Epidemiology, diagnosis and control of Taenia saginata and Taenia

Taenia solium Taenia saginata Taenia s. asiatica

A. Flisser et al. 2004, J. Parasitol. 90, 914-916

• Universal distribution

• Low clinical importance (man and cattle) • Low clinical importance (man and cattle)

• Economic losses: condemnation, refrigeration or

downgrading of infected carcasses

HumansHumans

Cattle

• Man only final host

• Cattle only intermediate host (no wildlife • Cattle only intermediate host (no wildlife

reservoir)

� Theoretically, control should be easy

• Developing countries

• High clinical importance in man, low in

pigs pigs

• Economic losses: condemnation of infected

carcasses

Global distribution of Taenia solium cysticercosis

High prevalence

Moderate prevalence

No information available/no evidence

Low prevalence (imported cases)

Source WHO (2002)

• Man only final host

• Pig only intermediate host (no wildlife • Pig only intermediate host (no wildlife

reservoir)

� Theoretically, control should be easy

• Taenia solium

– Transmission stopped in industrialized

countries

– Active transmission in developing countries– Active transmission in developing countries

– Sporadic import of cases through immigration

and traveling

• Taenia saginata

– Persistence of transmission ???

• Bovine ���� Human

Control of taeniasis by preventing infected meat to

reach the consumer: meat inspection (EU directive

64/433/EEC) (all cattle > 6 months)

• Human ���� Bovine

Regulations on use of domestic effluent and

sewage sludge in agriculture (no specific control

measures of bovine cysticercosis)

Humans

Meatinspection

Cattle

HygieneWaste watertreatment

• Lots of time and money spent for the control of

bovine cysticercosis

• However, in contrast to Taenia solium, not • However, in contrast to Taenia solium, not

eradicated in the EU

• In some countries even increasing prevalence of

cysticercosis in cattle

• Taeniasis not notifiable in EU

• Based on sales figures of taenicidal drugs

(niclosamide, praziquantel)

• Incidence between <0.01% and 10%

• Highest occurrence in Slovakia and Turkey

• Based on meat inspection in abattoirs

• Reporting in different countries not standardized

• Prevalence data are difficult to collate and to

comparecompare

• Only few countries report data to OIE

• OIE reports on prevalence between 0.007 and

6.8%

• Wide variation between countries, regions and

abattoirs

In general

• Lower prevalence in West and South vs East

European countriesEuropean countries

• Overall decrease in prevalence but recent increase

in some countries

* Based on official meat inspection records (FASFC)

• Type of animals:

– Seroprevalence positively correlated with the

age of animals (Dorny et al., 2000)age of animals (Dorny et al., 2000)

� risk for exposure increases with age

Dorny P., Vercammen F., Brandt J., Vansteenkiste W., Berkvens D., Geerts S. 2000.

Sero-epidemiological study of Taenia saginata cysticercosis in Belgian cattle. Vet.

Parasitol., 88, 43-49

• Low sensitivity!

• The success of the method depends on:

– Number and stage of development of the

cysticerci

– Skills and motivation of the meat inspector

• Underestimation of prevalence by 3-10

– Careful dissection of hearts and tongues

(Belgium, Italy): > 10% pos.

– Sero-prevalence data (Belgium): circulating

antigen in 3.1% of adult cattle vs vet. inspection

only 0.24%

Predilection sites?

• heart, masseter muscles, diaphragm, oesophagus

• Exp inf: 15.7% of cysts in heart; 6.5% in masseter

muscles (Kyvsgaard et al., 1990)

� Sensitivity of meat inspection increases with the

level of infection

�Possibility of detecting infected cattle limited

when majority are lightly infected

PCR for the detection of T. saginata DNA in muscle

lesions:

• 399 suspected C. bovis lesions from 335 carcasses sent from 3

abattoirs (Belgium)abattoirs (Belgium)

• 93.7% of suspected viable cysts confirmed by PCR

• 67.9% for suspected dead cysts (incl. calcified cysts)

• Moderate to high specificity of meat inspection

• Sensitivity of PCR decreases when calcified lesions

Geysen D., Kanobana K., Victor B., Rodriguez-Hidalgo R., De Borchgrave J., Brandt J.,

Dorny P. 2007. Validation of meat inspection results for Taenia saginata cysticercosis

by PCR-restriction fragment length polymorphism. J. Food Prot. 70, 236-240

• Mostly light infections, heavily infected animals

uncommon: meat inspection has a low sensitivity:

→ Most infected carcasses undetected

• Cattle reared on pasture: environmental contact• Cattle reared on pasture: environmental contact

• Consumption of raw or undercooked beef

• Taeniasis not notifiable

• Underdiagnosis of taeniasis (possibly inhibition of

reporting by patients)

• If diagnosed, no proper disposal of tapeworms

Survival of eggs in the environment:

• A few days in hay

• A few months in ensilated feed

• 6-8 months on pasture (humid, shade)

Real underlying reasons poorly understood:

• Direct transmission man-cattle uncommon

• “Water theory”?

– It is hypothesized that water plays an important

role as a route of transmission

• Epidemiological surveys on bovine cysticercosis,

including risk factor studies, are scarce in Europe

– Danish studies in the eighties (Kyvsgaard, Ilsøe, – Danish studies in the eighties (Kyvsgaard, Ilsøe, Henriksen, Nansen)

– French studies on sludge (Cabaret et al.)

– Belgian studies (Dorny, Geerts, Boone et al.)

– Swiss study (Flütsch, Deplazes et al.)

• Tapeworm carrier on farm (combined with poor

hygiene of farm staff)

• Tourism: defecation in open air

• Proximity of a railway

• Spreading of septic tank sludge

• Sewage treatment plants

• Accidental

• Low frequency• Low frequency

• Usually results in heavy infections in many cattle

on the same farm (France 2007)

• Tourism: open-air defecation: camping, walking,

farm tourism, mountain bike, ...

• Proximity of railway• Proximity of railway

• seem to be of minor importance in Denmark and

Belgium but important risk factors in Switzerland (60% of trains equipped with ‘open’ toilets which release sewerage

directly on to the tracks)

• Sludge from septic tanks illegally applied on

pastures or crops (in some cases mixed with

animal slurry) (Ilsøe et al., 1990)

� Important risk factor for heavy infections

(Denmark)

• Deposition of sewage sludge on land:

– Use of sludge as fertilizer not very common in

Europe:Europe:

• Implementation of more restrictive legislation for

use in agriculture (Cabaret et al., 2002)

– Seeding of T. saginata eggs from municipal

sludge on pasture is of limited risk if properly

sanitised (Cabaret et al., 2002)

• Proximity of sewage treatment plants

– Storm sewage overflow, birds and insects (Crewe,

1984)

• Streams carrying the effluent from sewage treatment plants:

– Cattle access to drink from streams carrying effluent from sewage treatment plants (Kyvsgaard

et al., 1991, Boone et al., 2007)

• Major risk factor:

– allowing cattle access to drink from streams carrying effluent from sewage treatment plants (odds ratio = 3.6). (odds ratio = 3.6).

• Minor importance:

– spreading of septic tank sludge through deliberate or accidental mixing with animal slurry,

– deposition of sewage sludge,

– proximity to railways, camping sites or sewage treatment plants

Kyvsgaard N;C., Ilsøe B., Willeberg P., Nansen P., Henriksen S.A. 1991. A case-control study of risk factors

in light Taenia saginata cysticercosis in Danish cattle. Acta Vet. Scand. 32, 243-252

• Major risk factors:

– location (province),

– number of slaughtered cattle,

– free access of cattle to surface water (OR = 1.91),– free access of cattle to surface water (OR = 1.91),

– flooding of pastures (OR = 1.76)

– proximity of the farm with a source of waste water effluent (OR = 1.55)

• Minor importance:

– spreading of septic tank sludge through mixing with animal slurry,

– proximity to railways, camping sitesBoone I., Thys E., Marcotty T., de Borchgrave J., Ducheyne E., Dorny P. 2007. Distribution and risk factors

of bovine cysticercosis in Belgian dairy and mixed herds. Prev. Vet. Med. 82, 1-11.

* estimated using the kernel-density interpolation function of ArcView 3.2

• Major risk factors: – presence of a railway line or a car park close to areas

grazed by cattle

– leisure activities around areas grazed by cattle

– use of purchased roughage – use of purchased roughage

– organized public activities on farms attracting visitors

• Minor importance: – Organic farming

– Transhumance in alpine regions

Flütsch F., Heinzmann D., Mathis A., Hertzberg H., Stephan R., Deplazes P. 2008. Case-control study

To identify risk factors for bovine cysticercosis in Switzerland. Parasitology 135, 641-656.

• All case-control studies

• Study design: case and control herds

• Denmark, Belgium: flat, frequent flooding, high demographic pressure, less tourism?high demographic pressure, less tourism?

dissemination of eggs through surface water

• Switzerland: hills, importance of tourism, most cattle have no access to streams (tap water)

infection of environment by tourists

• Farm infection

– Results in heavy infection of few animals

• Easy detection at slaughterhouse

• Environmental infection• Environmental infection

– Results in light infection of many animals

• Difficult detection at slaughterhouse

� Improved hygiene has led to increased

dissemination

Persistent problem:

– Insensitive meat inspection

– Possibility of spreading of eggs in – Possibility of spreading of eggs in

environment:

• Water treatment plants

• Rivers

• Flooding

• Trains

• Tourism

• Control should be based on prevention of taeniasis in man (meat inspection) andcysticercosis in cattle (taenia carrier)

� Sensibilisation campaigns to inform tapeworm carriers:

�Source of infection of cattle (even through toilet)

�Treatment

�Proper destruction of expelled worm

• Serology?

– Ante-mortem diagnosis

– Ab and Ag detection

– Ab detection measures exposure to infection, not – Ab detection measures exposure to infection, not

necessarily infection with the viable parasite

– Ag detection measures viable infection

– Sensitivity/specificity of tests?

• Histology or immunohistochemistry?

– Post-mortem diagnosis

– Confirmatory test

No. viable

cysticerci in

carcass

No. of

animals

No.

positive in

Ag-ELISA

%

0 4 0 0 0 4 0 0

1-10 4 1 25

11-20 6 6 100

21-50 3 2 66.7

1-50 13 9 69.2

>50 11 11 100

Total 28

• Experimental recombinant vaccine (TSA-9 and TSA-

18) against T. saginata induced up to 99.8%

protection against experimental challenge

infection with T. saginata eggsinfection with T. saginata eggs

• Operational characteristics of the vaccine will need

to be defined, such as duration of immunity and

protection of newborn calves

• Although the vaccine has the potential to be used

on a commercial scale for the control of bovine

cysticercosis, it is questionable whether it will be

commercialised

• Development of awareness of taeniasis/ cysticercosis among

medical doctors, veterinarians, meat animal producers and

the public through information and education

• Epidemiological surveillance of human taeniasis• Epidemiological surveillance of human taeniasis

• Improvement of abattoir testing of bovine cysticercosis

(serology ?)

• Reporting of Taenia saginata infection in a standardised

manner

• Re-evaluation of animal rearing system � production of

cysticercosis free animals in a quality controlled system

• Endemic in pig raising/pork consuming areas

• Associated with poverty

– inadequate sanitation, open air defecation

– lack of proper slaughtering facilities, meat inspection & control

– poor pig husbandry practices, free

roaming

• Spread by people/pig movement

– immigration

– overseas domestic workers

– international travel

– marketing and transport of pigs

Traditional pig husbandry systems:

• free roaming of pigs

• no proper feeding system

• no proper housing

• The absence or non-use of sanitary

installations: defecation in the bush or in

the piggery

• Coprophagous (or coprophylic) habit of

pigs

• Elimination of proglottids with the

faeces

• non-official slaughter of pigs

• absence of meat inspection

Absence of meat inspection

• Cysticercosis in swine is diagnosed in EU Member States as a

consequence of routine meat inspection procedures (Council

Directive 64/433/EEC).

• However, swine cysticercosis has virtually disappeared from

Europe Europe

– consequently the meat inspection does not pay much

attention to such control. It is based on visual observation

of the muscle surface of pig carcasses only.

• Cysticercosis in man seems to be eradicated in most of the EU;

small foci in Spain, Portugal and Eastern Europe exist;

information is very scarce

• Analysis of recent epidemiological data from the US (more

than 1000 cases each year) suggest that T. solium could

reemerge in Europe too

• Imported cases:

– Immigrants or travelers with cysticercosis

– Local human – human transmission: tapeworm carriers?

Country Publication type Number of

patients

Autochthonous

cases

France 2 case reports

1 epidemiological study

2

29

Total: 31

1

Total: 31

Portugal 3 epidemiological studies

1 large study on epilepsy in

NCC

505

143

Total: 648

No exact numbers

mentioned,

however, a large

part is locally

acquired

Spain 3 case reports

1 epidemiological study

7

52

4

52

Cases of NCC based upon case reports and surveys in the literature from 1990-2000

Overbosch D., Oosterhuis J.W., Kortbeek L.M., Garcia-Albea E. 2002. Neurocysticercosis in Europe.

In: Cestode Zoonoses: Echinococcosis and Cysticercosis, P. Craig and Z. Pawlowski (Eds) IOS Press

Literature search Own survey

Czech Republic 2 Czech Republic 1

France 1 Bosnia 1

Germany 1 Yugoslavia 2

Portugal (no exact

numbers)

Portugal 4

Spain 56 Spain 2

Italy 1

Autochthonous cases of NCC in Europe

SEQUELA Literature (n=779) Own survey (n=45)

Persistent seizures 101 18

Visual problems 2 2

Psychiatric changes 3 5

Neurological problems

(paresis, speech disorders)

2 2

Death 3

Unknown 672 3

Neuroimaging methods

Serology

• In most EU countries, no evidence of porcine

cysticercosis

• 0.006 – 0.6 % some areas of Spain (Garate, 1999)

• 0.0003% in Poland (Pawlowski, 1999)• 0.0003% in Poland (Pawlowski, 1999)

• Portugal (M. Vieira-Pinto, 2008; Direcção General

de Veterinária, 2008) :

Year No. pigs slaughtered No. cases

2005 4,859,108 0

2006 5,094,254 1

2007 5,470,708 0

• Portugal

– In period 1993-2004

• 1120 diagnoses of cysticercosis in public hospitals

• Mostly immigrants, but also local (Northern part of the

country)country)

– reports of porcine cysticercosis in abattoirs?

• Spain

– Extramadura

• Inconsistent and incomplete information

• Lack of controlled and compulsory registration in

Europe

• Conclusion: • Conclusion:

– autochthonous cases of human cysticercosis

are a rarity in Europe, but do still occur

– majority of cases are imported

• Possibility of reemergence?

– Example of the US: immigration from Mexico, Central

American countries, Europe?

– Opening the borders with Eastern Europe countries?

– Organic farming creates new opportunities?

– Main risk of introduction of infection by tapeworm

carriers

• Need of early warning system

• At the human level:

– Identification of tapeworm species after diagnosis of

taeniasis

– Information to public, physicians and veterinarians

– Routine examination of people coming or returning from

endemic areas

– Notification of human cysticercosis cases and taeniasis

– Epidemiological examination after diagnosis of human

cysticercosis

• At the pig (pork) level:

– Extensively reared pigs subject to more careful

examination

– Swine cysticercosis notifiable

Thank you for your attention