosis in developing countries (Cruz et al., 1989). The assumption was based on characteristics of T. solium which suggest it could be eradicated (Schantz et al., 1993; Krecek and Waller, 2006). The failure to control taeniosis/cysticercosis using taeniacidal drug administration (Sarti et al., 2000) and health education through large scale elimination programmes in Latin America (Sarti et al., 1997) and Asia (Allan et al., 2002) has shown that global eradication of this zoonosis is difficult to achieve in the context of persistence of free-roaming pig production. New strategies for controlling cysticercosis have been suggested by Flisser et al. (2006) who argue that intervention measures for control of cysticercosis might involve the international agencies and institutions, such as the World Health Organization, the Food and Agriculture Organization, as well as the commitment of policymakers, scientists and field workers as key means for a sustainable control. Considering the many problems faced by endemic countries and the understandable priority focused on diseases such as malaria, tuberculosis and AIDS, and also the limited resources available in these countries, T. solium is often not provided the attention it deserves and is a particularly neglected disease. In this situation, some researchers suggest that control of T. solium should be focused on the areas with high risk of infection (Molyneux et al., 2004; Ngowi et al., 2010). The objective of this review is to present the predisposing factors and the epidemiological data on T. solium cysticercosis available on the endemic areas of Africa including a critical comparison of various options for the control of this zoonotic disease. Emphasis will be put on the veterinary aspects.

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2.2. Pig production systems The management systems used by pig farmers in Africa are determined by various factors including the source of feed, lack of financial resource for investment in housing and health care requirement (Ajala et al., 2007; Deca et al., 2007; Kagira et al., 2010b; Mutua et al., 2010). In rural areas pig production can be classified into three main categories (Blench, 2000): scavenging/free range system where the pig finds most of its own food, and semi-intensive and intensive systems where the majority of the food consists of domestic kitchen waste (Table 1). About 90% of pigs are reared under scavenging/free range and semi-intensive in Western and Central African countries (Porphyre, 2009). In these pig production systems, poor sanitary conditions play an important role in the circulation of T. solium infection (Zoli et al., 2003). A free-range production system for pigs combined with open field defecation by humans are the conditions in which the animals can gain access to human faeces (Ngowi et al., 2004; Sikasunge et al., 2007; Ganaba et al., 2011). Intensive pig production systems do not always eliminate T. solium transmission because in Cameroon for instance some farmers are known to defecate directly in the pigsties (Shey-Njila et al., 2003). The characteristics of traditional pig production systems favouring T. solium taeniosis/cysticercosis in Eastern and Southern African countries are largely similar to those reported in West and Central Africa (Kagira et al., 2010b; Ngowi et al., 2010). Pig keeping is predominantly of the smallholder, traditional type, characterized by a free-range management system (Phiri et al., 2003; Kagira et al., 2010b). South Africa is the country with the highest number of pigs in the region with at least 25% of these pigs kept in free-range system and exposed to high risk of cysticercosis (Krecek et al., 2008). 2.3. Limited research interest and investments in pig production

2. Factors favouring T. solium taeniosis/cysticercosis complex in Africa 2.1. Limited use or absence of latrines Unhygienic sanitary conditions such as limited use or absence of latrines are prevalent in rural areas of Africa where pigs are raised (Assana et al., 2001; Zoli et al., 2003; Sikasunge et al., 2008a; Gweba et al., 2010). For example in North Cameroon, more than 40% of households keeping pigs in the rural areas have no latrine facility and almost 80% of the pig owners and the members of the household use open field defecation (Assana et al., 2010a). Severe poverty is not the source of this reluctance since even when a latrine is available this does not imply that it is used. In these conditions, tapeworm carriers can disseminate the parasite eggs in their environment leading to the contamination of soil, water, vegetables and other food resources (Gweba et al., 2010). In most studies carried out in Africa, the absence of latrines is found associated with the occurrence of porcine cysticercosis (Ngowi et al., 2004; Sikasunge et al., 2007; Kagira et al., 2010a; Krecek et al., 2012).

One of the characteristics of pig production in Africa is the lack of interest from policy makers and funding agencies for this agricultural activity. For reasons unconnected to their economic importance, pigs are the least well known of all the major species of domestic livestock in Africa (Blench, 2000). It is observed that most research institutes in the continent and funding organizations for agriculture development exclude pig from their activities, even for African swine fever, the most devastating pig disease in Africa (Penrith and Vosloo, 2009). This may be related to the questionable belief that pigs compete with humans for food and probably also for religious reasons. Since Islam forbids Muslims to eat pork and the Muslim population is important in Africa, prejudice against pigs from the governments and potential donor agencies may explain the limited research and funding interest for pigs compared to other domesticated livestock (Blench, 2000). The consequence of this situation is that forgotten smallholders keep 60–90% of total pigs in Africa which are mostly reared under traditional semi-intensive and free range systems favouring the T. solium life cycle (Boa et al., 2006; Porphyre, 2009). These pig production systems are increasing in Africa following the growing demand for meat, particularly

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Table 1 Systems of pig production in Africa. Characteristics

Scavenging Herded Semi-intensive

Intensive

Housing

Ownership

Feeding

Breeding

None None Semi-permanent construction from local materials Modern pens made of concrete with zinc roofing

Often communal Individual Individual smallholders

None Seasonal diet Household waste and sometimes specially grown cassava Agro-industrial by-products

Uncontrolled Uncontrolled Uncontrolled or use of local stud boars

Urban-based entrepreneurs and businessmen

Only selected boars used for stud

Source: Blench, R.M., 2000. A history of pigs in Africa. In: Blench, R.M., MacDonald, K.C (eds.), The Origins and Development of African Livestock. Archaeology, Genetics, Linguistics and Ethnography, UCL Press, pp. 355-367.

in urban areas (Porphyre, 2009; Muhanguzi et al., 2012). Recently, farmers’ perceptions about pig farming practices were assessed (Mutua et al., 2010). Income generation and a faster growth rate compared to other livestock were mentioned by pig farmers as key reasons to keep pigs. Because these systems are becoming the source for high demand of pork in urban areas, the proportion of taeniosis and cysticercosis transmission occurring in these areas is probably progressing. However there has been little research undertaken on human neurocysticercosis in urban areas in Africa. Most of studies on T. solium transmission have been undertaken on pigs in rural areas. 2.4. Low priority afforded to the control of cysticercosis Even though T. solium cysticercosis is one of the neglected tropical diseases targeted for control by the World Health Organization (WHO) Global plan for 2008–2015 (WHO, 2007), up to now no large-scale control programme has been undertaken in Africa. Poor sanitary conditions and free-roaming of pigs identified as important risk factors for swine cysticercosis are mostly related to the low level of education among the pig farmers that limits their knowledge on the management of pigs (Sikasunge et al., 2007; Kagira et al., 2010b). A nearly complete ignorance of the T. solium life cycle involving pigs (cysticercosis) and humans (taeniosis and neurocysticercosis) has been reported in studies carried out in Africa (Assana et al., 2010a; Pondja et al., 2010; Krecek et al., 2012). Most farmers in endemic areas know about the cysts in infected pigs, but few are aware of how pigs get the infection. Little is done in endemic countries to improve the situation. Existing legislation in most or all countries requires infected pigs to be destroyed by the veterinary services, but there is lack of veterinary inspection and most often the infected carcasses are consumed and marketed (Zoli et al., 2003). This situation is increasingly dangerous when it is considered that pork consumption is increasing in African sub-Saharan countries (Porphyre, 2009). This is clearly shown through the development of specific restaurants or places for pork consumption, especially in the cities of West and Central Africa: For example “porc braisé” (grilled or fried pork) in Cameroon, “porc au four” (pork from oven) in Burkina Faso (Koussou and Duteurtre, 2002; Porphyre, 2009). Very often cysticerci are not killed by these meat preparation methods, leading to

a high risk for the infection of consumers and the spread of the T. solium taeniosis. The spread of these pork cooking methods is mostly related to the preference of consumers. It was shown in an assessment of the preference of consumers in N’Jamena city (Chad) that the majority of them ate fried pork (Mopate et al., 2006). 3. Epidemiology and disease burden 3.1. Epidemiology of the taeniosis/cysticercosis complex T. solium cysticercosis is probably widespread in most African countries where pigs are reared under scavenging/free range systems and pork is eaten. However, there are many countries from which no information is available on both human and porcine cysticercosis. Even though epilepsy is a major problem in African countries and may often be associated with neurocysticercosis (Quet et al., 2010; Ndimubanzi et al., 2010), few studies have been undertaken on human cysticercosis. Moreover, the contribution of other parasitic infections of the human brain to epilepsy in Africa remains unclear (Preux and Druet-Cabanac, 2005). Recently it was reported that toxocarosis and paragonimosis could be an important cause of epilepsy in Cameroon in areas where T. solium cysticercosis is already hyper-endemic (Nkouawa et al., 2010, 2011). Although there is a significant association between cysticercosis and epilepsy in Africa (Quet et al., 2010), more studies are needed for the understanding of the various sources of epilepsy. Similarly few data are available about the prevalence of adult tapeworm carriers (taeniosis) who are the source of cysticercosis in humans and pigs. The major difficulty for carrying out studies on adult T. solium is the lack of a simple and sensitive diagnostic test which is able to distinguish eggs of T. solium and T. saginata. Coprological examination which is still often used for the detection of Taenia eggs lacks sensitivity and specificity (Dorny et al., 2005). The Taenia Copro-Ag ELISA that has been used in a few studies because it is not commercialized is more sensitive, but is unfortunately only genus–species (Dorny et al., 2005). However, more information is available about porcine cysticercosis. Tables 2 and 3 present epidemiological data in some African countries on T. solium taeniosis and cysticercosis, respectively. For cysticercosis, the results are based mainly on classical diagnostic tools as tongue or meat inspection and serology for pigs and

E. Assana et al. / Veterinary Parasitology 195 (2013) 14–23

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Table 2 Prevalencea of adult Taenia spp. in some African countries (updated from Zoli et al., 2003). Countries

Prevalence (%)

Target group

References

Burundi

0.22

Newell et al., 1997

Cameroon

0.09 T. soliumb 0.04 T. saginatab 0.37

School children (n = 13841) General population (n = 3109) All villagers > 1 year old (n = 816) 419 school children 384 food handlers School children (n = 1080) School children (n = 800) Pastoralists (n = 204) Hospital patients (n = 401) Hospital patients

D.R. Congo Ethiopiac Ghana

1.4 1.8 0

Guinée (Conakri)

3.8

Kenya Madagascar

2.5 T. saginatad 0.75

Namibia

0.9

Nigeria

8.7

Togo

8 0.01 T. soliume 0.03 T. saginatae 0.09–0.26

Zambia

6.3f

Tanzania

a b c d e f

Hospital patients (n = 1525) Villagers (n = 50) Villagers (n = 1057) Adult population (n = 1170) Village people (n = 708)

Vondou et al., 2002 Kanobana et al., 2011 Terefe et al., 2011 Abera et al., 2010 Nkrumah and Nguah, 2011 Gyorkos et al., 1996 Asaava et al., 2009 Buchy, 2003 Evans and Joubert, 1989 Onah and Chiejina, 1995 Gweba et al., 2010 Eom et al., 2011 Dumas et al., 1990 Mwape et al., 2012

Based on coprological examination (except where indicated). Morphological identification of proglottids. Older reports mention higher prevalences (3.2–6.9%; Tesfa-Yohannes and Ayele, 1983; Mamo et al., 1989). All T. saginata (PCR confirmed). T. solium and T. saginata (PCR confirmed). Based on copro-antigen ELISA.

serology and presence of cysticerci (based on autopsy results) for humans. Serological assays used to assess the epidemiology of T. solium cysticercosis in Africa are mostly the enzymelinked-immunosorbent assay (ELISA) for antigen (Dorny et al., 2004a) or the immunoblot test for antibody detection (Tsang et al., 1989). Prevalence figures are affected by the sensitivity and the specificity of the diagnostic tests (Dorny et al., 2004a). The ELISA for antigen detection has a high value with regard to sensitivity, but shows crossreaction in animals infected with T. hydatigena (Dorny et al., 2004b). Although ELISA for antibody detection is less sensitive than the Ag-ELISA for the detection of cysticercosis in pigs (Dorny et al., 2004a), the immunoblot is more sensitive than the Ag-ELISA for the diagnosis of human cysticercosis (Rodriguez et al., 2009). However, the presence of antibody indicates contact with the parasite and not always the disease. Considering these diagnostic limitations, the epidemiological data obtained on T. solium cysticercosis in Africa cannot be regarded as reflecting a perfectly accurate picture of disease prevalence. In West and Central Africa T. solium cysticercosis has been studied in detail in few countries in both pigs and humans during the past decade, particularly in Cameroon, Zambia and Burkina Faso (Zoli et al., 2003; Sikasunge et al., 2008a; Carabin et al., 2009; Assana et al., 2010a). Recently important foci of porcine and human cysticercosis have been identified in the Democratic Republic of Congo (Praet et al., 2010; Kanobana et al., 2011), Burkina Faso (Ganaba et al., 2011; Carabin et al., 2009) and Senegal (Secka et al.,

2011). In Eastern and Southern African countries, T. solium has been reported as a serious public health and agricultural problem (Mafojane et al., 2003; Phiri et al., 2003; Carabin et al., 2006; Krecek et al., 2008). The epidemiological data on cysticercosis clearly indicates that, with the exception of Muslim countries in North Africa, T. solium cysticercosis is endemic in the all regions of Africa. 3.2. Impact of T. solium cysticercosis Few studies have been undertaken on the disease burden of T. solium cysticercosis in endemic countries. To our knowledge only three publications report an evaluation of the disease burden of T. solium cysticercosis in Africa (Zoli et al., 2003; Carabin et al., 2006; Praet et al., 2009). Of these, the study of Praet et al. (2009) estimates the non-monetary burden of neurocysticercosis using the disability adjusted life year (DALY) as indicated by the Global Burden of Disease (GBD) study (WHO, 2011). In brief, the comprehensive economic impact studies of T. solium cysticercosis in Africa have been carried out in Cameroon and South Africa using Monte Carlo simulations based on combined research results and formal information (Carabin et al., 2006; Praet et al., 2009). In West Cameroon, the total annual costs due to T. solium cysticercosis were estimated at 10,255,202 Euro (6,717,157,310 FCA, local currency), of which 4.7% were due to losses in pig husbandry and 95.3% to direct and indirect losses caused by human cysticercosis. The number of people with neurocysticercosis-associated epilepsy was estimated at

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E. Assana et al. / Veterinary Parasitology 195 (2013) 14–23

Table 3 Prevalence of porcine and human cysticercosis in sub-Saharan Africa (updated from Geerts et al., 2004). Countries

Porcine cysticercosis

Human cysticercosis

Prevalence in pigs

References

Prevalence in humans

Angola Benin

0–6.8a ND

Kama, 1998

ND 1.3b

Burkina Faso Burundi Cameroon

Ganaba et al., 2011 Newell et al., 1997 Pouedet et al., 2002 Assana et al., 2001 Assana et al., 2010a

Central Afr. Republic

32.5–39.6a 2–39a 11.0b , 21.8b 39.8b 24.6b ND

Chad Côte d’Ivoire

40.8b 2.5a

ND ND

D.R. Congo

38.8–41.2b

Assana et al., 2001 Mishra and N’Depo, 1978 Praet et al., 2010

Gambia Ghana Kenya

4.8b 11.7 a 10–14a

Secka et al., 2010a Permin et al., 1999 Phiri et al., 2003

0 ND 2.4b

b

3.5b 10.3b 2.8b 0.7–4.6b

2.4b

21.6b

4 ND

Kagira et al., 2010a

Mozambique Nigeria

39.9b 20.5a 5.85–14.40a

15–21b ND

Rwanda

20a

Senegal South Africa

6.4–13.2b 56.7b

Pondja et al., 2010 Onah and Chiejina, 1995; Gweba et al., 2010 Thienpont et al., 1959 Secka et al., 2010a Krecek et al., 2011

Tanzania

17.4a 7.6a –16.9a 5.9a

ND

Togo Uganda

17a 34–45a

Zambia

8.5b 23.3b

Zimbabwe

28.6a

Ngowi et al., 2004 Boa et al., 2006 Mkupasi et al., 2011 Dumas et al., 1990 Mafojane et al., 2003; Phiri et al., 2003 Waiswa et al., 2009 Sikasunge et al., 2008a Phiri et al., 2003

Madagascar

7–21b

7c 11.9b 8.5 (0.7–20.4)b

References

Houinato et al., 1998 Adjidé et al., 1996 Carabin et al., 2009 Newell et al., 1997 Zoli et al., 2003

Druet-Cabanac et al., 1999

Kanobana et al., 2011 Secka et al., 2010b Waruingi et al., 2002 Andriantsimahavandy et al., 2003 Afonso et al., 2011

Vanderick and Mboryingabo, 1972 Secka et al., 2011 Mafojane et al., 2003

2.4b ND

Dumas et al., 1989

5.8b

Mwape et al., 2012

ND

ND, no available data. a Meat or tongue inspection. b Serology. c Based on presence of cysticerci (at autopsy).

50,326 (1.0% of the local population), whereas the number of pigs diagnosed with cysticercosis was estimated at 15,961 (5.6% of the local pig population). However this estimation gives only an indication rather than an accurate determination of the economic and health impacts. As highlighted by Zoli et al. (2003) the variable picture of human cysticercosis, going from asymptomatic to severe headache, epilepsy and even death, makes it difficult to estimate. Carabin et al. (2006) and Praet et al. (2009) recognize that the calculated economic costs were probably underestimated because the parameters which were taken into account in the studies were only epilepsy in humans and tongue examination of pigs. Other symptoms like chronic headache, hydrocephalus, encephalitis or

ocular cysticercosis in humans were not considered. Besides the economic impact, the social impact due to neurocysticercosis such as stigma of epilepsy, was not taken into account since there is lack of the data to evaluate this social component. Concerning porcine cysticercosis, losses in pig production are likely to be higher than were estimated. 4. Tools for the control of T. solium cysticercosis Avoiding pigs to have access to human faeces, such as through confinement of the animals, is an obvious measure that would reduce T. solium transmission. However, it appears that this will not be realized in the short term

E. Assana et al. / Veterinary Parasitology 195 (2013) 14–23

in the areas where the free roaming system offers an economic advantage to pig breeders (Kagira et al., 2010b). To reduce transmission of the disease, meat inspection should be recommended. However there is a lack of slaughterhouse facilities for pigs in most African countries and the inspection of pork is poorly organized (Zoli et al., 2003). Health education is another approach for control, which has been evaluated in a rural community of Mexico. In a well designed experiment where the situation before and 6 months after an intensive educational intervention was compared, Sarti et al. (1997) showed that there were some changes in the behaviour of the villagers (less free roaming pigs, lower consumption of infected pork, use of latrine), but the long term sustainability of such an intervention is unclear. More recently, Ngowi et al. (2008, 2009) examined the effects of an intensive public education in an endemic area in Tanzania. The most important effect was a significant decrease in the level of consumption of measled pork, but there were no significant changes in the knowledge about the transmission of cysticercosis. Approaches such as the Community Led Total Sanitation (CLTS) (http://www.communityledtotalsanitation.org/page/cltsapproach) aim at reducing open defecation by a participatory approach involving the whole village, but the efficacy has not yet been evaluated for the control of T. solium. It seems to be difficult to control cysticercosis by using health education. General improvement of the economic situation of the endemic areas together with improvements in public health and sanitation and improved pig husbandry are key factors to decrease transmission of T. solium. As a result of improvements in public sanitation and pig husbandry, T. solium cysticercosis has been eliminated in most parts of Western Europe over the last century without any recorded special intervention measure. The impact of mass chemotherapy against human taeniosis using praziquantel was assessed in a rural community in Mexico (Sarti et al., 2000). A reduction of at least 50% of human taeniosis was seen after the treatment programme. Obviously, the effect of chemotherapy against human taeniosis is partial and cannot achieve the goal of elimination of the taeniosis/cysticercosis complex if the entire targeted population is not treated repeatedly. Oxfendazole (OFZ) is effective when used as a single-dose treatment for porcine cysticercosis at 30 mg/kg bodyweight (Gonzalez et al., 1997). The cysticerci survived only in the brain of treated pigs, but this is not considered a source of re-infection since the brain is usually not consumed. Moreover, as a result of concomitant immunity (Richard and Williams, 1982), it was demonstrated that up to 3 months after treatment with OFZ, pigs with cysticercosis did not acquire a new infection (Gonzalez et al., 2001). Although OFZ kills the muscle cysts within 4 weeks, it takes between 8 and 26 weeks before the cysticerci are cleared (Sikasunge et al., 2008b). In a recent study undertaken in an endemic area of Mozambique, Pondja et al. (2012) observed a significant reduction of the risk of cysticercosis if pigs are treated with OFZ at 4 or 9 months of age. At the time of slaughter (12 months old), however, 21.4 and 9.1% of the animals treated at 4 or 9 months were still positive for cysticercosis. The problem of using mass treatment of pigs with OFZ as a control measure arises from the fact that

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the prevalence of porcine cysticercosis in most endemic areas is lower than 50%, indicating that the majority of pigs remain susceptible to T. solium infection after a mass treatment with OFZ. A combined human and porcine mass chemotherapy programme has been undertaken in some Peruvian villages (Garcia et al., 2006). This approach was effective in reducing infection pressure, but did not eliminate the transmission of taeniosis/cysticercosis complex. An attractive option is the use of a vaccine against pig cysticercosis. Several immunogens have been used as vaccines against T. solium cysticercosis in pigs (Plancarte et al., 1999; Huerta et al., 2001; Mayta et al., 2007; Parkhouse et al., 2008). A vaccine candidate against porcine cysticercosis that was widely reported is the synthetic peptide vaccine derived from T. crassiceps antigen, commonly named S3Pvac (Sciutto et al., 2007, 2008). However, under field conditions the S3Pvac gave a protection level of only 50% of the vaccinated pigs (Sciutto et al., 2007). Moreover its initially reported therapeutic value was recently criticized and demonstrated to be low (Lightowlers, 2010a; Aluja de et al., 2011). Obviously S3Pvac will not be useful for a control programme of taeniosis/cysticercosis in endemic areas of Africa. Today, the most effective immunogen is the recombinant antigen designated TSOL18. This vaccine comprises a host-protective protein from the oncosphere of T. solium. It was cloned from mRNA and expressed in Escherichia coli as a fusion protein with glutathione S-transferase (Gauci et al., 1998; Gauci and Lightowlers, 2001). The results of the experimental trials showed that TSOL18 antigen induced almost complete protection against the development of parasites in all vaccinated pigs (Flisser et al., 2004). The TSOL18 vaccine was recently tested under field conditions in Cameroon in combination with OFZ against porcine cysticercosis. The trial was an outstanding success, with parasite transmission being entirely eliminated through the use of three doses of TSOL18 vaccine and a single treatment of the animals with OFZ (Assana et al., 2010b). In a field trial in Peru Jayashi et al. (2012) showed that a combination of TSOL16 and TSOL18 vaccines without OFZ treatment reduced 99.9% the number of viable cysts. Since these recombinant oncosphere vaccines do not affect established metacestodes (Lightowlers, 2010b), it is unclear whether the cysts found at the necropsy in vaccinated pigs were established before or after the vaccination. The OFZ treatment was used in the field trial conducted in Cameroon in the objective to kill any parasite that may have established in pigs prior to vaccination (Assana et al., 2010b). TSOL18 vaccine in combination with OFZ can be considered a novel disease control tool that could reduce human neurocysticercosis in endemic areas in Africa. The drawback of using the TSOL18 is the need of at least two doses to achieve the protection. Assuming that multiple doses increase the cost of vaccination for poor communities in endemic areas, further studies were recommended to examine the effects of a single dose of the vaccine (Lightowlers, 2010b). In the absence of a single dose of vaccine, the approach with two doses TSOL16 + TSOL18 in combination with single treatment of OFZ should be recommended for a programme that has the objective to eliminate T. solium cysticercosis in an area with two distinct

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Table 4 Proposed routine vaccination programme against Taenia solium transmission in the north of Cameroon. Season

Interventions

End of rainy season

Vaccination of all pigs (first dose of TSOL18 + TSOL16) Vaccination of previously vaccinated pigs (second dose of TSOL18 + TSOL16) + oxfendazole treatment Vaccination of unvaccinated piglets born in rainy season (first dose) Vaccination of previously vaccinated pigs born in rainy season (second dose) + treatment with oxfendazole

Beginning of the dry season

Dry season

seasons as the North of Cameroon (Table 4). A survey by Assana (unpublished results, 2012) has shown that the farmers are ready to pay for a vaccine to avoid losses (about 30% of the carcass value) when cysticercosis is detected. 5. Conclusions and prospects Although we have more epidemiological data than 10 years ago T. solium taeniosis/cysticercosis remains “an under-recognized but serious public health problem” in Africa. Seventeen years ago, this statement was a title of an article published in Parasitology Today (Tsang and Wilson, 1995). It is unlikely that T. solium will be considered as a notifiable disease in many African countries in the foreseeable future because of the administrative challenges this would present. Also, the absence of a First World market for cysticercosis intervention tools limits investment of production and registration of new vaccines or chemotherapies (Lightowlers, 2011). However, there is a significant positive evolution in developing countries and farmers are able to invest money for livestock medicines. For example, in Cameroon, since the price paid for a pig decreases with at least 30% if it is found to have cysticerci in the tongue (Zoli et al., 2003), the pig farmers are in search for a tool that can prevent their animals from cysticercosis (Assana, unpublished results). What is needed is to have the vaccine manufactured on a commercial scale and registered for general use (Lightowlers, 2011). Porcine vaccination should be integrated in local or national programmes through a simple strategy of shortterm and long-term interventions, which can be carried out by existing services and structures. Recently it was argued that an elimination programme for a neglected tropical disease may begin with a “vertical control program” as a pilot project followed by a sustainable long term “horizontal program” (Gyapong et al., 2010). This approach should be advisable for T. solium cysticercosis control. A programme is called vertical when it is directed, supervised and executed by specialized services (Gyapong et al., 2010). The rationale for using a vertical strategy at the beginning of the control programme is that it may provide rapid results. In the case of taeniosis/cysticercosis transmission, a pilot control programme may reduce greatly the source

of infection if the coverage is at least 90% (Gonzalez et al., 2002). Re-emergence of the infection in pigs and new cases of taeniosis after the pilot programme could be reduced by continued vaccination of pigs. Through the application of these new disease control measures it is hoped that more attention will be paid to the prevention of T. solium transmission in Africa so as to reduce the burden of neurocysticercosis on the continent.

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