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Veterinary Parasitology 195 (2013) 14– 23

Contents lists available at SciVerse ScienceDirect

Veterinary Parasitology

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eview

aenia solium taeniosis/cysticercosis in Africa: Risk factors,pidemiology and prospects for control using vaccination

mmanuel Assanaa,c,∗, Marshall W. Lightowlersb, André P. Zoli a, Stanny Geertsd

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

r t i c l e i n f o

rticle history:eceived 30 April 2012eceived in revised form 4 December 2012ccepted 11 December 2012

eywords:aenia solium

a b s t r a c t

Poor sanitary conditions, free-roaming of domestic pigs and lack of awareness of the diseaseplay an important role in the perpetuation of the Taenia solium taeniosis and cysticercosisin Africa. Traditional pig production systems known as the source of T. solium taenio-sis/cysticercosis complex are predominant in the continent, representing 60–90% of pigproduction in rural areas. It has been reported that T. solium cysticercosis is the main causeof acquired epilepsy in human population and results in considerable public health prob-lems and economic costs to the endemic countries. Although the socioeconomic impact and

ysticercosis

ontrolfricareatmentaccination

public health burden of cysticercosis have been demonstrated, up to now no large-scale con-trol programme has been undertaken in Africa. Most disease control trials reported in theliterature have been located in Latin America and Asia. This review discusses the risk fac-tors and epidemiology of T. solium cysticercosis in Africa and critically analyzes the optionsavailable for implementing control of this zoonotic disease in the continent.

© 2012 Elsevier B.V. All rights reserved.

ontents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 142. Factors favouring T. solium taeniosis/cysticercosis complex in Africa . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15

2.1. Limited use or absence of latrines . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152.2. Pig production systems . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152.3. Limited research interest and investments in pig production . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 152.4. Low priority afforded to the control of cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 16

3. Epidemiology and disease burden. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163.1. Epidemiology of the taeniosis/cysticercosis complex . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 163.2. Impact of T. solium cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17

4. Tools for the control of T. solium cysticercosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 185. Conclusions and prospects . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .

∗ Corresponding author. Tel.: +237 79856332; fax: +237 33322829.E-mail addresses: assana@uidb-cameroon.net, assana e@yahoo.fr

E. Assana).

304-4017/$ – see front matter © 2012 Elsevier B.V. All rights reserved.ttp://dx.doi.org/10.1016/j.vetpar.2012.12.022

. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 20

1. Introduction

The Taenia solium taeniosis/cysticercosis complex con-stitutes an important public health problem and a serioussocioeconomic obstacle for pig breeders in many African

ry Parasi

E. Assana et al. / Veterina

countries (Zoli et al., 2003; Willingham and Engels, 2006;Carabin et al., 2006).

During the 1990s there was optimistic opinion on thecontrol 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 controltaeniosis/cysticercosis using taeniacidal drug administra-tion (Sarti et al., 2000) and health education through largescale elimination programmes in Latin America (Sarti et al.,1997) and Asia (Allan et al., 2002) has shown that globaleradication of this zoonosis is difficult to achieve in thecontext of persistence of free-roaming pig production.New strategies for controlling cysticercosis have been sug-gested by Flisser et al. (2006) who argue that interventionmeasures for control of cysticercosis might involve theinternational agencies and institutions, such as the WorldHealth Organization, the Food and Agriculture Organiza-tion, as well as the commitment of policymakers, scientistsand field workers as key means for a sustainable con-trol. Considering the many problems faced by endemiccountries and the understandable priority focused on dis-eases such as malaria, tuberculosis and AIDS, and also thelimited resources available in these countries, T. solium isoften not provided the attention it deserves and is a partic-ularly neglected disease. In this situation, some researcherssuggest that control of T. solium should be focused on theareas with high risk of infection (Molyneux et al., 2004;Ngowi et al., 2010). The objective of this review is to presentthe predisposing factors and the epidemiological data on T.solium cysticercosis available on the endemic areas of Africaincluding a critical comparison of various options for thecontrol of this zoonotic disease. Emphasis will be put onthe veterinary aspects.

2. Factors favouring T. soliumtaeniosis/cysticercosis complex in Africa

2.1. Limited use or absence of latrines

Unhygienic sanitary conditions such as limited use orabsence of latrines are prevalent in rural areas of Africawhere pigs are raised (Assana et al., 2001; Zoli et al., 2003;Sikasunge et al., 2008a; Gweba et al., 2010). For examplein North Cameroon, more than 40% of households keepingpigs in the rural areas have no latrine facility and almost80% of the pig owners and the members of the house-hold use open field defecation (Assana et al., 2010a). Severepoverty is not the source of this reluctance since evenwhen a latrine is available this does not imply that it isused. In these conditions, tapeworm carriers can dissemi-nate the parasite eggs in their environment leading to thecontamination of soil, water, vegetables and other foodresources (Gweba et al., 2010). In most studies carried out

in Africa, the absence of latrines is found associated withthe occurrence of porcine cysticercosis (Ngowi et al., 2004;Sikasunge et al., 2007; Kagira et al., 2010a; Krecek et al.,2012).

tology 195 (2013) 14– 23 15

2.2. Pig production systems

The management systems used by pig farmers in Africaare determined by various factors including the source offeed, lack of financial resource for investment in housingand health care requirement (Ajala et al., 2007; Deca et al.,2007; Kagira et al., 2010b; Mutua et al., 2010). In ruralareas pig production can be classified into three main cate-gories (Blench, 2000): scavenging/free range system wherethe pig finds most of its own food, and semi-intensive andintensive systems where the majority of the food consistsof domestic kitchen waste (Table 1). About 90% of pigs arereared under scavenging/free range and semi-intensive inWestern and Central African countries (Porphyre, 2009).In these pig production systems, poor sanitary conditionsplay an important role in the circulation of T. solium infec-tion (Zoli et al., 2003). A free-range production system forpigs combined with open field defecation by humans arethe conditions in which the animals can gain access tohuman faeces (Ngowi et al., 2004; Sikasunge et al., 2007;Ganaba et al., 2011). Intensive pig production systems donot always eliminate T. solium transmission because inCameroon for instance some farmers are known to defecatedirectly in the pigsties (Shey-Njila et al., 2003). The char-acteristics of traditional pig production systems favouringT. solium taeniosis/cysticercosis in Eastern and SouthernAfrican countries are largely similar to those reported inWest and Central Africa (Kagira et al., 2010b; Ngowi et al.,2010). Pig keeping is predominantly of the smallholder, tra-ditional type, characterized by a free-range managementsystem (Phiri et al., 2003; Kagira et al., 2010b). South Africais the country with the highest number of pigs in the regionwith at least 25% of these pigs kept in free-range system andexposed to high risk of cysticercosis (Krecek et al., 2008).

2.3. Limited research interest and investments in pigproduction

One of the characteristics of pig production in Africa isthe lack of interest from policy makers and funding agen-cies for this agricultural activity. For reasons unconnectedto their economic importance, pigs are the least well knownof all the major species of domestic livestock in Africa(Blench, 2000). It is observed that most research institutesin the continent and funding organizations for agriculturedevelopment exclude pig from their activities, even forAfrican swine fever, the most devastating pig disease inAfrica (Penrith and Vosloo, 2009). This may be related tothe questionable belief that pigs compete with humans forfood and probably also for religious reasons. Since Islamforbids Muslims to eat pork and the Muslim population isimportant in Africa, prejudice against pigs from the gov-ernments and potential donor agencies may explain thelimited research and funding interest for pigs comparedto other domesticated livestock (Blench, 2000). The con-sequence of this situation is that forgotten smallholderskeep 60–90% of total pigs in Africa which are mostly reared

under traditional semi-intensive and free range systemsfavouring the T. solium life cycle (Boa et al., 2006; Porphyre,2009). These pig production systems are increasing inAfrica following the growing demand for meat, particularly

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

Table 1Systems of pig production in Africa.

Characteristics

Housing Ownership Feeding Breeding

Scavenging None Often communal None UncontrolledHerded None Individual Seasonal diet UncontrolledSemi-intensive Semi-permanent

construction from localmaterials

Individual smallholders Household waste andsometimes speciallygrown cassava

Uncontrolled or use oflocal stud boars

Intensive Modern pens made ofconcrete with zinc

Urban-basedentrepreneurs and

Agro-industrialby-products

Only selected boarsused for stud

S onald, KG

iRwattotptMt

2

nW2p

tmpmAinietgiceamdi2sc“aDn

roofing businessmen

ource: Blench, R.M., 2000. A history of pigs in Africa. In: Blench, R.M., MacDenetics, Linguistics and Ethnography, UCL Press, pp. 355-367.

n urban areas (Porphyre, 2009; Muhanguzi et al., 2012).ecently, farmers’ perceptions about pig farming practicesere assessed (Mutua et al., 2010). Income generation and

faster growth rate compared to other livestock were men-ioned by pig farmers as key reasons to keep pigs. Becausehese systems are becoming the source for high demandf pork in urban areas, the proportion of taeniosis and cys-icercosis transmission occurring in these areas is probablyrogressing. However there has been little research under-aken on human neurocysticercosis in urban areas in Africa.

ost of studies on T. solium transmission have been under-aken on pigs in rural areas.

.4. Low priority afforded to the control of cysticercosis

Even though T. solium cysticercosis is one of theeglected tropical diseases targeted for control by theorld Health Organization (WHO) Global plan for

008–2015 (WHO, 2007), up to now no large-scale controlrogramme has been undertaken in Africa.

Poor sanitary conditions and free-roaming of pigs iden-ified as important risk factors for swine cysticercosis are

ostly related to the low level of education among theig farmers that limits their knowledge on the manage-ent of pigs (Sikasunge et al., 2007; Kagira et al., 2010b).

nearly complete ignorance of the T. solium life cyclenvolving pigs (cysticercosis) and humans (taeniosis andeurocysticercosis) has been reported in studies carried out

n Africa (Assana et al., 2010a; Pondja et al., 2010; Krecekt al., 2012). Most farmers in endemic areas know abouthe cysts in infected pigs, but few are aware of how pigset the infection. Little is done in endemic countries tomprove the situation. Existing legislation in most or allountries requires infected pigs to be destroyed by the vet-rinary services, but there is lack of veterinary inspectionnd most often the infected carcasses are consumed andarketed (Zoli et al., 2003). This situation is increasingly

angerous when it is considered that pork consumptions increasing in African sub-Saharan countries (Porphyre,009). This is clearly shown through the development ofpecific restaurants or places for pork consumption, espe-ially in the cities of West and Central Africa: For example

porc braisé” (grilled or fried pork) in Cameroon, “porcu four” (pork from oven) in Burkina Faso (Koussou anduteurtre, 2002; Porphyre, 2009). Very often cysticerci areot killed by these meat preparation methods, leading to

.C (eds.), The Origins and Development of African Livestock. Archaeology,

a high risk for the infection of consumers and the spreadof the T. solium taeniosis. The spread of these pork cookingmethods is mostly related to the preference of consumers.It was shown in an assessment of the preference of con-sumers in N’Jamena city (Chad) that the majority of themate 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 mostAfrican countries where pigs are reared under scaveng-ing/free range systems and pork is eaten. However, thereare many countries from which no information is avail-able on both human and porcine cysticercosis. Even thoughepilepsy is a major problem in African countries andmay often be associated with neurocysticercosis (Quetet al., 2010; Ndimubanzi et al., 2010), few studies havebeen undertaken on human cysticercosis. Moreover, thecontribution of other parasitic infections of the humanbrain to epilepsy in Africa remains unclear (Preux andDruet-Cabanac, 2005). Recently it was reported that toxo-carosis and paragonimosis could be an important cause ofepilepsy in Cameroon in areas where T. solium cysticerco-sis is already hyper-endemic (Nkouawa et al., 2010, 2011).Although there is a significant association between cys-ticercosis and epilepsy in Africa (Quet et al., 2010), morestudies are needed for the understanding of the varioussources of epilepsy. Similarly few data are available aboutthe prevalence of adult tapeworm carriers (taeniosis) whoare the source of cysticercosis in humans and pigs. Themajor difficulty for carrying out studies on adult T. soliumis the lack of a simple and sensitive diagnostic test whichis able to distinguish eggs of T. solium and T. saginata.Coprological examination which is still often used for thedetection of Taenia eggs lacks sensitivity and specificity(Dorny et al., 2005). The Taenia Copro-Ag ELISA that hasbeen used in a few studies because it is not commercializedis more sensitive, but is unfortunately only genus–species(Dorny et al., 2005). However, more information is avail-able about porcine cysticercosis. Tables 2 and 3 present

epidemiological data in some African countries on T. soliumtaeniosis and cysticercosis, respectively. For cysticercosis,the results are based mainly on classical diagnostic toolsas tongue or meat inspection and serology for pigs and

E. Assana et al. / Veterinary Parasitology 195 (2013) 14– 23 17

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

Countries Prevalence (%) Target group References

Burundi 0.22 School children(n = 13841)

Newell et al., 1997

Cameroon 0.09 T. soliumb

0.04 T. saginatabGeneral population(n = 3109)

Vondou et al., 2002

D.R. Congo 0.37 All villagers > 1 year old(n = 816)

Kanobana et al., 2011

Ethiopiac 1.4 419 school children Terefe et al., 20111.8 384 food handlers Abera et al., 2010

Ghana 0 School children(n = 1080)

Nkrumah and Nguah,2011

Guinée (Conakri) 3.8 School children(n = 800)

Gyorkos et al., 1996

Kenya 2.5 T. saginatad Pastoralists (n = 204) Asaava et al., 2009Madagascar 0.75 Hospital patients

(n = 401)Buchy, 2003

Namibia 0.9 Hospital patients Evans and Joubert,1989

Nigeria 8.7 Hospital patients(n = 1525)

Onah and Chiejina,1995

8 Villagers (n = 50) Gweba et al., 2010Tanzania 0.01 T. soliume Villagers

(n = 1057)Eom et al.,20110.03 T. saginatae

Togo 0.09–0.26 Adult population(n = 1170)

Dumas et al., 1990

Zambia 6.3f Village people (n = 708) Mwape et al., 2012

a Based on coprological examination (except where indicated).b Morphological identification of proglottids.c Older reports mention higher prevalences (3.2–6.9%; Tesfa-Yohannes and Ayele, 1983; Mamo et al., 1989).d

All T. saginata (PCR confirmed).e T. solium and T. saginata (PCR confirmed).f Based on copro-antigen ELISA.

serology and presence of cysticerci (based on autopsyresults) for humans.

Serological assays used to assess the epidemiology ofT. solium cysticercosis in Africa are mostly the enzyme-linked-immunosorbent assay (ELISA) for antigen (Dornyet al., 2004a) or the immunoblot test for antibody detec-tion (Tsang et al., 1989). Prevalence figures are affected bythe sensitivity and the specificity of the diagnostic tests(Dorny et al., 2004a). The ELISA for antigen detection hasa high value with regard to sensitivity, but shows cross-reaction in animals infected with T. hydatigena (Dorny et al.,2004b). Although ELISA for antibody detection is less sen-sitive than the Ag-ELISA for the detection of cysticercosis inpigs (Dorny et al., 2004a), the immunoblot is more sensitivethan the Ag-ELISA for the diagnosis of human cysticercosis(Rodriguez et al., 2009). However, the presence of anti-body indicates contact with the parasite and not alwaysthe disease. Considering these diagnostic limitations, theepidemiological data obtained on T. solium cysticercosis inAfrica cannot be regarded as reflecting a perfectly accuratepicture of disease prevalence.

In West and Central Africa T. solium cysticercosis hasbeen studied in detail in few countries in both pigs andhumans 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 havebeen identified in the Democratic Republic of Congo (Praetet al., 2010; Kanobana et al., 2011), Burkina Faso (Ganabaet al., 2011; Carabin et al., 2009) and Senegal (Secka et al.,

2011). In Eastern and Southern African countries, T. soliumhas been reported as a serious public health and agricul-tural problem (Mafojane et al., 2003; Phiri et al., 2003;Carabin et al., 2006; Krecek et al., 2008). The epidemio-logical data on cysticercosis clearly indicates that, with theexception of Muslim countries in North Africa, T. soliumcysticercosis is endemic in the all regions of Africa.

3.2. Impact of T. solium cysticercosis

Few studies have been undertaken on the disease bur-den of T. solium cysticercosis in endemic countries. To ourknowledge only three publications report an evaluation ofthe disease burden of T. solium cysticercosis in Africa (Zoliet al., 2003; Carabin et al., 2006; Praet et al., 2009). Of these,the study of Praet et al. (2009) estimates the non-monetaryburden of neurocysticercosis using the disability adjustedlife year (DALY) as indicated by the Global Burden of Dis-ease (GBD) study (WHO, 2011).

In brief, the comprehensive economic impact studiesof T. solium cysticercosis in Africa have been carried outin Cameroon and South Africa using Monte Carlo simu-lations based on combined research results and formalinformation (Carabin et al., 2006; Praet et al., 2009). In WestCameroon, the total annual costs due to T. solium cysticer-cosis were estimated at 10,255,202 Euro (6,717,157,310

FCA, local currency), of which 4.7% were due to lossesin pig husbandry and 95.3% to direct and indirect lossescaused by human cysticercosis. The number of people withneurocysticercosis-associated epilepsy was estimated at

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

Table 3Prevalence 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 inhumans

References

Angola 0–6.8a Kama, 1998 NDBenin ND 1.3b Houinato et al.,

19983.5b Adjidé et al., 1996

Burkina Faso 32.5–39.6a Ganaba et al., 2011 10.3b Carabin et al., 2009Burundi 2–39a Newell et al., 1997 2.8b Newell et al., 1997Cameroon 11.0b, 21.8b Pouedet et al., 2002 0.7–4.6b Zoli et al., 2003

39.8b Assana et al., 200124.6b Assana et al., 2010a

Central Afr. Republic ND 2.4b Druet-Cabanacet al., 1999

Chad 40.8b Assana et al., 2001 NDCôte d’Ivoire 2.5a Mishra and N’Depo,

1978ND

D.R. Congo 38.8–41.2b Praet et al., 2010 21.6b Kanobana et al.,2011

Gambia 4.8b Secka et al., 2010a 0 Secka et al., 2010bGhana 11.7 a Permin et al., 1999 NDKenya 10–14a Phiri et al., 2003 2.4b Waruingi et al.,

20024b Kagira et al., 2010a

Madagascar ND 7–21b Andriantsimahavandyet al., 2003

Mozambique 39.9b Pondja et al., 2010 15–21b Afonso et al., 2011Nigeria 20.5a

5.85–14.40aOnah and Chiejina,1995;Gweba et al., 2010

ND

Rwanda 20a Thienpont et al.,1959

7c Vanderick andMboryingabo, 1972

Senegal 6.4–13.2b Secka et al., 2010a 11.9b Secka et al., 2011South Africa 56.7b Krecek et al., 2011 8.5 (0.7–20.4)b Mafojane et al.,

2003Tanzania 17.4a Ngowi et al., 2004 ND

7.6a–16.9a Boa et al., 20065.9a Mkupasi et al.,

2011Togo 17a Dumas et al., 1990 2.4b Dumas et al., 1989Uganda 34–45a Mafojane et al.,

2003; Phiri et al.,2003

ND

8.5b Waiswa et al., 2009Zambia 23.3b Sikasunge et al.,

2008a5.8b Mwape et al., 2012

Zimbabwe 28.6a Phiri et al., 2003 ND

ND, no available data.a

5b1erAhheratht

Meat or tongue inspection.b Serology.c Based on presence of cysticerci (at autopsy).

0,326 (1.0% of the local population), whereas the num-er of pigs diagnosed with cysticercosis was estimated at5,961 (5.6% of the local pig population). However thisstimation gives only an indication rather than an accu-ate determination of the economic and health impacts.s highlighted by Zoli et al. (2003) the variable picture ofuman cysticercosis, going from asymptomatic to severeeadache, epilepsy and even death, makes it difficult tostimate. Carabin et al. (2006) and Praet et al. (2009)ecognize that the calculated economic costs were prob-

bly underestimated because the parameters which wereaken into account in the studies were only epilepsy inumans and tongue examination of pigs. Other symp-oms like chronic headache, hydrocephalus, encephalitis or

ocular cysticercosis in humans were not considered.Besides the economic impact, the social impact due to neu-rocysticercosis such as stigma of epilepsy, was not takeninto account since there is lack of the data to evaluate thissocial component. Concerning porcine cysticercosis, lossesin pig production are likely to be higher than were esti-mated.

4. Tools for the control of T. solium cysticercosis

Avoiding pigs to have access to human faeces, such asthrough confinement of the animals, is an obvious mea-sure that would reduce T. solium transmission. However,it appears that this will not be realized in the short term

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E. Assana et al. / Veterina

in the areas where the free roaming system offers aneconomic advantage to pig breeders (Kagira et al., 2010b).To reduce transmission of the disease, meat inspectionshould be recommended. However there is a lack ofslaughterhouse facilities for pigs in most African countriesand 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 beforeand 6 months after an intensive educational interventionwas compared, Sarti et al. (1997) showed that there weresome changes in the behaviour of the villagers (less freeroaming pigs, lower consumption of infected pork, use oflatrine), but the long term sustainability of such an inter-vention is unclear. More recently, Ngowi et al. (2008, 2009)examined the effects of an intensive public education in anendemic area in Tanzania. The most important effect was asignificant decrease in the level of consumption of measledpork, but there were no significant changes in the knowl-edge about the transmission of cysticercosis. Approachessuch as the Community Led Total Sanitation (CLTS)(http://www.communityledtotalsanitation.org/page/clts-approach) aim at reducing open defecation by a participa-tory approach involving the whole village, but the efficacyhas not yet been evaluated for the control of T. solium. Itseems to be difficult to control cysticercosis by using healtheducation. General improvement of the economic situa-tion of the endemic areas together with improvements inpublic health and sanitation and improved pig husbandryare key factors to decrease transmission of T. solium. Asa result of improvements in public sanitation and pighusbandry, T. solium cysticercosis has been eliminatedin most parts of Western Europe over the last centurywithout any recorded special intervention measure.

The impact of mass chemotherapy against humantaeniosis using praziquantel was assessed in a rural com-munity in Mexico (Sarti et al., 2000). A reduction of atleast 50% of human taeniosis was seen after the treat-ment programme. Obviously, the effect of chemotherapyagainst human taeniosis is partial and cannot achieve thegoal of elimination of the taeniosis/cysticercosis complexif the entire targeted population is not treated repeatedly.Oxfendazole (OFZ) is effective when used as a single-dosetreatment for porcine cysticercosis at 30 mg/kg body-weight (Gonzalez et al., 1997). The cysticerci survived onlyin the brain of treated pigs, but this is not considered asource of re-infection since the brain is usually not con-sumed. Moreover, as a result of concomitant immunity(Richard and Williams, 1982), it was demonstrated that upto 3 months after treatment with OFZ, pigs with cysticerco-sis did not acquire a new infection (Gonzalez et al., 2001).Although OFZ kills the muscle cysts within 4 weeks, it takesbetween 8 and 26 weeks before the cysticerci are cleared(Sikasunge et al., 2008b). In a recent study undertaken in anendemic area of Mozambique, Pondja et al. (2012) observeda significant reduction of the risk of cysticercosis if pigsare treated with OFZ at 4 or 9 months of age. At the time

of slaughter (12 months old), however, 21.4 and 9.1% ofthe animals treated at 4 or 9 months were still positivefor cysticercosis. The problem of using mass treatment ofpigs with OFZ as a control measure arises from the fact that

tology 195 (2013) 14– 23 19

the prevalence of porcine cysticercosis in most endemicareas is lower than 50%, indicating that the majority ofpigs remain susceptible to T. solium infection after a masstreatment with OFZ. A combined human and porcine masschemotherapy programme has been undertaken in somePeruvian villages (Garcia et al., 2006). This approach waseffective in reducing infection pressure, but did not elimi-nate the transmission of taeniosis/cysticercosis complex.

An attractive option is the use of a vaccine againstpig cysticercosis. Several immunogens have been used asvaccines against T. solium cysticercosis in pigs (Plancarteet al., 1999; Huerta et al., 2001; Mayta et al., 2007;Parkhouse et al., 2008). A vaccine candidate against porcinecysticercosis that was widely reported is the synthetic pep-tide vaccine derived from T. crassiceps antigen, commonlynamed S3Pvac (Sciutto et al., 2007, 2008). However, underfield conditions the S3Pvac gave a protection level of only50% of the vaccinated pigs (Sciutto et al., 2007). Moreoverits initially reported therapeutic value was recently crit-icized and demonstrated to be low (Lightowlers, 2010a;Aluja de et al., 2011). Obviously S3Pvac will not be useful fora control programme of taeniosis/cysticercosis in endemicareas of Africa.

Today, the most effective immunogen is the recombi-nant antigen designated TSOL18. This vaccine comprises ahost-protective protein from the oncosphere of T. solium.It was cloned from mRNA and expressed in Escherichia colias a fusion protein with glutathione S-transferase (Gauciet al., 1998; Gauci and Lightowlers, 2001). The results of theexperimental trials showed that TSOL18 antigen inducedalmost complete protection against the development ofparasites in all vaccinated pigs (Flisser et al., 2004). TheTSOL18 vaccine was recently tested under field conditionsin Cameroon in combination with OFZ against porcinecysticercosis. The trial was an outstanding success, withparasite transmission being entirely eliminated throughthe use of three doses of TSOL18 vaccine and a singletreatment of the animals with OFZ (Assana et al., 2010b).In a field trial in Peru Jayashi et al. (2012) showed thata combination of TSOL16 and TSOL18 vaccines withoutOFZ treatment reduced 99.9% the number of viable cysts.Since these recombinant oncosphere vaccines do notaffect established metacestodes (Lightowlers, 2010b), it isunclear whether the cysts found at the necropsy in vacci-nated pigs were established before or after the vaccination.The OFZ treatment was used in the field trial conductedin Cameroon in the objective to kill any parasite that mayhave established in pigs prior to vaccination (Assana et al.,2010b). TSOL18 vaccine in combination with OFZ can beconsidered a novel disease control tool that could reducehuman neurocysticercosis in endemic areas in Africa. Thedrawback of using the TSOL18 is the need of at least twodoses to achieve the protection. Assuming that multipledoses increase the cost of vaccination for poor communi-ties in endemic areas, further studies were recommendedto 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 + TSOL18in combination with single treatment of OFZ should berecommended for a programme that has the objective toeliminate T. solium cysticercosis in an area with two distinct

20 E. Assana et al. / Veterinary Parasi

Table 4Proposed routine vaccination programme against Taenia solium transmis-sion in the north of Cameroon.

Season Interventions

End of rainy season Vaccination of all pigs (firstdose of TSOL18 + TSOL16)

Beginning of the dry season Vaccination of previouslyvaccinated pigs (second dose ofTSOL18 + TSOL16) + oxfendazoletreatment

Dry season Vaccination of unvaccinatedpiglets born in rainy season(first dose)Vaccination of previouslyvaccinated pigs born in rainyseason (second

sAf3

5

yuAa1nawkpapaia(tucf

ntbtdaispaTnra

dose) + treatment withoxfendazole

easons as the North of Cameroon (Table 4). A survey byssana (unpublished results, 2012) has shown that the

armers are ready to pay for a vaccine to avoid losses (about0% of the carcass value) when cysticercosis is detected.

. Conclusions and prospects

Although we have more epidemiological data than 10ears ago T. solium taeniosis/cysticercosis remains “annder-recognized but serious public health problem” infrica. Seventeen years ago, this statement was a title of anrticle published in Parasitology Today (Tsang and Wilson,995). It is unlikely that T. solium will be considered as aotifiable disease in many African countries in the foresee-ble future because of the administrative challenges thisould present. Also, the absence of a First World mar-

et for cysticercosis intervention tools limits investment ofroduction and registration of new vaccines or chemother-pies (Lightowlers, 2011). However, there is a significantositive evolution in developing countries and farmers areble to invest money for livestock medicines. For example,n Cameroon, since the price paid for a pig decreases witht least 30% if it is found to have cysticerci in the tongueZoli et al., 2003), the pig farmers are in search for a toolhat can prevent their animals from cysticercosis (Assana,npublished results). What is needed is to have the vac-ine manufactured on a commercial scale and registeredor general use (Lightowlers, 2011).

Porcine vaccination should be integrated in local orational programmes through a simple strategy of short-erm and long-term interventions, which can be carried outy existing services and structures. Recently it was arguedhat an elimination programme for a neglected tropicalisease may begin with a “vertical control program” as

pilot project followed by a sustainable long term “hor-zontal program” (Gyapong et al., 2010). This approachhould be advisable for T. solium cysticercosis control. Arogramme is called vertical when it is directed, supervisednd executed by specialized services (Gyapong et al., 2010).

he rationale for using a vertical strategy at the begin-ing of the control programme is that it may provide rapidesults. In the case of taeniosis/cysticercosis transmission,

pilot control programme may reduce greatly the source

tology 195 (2013) 14– 23

of infection if the coverage is at least 90% (Gonzalez et al.,2002). Re-emergence of the infection in pigs and new casesof taeniosis after the pilot programme could be reducedby continued vaccination of pigs. Through the applicationof these new disease control measures it is hoped thatmore attention will be paid to the prevention of T. soliumtransmission in Africa so as to reduce the burden of neuro-cysticercosis on the continent.

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