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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