control of taenia solium in zambia€¦ · taenia solium is endemic mainly in developing countries...

Control of Taenia solium in Zambia Impact of health education on the control of Taenia solium.

Word count: 18 315

Jacoba Baauw Student number: 01509111

Promotor: Prof. dr. Sarah Gabriël

Copromotor: Dr. Inge Van Damme

Local Promotor: Dr. Evans Mwape

A dissertation submitted to Ghent University in partial fulfilment of the requirements for the degree of

Master of Veterinary Medicine

Academic year: 2017 - 2018

Ghent University, its employees and/or students, give no warranty that the information provided in this

thesis is accurate or exhaustive, nor that the content of this thesis will not constitute or result in any

infringement of third-party rights.

Ghent University, its employees and/or students do not accept any liability or responsibility for any use

which may be made of the content or information given in the thesis, nor for any reliance which may

be placed on any advice or information provided in this thesis.

Preface

If you followed what a chicken eats, would you eat the chicken? – Zambian proverb

I’ve read this proverb on a sunny afternoon a couple of weeks ago, when I was pretending to write a

part of this master thesis. But instead of writing I started dreaming again about the wonderful time I

had in Zambia and instead of reading scientific articles, I started reading about the beautiful country

Zambia. And then I found this proverb. If you replace the word ‘chicken’ with the word ‘pig’; you’ll have

one of the key points of this research.

After six years of studying and being around in the clinics, a master thesis is one of the final parts of the studies. It’s a final opportunity to learn more about one topic. This master thesis about the control of Taenia solium in Zambia for me includes some interesting aspects of our study, where veterinary medicine meets public health and a One Health approach is necessary. So I’m very happy I got the opportunity to learn more about these aspects in the beautiful context of rural Zambia. I want to thank some people who made it possible to finish this project. First of all, a very special thanks to my promotor Prof. Dr. Sarah Gabriël, who was always patient and friendly, took time for revising my work and giving advices. Thanks to my copromotor Dr. Inge Van Damme for advices and her help in analysing the data of ‘The Vicious Worm’. And thanks to Dr. Evans Mwape, who gave me a warm welcome in Zambia at UNZA and an introduction in the CYSTISTOP project. Thanks to all members of the team in the field, who makes the days in Zambia even brighter and sunnier. And special thanks to the people who I always will remember with a smile: the heart-warming Zambian people. And last, I want to thank all the lovely friends and family who always supported me in the last six years. A special thanks to those who spend a part of their time revising my text. And no, I never followed what a chicken eats. And yes, I still want to eat the absolutely good and tasty Zambian village chicken.

Table of Contents Preface ..................................................................................................................................................... 3

1 Summary.......................................................................................................................................... 6

Nederlandse samenvatting ..................................................................................................................... 6

2 Literature study ............................................................................................................................... 7

2.1 Background .............................................................................................................................. 7

2.2 Health education ................................................................................................................... 13

2.3 Other foodborne pathogens ................................................................................................. 16

3 Objectives ...................................................................................................................................... 19

4 Material and methods ................................................................................................................... 20

4.1 Systematic review .................................................................................................................. 20

4.2 Vicious Worm ........................................................................................................................ 21


5 Results ........................................................................................................................................... 25

5.1 Systematic review .................................................................................................................. 25

5.2 Vicious worm ......................................................................................................................... 29


6 Discussion and conclusion ............................................................................................................. 37

7 References ..................................................................................................................................... 39

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List of abbreviations

CC= Cysticercosis

CT= Computed Tomography

DALY= Disability-Adjusted Life Years

EITB= Enzyme-linked immune electrotransfer blot

ELISA= Enzyme-linked immunosorbent assay

FAO= Food and Agriculture Organization

HCC= Human cysticercosis

MDA= Mass drug administration

MRI= Magnetic Resonance Imaging

NCC= Neurocysticercosis

NTDs= Neglected Tropical Diseases

PCC= porcine cysticercosis

SSA= Sub-Saharan Africa

TS= Taenia solium

TSTC= Taenia solium taeniasis/ cysticercosis

WHO= World Health Organisation

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1 Summary The zoonotic parasite Taenia solium is endemic mainly in developing countries, such as Zambia. The

World Health Organisation (WHO) has classified T. solium as one of the neglected tropical diseases

(NTDs). T. solium causes three diseases in two hosts: porcine cysticercosis (PCC) in pigs and

taeniasis and cysticercosis in humans. The parasite commonly migrates to the central nervous

system, causing neurocysticercosis (NCC) (Garcia et al., 2003). NCC is responsible for the majority of

acquired epilepsy worldwide. A combination of different approaches is necessary to combat T. solium

taeniasis/cysticercosis (TSTC) (Gabriël et al., 2016; Mwape et al., 2015). There are different

intervention components i.e. preventive chemotherapy, health education, improved pig husbandry,

improved sanitation, vaccination of pigs, improved meat inspection and processing of meat. The

objective of this master thesis is to evaluate the effect of health education on T. solium and potential

impact on other foodborne pathogens in rural Zambia. A systematic review is done to identify all

published articles since 2014 regarding health education as control tool. The computer-based

education tool ‘The Vicious Worm’ is evaluated with questionnaires. Major findings are that health

education leads to an increase of knowledge and can also have a potential impact on other foodborne

pathogens.

Nederlandse samenvatting De zoönotische parasiet Taenia solium komt met name in ontwikkelingslanden, waaronder Zambia,

endemisch voor. De Wereldgezondheidsorganisatie heeft T. solium onder de verwaarloosde tropische

ziekten geclassificeerd. T. solium veroorzaakt drie ziekten in twee gastheren: porcine cysticercosis

(PCC) in varkens en taeniasis en cysticercosis bij de mens. De parasiet migreert met name naar het

centraal zenuwstelsel en veroorzaakt daar neurocysticercosis (NCC) (Garcia et al., 2003). NCC is

wereldwijd de belangrijkste reden van verkregen epilepsie. Een combinatie van verschillende

interventies is vereist om T. solium taeniasis/cysticercosis(TSTC) aan te pakken (Gabriël et al., 2016;

Mwape et al., 2015). Onder de verschillende interventie strategieën vallen: preventieve

chemotherapie, gezondheidsonderwijs, betere varkenshouderij, betere sanitaire voorzieningen,

vaccinatie van varkens, betere controle op vlees en de bereiding van het vlees. Het doel van deze

masterproef is het lange termijn effect van het gezondheidsonderwijs te evalueren op Taenia solium

en de mogelijke impact op andere voedseloverdraagbare ziekten. Een systematic review is uitgevoerd

op basis van recente artikelen sinds 2014 met betrekking tot gezondheidsonderwijs als interventie. Het

computerprogramma ‘The Vicious Worm’, als educatie hulpmiddel is geëvalueerd met behulp van een

vragenlijst. De belangrijkste bevindingen zijn dat gezondheidsonderwijs zorgt voor een vergroting van

kennis en kan potentieel een invloed hebben op andere voedseloverdraagbare ziekten.

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2 Literature study

2.1 Background Taenia solium is endemic mainly in developing countries (Fig. 1) and has pigs as intermediate host and humans as the definitive host or accidental intermediate host. Ingestion of the eggs by pigs leads to porcine cysticercosis (PCC). In humans, taeniasis is acquired by ingestion of infected pork and human cysticerosis (HCC) is acquired by accidentally faecal-oral infection of tapeworm eggs (Garcia et al., 2013). Of all foodborne parasites, T. solium has the highest disease burden worldwide (WHO, 2015). The Food and Agriculture Organization (FAO) and the World Health Organisation (WHO) have indeed ranked T. solium on the first place on the global scale of foodborne parasitoses (FAO and WHO, 2014). The WHO has classified T. solium as one of the neglected tropical diseases (NTDs). The WHO has declared, by resolution WHA66-12

1, to target for control, elimination and possibly

erardication of T. solium taeniasis/cysticercosis (TSTC) (WHO, 2012). It was planned to have a validated strategy for control and elimination of TSTC available by 2015, and scaled up interventions in selected countries by 2020 (WHO, 2012). Despite that this disease is declared eradicable, up till now T. solium remains endemic in most countries. To achieve the goals set for 2020 several challenges remain i.e. development of new vaccines and accurate, economically-viable and discriminative diagnostics in humans, randomised clinical field trials to assess pig focussed strategies, implementing a progression of behaviour interventions and developing transmission models to evaluate intervention strategies

2. T. solium is a public health problem due to the severity of

neurocysticercosis (NCC) and an economic burden because of the medical costs and losses in pig production. Due to the lack of good quality data it’s difficult to estimate the social and economic impact of this disease (WHO, 2015).

2.1.1 Prevalence T. solium is endemic in low and middle income countries in Sub-Saharan Africa (SSA), Asia and Latin

America (Fig. 1). An epidemiological study on the seroprevalence of HCC shows that the estimated

prevalence of circulating T. solium antigens for Africa, Asia and Latin America is 7,30%, 3,98% and

4,08% respectively, with substantial variation within regions. Seroprevalence of T. solium antibodies is

estimated on 17,37%, 15,68% and 13,03% respectively. Taeniasis reported prevalences ranged from

0 to 17, 25%. The broad distribution is due to regional differences and variations in used research

techniques (Coral-Almeida et al., 2015). In Zambia the prevalence of PCC, was depending on used

technique ranging from 12,7% to 32,1% on tongue examination and from 30,0% to 51,7% on antigen

enzyme-linked immunosorbent assay (Ag-ELISA) (Sikasunge et al., 2007). According to Mwape et al.

(2015) 51,8% of people with epilepsy were diagnosed with probable or definitive NCC, when using Del

Brutto diagnostic technic, combining computed tomography (CT) and serology enzyme-linked immune

electrotransfer blot, or 57,1% when using sero-Ag-ELISA as major criteria.

1 World Health Organisation, 2013. World Health Assembly resolution WHA 66-12

2 World Health Organisation, 2012. Accelerating work to overcome the global impact of neglected

tropical diseases. A roadmap for implementation.

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Figure 1. Endemicity of Taenia solium3

2.1.2 Life cycle Pigs with free access to human faeces containing T. solium eggs can be infected by eating human

faeces (Fig. 2). After ingestion, the parasite migrates in pigs mainly to muscles, central nervous

system and subcutaneous tissue, which leads to PCC. Taeniasis occurs in human hosts after

ingestion of undercooked pork meat infected with cysticerci. The larvae develop in the small intestines

to adult tapeworms and two months after infection gravid proglottids, containing fertile eggs, are

excreted in human stool. Accidental faecal-oral infection with tapeworm eggs can cause HCC. The

larvae migrate through the intestinal wall, enter the bloodstream and migrate to other tissues. Very

often the parasite migrates to the central nervous system causing neurocysticercosis (NCC). Clinical

manifestation depends on the affected organs; NCC gives headaches and severe seizures as clinical

symptoms, while migration to other tissues causes no major problems (Garcia et al., 2003).

3 World Health Organisation, 2016

http://www.who.int/taeniasis/Endemicity_Taenia_Solium_2015.jpg?ua=1, last visited March, 2018

http://www.who.int/taeniasis/Endemicity_Taenia_Solium_2015.jpg?ua=1

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Figure 2. Life cycle of Taenia solium4

2.1.3 Risk factors of transmission In endemic countries transmission of T. solium to humans, causing taeniasis (pig-to-human

transmission) or HCC (human-to-human transmission), is related to several risk factors: environmental

conditions, level of socio-economic development, lack of knowledge about the biology of the parasite,

presence of a T. solium carrier, low level of sanitation and personal hygiene, free roaming pigs,

inadequate pork inspection and control and eating raw or inadequately cooked infected pork (Carabin

et al., 2015; Mwanjali et al., 2013). Risk factors for porcine cysticercosis are a free-range pig

husbandry system, lack of knowledge of the owner about transmission, contaminated water sources

and the absence of latrines in pig-keeping families (Sikasunge et al., 2007; Kungu et al., 2017).

2.1.4 Diagnosis Different diagnostic tools are used for the diagnosis of the various presentations of T.solium (Murrell et

al., 2005). The main problem in diagnosis is the lack of applicable, cheap, sensitive and specific

diagnostic tools, in both human and pig host, which leads to misdiagnosis or under-diagnosis of the

4 Centers for Disease Control and Prevention, 2013,

https://www.cdc.gov/parasites/taeniasis/biology.html, last visited, March 2018

https://www.cdc.gov/parasites/taeniasis/biology.html

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disease (Johansen et al., 2016). For the detection of antibodies against the parasite or specific

parasite antigens EITB and ELISA are most often used respectively. Antibody detection is most

optimal for clinical diagnosis, while antigen detection can be used as monitoring tool after

anthelminthic treatment. Although the EITB gives satisfactory results for human diagnosis, serological

tools are suboptimal for the detection of PCC. Since 2006 molecular techniques are available to show

T. solium DNA in cerebrospinal fluid (Rodriguez et al., 2012). A diagnostic tool for the detection of

PCC which is cheaper and easier to apply in the field is tongue palpation; however this technique is

only effective for the detection of highly infected pigs. Meat of pigs can be inspected for cysts after

slaughtering, but also this technique has a low sensitivity for moderate or lightly infected pigs (Dorny et

al., 2004; Chembensofu et al., 2017). The eggs can be detected in faeces of a tapeworm carrier. Stool

can also be used for copro-antigen detection, to detect the parasite’s specific antigens (Praet et al.,

2013). Because diagnosis of NCC is complex, Del Brutto (2012) defined diagnostic criteria, which are

subdivided in absolute, major and minor criteria. Combination of these criteria leads to a diagnosis of

definitive NCC, probable NCC or no NCC. Diagnostic criteria are primarily based on neuroimaging like

Computed Tomography (CT) and Magnetic Resonance Imaging (MRI), which can provides information

about number and location of lesions in the brains and their stage of evolution. Besides neuroimaging,

detection of anticysticercal antibodies can be done by EITB or ELISA. Antigen detection by sero-Ag-

ELISA is recommended as major criterion in resource poor regions, where neuroimaging is not

available (Gabriël et al., 2012).

2.1.5 Burden of the disease In humans the migration of cysticerci to the central nervous system causes neurological symptoms,

such as epileptic seizures, chronic headaches, blindness, mental confusion and stroke. In low and

middle income countries 2,8 million disability-adjusted-life-years (DALYs) per year are related to

cysticercosis (WHO, 2015). Besides the societal burden of the disease, T. solium also has an

economical impact. The direct and indirect costs are due to hospitalization, doctor visits, drugs,

inactivity and pig losses. A study in Tanzania showed that around 5 million USD were spent due to

NCC-epilepsy and almost 3 million USD due to the potential lost because of PCC (Trevisan et al.,

2017).

2.1.6 Control and prevention A single intervention control strategy will not lead to a significant reduction of the disease. A

combination of different approaches is necessary to combat T. solium taeniasis/cysticercosis (Gabriël

et al., 2016; Mwape et al., 2015). Most strategies are capable to reduce the disease, but maintaining

and further reducing the disease is still problematic (Johansen et al., 2016). There are different

intervention components, due to the complex transmission dynamics, i.e. human treatment, porcine

treatment, vaccination of pigs, improved pig husbandry, health education, improved hygiene sanitation

and hygiene, improved meat inspection and processing of meat.

Human treatment

Preventive chemotherapy (PC) is an important intervention tool and involves the distribution of

anthelmintic drugs to populations at risk. Safe and effective drugs for the treatment of taeniasis are

praziquantel and niclosamide. The efficacy of praziquantel is around 95% and of niclosamide is

around 85% (Gabrielli et al., 2011).

There are different ways to implement PC (Thomas, 2015):

Mass drug administration (MDA): the entire population of an area is treated at regular intervals

(irrespective of clinical status)

Targeted chemotherapy: specific risk groups are treated (irrespective of clinical status)

Selective chemotherapy: infected or suspected infected individuals are treated

The MDA of praziquantel is also used in control programmes of schistosomiasis, so in co-endemic

areas the control of both diseases can potentially be integrated. The major problem in this approach is

that treatment of schistosomiasis requires four times the dose of praziquantel compared with taeniosis.

The higher dose of praziquantel may cause side-effects in people with neurocysticercosis (Braae et

al., 2016). Another option of anthelminthic treatment is the use of triple doses of albendazole (400

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mg/day for 3 consecutive days) or mebendazole (500 mg/day for 3 consecutive days). This treatment

has been proven effective and acts also against soil transmitted helminths (Ash et al., 2015).

Porcine treatment

Oxfendazole, a benzimidazole, is the most effective anthelmintic against muscle cysts and is active

against common gastro-intestinal helminths as well. It does cause no or little side-effects, but it is not

very effective against brain cysts (Johansen et al., 2016). Oxfendazole is not registered for pigs and

not available in most endemic countries. Besides this, farmers are more willing to participate in a

treatment programme, if there is an economic benefit of selling clean pork (Garcia et al., 2003).

Vaccination of pigs

Vaccination should lead to an interruption of the life cycle of Taenia solium and a decrease of infected

pigs and people (Garcia et al., 2003). Main problems associated with the currently available vaccines

are the need for a cold chain, the distribution dosing schedule, the costs and the willingness of farmers

to implement the vaccination. There are several vaccines, two of them are most developed and giving

a high degree of protection. The first, SP3Vac, is a synthetic vaccine comprised of protective peptides.

Field trials in Mexico showed a reduction of 52,6% of PCC, a significant (p<0,05) reduction in viable

cyst numbers at necropsy and a reduction of parasite load in pigs born from vaccinated sows (Huerta

et al., 2001). The second, TSOL18 corresponds to an oncosphere antigen-coding gene in T. solium. It

gives 100% protection both in experimental challenges and natural exposure in the field. According to

Lightowlers (2013) a combination of vaccination and treatment with oxfendazole would give an optimal

effect, if given every 4 months.

Improved pig husbandry

In many countries where TSTC is endemic, pigs are held in a free-ranging system. They keep the

environment clean and are cheap in their nourishment. Free-roaming pigs have access to human

faeces and the life cycle of the tapeworm as described above will continue. In areas where pig

confinement is the norm, cysticercosis has not been found, provided that pigs are not fed with human

stool (Flisser et al., 2003). According to Thys et al. (2016) there are different reasons why pigs are

free-roaming. First, the main problems in pig management are related to feeding issues, because feed

is very limited and expensive, so it is economically difficult to confine pigs. A second challenge is the

difficulty to build enclosures. Third, according to women in the focus group discussions, pigs became

lame, weak, unhappy and thinner when they’re enclosed. The last reason for free-roaming according

to the farmers is that they are used to this system. However, enclosing pigs will avoid disease

transmission and allow a better control of pig feed. An added value of confinement is a reduction of

the risk for African swine fever, because the contact between the pigs is reduced (Gabriël et al., 2016).

Migration of infected pigs and pork to non-infected areas might lead to new endemic areas (Gabriël et

al., 2015).

Health education

Several studies show that health education is an important aspect of TSTC control (Sarti et al., 1997;

Lansdown et al., 2002; Ngowi et al., 2008; Ngowi et al., 2011; Ertel et al., 2015; Mwidunda., 2015;

Carabin et al., 2018; Hobbs et al., 2018). Health education can be applied in different ways and can be

integrated as a non-specific measure with other health-care messages. It can be a part of the

sensitisation of preventive chemotherapy, but it can also be a stand-alone intervention. In the past

there were already different health education programmes. The focus of health education can be on

the biology of the tape-worm, hygiene, improvements in meat preparation, and the need for adequate

sanitation or improved pig husbandry. It can be focussed on different target groups: specialists like

health workers, pig farmers, meat workers; and the general population like school going children.

Health education contains educational interventions, pamphlets and posters, training of farmers,

workshops, one-to-one interviews, discussions, mass media and street plays and songs. Due to the

fact that there are different methodologies to apply health education, it’s difficult to compare these

methodologies. And besides, there are just a few studies evaluating efficacy, effectiveness and impact

of health education as stand-alone strategy (Thomas, 2015). A study of Carabin et al. (2018) in

Burkina Faso shows a community-based educational intervention can be effective in reducing the

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incidence and prevalence of cysticercosis. More about health education as intervention tool will be

discussed below.

Improved sanitation and hygiene

Beside free-roaming pigs, open defecation is the other main risk factor. If there is a combination of

free-roaming and human open defecation, pigs will have access to human faeces and the cycle will

continue. Good sanitation and hygiene are highly recommended as part of any long-term control

strategy. Practicing open air defecation is linked not only to the presence or absence of water or

latrines, but also to social and cultural determinants. However due to many toilet-associated taboos

even when latrines are available, the population won’t use them, especially men (Thys et al., 2016).

Latrines are an important intervention to interrupt the life cycle of the tape-worm. Studies show that in

Africa in general a lack and use of sanitary facilities are major risk factors for cysticercosis (Sikasunge

et al., 2007; Braae et al., 2015; Nkouawa et al., 2015). Improved latrine use as a control measure

potentially has implications for many other sanitation-related pathogens. Community-Led Total

Sanitation (CLTS) is a community approach that facilitates a process of improvement in sanitation and

hygiene. An assessment of CLTS by Bulaya et al. (2015) shows no difference in sanitation practices

and awareness of cysticercosis resulting in no reduction of T. solium infections in pigs. This approach

can be potentially effective, if there is an implementation of health education, mass drug administration

and pig vaccination. Also a colloboration between medical and veterinary services and involvement of

local policy makers is needed.

Improved meat inspection and processing of meat

The main problem with meat inspection is the lack of implementation and the lack of sensitivity. Meat

inspection seems a relatively manageable intervention, but should preferably be done by a

veterinarian (Joshi et al., 2003; Gabriël et al., 2016). There is no inspection for pigs slaughtered at

home and for the pork served at e.g. funerals. An alternative here is to teach pig farmers to do it

themselves. Health education plays an important role, by informing the population about the risk of

infected meat. If the population refuses to buy infected pork, farmers/traders should change their

management as well (Edia-Asuke et al., 2014). A limitation of meat inspection is the low sensitivity

(22%), which is increasing with a higher number of viable cysts. It is important to include the following

organs: liver, kidneys, spleen and lungs (Dorny et al., 2004; Chembensofu et al., 2017). People are

afraid of the consequences of meat inspection, especially because they don’t want to throw away

meat. Another problem with meat inspection is corruption: lying about meat that have been inspected,

selling uninspected meat elsewhere and inspectors being accused of cheating. Meat inspection is also

considered as waste of time and money (Thys et al., 2016). There are different steps in the processing

of pork, which can successfully reduce the viability of T.solium cysticerci: freezing, gamma-radiation,

cooking and salt pickling. An important advice to the population is to avoid eating and/or handling raw

meat (Thomas, 2015).

Combinations

All the interventions described above have their advantages and disadvantages. A study of Johansen

et al. (2016) based on a mathematical model shows that the effect of most single interventions stops

at the moment the intervention ends and does not lead to a substantial reduction of disease morbidity

or transmission. Although a combination of interventions gives a significant effect, it will not be able to

eliminate the infection in neither man nor pigs. Winskill et al. (2017) used the EPICYST transmission

model to assess the impact of six intervention strategies in a single approach or combined

approaches. The interventions consist of two pig focussed interventions i.e. vaccination of pigs and

MDA; three behavioural interventions i.e. improved animal husbandry, improved sanitation and

improved meat inspection; and a last intervention of testing and treating of humans with taeniasis. The

human focussed intervention was highly effective. The pig focussed and behavioural interventions

were more effective when applied in combination than as single intervention.

A comprehensive control strategy will include a combination of health education, improvements in

personal hygiene and sanitation, improvement in pig husbandry, treatment of taeniasis (MDA),

treatment and/or vaccination of pigs, and meat hygiene and inspection. A One Health approach,

involving medical, veterinary, environmental and social sectors, is needed to cover the human and

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animal host and the environment. An alternative is a focused approach with a selection of the most

cost-effective interventions. In this context it can be cost-effective to integrate interventions in other,

already existing control programmes for NTDs (for example schistosomiasis). The success of

interventions depends on social, cultural and political acceptance (Gabriël et al., 2016).

An agent-based model, cystiSim was used to asses three interventions and the combinations thereof:

treatment of humans, treatment of pigs and pig vaccination. The model predicts that targeting the

porcine host will be an efficient intervention tool if the coverage is high, or in case of a lower coverage

in combination with an intervention targetting the human host. CystiSim shows that a combination of

interventions in both hosts has high probabilities of success if a coverage of 75% can be maintained

over a four year period (Braae et al., 2016).

Although it’s recommended to combine several interventions, in many developing areas where T.

solium is endemic, there is no good human or veterinary community care and a multidisciplinary

approach is complex and expensive. This means that there is a need for a minimal intervention

strategy. Because of this, Lightowlers and Donadeu (2017) focussed only on pig related interventions.

They evaluated mathematically the impact of different intervention strategies with a three monthly

intervention with vaccination and oxfendazole treatments and of the impact of an oxfendazole

treatment alone. Two intervention strategies have the potential to prevent T. solium transmission by

animals of slaughter age. Both interventions involve simultaneous application of vaccination and

oxfendazole treatments in young animals and oxfendazole treatment in older animals. Effective

intervention in pigs alone would be expected to impact the incidence of human cysticercosis in two or

three years (Lightowlers, 2010).

To evaluate the most effective control intervention it is important to measure the reduction on taeniasis

and/or human or porcine cysticercosis. The strategy should also be analysed on cost-effectiveness

(Gabriël et al., 2016). There is a need for monitoring and surveillance to ensure the effect of

interventions remains. Monitoring and surveillance can be done by measuring prevalence of taeniasis,

HCC or PCC with different diagnostic tools (Thomas, 2015). It is also important to pay attention to new

people or pigs entering the controlled area, through diagnosis and treatment.

2.2 Health education The WHO describes health education as follows: “Health education comprises consciously

constructed opportunities for learning involving some form of communication designed to improve

health literacy, including improving knowledge, and developing life skills which are conductive to

individual and community health” (WHO, 1998). Health education as an intervention tool is applied in

health programs for many diseases and different target groups all around the world. Here, the focus

will be on health education in the control and elimination of T. solium.

2.2.1 Main goals of health education The purpose of health education is to increase knowledge about the different aspects of T. solium,

which should lead to a change in behaviour and as result a decrease of TSTC. Health education can

be a support and a part of a sensitisation campaign for other interventions and therefore should be

implemented at the beginning of a prevention and control program. Education as a support of other

interventions is important for a sustainable long term effect (Murrell et al., 2005). A lot of health

education interventions show an improvement in knowledge. However behaviour change is mostly

less pronounced than improvements in knowledge, which is potentially due to limited resources (Sarti

et al., 1997). Though Wohlgemut and colleagues (2010) described health-education leading to a

change in farmers’ knowledge and behaviour (for example: tethering pigs), empowering farmers to

prevent transmission of T. solium. Also according to Johansen et al. (2016) and Ngowi et al. (2011)

health education leads to a reduction of the consumption of infected pork and an increase of

consumption of better cooked meat, reduction of open defecation, use of more safe water and a better

confinement of pigs. All these improvements together reduce the transmission of T. solium. Although

there was no improvement seen in observed practices in a study in Tanzania, an Ag-ELISA shows a

decrease in the incidence rate of porcine cysticercosis after health education (Ngowi et al., 2008). In

Burkina Faso an intervention strategy was developed to control T. solium using the PREDECE model

(Predisposing, Reinforcing, and Enabling Constructs in Educational Diagnosis and Evaluation), which

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was effective in reducing the incidence and prevalence in two of the three study areas (Ngowi et al.,

2017; Carabin et al., 2018). This study will be discussed below in the results of the systematic review.

Although several studies show an effect of health education in creating awareness, the evaluation of

health education for control of T. solium taeniosis/cysticercosis is scarce and an assessment is

needed. Because of these reasons the computer-based health education tool ‘The Vicious Worm’ is

developed. ‘The Vicious Worm’ is a computer-based education tool that provides information on

transmission, diagnosis, treatment, risk factors, prevention and control of TSTC to different

stakeholders as an evidence-based specific intervention (Johansen et al., 2014). Ertel et al. (2015)

did an assessment of ‘The Vicious Worm’ on knowledge uptake among professionals by

administration of questionnaires immediately after health education, two weeks after health education

and focus group discussions. The study showed a highly significant effect on knowledge uptake and a

positive attitude towards the tool. There was an improvement in knowledge of most aspects of TSTC,

but a lack of knowledge about neurocysticercosis remained. For a long term effect it is preferable to

combine interventions, like MDA with a health education program.

2.2.2 Target groups Health education can be used in different target groups. Students, adults, professionals and

community leaders should be informed about the risks of T.solium. Participation of different members

of the community increases the chance of success.

School going children

A lot of interventions have school going children as a target group because they are good knowledge

carriers to their communities. According to Lansdowns et al. (2002) the effect of knowledge

transmission from the children to their families depends on the financial situation and the willingness of

the parents. A study in Tanzania showed that health education at schools is efficacious in improving

knowledge and attitude and that improvement is persistent in time. Only knowledge about pig keeping

and the attitude of reporting to a veterinarian if a pig had cysticercosis was not increased by health

education. In secondary schools there was even an improvement in knowledge and attitude in the

control group when there was only monitoring and no intervention. This is possibly due to the fact that

secondary school children share information with their peers from other schools (Mwidunda et al.,

2015).

Professionals

It’s important to train different groups of professionals, which are working with pig or pork or working in

healthcare. Professionals play an important and continuing role in transfer of information to the

population (Wohlgemut et al., 2010; Ertel et al., 2015). Meat inspectors at official slaughterhouses are

responsible for the detection of the cysticerci. Although, as discussed above, the sensitivity is low, a

proper training is essential for a good inspection. Also, processors of meat have their responsibility

and should know the risks of cysticerci, because they can reduce the viability of the cysts in different

process steps (Thomas, 2015). Health workers are locally responsible for detection and prevention of

taeniasis and cysticercosis. They should have a general training in schools of public health, but also

need some information about the aspects of the local situation. Because of the complex life cycle of T.

solium a manual can be useful to avoid confusion. Farmers should get health education about the life

cycle, health risks to their families and the consumers of their pork. They should get advice about

prevention of pigs having contact with human faeces, meat inspection at slaughterhouse or if this not

possible how to detect the cysticerci themselves, preparation of infected meat and reporting and

treatment of taeniasis cases (Murrell et al., 2005).

Community education

The community should be informed about the health risks of T.solium. Health education should

provide information about the life cycle and ways of prevention, like no open defaecation, meat

preparation and good husbandry practices. Because of their complementary role in family and society

it’s important that both sexes are encouraged to take part in workshops and individual trainings.

Because women are the key contributors to the agricultural workforce, it’s important that women have

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access to education (according to the United States Agency for International Development)

(Wohlgemut et al., 2010).

2.2.3 Educational material Health education should include information about transmission of TSTC, risk factors, clinical signs,

detection, prevention and treatment (Johansen et al., 2014). This information should be illustrated by

pictures of how porcine cysticercosis and proglottids in human stool look like. The way of providing

information depends on the target group and the cultural context. Educational material which is

adapted to the local language and cultural context will have a better effect. For example the computer-

based tool ‘The Vicious Worm’ is illustrated in the local context of sub-Saharan Africa, which makes

students more engaged (Hobbs et al., 2018). The prior education level also has an impact on the final

effect of health education. Wohlgemut et al. (2010) described that those who already had a grade

eight education were more likely to correctly describe how people become infected with the tapeworm

and how people develop epilepsy. Farmers with grade eight education can learn from the written

teaching tools, whilst others are limited to oral and visual presentations. Also studies of Maridadi et al.

(2011) and Mwidunda et al. (2015) show a higher knowledge uptake among boys/males, higher level

of education and older age groups. This is in contrast with findings by Ertel et al. (2015), who shows

no significant impact of gender, educational level or either former experiences with T. solium on

knowledge uptake. Only employment in the health sector compared with the agricultural sector was a

significant factor for knowledge uptake. Different tools can be used for the approach of health

education. A leaflet or manual has the advantage that it can be read again, after the health education

moment. Disadvantage of this application is the high rate of illiteracy in most of the endemic countries.

This problem can be avoided by using more illustrations instead of text (Ngowi et al., 2008). A poster

with illustrations can be used for both literate and illiterate people as a summary and highlights

covering the most important aspects of T. solium. The poster may remain present in classrooms and

health centres and will be a reminder of the message about T.solium. To reach illiterate people a video

can be used as well. Besides this more traditional education material, there are upcoming electronic

technics. These technics have the advantage of a dynamic way of learning, interactive self-

assessment and understanding checks. Another advantage is the possibility of producing a

standardized template which can be adapted to different target groups, language and local situation

and is, if necessary, easy to update. A disadvantage is the higher cost of the initial investment

(Sanchez and Fairfield, 2003). Rural areas are often very basic and implementation of electronic

technology is not always evident. The computer-based tool ‘The Vicious Worm’, as mentioned above

is an example of using electronic technology. This tool requires only a laptop, projector and small

generator and was easy to apply in different rural areas (Hobbs et al., 2018). Most of the health

education interventions are conducted in group-sessions. A study in Kenya shows that a one-on-one

training was important to provide information for a second time and farmers had an opportunity to ask

questions in a safe and private environment about the complex life cycle (Wohlgemut et al., 2010). To

make sure that local trainers provide the right information to the community, health education often

starts with a training of trainers (TOT). Local trainers are mainly health workers, teachers, local

veterinary technicians and livestock or agricultural officers. An advantage of starting with the training of

trainers is to assess if the training is clear and fits to the local situation (Ngowi et al., 2008). It is

recommended that the local trainers have supervision at their first training to avoid misunderstanding

(Wohlgemut et al., 2010).

2.2.4 Sociocultural context An important aspect of health education is to fit in the sociocultural context. The programs need to be

adapted to local conditions (Murrell et al., 2005). For example, in Zambia (Thys et al., 2015) and

Kenya (Wohlgemut et al., 2010) it is unacceptable for men to share a latrine with his daughter-in-law,

so he is more likely to defecate outside. On the other hand, men are more likely to have seen

proglottids, due to their habit of open defaecation. Also the economic situation plays a role in decision

making, even if people have knowledge about transmission. A study of Ngowi et al. (2011) shows that

a large proportion of the population would still consume infected pork, which is likely an indication of

poverty. A study in Tanzania, as mentioned above, shows that education to farmers leads to an

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important reduction in the incidence rate of porcine cysticercosis, despite minimal improvement in

behaviour related to transmission. This fact can be due to information contamination. There was a

significant reduction in the reported cases of household consumption of infected pork, but also an

increase of selling infected pork. There could be a link between these behaviours seen from the

sociological point of view, by using the Health Belief Model (HBM). The HBM explains health-

behaviour in terms of individual decision making. A person will be more likely to adapt a change in

behaviour if it is reducing a personal threat. So after health education they do not want to eat infected

pork anymore which leads to a reduction of consumption of infected pork. On the other hand selling

infected pork does not affect their personal health so they sell the pork (Ngowi et al., 2008).

2.2.5 Assessment of health education Evaluation of the effectiveness of a health education trial is often done by focus group discussions

and/or questionnaires. Questionnaires are mostly used to measure the knowledge-uptake. The same

questionnaire is used at baseline and at different time intervals after health education. This makes it

possible to evaluate knowledge uptake on the short and long term (Ngowi et al., 2008; Ngowi et al.,

2011; Mwidunda et al., 2015; Hobbs et al., 2018). Group discussions can be used to assess the

perceptions of the community about different aspects in the control of T. solium (Ngowi et al., 2017).

Mwidunda et al. (2015) remark minor differences in attitude in the comparison between questionnaire

and focus group discussions. This is probably due to the fact that people in group discussion are more

likely to tell the truth in presence of their peers and answer in questionnaires the desired response. A

change in behaviour is also measured by observation of environmental risk factors for the

transmission of T.solium such as free-ranging pigs, use and statuses of latrines, eating infected pork,

drinking un-boiled water and presence of tapeworm carriers (Ngowi et al., 2008).

2.3 Other foodborne pathogens

2.3.1 Introduction As discussed above health education can be used to provide information about basic health. Health

education as intervention strategy for T. solium can be integrated as a specific control measure or as a

non-specific measure. Health education as a specific control measure includes messages about

prevention and control of a particular pathogen, while health education as a non-specific measure is

used to prevent a range of infectious diseases. In case of health education about T. solium it provides

specific information about the life cycle, detection and treatment of tapeworm carriers and treatment of

cysticercosis-positive animals. But next to that it also provides non-specific information about basic

sanitation and hygiene, meat inspection and well cooking of meat (Murrell et al., 2005).

Health education can thus be used in a broader perspective. In rural villages in Zambia, where health

education is used as one of the intervention strategies against T. solium, a lot more infectious

diseases can partially be prevented by health education. This section will focus on the broader aspects

of health education as non-specific measure. Although health education can affect a lot of infectious

diseases, this master thesis focus on other foodborne related pathogens associated with pork in rural

Zambia. These criteria give a non-limited list of the most important foodborne related pathogens in

Zambia. Although limited to these criteria, information and measures can probably be applicable for

comparable pathogens (like other zoonoses) and comparable countries, with the same diseases and

state of welfare (like other SSA-countries). According to the WHO, foodborne diseases are a result of

ingestion of foodstuffs contaminated from food production to consumption and can result from

environmental contamination, including pollution of water, soil or air. The most common symptoms of

foodborne diseases are gastrointestinal symptoms, like stomach pain, vomiting and diarrhoea. But

also neurological, gynaecological, immunological, multiorgan failure and even cancer may result from

ingestion of contaminated food5 .

2.3.2 Non-specific health education messages Health education as intervention tool against T. solium provides some non-specific health messages.

These messages contain information about hygiene, open defecation, preparation and inspection of 5 http://www.who.int/topics/foodborne_diseases/en/, last visited May, 2018

http://www.who.int/topics/foodborne_diseases/en/

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meat and pig keeping. In general it gives information about personal and food hygiene and good

husbandry practices. The WHO provides 5 keys to safer food: keep clean to prevent contamination,

separate raw and cooked food, cook thoroughly, keep food at safe temperatures and use safe water

and raw materials.

Some of these keys are implemented in the non-specific health messages. The WHO mentions as well

that knowledge is a key in prevention and illustrates in this way the importance of health education.

2.3.3 Foodborne pathogens in Zambia An overview of zoonotic diseases was not available in Zambia. In 2017 there was a study aiming to

pilot an assessment of district level situations and test tools for a national survey of the burden of

zoonotic diseases and associated systems capacities for their sustainable surveillance and control. An

integrated One Health approach is recommended as a control intervention for zoonotic diseases. The

study listed some indicators and options for first screening questions (School of public health Zambia,

2017). T. solium is not the only foodborne zoonosis associated with pigs in Zambia. Other important

pig related foodborne zoonoses include the parasites Toxoplasma gondii, Sarcocystis suihominis and

Trichinella spp., the bacteria Salmonella spp., Campylobacter spp. E.coli and Yersinia spp., and the

Hepatitis E virus. The major risk factor for human infection with these zoonotic diseases is the

consumption of undercooked pork.

Toxoplasma gondii The worldwide prevalent and zoonotic T. gondii is an obligate intracellular cyst-forming coccidian parasite. Domestic and wild felids are definitive hosts where sexual replication takes place in the gastrointestinal tract. Any warm-blooded animal can be an intermediate host where the life cycle consists of an acute and a chronic phase. The acute phase is a fast asexual intracellular replication of tachyzoites in almost all tissues. This phase is followed by a chronic phase where tissue cysts, containing bradyzoites, are developed. Different infection routes to humans are possible; the first and main route is consumption of meat of an infected animal (Cook et al., 2000). The second is ingestion of sporulated oocysts (resulting from sexual replication in felids) via contaminated water, soil or vegetables. The last infection route is a vertical transmission through the placenta. Pork is considered as the highest risk meat because of the seroprevalence rate in pigs and the leading proportion of pork among other meats (Djurković- Djaković et al., 2013). A study of Algaba et al. (2018) on the potential effect of different parasite stages and different strains on the parasite burden in pigs during acute and chronic infections shows a high burden of infection in heart and lungs during the active phase and a high burden in heart and brain during the chronic phase. Consuming latter tissues means a higher risk of infection for consumers. Fifty percent of the infections in developed countries are estimated to be meatborne. According to Daka (2014) T. gondii is also an endemic disease in Zambia. The four major categories of infection are: acquired toxoplasmosis in immune competent individuals, congenital toxoplasmosis, ocular toxoplasmosis (acquired or congenital) and cerebral toxoplasmosis resulting from reactivated infections in immune deficient patients (Halonen and Weiss, 2013). Good hygienic measures and thoroughly cooked meat remain important preventive measures to reduce foodborne transmission (Jones and Dubey, 2012). Sarcocystis suihominis S. suihominis can cause an intestinal infection in humans after consumption of pork. The parasite has pigs as intermediate host and is present as cysts in muscles. After ingestion of meat humans act as definitive host with excretion of sporocysts in their faeces. Infection can be asymptomatic or symptomatic with nausea, bloat, loss of appetite, stomach pain, vomiting, diarrhoea, difficulty in breathing and rapid pulse. Sarcocystic is a self-limiting infection and prophylaxis and treatment are usually not needed. The infection is acquired by ingestion of raw pork. Preventing the infection however is done by cooking meat thoroughly (Djurković- Djaković et al., 2013). Trichinella spp. The parasite cycle consists of two phases; an intestinal and a muscular. After ingestion of meat the larvae are released in the stomach and penetrate the mucosa of the small intestine and mature into adult worms. After mating in the intestines adult females shed larvae into the blood and lymphatic vessels, whereafter they migrate to the musculoskeletal fibre. Most outbreaks are related to the consumption of raw pork. Free-ranging pigs are the pigs at risk for getting infected (Djurković- Djaković et al., 2013). Unfortunately the current data about Trichinella spp. infection in sub-Saharan Africa are

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limited. Because consumption of raw or undercooked pork is a major risk factor there seems to be an increased risk of infection in regions where undercooked or even raw pork is habitually consumed. Preventive measures are improved pig husbandry, meat inpection and improved sanitation. Besides meat inspection, health education is essential for the control of trichinellosis (Mukaratirwa et al, 2013). Bacterial infections Bacterial gastro-intestinal infections with Salmonella spp., Shigella, Campylobacter spp., Listeria monocytogenes and Yersinia spp., causing mainly diarrhoea, are endemic in developing countries and are transmitted mainly through fecal-oral transmission by eating and drinking of contaminated food or water. Contamination often occurs during slaughter and meat processing (Baer et al., 2013). Due to the fact that all these bacteria are transmitted through similar routes, they can be controlled at the same time. Important control measures are improved sanitation, hygienic measures (especially hand hygiene), hygienic slaughter and drinking water quality (Fletcher et al, 2011; Baer et al., 2013). Hepatis E virus Finally the Hepatitis E Virus (HEV) also is an important disease in developing countries and is also transmitted by the faecal-oral route through contaminated water or food (Meng, 2010). Pigs act as a reservoir species for HEV transmission to humans with a link between the disease and handling of infected pigs, consumption of raw or undercooked meat and drinking of manure-contaminated water (Yugo, 2013).

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3 Objectives The general objective of this masterthesis is to evaluate the effect of health education on T. solium

and the potential impact on other foodborne pathogens in rural Zambia.

The specific objectives are:

To identify all recently (since 2014) published studies regarding health education as a tool for

control of T. solium in a systematic review.

To evaluate the long term knowledge uptake by primary school children one year after health

education with the Vicious Worm educational tool about T.solium by a questionnaire.

To assess the potential impact of health education designed for control of T. solium on other

foodborne pathogens associated with pork by consultation of the literature.

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4 Material and methods

4.1 Systematic review The WHO published in 2015 a landscape analysis about the control of T. solium to identify the empirical data available for all the different control strategies (Thomas, 2015). Available literature till 2014 was used for this landscape analysis. In collaboration with another MSc student, Tine De Coster, a systematic review was conducted of the available literature since 2014 to define new evidence on the efficacy and development of the different intervention tools on the control or elimination of T.solium. The literature search was according to the same method as used for the landscape analysis. Articles since 01/01/2014 with the key words Taenia solium OR cysticercosis OR taeniosis AND control OR elimination were used for the systematic review. The following search enginges were used: IngentaConnect, PubMed, Library of Congress, British Library, ScienceDirect, African Journals Online and Google Scholar. Duplicates were removed and the articles were screened consecutively on title, abstract and on full text. Articles were excluded according to following criteria:

- Studies published before 01/01/2014 - Studies not relating to humans or pigs - Studies not related to NTDs - Studies on aspects of NTD’s which do not discuss issues relevant to T.solium control or

elimination - Studies on epilepsy not related to neurocysticercosis, - Papers relating to clinical symptoms, diagnoses and treatment of NCC including case studies - Purely epidemiological studies - Papers on diagnoses of TSTC - Papers on aspects of basic sciences - Studies about control in non-endemic regions - Papers not written in English language - Review articles

The initial search gave 458 records, after exclusions based on these criteria; 31 papers remained (Fig.3). I contributed to this systematic review to the search and selection of publications, after which I focused on the health education intervention tools. These results will be presented in this thesis.

Figure 3. Flow chart diagram

6

6 De Coster, T., 2018. Control of Taenia solium in Zambia. Master thesis, Master of Veterinary

Medicine, Faculty of Veterinary Medicine, University Ghent, Belgium.

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4.2 The Vicious Worm

4.2.1 Study area The study area was in Eastern Province, a rural area in Zambia in the neighbourhoods Nyembe

(elimination study arm), Chimvira (control study arm) and Herode (negative study arm). This rural

region is endemic for T. solium infections. In a community based study of this area 6.3% of the faecal

samples collected were positive for taeniasis on copro-Ag ELISA. The circulating cysticercosis antigen

was detected in 5,8% of the individuals (Mwape et al., 2012). The following risk factors were present in

the study area: lack of pork inspection at slaughter, consumption of pork with cysts, selling of pork

infected with T. solium cysticerci, free-range pig husbandry system and absence of latrines (Sikasunge

et al., 2007).

4.2.2 Study design The objective of the study was to evaluate the effect of a computer-based health education tool ‘The

Vicious Worm’ on long term knowledge uptake about T. solium. The master thesis is framed in the

CYSTISTOP-project, which is a large-scale community-based intervention study with as main

objective to evaluate the cost-effectiveness/acceptability of elimination and control of T. solium. One of

the work-packages of CYSTISTOP is the interventional field study. The interventional field study

consists of three study arms: a negative, where participants only receive health education, a control

and a elimination study arm. In the control study arm humans get health education and pigs receive

treatment with oxfendazole, (which is conducted at 12 monthly intervals, for five iterations). In the

elimination study arm people get health education and mass drug administration and pigs receive

treatment with oxfendazole and vaccination, (which is conducted at a 4 monthly intervals, for six

iterations), followed by a 3 year monitoring phase. School-aged children got health education by using

the computer-based tool ‘The Vicious Worm’ (https://theviciousworm.sites.ku.dk/). The efficacy of

health education as an intervention tool is evaluated by a questionnaire. At baseline in July 2016, the

children were tested first using the questionnaire before the educational intervention, and also

immediately after the education. In July 2017, one year after the first education moment they were

tested again by the same questionnaire to determine the effects on long term knowledge uptake.

4.2.3 Ethical considerations This study was conducted within the ongoing CYSTISTOP project. Ethical clearance was obtained

from the University of Zambia Biomedical Research Ethics Committee (004-09-15) and the Ethical

Committee of the University of Antwerp, Belgium (B300201628043, EC UZA16/8/73). The study was

introduced and explained to all project participants, both in village group settings and within individual

households, prior to each field visit. Written informed consent to participate in the workshop, voluntarily

provided by a parent or guardian, was obtained for each student, and the students’ attendance at the

educational workshops was voluntary.

https://theviciousworm.sites.ku.dk/

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4.2.4 Computer- based education tool ‘The Vicious Worm’ The Vicious Worm is developed as an evidence-based, specific health-education control tool (Fig. 4).

The tool is designed for different target groups and contains illustrated stories, videos, quizzes and

scientific texts. It provides information on transmission, diagnosis, treatment, risk factors, prevention

and control of T. solium. Beside the specific information about T. solium, the tool gives a more general

advice about sanitation, hygiene, meat cooking, meat inspection and pig husbandry. The tool can be

downloaded for free on the website. At the start-page the user can choose between three levels:

village, town and city. At village level there is information available about TSTC, hygiene, meat

handling, medical assistance and pig keeping. Nine different scenes are available at village level to

provide the information. At town level, with a slaughter house, veterinary clinic, hospital and book

store, more detailed and technical information about diagnosis, risk factors, treatment and prevention

of T. solium is provided for practitioners like medical doctors, veterinarians, meat inspectors, and

livestock/agricultural officers. City level contains a policy brief, an information sheet about T. solium,

relevant internet links and references, which targets decision makers. To have a significant impact it

is important to distribute a simple and meaningful message. The information about zoonotic diseases

is often complicated (Johansen et al, 2014), which makes it difficult to change habits concerning

hygiene, sanitation, food-handling and animal husbandry practices. Despite the complexity of the

information ‘The Vicious Worm’ turns out to have a significant effect on knowledge uptake among

professionals and school-aged children on short term (Ertel et al., 2015; Hobbs et al., 2018). The

effect on knowledge uptake among school-aged children on long term will be evaluated in this thesis.

Figure 4. Pictures from the computer-based health education tool The Vicious Worm. Top left is

the start page; top right is village level; bottom left is town level and bottom right is city level.

4.2.5 Questionnaire The questionnaire used in Nyembe contains 24 multiple-choice questions, each with five to seven

possible answers (Table 1). The questions were subdivided in eight different categories: acquisition

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and transmission of T. solium infections, acquisition of NCC, T. solium in general, NCC in general,

PCC diagnosis, PCC treatment, relationship between PCC/TS/NCC and prevention of PCC/TS/NCC.

Because the questionnaire used in Nyembe took to much time and was complicated, a revised

questionnaire was used in Chimvira and Herode (Hobbs et al., 2018). The questionnaire in Chimvira

and Herode contains 15 multiple-choice questions, with four possible answers (Table 2). The

questions were subdivided in categories about general knowledge, transmission and prevention.

Questions and answers in English were projected on a screen and read aloud by the local health

worker. The students replied by using a Bluetooth-connected TurningPoint © clicker device.

Table 1. Questionnaire Nyembe (elimination study arm)

Have you ever heard of Masese? (=PCC in the local language Chewa)

Category 1: Acquisition and transmission of T.solium infections

- How can a pig become infected with PCC?

- How do people get T. solium tapeworm infection?

- A person infected with a T. solium tapeworm will shed many eggs through…?

Category 2: Acquisition of neurocysticercosis

- A person with (N)CC might have got the infection by…?

- A person with NCC can transmit the disease to other’s through…?

Category 3: T. solium in general

- What is human tapeworm infection?

- How can human tapeworm infection be diagnosed?

- How can T. solium be treated?

Category 4: NCC in general

- What is human NCC?

- What are the symptoms of NCC?

- What should a person who experiences seizures/chronic headache do?

Category 5: PCC diagnosis

- What is PCC?

- What does PCC look like?

- How can you test for PCC in a live pig?

- How can PCC be diagnosed in a slaughtered pig?

Category 6: PCC treatment

- What should ideally be done with a live pig that has PCC?

- What should be done with a slaughtered pig that has PCC?

Category 7: Relationship between PCC/ T. solium/ NCC

- Is PCC a problem for human health?

- Are PCC and human tapeworm related?

- What problems can an adult T.solium tapeworm cause?

Category 8: Prevention of PCC/ T. solium/ NCC

- How can you prevent pigs getting PCC?

- How can you prevent human tapeworm infections?

- How can human (N)CC be prevented?

Table 2. Questionnaire Chimvira (control study arm) & Herode (negative study arm)

Category 1: General knowledge

- Have you ever heard of Masese? (=PCC in the local language Chewa)

- What is PCC?

- What does PCC look like in pigs?

- What is human tapeworm?

- What are the symptoms of NCC?

Category 2: Transmission

- How can a pig become infected with PCC?

- How do people get T. solium?

- How does a person with T. solium shed eggs into the environment?

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- How do people get CC?

- Can people with NCC transmit it to others?

Category 3: Prevention

- Can you eat the meat of a slaughtered pig with PCC?

- Can you prevent pigs getting PCC?

- How can T. solium be treated?

- How can you prevent T. solium?

- How can (N)CC be prevented?

4.2.6 Data management and statistics All questionnaire data were collected by the TurningPoint © clicker devices, and downloaded to an

excel file, used for the descriptive statistics of the data. The effect of different explanatory variables

(time (baseline vs. follow-up), age (≤15 vs. >15), grade, gender (male vs. female) and village

(Chimvara vs. Herode) was evaluated with Poisson regressions. ‘Knowledge-uptake’ was defined as

the number of questions that changed from incorrect (‘baseline’) to correct (‘follow-up’). Whether this

knowledge uptake was significantly different from zero, was tested with Wald Chi2 test.

4.3 Other foodborne pathogens The impact of interventions, especially health education, for the control of T. solium on other

foodborne pathogens associated with pork in rural Zambia is done by a consultation of the literature.

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5 Results

5.1 Systematic review After search and exclusion of the papers, 31 papers were eligible for the systematic review. The articles can be subdivided in different categories: health education, human treatment, improving pig husbandry (vaccination of pigs, pig treatment, improved sanitation), combinations hereof and mathematical models. The results of this systematic review will be summarized below. The focus will be on health education because this is the main subject of this master thesis.

5.1.1 Health education According to the landscape analysis education is an important aspect of control, although more research is needed for evidence of sustained control and evidence of cost-effectiveness without development of infrastructure. Johansen et al. (2014) developed a computer-based education tool ‘The Vicious Worm’. This tool is created as an evidence-based, specific health education control tool. ‘The Vicious Worm’ is designed for different target groups, like policy makers, professionals and laypeople, with a simple and meaningful message. According to Johansen et al. the current problem with health education is that it’s usually included as non-specific measure, with no proper assessment of its efficacy, effectiveness and impact and the traditional educational material is often stuck in offices. An additional problem specific for the zoonotic parasite T.solium is the complicated name and complicated life cycle with one worm causing three diseases in two hosts. In ‘The Vicious Worm’, information about the life cycle of T.solium, risks and prevention can be obtained at different levels (village, town, and city in an African setting) for different target groups. The information is provided using illustrated short stories, pictures, videos, quizzes, scientific text and relevant internet links. A computer-based tool was found to be the optimal approach for sharing and assessing best practices globally, reducing training costs and providing uniform training options and improving the teaching material continuously. Ertel et al. (2015) did an assessment of ‘The Vicious Worm’ on knowledge uptake among professionals and their attitudes towards the program in the highly endemic Mbeya Region, Tanzania. The intervention contains a presentation of the purpose of the study and health education program, the prevalence and burden of T.solium taeniasis, cysticercosis in local area, followed by 1,5 hour individually or group work on a computer with ‘The Vicious Worm’. Knowledge uptake was measured by a qyuestionnaire (at baseline, immediately after and two weeks after the education) and the study shows a significantly improvement in most aspects, except for acquisition and transmission of T.solium infections and the relation between porcine cysticercosis, human cysticercosis and taeniasis. Focus group discussions show positive attitudes towards the program and participants thought ‘The Vicious Worm’ efficient, simple and appealing. Being employed in the health sector compared to the agriculture sector was found to be a significant factor for improvement of knowledge in both post-intervention studies; other factors were not significant. A limitation of this field-trial was the limited number of participants. Hobbs et al. (2018) did a preliminary assessment of ‘The Vicious Worm’ in Eastern Province, an endemic region, in Zambia among 99 primary school children. The children were invited to attend a half-day educational workshop that consisted of an introductory session, a fun practice quiz, a pre-questionnaire, ‘The Vicious Worm’ educational component and a post-questionnaire. The pre-questionnaire was used to measure the baseline knowledge. Because the questionnaire in Nyembe (elimination study arm) took approximately 90 minutes to complete and was complicated, a revised, simplified questionnare was used in Chimvira (control study arm) and Herode (negative study arm). The questions were subdivided into different categories. An increased knowledge was seen in seven of the eight categories (elimination study arm) and three of three categories (control and negative study arm). Acquisition of NCC was and remained a poorly understood concept. The study had some limitations: the differences in used questionnaires and unavailability of individuals’ response data from the Nyembe workshop prevented a comprehensive comparison of knowledge and knowledge uptake across the three study groups on the individual level and lastly the sample size was relatively small. Also the transfer of knowledge from students to the community was difficult to quantify. Mwidunda et al. (2015) did a school based cluster randomized health education trial in Northern Tanzania to evaluate the effectiveness of health education in improving school children’s knowledge and attitudes related to T. solium cysticercosis and taeniasis. The children in the intervention group received health education by a leaflet and a video show, addressed by a trained teacher. Immediately after, six months and twelve months after health education there were post-intervention re-assessments by questionnaires and group discussions. The health education trial in the intervention group was linked to improvements in knowledge regarding taeniasis, porcine cysticercosis, epilepsy

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and the attitude condemning infected meat, but children were less inclined to contact a veterinarian if a pig was found to be infected with cysticercosis. In the control group there was an improvement in how best to raise pigs. In Burkina Faso an intervention strategy was developed to control T. solium using the PREDECE model (Predisposing, Reinforcing, and Enabling Constructs in Educational Diagnosis and Evaluation). In order to understand the community perceptions related to T.solium, cysticercosis, taeniasis and the transmission of risk factors the authors conducted group discussions and questionnaire interviews. Main risk factors for the transmission of T.solium were the lack of latrines and access to safe water. The obtained information about knowledge and practices was used to develop a community-adapted health education intervention strategy to control TSTC. Four factors were important for intervention: 1/ knowledge on T. solium transmission, impact and control; 2/ perceived financial benefits of controlling PCC; 3/ public sensitization and 4/ self-efficacy, particularly regarding the construction of latrines. As intervention tool they used a comedy film and accompanying comic book combined with the PHAST method (Participatory Hygiene and Sanitation Transformation). The aim of the intervention was to improve the community knowledge on T. solium transmission, impact, and benefits of control measures and to improve self-efficacy through the PHAST method in implementing control measures (Ngowi et al., 2017). Results of this intervention were described by Carabin et al. (2018) demonstrating effectiveness in reducing the incidence and prevalence of HCC, though this effect could only be obtained in Nayala and Sanguié but not in Boulkiemdé. Although there was no objective evidence for this difference, it is probably due to sociocultural differences of the provinces. In contrast to Boulkiemdé, Nayala and Sanguié have a less hierarchical society and value more individual decision making. In the intervention villages in Nayala and Sanguié prevalence of HCC decreased and there were an increasing number of recently built or new under construction latrines. In Boulkiemdé the prevalence of HCC increased and although the number of latrines increased, the prevalence proportion ratio of the latrines was lower than in Nayala and Sanguié.

5.1.2 Human treatment According to the landscape analysis, MDA is efficient in the short term, but longer term trials are needed. A combined approach and community sensitization/participatory approach are important for success. Standardized guidelines on drug administration are needed. O’Neal et al. (2014) evaluated whether screening for taeniasis within a defined geographic radius around heavily infected pigs (ring-screening), followed by treatment of identified carriers, can reduce transmission of T. solium in a rural endemic setting. In the intervention village every four months all the pigs were examined by tongue palpation for characteristic white nodules. Afterwards all people living within 100-meters of any tongue-positive pig were screened using ELISA to detect Taenia antigens in stool. Residents with taeniasis were treated with niclosamide. After one year a reduction of 41% in sero-incidence was observed in the intervention village compared to baseline while the sero-incidence in the control village remained unchanged. At study end, the prevalence of taeniasis was nearly four times lower in the intervention than in the control villages. Ring-screening reduced transmission of T. solium in this pilot study and may provide an effective and practical approach for regions where resources are limited. Braae et al (2016) did an assessment of the effect of the national schistosomiasis control program for Schistosomiasis on T. solium in rural communities in Tanzania. Human stool samples were collected for copro-Ag-ELISA and pig serum samples for Ag-ELISA in the Mbozi and Mbeya districts. Three rounds of school based MDA (praziquantel) were carried out in Mbozi and two in Mbeya based on schistosomiasis endemicity; combined with ‘track and treat’ of taeniosis cases. The study suggests a single approach intervention of three rounds of MDA targeting schistosomiasis in school-aged children combined with track and treat, contributed to a reduction in prevalence of T. solium, and also had a spillover effect on adults in treated areas as well as reducing the prevalence of PCC. An evaluation of the effect of MDA with praziquantel administered to school-aged children in the same region in Tanzania, was done by Braae et al. (2017), combined with track and treat of taeniasis cases in the general population on the copro-Ag prevalence of taeniosis. Positive cases were treated with niclosamide six to eight months after sampling. Three cross sectional population based surveys were done in 2012, 2013 and 2014 and a short questionnaire to collect information on demographics, latrine availability, recent anthelmintic treatments and presence of pigs in the household. School-based MDA with praziquantel in combination with track and treat of taeniosis cases significantly reduced the copro-Ag prevalence of taeniosis and annual MDA was significantly better than single MDA. No spillover effect was seen into the adult population, but this would take time to become evident.

27

Ash et al. (2017) evaluated the impact of a two albendazole triple dose regime (three consecutive days 400 mg) undertaken five months apart on the prevalence of T.solium and soil transmitted helminths (STHs) within a community in Lao PDR. Faecal samples pre and post MDA1 and MDA2 were collected. The McMaster technique was used to measure the prevalence and intensity of infection and molecular characterization of T.solium and hookworm species was conducted to detect zoonotic species. A triple dose albendazole 400 mg treatment leads to a significant reduction in the level of taeniasis and reduced the STH burden. Increased STH prevalence between MDAs reflected the need for behavioral changes and sustained chemotherapy program.

5.1.3 Improving pig husbandry Vaccination The landscape analysis shows vaccination gives a high grade of protection. The difficulty was to find an appropriate dosing schedule. Lightowlers et al. (2016) did an assessment of the specific antibody responses in pigs immunized with the TSOL18 vaccine with variating time intervals between primary and secondary immunization. Fifty Landrace-Pietrain (randomly allocated to five treatment groups, T1-T5) of 12 weeks old get a primary immunization at day 0 and a secondary identical immunization after 4, 8, 12, 16 or 20 weeks. Two weeks after the second immunization serum samples were collected and analyzed by ELISA on anti-TSOL18-specific IgG titers. There was a 100% anamnestic response. Comparing different groups shows that groups receiving the second immunization more than 4 weeks after the primary immunization developed higher mean titers than pigs receiving their two immunizations 4 weeks apart. This trial suggests that more flexible vaccination schedules can be used during studies addressing logistical difficulties associated with implementation of pig vaccination for T.solium control while the cost is minimized and effectiveness and sustainability are maximized. TSOL18 vaccination given at a three months interval can provide continued protection. Pig treatment Calla et al. (2016) did an evaluation of activity of triclabendazole against T. solium metacestode in naturally infected pigs. Eighteen naturally infected cysticercosis pigs were divided into three groups of six individuals. The first group was treated orally with triclabendazole at a single dose of 30mg/kg. The second group was treated with a single oral dose of 30 mg/kg oxfendazole and the third group received a placebo (sugar water, control group). Seventeen weeks post-treatment, the pigs were euthanized and analyzed for the number of surviving cysts in muscles and cysts were classified as viable or degenerated. The overall parasite load including viable or degenerated cysts for each group was 1658 cysts for control group, 1414 cysts for triclabendazole treated group, and 259 cysts for the group treated with oxfendazole. All remaining cysts in the oxfendazole pigs were evidently degenerated. Furthermore, the numbers of cysts were statistically significantly smaller in the oxfendazole group compared with the triclabendazole and control groups (P<0.01). According to this study triclabendazole is not recommended for the treatment of porcine cysticercosis, while a single dose of oxfendazole is effective for muscle cysticercosis cysts. Sanitation Bulaya et al. (2017) did a preliminary evaluation of Community-Led Total Sanitation (CLTS) for the control of T. solium cysticercosis in the Katete District of Zambia, by a comparative research with pre- and post-intervention assessments in nine villages. The program aims at reducing open-air defecation in rural communities through the construction of pit latrines. It is assumed that the success of CLTS will lead to the control of poor sanitation-related diseases, including human/porcine cysticercosis infections. One hundred four pre-intervention and 275 post-intervention pigs were sampled, of which 14 (13.5%) and 45 (16.4%) were positive, respectively. At the baseline survey (during the crop harvest season) the majority (89,8%) kept their pigs free-range, and only 10.2% kept their pigs in pens. At the post-intervention survey (during the crop planting season) 30.3% kept their pigs free-range, 25.8% in pens and 43.8% were kept in a semi-intensive system of free range during the day and in pens at night. There was only an increase of 33,9% in toilet usage. CLTS as control measure did not significantly improve T.solium infections in pigs after eight months and sanitation practices, risk factors and awareness of cysticercosis did not change. Furthere research is needed if implementation of health education, mass drug administration and pig vaccination can make this approach effective.

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5.1.4 Combinations Garcia et al. (2016) evaluated a three-phase control program in a highly endemic region in northern Peru. Phase 1 was the assessment of the effectiveness and feasibility of six intervention strategies involving mass treatment, minimal mass treatment, screening of humans and pigs, strategic antiparasitic treatment, prevention education and pig replacement in 42 villages. In phase 2 the most effective strategies of phase 1 where compared in 17 villages (MDA of humans and mass screening). Phase 3 was the final strategy of mass treatment of humans along with the mass treatment and vaccination of pigs in the entire rural region of Tumbes. The study shows that the transmission of T. solium infection was interrupted on a regional scale by elimination of the reservoir of the infection in the intermediate host through a one year intervention approach. Elimination persisted in most areas for at least one year without further intervention. Pray et al. (2016) evaluated ring strategies for control of cysticercosis/taeniasis by GPS tracking in Peru. They describe the roaming ranges of pigs and evaluate whether the 100 m radius rings enclose areas where risk factors for T. solium as open defecation and dense pig activity, are concentrated. Forty-one pigs from two villages were GPS tracked for 48h. Additionally a survey of all households was done to record the locations of open human defecation and the use of latrines if available. Different pigs spent 26% to 99% of time inside the 100meter radius ring. The time spent interacting with an open defecation area ranged from zero to nearly four hours per day. Pigs spent a median of 29.6 minutes per day interacting with open human defecation area. Pigs spent a median of 69,8%, 82.8%, 87% and 93,8% resp. of their time within 50, 100, 150 and 200 meters of their homes. Ninety-three percent of the total within time spent interacting with open human defecation areas occurred 100 meters of pig residences. The study shows that control interventions should be focused in areas surrounding heavily infected pigs. Okello et al. (2017) assessed the impact of a joint human-porcine anthelminthic intervention package for T. solium control in a hyperendemic village in Northern Lao PDR. Three hundred humans were treated with albendazole 400 mg for three days and 48 pigs were treated with TSOL18 vaccination and an oral dose of oxfendazole at 30 mg/kg. Human faecal samples were tested on copro-Ag ELISA and there was a significant reduction of community taeniasis prevalence from 30,6% to 6,5%. Individual taeniasis prevalence decreased significantly from 22,9% to 6,25%. A review of the different control tools and long term effect on T.solium was done by Gabriël et al. (2016). A single MDA with niclosamide or praziquantel is not sufficient, but the number and frequency of MDA should be adapted using an updated transmission model with parameters for the specific region. Although health education is successful in terms of increased knowledge there are limitations as stand-alone approach, because more knowledge does not necessary lead to a behavioral change. Improvements in hygiene and sanitation reduce the risk for NCC. It is important not only to promote latrine use, but also address sanitary related taboos and concentrate on men. Meat inspection has a low sensitivity, especially for light infections and does not influence the management practices. Health education and informing consumers can lead to a change in management practices as the farmer will acknowledge a clearer economic loss. The national legislation for pork inspection and control should be reviewed and enforced. Raising pigs in confinement can minimize the risk of cysticercosis and African swine fever and should be put forward as an advantage when educating farmers. Strategies for development of pig husbandry include improvement of feeding, local feed stuffs, develop affordable and simple pig houses, improve genetics for productive performances, disease resistance and education of farmers. Movement control should be implemented, informing farmers about the possibility of importing infection when purchasing pigs and the possibility of treatment to avoid the latter. Oxfendazole is an effective drug against muscle cysts, but price and accessibility of the drug have to be taken in consideration. Pig vaccination can be a safe option to interrupt the life cycle of the parasite and decrease the number of infected pigs and people, however, here as well, cold chain, price and accessibility remain problematic. A combination of strategies is recommended focusing on the human and animal host. The selection of the strategy depends on cost-effectiveness analyses based on solid field data are currently not available. A One Health approach involving multiple sectors is essential for control or elimination. Success of intervention depends on the level of societal and political acceptance, commitment, engagement and a good coverage is essential.

5.1.5 Mathematical models Different studies use mathematical models to estimate the effect of (combinations of) different intervention strategies. Johansen et al. (2016) used a mathematic transmission model to estimate the theoretical outcomes of various control options suggested for TSTC elimination in SSA over a 4-year period. The Reed-Frost mathematic transmission model is used to predict the effect of interventions of mass drug

29

administration with praziquantel of humans, vaccination of pigs, treatment with oxfendazole of pigs and health education of communities, which potentially leads to a change in bad practices and reducing transmission risks. Treatment with praziquantel (one or four times a year) or oxfendazole leads to a reduction in taeniasis and porcine cysticercosis. However, both are increasing as soon as treatment stops. Also vaccination of pigs leads to a decrease of taeniasis (to less than 1%) and porcine cysticercosis (to less than 5%), but once treatment stops the levels raise again. Health education reduced pig-human and man to pig transmission rates by 50%. All options are able to reduce, but not to eliminate TSTC. Prevalence starts to rise as soon as the program ends. A mathematic agent-based model cystiSim, was used by Braae et al. (2016) to provide insight into the transmission dynamics of taeniasis and PCC and subsequently explore the effect of feasible interventions to be used in the control of T.solium in SSA. The model consists of two entities, human and pig host, and allows the evaluation of three interventions and combinations thereof: treatment of humans, treatment of pigs and vaccination of pigs. Control by an intervention only targeting porcine hosts is possible, but coverage and efficacy must be high if elimination is the goal. Including an additional intervention targeting the human host can compensate for a lower coverage. Combining interventions in both hosts have a high success rate if coverage of 75 % can be maintained over at least four years. A two host targeting strategy is most optimal to reach elimination. Winskill et al. (2017) developed a deterministic, compartmental transmission model (EPICYST) to capture the dynamics of the taeniasis/cysticercosis disease system in human and pigs and assessed a range of interventions applied singly or in combination. An assessment of the following interventions was done: improved sanitation, meat inspection, animal husbandry and pig targeted interventions (MDA and vaccination). All single interventions were able to reduce the prevalence singly or in combination. Behavioral and/or pig-targeted interventions were more effective in combination. Combination of improved sanitation and meat inspection had the highest suppressive effect on infection prevalence of the strategies. The most efficacious interventions were human- and pig-targeted drug-focused interventions. A minimal intervention strategy to control T. solium using a basic mathematic model for pig intervention strategies, was designed by Lightowlers et al. (2017). The risk was assessed by taking into consideration the biology of T. solium infections in pigs and the effects of different interventions that are applied. Three of the interventions included 3-monthly treatments with oxfendazole alone or a combination of vaccination and oxfendazole. Interventions including combined application of vaccination plus chemotherapy in young animals were the most effective. The aim of a study of Thomas et al. (2017) was to estimate the risk of any pork meal in western Kenya containing a potentially infective T. solium cysticercus at the point of consumption. Any pork meal consumed in western Kenya has a 0.006 probability of containing at least one viable T. solium

cysticercus at the point of consumption. This equates to 22,282 potentially infective pork meals consumed in one year in the Busia District. Meat inspection, as is currently practised in western Kenya is responsible, according to the model, for avoiding only 1,397 potentially infective meals a year. This model indicates a high risk of T. solium infection associated with pork consumption in western Kenya.

5.2 Vicious worm Hobbs et al. (2018) did already a preliminary assessment of the health education tool ‘The Vicious

Worm’, by comparing the knowledge at baseline with the knowledge after health education. After the

health education knowledge was significantly increased, in particular for parasite transmission and

disease prevention. This master thesis will focus on the long term effect of health education. The

responses one year after health education will be compared with the answers at baseline.

5.2.1 Nyembe – Elimination study arm At baseline 40 students participated: 29 girls and 11 boys. The age ranged between 10 to 18 years.

One year later 33 students participated: 16 girls and 17 boys, between 11 and 17 years.

The average correct score covering all questions was 74%, ranging from 39% to 100%. The question

‘what are the symptoms of NCC?’ was answered correctly by everyone. The lowest percentages of

good answers (39%) had the questions ‘what should be done with a slaughtered pig that has PCC?’

and ‘a person with NCC/CC might have got the infection by…?’. Thirteen questions were answered

correctly by 75% or more and 6 questions by 90% of the group or more. Five questions were

answered correctly by less than 50%. The correct scores per category ranged between 41% and 89%.

The lowest score was on the category ‘PCC treatment’ and the category ‘PCC diagnoses had the

30

highest score. Except the category ‘PCC treatment’ all the categories were answered correctly by

more than 50% of the group.

Compared with the pre-questionnaire at baseline the knowledge uptake was 12% and there was no

difference in average score compared with the post-questionnaire. The categories acquisition of NCC,

TS in general and PCC diagnosis were answered correctly by a higher average percentage of the

group than the post-baseline questionnaire. Compared with the pre-baseline questionnaire four

questions were now answered correctly by a lower percentage. All the other questions had a higher

score. Compared with baseline pre-questionnaire only the knowledge of the category ‘relationship

between PCC/TS/NCC’ had decreased. Compared with the post- questionnaire the knowledge of five

categories had decreased, while the knowledge of three categories had increased. Category

‘acquisition of NCC’ had the biggest increase (31%), while ‘relationship between PCC/TS/NCC’ had

the biggest decrease (13%) (Table 3).

Table 3. Average results Vicious Worm questionnaires at baseline and follow-up, Nyembe

Question Nyembe % Correct

answers pre-

questionnaire

(baseline)

% Correct

answers post-

questionnaire

% Correct

answers at

follow-up

Knowledge

uptake (%)

Pre-post

Knowledge

uptake (%)

Pre-follow

up

Knowledge

uptake (%)

post- follow

up

Have you ever heard

of Masese? (=PCC in

the local language

Chewa)

70 75 85 5 15 10

Category 1:

Acquisition and

transmission of

T.solium infections

65,3 85 80 19,7 15 -5

- How can a

pig become

infected with

PCC

78 90 88 12 10 -2

- How do

people get

TS

50 85 73 35 23 -12

- A person

infected with

TS will shed

many eggs

through…?

68 80 79 12 11 -1

Category 2:

Acquisition of NCC

26,5 20,5 52 -6 25 31

- A person

with NCC

might have

got the

infection

by…?

25 13 39 -12 14 26

- A person

with NCC

can transmit

the disease

to other’s

through…?

28 28 64 0 36 36

Category 3: T. solium

in general

74,3 85,3 88 11 14 3

- What is

human

tapeworm

infection?

65 80 79 15 14 -1

31

- How can TS

infection be

diagnosed?

75 88 97 13 22 9

- How can TS

be treated?

83 88 88 5 5 0

Category 4: NCC in

general

69,7 87 76 17,3 -16 -34

- What is

human

NCC?

35 73 85 38 50 12

- What are the

symptoms of

NCC?

100 98 100 -2 -67 -65

- What should

a person

who

experiences

seizures/chr

onic

headache

do?

73 90 42 17 -31 -48

Category 5: PCC

diagnosis

68,8 83,8 89 15 21 6

- What is

PCC?

75 100 94 25 19 -6

- What does

PCC look

like?

60 85 94 25 34 9

- How can

you test for

PCC in a

live pig?

60 90 97 30 37 7

- How can

PCC be

diagnosed in

a

slaughtered

pig?

80 60 73 -20 -7 13

Category 6: PCC

treatment

35 41,5 41 6,5 6 -1

- What should

ideally be

done with a

live pig that

has PCC?

52 75 42 23 -10 -36

- What should

be done with

a

slaughtered

pig that has

PCC?

18 8 39 -10 21 31

Category 7:

Relationship between

PCC/TS/ NCC

61 67,7 55 6,7 -6 -13

- Is PCC a

problem for

human

health?

88 88 58 0 -30 -30

32

- Are PCC

and human

tapeworm

related?

65 55 45 -10 -20 -10

- What

problems

can an adult

T.solium

tapeworm

cause?

30 60 61 30 31 1

Category 8:

Prevention of PCC/

TS/ NCC

70,3 85,3 82 15 -12 -27

- How can

you prevent

pigs getting

PCC?

93 98 97 5 -66 -71

- How can

you prevent

human

tapeworm

infections?

52 70 67 18 15 -3

- How can

human

(N)CC be

prevented?

66 88 81 22 15 -7

Average 62 74 74 12 12 0

(N)CC: (neuro)cysticercosis, PCC: porcine cysticercosis, TS: Taenia solium

5.2.2 Chimvira – Control study arm At baseline 26 students were participating: 14 boys and 12 girls. One year later 13 boys and 12 girls

participated.The lowest correct percentage was 24% for the question ‘how do people get CC?’. The

question ‘how can TS be treated’ was answered correctly by all the students. The average score of the

follow-up quiz was 68%. Seven questions were answered correctly by 75% or more and two questions

by less than half of the group. The scores per category ranged between 56% for knowledge about

transmission and 78% for the category prevention. The knowledge uptake compared with the

knowledge at baseline is 5,44%. Compared with knowledge at baseline only the category of general

knowledge had decreased with 2,71%. Compared however with the post-questionnaire there is a

decrease of knowledge of all categories ranging between 6,98% and 22,71%, with an average of 13,

86%. The only two questions with an increased percentage of correct answers were ‘can people with

NCC transmit it to others?’ and ‘how can CC and NCC be prevented?’ (Table 4).

Table 4. Average results Vicious Worm questionnaires at baseline and follow-up, Chimvira

Question Chimvira % Correct

answers pre-

questionnaire

(baseline)

% Correct

answers post-

questionnaire

%

Correct

answers

at follow-

up

Knowledge

uptake (%)

pre-post

Knowledge

uptake (%)

Pre- follow-

up

Knowledge

uptake (%)

post- follow-

up

Category 1: General

knowledge

72,31 92,31 70 20 -2,71 -22,71

33

- Have you ever

heard of

Masese? (=PCC)

in the local

language

Chewa)

92,31 100,00 84 7,69 -8,31 -16,00

- What is PCC? 80,77 100,00 72 19,23 -8,77 -28,00

- What does PCC

look like in pigs?

69,23 92,31 76 23,08 6,77 -16,31

- What is human

tapeworm?

50,00 73,08 52 23,08 2,00 -21,08

- What are the

symptoms of

NCC?

69,23 96,15 64 26,92 -5,23 -32,15

Category 2: Transmission 50,00 67,89 56 17,89 6,00 -11,89

- How can a pig

become infected

with PCC?

34,62 93,31 60 58,69 25,38 -33,31

- How do people

get TS?

65,38 100,00 68 34,62 2,62 -32,00

- How does a

person with TS

shed eggs into

the environment?

46,15 92,31 80 46,16 33,85 -12,31

- How do people

get CC?

53,85 26,92 24 -26,93 -29,85 -2,92

- Can people with

NCC transmit it

to others?

50,00 26,92 48 -23,08 -2,00 21,08

Category 3: Prevention 65,38 85,38 78 20,00

13,02 -6,98

- Can you eat the

meat of a

slaughtered pig

with PCC?

26,92 88,46 76 61,54 49,08 -12,46

- Can you prevent

pigs getting

PCC?

57,69 88,46 80 30,77 22,31 -8,46

34

- How can TS be

treated?

100,00 100,00 100 0 0 0

- How can you

prevent TS?

84,62 92,31 72 7,69 -12,62 -20,31

- How can (N)CC

be prevented?

57,69 57,69 64 0 6,31 6,31

Overall average 62,65 81,86 68 19,30 5,44 -13,86


5.2.3 Herode – Negative study arm At baseline 33 students participated: 19 boys and 14 girls. At follow-up 29 students were present: 11

boys and 18 girls. The average score was 74%, ranging between 31% and 97%. The question ‘how do

people get CC?’ had the lowest percentage of correct answers. The questions ‘have you ever heard of

Masese?’, ‘what does PCC look like?’ and ‘how do people get TS?’ were all answered correctly by

97% of the participants. Nine questions were answered correctly by 75% or more, five by 90% or more

and three by less than 50% of the group. The category transmission had the lowest percentage of

right answers with 63%. The category with the most correct answers was about general knowledge

(82%). The knowledge uptake compared with baseline was 14%, with only a decrease for the

questions ‘what is human tapeworm/TS?’ and ‘how can TS be treated?’. There is a decrease in

knowledge uptake compared with the post-questionnaire of 8,16%. Just three questions had increased

in knowledge uptake (Table 5).

Table 5. Average results Vicious Worm questionnaires at baseline and follow-up, Herode

Question Herode % Correct

answers pre-

questionnaire

(baseline)

% Correct

answers post-

questionnaire

%

Correct

answers

at follow-

up

Knowledge

uptake (%)

pre-post

Knowledge

uptake (%)

Pre- follow-

up

Knowledge

uptake (%)

post- follow-

up

Category 1: General

knowledge

69,70 89,70 82 20,00 11,90 -8,10

- Have you ever

heard of

Masese? (=PCC

in the local

language

Chewa)

63,64 93,94 97 30,30 33,36 3,06

- What is PCC? 87,88 100,00 90 12,12 2,12 -10,00

- What does PCC

look like in pigs?

78,79 90,91 98 12,12 18,21 6,09

- What is human

tapeworm?

66,67 72,73 48 6,06 -18,21 -24,73

35

- What are the

symptoms of

NCC?

51,52 90,91 76 39,39 24,48 -14,91

Category 2: Transmission 46,67 69,70 63 23,03 16,13 -6,90

- How can a pig

become infected

with PCC?

33,33 90,91 62 57,58 28,67 -28,91

- How do people

get TS?

87,88 100,00 97 12,12 9,12 -3,00

- How does a

person with TS

shed eggs into

the environment?

51,52 81,82 76 30,30 24,48 -5,82

- How do people

get CC?

18,18 36,36 31 18,18 12,82 -5,36

- Can people with

NCC transmit it

to others?

42,42 39,39 48 -3,03 5,58 8,61

Category 3: Prevention 66,06 87,27 78 21,21

11,74 -9,47

- Can you eat the

meat of a

slaughtered pig

with PCC?

66,67 90,91 79 24,24 12,33 -11,91

- Can you prevent

pigs getting

PCC?

33,33 84,85 72 51,52 38,67 -12,85

- How can TS be

treated?

100,00 96,97 86 -3,03 -14,00 -10,97

- How can you

prevent TS?

78,79 100,00 90 21,21 11,21 -10,00

- How can (N)CC

be prevented?

51,52 63,64 62 12,12 10,48 -1,64

Overall average 60,81 82,22 74 21,41 13,26 -8,16


Overall, the knowledge-uptake improved significantly over time (Wald Chi2 p=0.001), this was also true

for category 2 (Wald Chi2 p<0.001), and also at the 90% confidence level for category 3 (Wald

36

Chi2 p=0.065), although the uptake was still positive (Table 4). For category 1, the knowledge-uptake

was negative, however, this was not significant (Wald Chi2 p=0.420). None of the other variables had

significant explanatory value in the overall model (age: Wald Chi2 p=0.451; grade: Wald Chi

2p=0.554;

gender: Wald Chi2 p=0.694; village: Wald Chi

2 p=0.570), nor in any of the individual categories.

5.3 Other foodborne pathogens For all diseases, mentioned in section 2.3 the risk of infection is at his highest when people have inadequate knowledge of infection and basic hygiene, poor animal husbandry practices, unsafe management and disposal of human and animal waste products (Murrell, 2013). Because these are the same risk factors as for T. solium some of the discussed intervention strategies can also tackle these diseases. Confinement of pigs, meat inspection, (food) hygiene, improved sanitation and health education are important interventions. The non-specific health messages, like hygiene, open defecation, preparation and inspection of meat and pig husbandry, in the intervention for control of T. solium can be used in a broader perspective as intervention for the control of other foodborne pathogens.

37

6 Discussion and conclusion

6.1 Systematic review Since the publication of the landscape analysis about the control of T. solium (Thomas, 2015) more research is done to assess and improve different interventions. Although health education tools improved since the landscape analysis, they still use some different methodologies, which makes it difficult to compare them. Introduction of an evidence based computer education tool leads to an increase of knowledge, but long term assessments are necessary to evaluate sustainable behavior change. Albendazole, praziquantel and niclosamide are effective in human treatment in MDA of more targeted ring-screening. Human treatment can be combined with already consisting control programs. Vaccination of pigs with TSOL18 with a 3-monthly interval and treatment with oxfendazole are effective pig-targeted interventions. Combinations of the different intervention strategies will lead to more sustainable results. Mathematical models show indeed that combinations of intervention targeting both hosts are able to eliminate the tapeworm, but as soon as an intervention stops the prevalence will raise again. Monitoring and surveillance are important factors in the control of prevalence of taeniasis, HCC and PCC. Further research needs to be done on how the prevalence will remain at the same level as soon interventions ends. A draft manuscript, based on the work of T. De Coster and J. Baauw is currently prepared for submission.

6.2 The Vicious Worm The aim of this thesis was to assess the long term effect of health education, focused on ‘The Vicious

Worm’, and the potential impact of health education about T. solium on other foodborne pathogens

associated with pork in rural Zambia. Hobbs et al. (2018) already did an assessment of short term

knowledge uptake by comparing knowledge in questionnaires before and after health education. This

study showed that ‘The Vicious Worm’ is an effective tool for short term knowledge uptake about

T.solium.

At the baseline the average knowledge of the three study areas was 62%. After health education

knowledge increased with. 12%, 19% and 21% for Nyembe (elimination), Chimvira (Control) and

Herode(negative) respectively. In all of the study areas the knowledge is still higher in the follow-up

one year later compared to the baseline questionnaire. Compared to the knowledge in the post-

questionnaire, knowledge in general remained the same for Nyembe and decreased for Chimvira and

Herode. Overall, the knowledge uptake increased significant, which was also true for the categories

about transmission and prevention. Other factor had no significant effect on knowledge uptake. The

difference in knowledge uptake at the follow-up moment between the study areas can be due to

different facts. The study in Nyembe is the elimination study arm with an intervention every four

months. The studies in Chimvira and Herode are respectively the control and negative study arm and

are visited every twelve months. Higher frequency of interventions, combined with health education

each time, in Nyembe, can be the cause of sensibilization and a higher knowledge uptake. The

difference between Nyembe and Chimvira and Herode at the other hand is also a different

questionnaire, which possibly affects the results. In every school another teacher is giving health

education. Normally every teacher gets the same information of the intervention team so this shouldn’t

affect the results. In Nyembe it takes approximately 90 minutes to do the questionnaire. This made the

children impatient and there was a loss of concentration. Besides, there were a lot of answers to

choose from, which makes the questionnaire more confusing and difficult than necessary. Although

the teacher speaks the both English as the local language, the questionnaires were in English, which

can have an effect on the understanding of the questions

Although there is a long term effect of health education in knowledge uptake, this particular study did

not evaluate the change in behavior and the effect on prevalence of human taeniasis, porcine

cysticercosis and human cysticercosis/neurocysticercosis. Focus group discussions and interviews in

the future can give clarity about behavior change. Further research needs to be done to assess the

impact on prevalence. As mentioned above knowledge is not the only needed factor for a change in

behavior. A lot of cultural, economic and/or practical objections can interfere with behavior change.

38

6.3 Other foodborne pathogens In rural Zambia a lot more infectious diseases are present and can be targeted with same intervention

strategies as T. solium. Non-specific health messages for the intervention of T. solium can affect these

diseases as well. The current health education programmes do not pay attention to these other

pathogens. In the future health education can emphasize the non-specific messages as prevention for

a lot of diseases. Further research on the potential and effect of health education against T. solium on

other foodborne pathogens needs to be done.

In conclusion, health education as intervention tool for the control of T. solium leads to a higher level of

knowledge about the tapeworm. This effect of knowledge-uptake will be higher if there are more

frequent educational moment. However more research needs to be done on the effect of health

education on behavior change and impact on prevalence of T. solium. Health education for control of

T. solium can also be effective against other foodborne diseases.

39

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control of taenia solium in zambia€¦ · taenia solium is endemic mainly in developing countries...

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