The use of urban sewage sludge on pastures: The cysticercosis threat;L'utilisation des boues d'épuration urbaine sur les pâturages: Le risque de cysticerose

Veterinary Research

Volumn 33, Issue 5, 2002, Pages 575-597

  Cabaret, Jacques ^a   Geerts, Stanny ^b   Madeline, Marylin ^c   Ballandonne, Céline ^c   Barbier, Dominique ^c  

^a CEMAGREF   (France)

^b INSTITUTE OF TROPICAL MEDICINE   (Belgium)

^c Parasitology Laboratory   (France)

Author keywords

Cattle; Cysticercosis; Human; Parasite; Urban sludge

Indexed keywords

FERTILIZER;

AFRICA; ANIMAL PARASITOSIS; ASIA; CATTLE; COMPOSTING; CONTROLLED STUDY; CYSTICERCOSIS; DENMARK; EPIDEMIC; GERMANY; GRAZING; HUMAN; INFECTION RISK; NONHUMAN; NORTH AMERICA; PASTURE; PATHOGENICITY; PERSONAL HYGIENE; PREVALENCE; REVIEW; RISK FACTOR; SEWAGE TREATMENT PLANT; SLUDGE; TAENIA SAGINATA; TAENIA SOLIUM; UNITED KINGDOM; URBAN AREA;

ANIMALIA; BOS TAURUS; TAENIA; TAENIA SAGINATA; TAENIA SOLIUM;

EID: 0036747024     PISSN: 09284249     EISSN: None     Source Type: Journal    
DOI: 10.1051/vetres:2002040     Document Type: Review

References (101)

1. Amin O.M., Pathogenic micro-organisms and helminths in sewage products, Arabian gulf, country of Bahrain, Am. J. Publ. Health 78 (1988) 314-315.
2. Arther R.G., Fitzgerald P.R., Fox J.C., Parasite ova in anaerobically digested sludge, J. Water Pollut. Control Fed. 53 (1981) 1333-1338.
3. Barbier D., Duhamel C., Perrine D., Georges P., Evaluation du risque parasitaire lié à l'utilisation agricole des boues résiduaires, Bull. Soc. Fr. Parasitol. 7 (1989) 259-264.
4. Barbier D., Perrine D., Duhamel C., Doublet R., Georges P., Parasitic hazard with sewage sludge applied to land, Appl. Environ. Microbiol. 56 (1990) 1420-1422.
5. Bergstrom K., Forekomst av parasittegg i avvatna ralam fra koakkreinseverk og septitankar in Noreg, Nor Veterinaertidsskr. 93 (1981) 323-330.
6. Bern C., Garcia H.H., Evans C., Gonzalez A.E., Verastegui M., Tsang V.C.W., Gilman R.H., Magnitude of the disease burden from neurocysticercosis in a developing country, Clin. Infect. Dis. 29 (1999) 1203-1209.
7. Blazek K., Schramlova J., Tissue reaction in experimental cysticercosis of sheep and goats caused by infection with Taenia saginata eggs, Folia Parasitol. 30 (1983) 131-139.
8. Boev S.N., On cysticerci of muscles of roe-deer in Kazakhstan, Helminthologia (Bratislv) 2 (1960) 47-54.
9. Borraz O., L'utilisation des boues d'épuration en agriculture: les ressorts d'une controverse, Courrier de l'environnement de l'INRA 41 (2000) 25-32.
10. Bouchet F., Léger N., Pollution parasitaire dans les boues des stations d'épuration des eaux usées de la région champenoise, Bull. Soc. Fr. Parasitol. 4 (1986) 13-18.
11. Bouhoum K, Schwartzbrod J., Quantification of helminth eggs in Waste water, Zbl. Hyg. Umweltmedizin 188 (1989) 322-330.
12. Bouhoum K., Habbari K., Schwarzbrod J., Epidemiological study of helminth infections in Marrakech waste water spreading zone. Second international Symposium on waste water reclamation and reuse, Iraklio, Greece, 14-20 October, 1995, pp. 221-231.
13. Brandt J.R.A., Geerts S., De Deken R., Kumar V, Ceulemans F., Brijs L., Falla N., A monoclonal antibody-based ELISA for the detection of circulating excretory secretory antigens in Taenia saginata cysticercosis, Int. J. Parasitol. 22 (1992) 471-477.
14. Cabaret J., Barbier D., Les risques parasitaires liés à l'utilisation des boues résiduaires urbaines: utopic on réalité? Bull. Soc. Fr. Parasitol. 19 (2001) URL http: //www.tours.inra.fi-/spar/bulletin/bulletin.htm.
15. Collomb J., Baradel J.M., Thevenot M.T., Schwartzbrod J., Recovery of helminth eggs in sludge from wastewater treatment plant, in: Proceedings 3rd International Symposium on Processing and Use of Sewage Sludge Brighton UK, Sept. 27-30, 1983, pp. 230-231.
16. Corwin R.M., Bovine cysticercosis in feedlots-Kansas, Veterinary Public Health Notes, Center for Disease Control, September, 1980.
17. Dada B.J.O., Taeniasis, cysticercosis and echinococcosis/hydatidosis in Nigeria: III - prevalence of bovine and porcine cysticercosis, and hydatid cyst infection based on joint examination of slaughtered food animals, J. Helminthol. 54 (1980) 293-297.
18. Deka D.K., Borkakoty M.R., Lahkar B.C., Cysticercosis in domestic animals in north eastern region of India, Indian J. Parasitol. 9 (1985) 83-85.
19. Devaux I., Intérêts et limites de la mise en place d'un suivi sanitaire dans le cadre de la réutilisation agricole des eaux usées traitées de l'agglomération clermontoise, Thése de Doctorat, Joseph Fournier University, Grenoble 1, 1999, 333 p.
20. Doby J.M., Guillou L., Robin L., Gielfrich G., Fréquence de la cysticercose bovine chez le bétail dans l'Ouest de la France, Méd. Mal. Infect. 8 (1978) 334-338.
21. Dorny P., Vercammen F., Brandt J., Vansteenkiste W., Berkvens D., Geerts S., Sero-epidemiological survey of Taenia saginata cysticercosis in Belgian slaughter cattle, Vet. Parasitol. 88 (2000) 43-49.
22. Dudkowski A., L'épandage agricole des boues de station d'épuration des eaux usées urbaines, Le Courrier de l'Environnement de l'INRA, 41 (2001) 134-135.
23. Dumontet S., Dinel H., Baloda B., Pathogen reduction in biosolids by composting and other biological treatments: A literature review, Proceedings of the 1Oth International Congress on environmental and sanitary problems in the Mediterranean areas, Vol. 1, Maratea, Italy, 10-13 October, 1997, pp. 251-295.
24. Duvaud E., Mugnier E., Gazzo A., Aubain P., Wiart J., Situation du recyclage agricole des bones d'épuration urbaines en Europe et dans divers pays du monde, Ademe Editions, Paris, 1999, 159 p.
25. Eckert J., Birbaum C., Abtotung von Wurmeiern in Hygienisierungsanlagen, Schweiz. Arch. Tierheilk. 125 (1983) 671-672.
26. Emery I., Bories C., Liance M., Houin R., In vitro quantitative assessment of Echinococcus multilocularis metacestode viability after in vivo and in vitro maintenance, Int. J. Parasitol. 25 (1995) 275-278.
27. Engelbrecht H., Mentzel U., Der urbane Wirtswechselzyklus von Taenia saginata im Kreis Wittstock, Bezirk Potsdam, Angew. Parasitol. 25 (1984) 126-132.
28. Fan P.C., Chung W.C., Sob C.T., Kosman M.L., Eating habits of East Asian people and transmission of taeniasis, Acta Trop. 50 (1992) 305-315.
29. Faust E.C., D'Antoni J.S., Odon V., Miller M.J., Peres C., Sawitz W., Thomen L.F., Tobie J., Walker J.H., A critical study of clinical laboratory techniques for the diagnosis of protozoan cysts and helminth eggs in faeces, Am. J. Trop. Hyg. 18 (1938) 169-183.
30. Feachem R.G., Bradley D.J., Garelick H., Mara D.D., Sanitation and disease: Health aspects of excreta and waste water management, New-York, John Wiley & Sons, 1983.
31. Fertig D., Dorn R., Taenia saginata cysticercosis in an Ohio cattle feeding operation, J. Am. Vet. Med. Assoc. 186 (1985) 1281-1285.
32. Forbes G.I., Collier P., Reilly W.J., Sharp J.C.M., Outbreaks of cysticercosis and salmonellosis in cattle following the application of sewage sludge to grazing land in Scotland, in: Proceedings of the 1st World Congress on foodborne infections and intoxications, 29 June-3 July 1980, West Berlin, Germany, 1980, pp. 439-440.
33. French Government, Arrêté du 8 Janvier 1998 fixant les prescriptions techniques applicables aux épandages de boues sur les sols agricoles pris en application du décret no 97-1133 du 8 décembre 1997 relatif à l'épandage des boues issues du traitement des eaux usées, Journal Officiel 31 Janvier 1992, pp. 6605-6612.
34. Fries G.F., Ingestion of sludge applied organic chemicals by animals, Sci. Total Environ. 185 (1996) 93-108.
35. Furet G., Birraux D., Wiart J., Deportes I., Epandage de boues d'épuration sur prairies et culture fourragères. Aspects microbiologiques, Ademe Editions, Paris, 1999, 155 p.
36. Gasnier N., Cabaret J., Moulia C., Allozyme variation between laboratory reared and wild populations of Teladorsagia circumcincta (Nematoda), Int. J. Parasitol. 22 (1992) 581-587.
37. Gaspard P., Schwarzbrod J., Helminth eggs in wastewater: quantification technique, Water Sci. Technol. 31 (1995) 443-446.
38. Gaspard P., Wiart J., Schwartzbrod J., A method for assessing the viability of nematode eggs in sludge, Environ. Technol. 17 (1996) 415-420.
39. Gaspard P., Wiart J., Schwartzbrod J., Parasitological contamination of urban sludge used for agricultural purposes, Waste Manag. Res. 15 (1997) 429-436.
40. Gauthier D., Rosaz C., Le Pimpec P., Lehy J.B., Valorisation des boues d'épuration de montagne - Risque sanitaire lié à l'épandage des boues en revégétalisation des pistes de ski. Évaluation et recommandations, Rapport de Synthèse, Conseil Général de Savoie, 1991, 37 p.
41. Geerts S., Taenia saginata: een eeuwig probleem?, Verhand. Kon. Acad. Geneesk. Belg. 52 (1990) 537-564.
42. Geerts S., The taeniasis-cysticercosis complex in Africa, Meded. Zitt. Kon. Acad. Overz. Wet. 38 (1993) 245-264.
43. Geerts S., Kumar V., Van den Abbeele, Taenia saginata cysticercosis in slaughter cattle in Belgium, VI. Diergeneesk. Tijdschr. 49 (1980) 365-374.
44. Geerts S., Kumar V., Mortelmans J., Sheep as an experimental model of Taenia saginata cysticercosis, Trop. Anim. Health Prod. 13 (1981) 37-40.
45. Geerts S., Brandt J., Kumar V., De Deken R., De immunodiagnose van Taenia saginata cysticerkose, Verhand. Kon. Acad. Geneesk. Belg. 54 (1992) 329-346.
46. Geerts S., De Borchgrave J., Brandt J., Kumar V, De Deken R., Infectivity of irradiated and non-irradiated cysticerci of Taenia saginata, Trans. R. Soc. Trop. Med. Hyg. 86 (1992) 421-422.
47. Gonzalez L.M., Montero E., Harrison L.J.S., Parkhouse R.M.E., Garate T., Differential diagnosis of Taenia saginata and Taenia solium infection by PCR, J. Clin. Microbiol. 38 (2000) 737-744.
48. Habtemariam S., Catechols and quercetin reduce MTT through iron ions: a possible artefact in cell viability assays, Phytother. Res. 9 (1995) 603-605.
49. Hammerberg B., MacInnis G.A., Hyler T., Taenia saginata cysticerci in grazing steers in Virginia, J. Am. Vet. Med. Assoc. 173 (1978) 1462-1464.
50. Harrison L., Joshua G., Wright S., Parkhouse R., Specific detection of circulating surface secreted glycoproteins of viable cysticerci in Taenia saginata cysticercosis, Parasite Immunol. 11 (1989) 351-380.
51. Harrison L.J.S., Holt K., Sewell M.M.H., Serum antibody levels to Taenia saginata in cattle grazed on Scottish pastures, Res. Vet. Sci. 40 (1986) 344-346.
52. Harrison Z., McBride M.B., Bouldin D.R., The case for caution. Recommendations for land application of sewage sludges and an appraisal of the US EPA's part 503 sludge rules, Cornell Waste Management Institute, 1999, URL http: //www.cfe.cornell.edu/wmi/PDFS/landApp.pdf.
53. Haugaard P., Cysticercosis and salmonellosis in cattle caused by sewage sludge on Danish farmland, Waste Manage. Res. 2 (1984) 163-168.
54. Horak P., Helminth eggs in the sludge from three sewage plants in Czechoslovakia, Folia Parasitol. 39 (1992) 153-157.
55. Hughes D.L., Norrington I.J., Morris D.L., Waite W.M., The effect of pasteurisation and stabilisation of sludge on Taenia saginata eggs, in: Inactivation of microorganisms in sewage sludge by stabilisation processes, Strauch, havelaar & l'Hermite eds., Elsevier, 1985, pp. 126-134.
56. Ilsoe B., Kyvsgaard N.C., Nansen P., Henriksen S.A., A study on survival of Taenia saginata eggs on soil in Denmark, Acta Vet. Scand. 31 (1990) 153-158.
57. Ilsoe B., Kyvsgaard N.C., Nansen P., Henriksen S.A., Bovine cysticercosis in Denmark. A study of possible causes of infection in farms with heavily infected animals, Acta Vet. Scand. 31 (1990) 159-168.
58. Kanazawa T., Asahi H., Mochida K., Simple techniques for preparation of small vesicles from Echinococcus multilocularis metacestodes and colorimetric quantitation of the viability of germinal cells, Jpn. J. Parasitol. 44 (1995) 441-446.
59. Kerckhoven van I., Vansteenkiste W., Claes M., Geerts S., Brandt J., Improved detection of circulating antigen in cattle infected with Taenia saginata metacestodes, Vet. Parasitol. 76 (1998) 269-274.
60. Khallaayoune K., Réutilisation des eaux usées en agriculture. Risque de transmission de parasites à l'homme et l'animal, Hommes, Terre et Eaux 103 (1996) 14-19.
61. Khizhnyak N.I., Romanenko N.A., Disinfection of sewage sludge from helminth ova at the sewage plants of the town of Kiev. Parasitological problems, Proceedings of the VIII scientific conferences in parasitology of Ukraine socialist republic, Part 2, "Science Academy", Kiev, Ukraine, 1975, pp. 252-253.
62. Kirichek V.S., Belousov M.N., Nikitin A.S., New data on the epidemiology of taeniasis in the extreme north of the USSR (data of investigations made in the Yamalo-Nenets autonomous region), Med. Parazitol. Parazit. Bolezni 6 (1984) 27-33.
63. Klebanovskii V.A., Klimshin A.A., Shpil'ko V.N., The spread of taeniasis on the Yamal peninsula. Voprosy kraevoi infektsionnoi patologii. (Kishechnye infektsii i invazii.) (Tezisy dokladov.) Tyumenskoe Otdelenie Vserossiiskogo Nauchnogo Meditsinskogo Obshchestva Epidemiologov, Mikrobiologov i Infektsionistov, Tyumen', USSR, 1974, pp. 172-174,
64. Kozakiewicz B., Taenia saginata cysticercosis in experimentally infected sheep and goats, Med. Weter. 33 (1977) 461-463.
65. Kyvsgaard N.C., Ilsoe B., Willeberg P., Nansen P., Henriksen S.A., A case-control study of risk factors in light Taenia saginata cysticercosis in Danish cattle, Acta Vet. Scand. 32 (1991) 243-252.
66. Lightowlers M.W., Eradication of Taenia solium cysticercosis: a role for vaccination of pigs, Int. J. Parasitol. 26 (1999) 811-817.
67. Madeline M., Ballandonne C., Guyon R., Malas J.P., Vilagines P., Cabaret J., Barbier D., Mise en evidence de la viabilité des œufs de Taeniidés dans les boues résiduaires urbaines, J. Eur. Hydrol. 31 (2001) 85-90.
68. Madeline M., Lendormy C., Guyon R., Malas. J.P., Barbier D., Boues résiduaires - Réglementation actuelle et œufs de taeniidés, Bull. Soc. Fr. Parasitol. 18 (2000) 1. URL http://tours.inra.fr/sfpar/bulletin.htm
69. Madeline M., Ballandonne C., Eldin de Pecoulas P., Guyon R., Malas J.P., Tourte-Schaeffer C., Cabaret J., Barbier D., Étude parasitologique des boues résiduaires urbaines: mise en évidence de la viabilité des œufs de Taeniidés, Bull. Soc. Fr. Parasitol. 19 (2001) 1, http: /www.tours.inra.fr/sfpar/bulletin/bulletin.htm
70. McCool C.J., Distribution of Cysticercus bovis in lightly infected young cattle, Aust. Vet. J. 55 (1979) 214-216.
71. McGrath S.P., Chaudri A.M., Giller K.E., Long-term effects of metals in sewage sludge on soils microorganisms and plants, J. Ind. Microbiol. 14 (1995) 94-104.
72. McManus D.P., Bowles J., Asian (Taiwan) Taenia: species or strain? Parasitol. Today 10 (1994) 273-275.
73. Morris D.L., Hughes D.L., Hewitt R.J., Norrington I.J., Pathogens in sewage sludge: (ii) effects of sludge stabilization and treatment processes on viability and infectivity of beef tapeworm eggs, Water Pollut. Control 85 (1986) 476-481.
74. Nansen P., Henriksen S.A., The epidemiology of bovine cysticercosis (C. bovis) in relation to sewage and sludge application on farmland, in: Block J.C., Havelaar A.H., L'Hermite P. (Eds.), Epidemiological studies of risks associated with the Agricultural use of sewage sludge: knowledge and needs, Elsevier Applied Science Publishers, London UK, 1986, pp. 76-82.
75. Nelson G.S., Pester F.R.N., Rickman R., The significance of wild animals in the transmission of cestodes of medical importance in Kenya, Trans. R. Soc. Trop. Med. Hyg. 59 (1965) 507-524.
76. Olsen J.E., Nansen P., Infectivity of eggs of Taenia taeniaeformis after anaerobic digestion of sewage sludge-a possible model for Taenia saginata egg resistance, Acta Vet. Scand. 31 (1990) 377-379.
77. Pawlowsky Z., Schultz M.G., Taeniasis and cysticercosis (Taenia saginata), Adv. Parasitol. 10 (1972) 269-343.
78. Pike E.B., Recent UK research on incidence, transmission and control of Salmonella and parasitic ova in sludge, in: Block J.C., Havelaar A.H., L'Hermite P. (Eds.), Epidemiological studies of risks associated with agricultural use sewage sludge: knowledge and needs, Elsevier Applied Science Publishers, London, UK, 1986, pp. 50-59.
79. Plachy P., Juris P., Transmission risk of helminth germs with sewage sludge to agricultural soil, Slovensky Veterinarky Casopis 19 (1994) 15-18.
80. Reilly W.J., Collier P.W., Forbes G.I., Cysticercus bovis surveillance-an interim report, Proceedings of the 8th International Symposium of the World Association of Veterinary Food Hygienists, Dublin, 30th August-4th September 1981, p. 298.
81. Rodriguez R.I., Differential diagnosis between Taenia saginata and Taenia solium; prevalence of Cysticercus bovis in the north of Ecuador, MSc-thesis No. 100, Institute of Tropical Medicine, Antwerpen, Belgium, 2001, 50 p.
82. Roy B., Tandon V., Metacestodiasis in north east India: a study on the prevalence of hydatidosis and cysticercosis in Mizoram, Nagaland and Assam, Ind. J. Anim. Health 28 (1989) 5-10.
83. Salm A., Erhebung zur Epidemiologie der zystizerkose des rindes im Raum Aachen, Doctorate in veterinary medicine Thesis, Hannover Veterinary Faculty, 1989, 93 p.
84. Schmidt G.D., Roberts L.S., Foundations of parasitology, Sixth edition, McGraw-Hill International Editions, New-York, 2000.
85. Schramlova J., Blazek K., Prokopic J., Some aspects of the presence of surface-associated acid mucosubstances on larval Taenia saginata infecting suitable and unsuitable hosts, Folia Parasitol. 37 (1990) 307-312.
86. SCVMPH 2000, Opinion of the Scientific Committee on Veterinary Measures relating to Public Health on the Control of Taeniosis/cysticercosis in man and animals, http://europa.eu.int/comm/food/fs/sfp/mr/mrℬien.html
87. Semenas L., Brugni N., Viozzi G., Kreiter A., Monitoreo de parasitos en efluentes domiciliarios, Rev. Saude Publica 33 (1999) 379-384.
88. Sewell M.M.H., Haris L.J.S., Holt K., Serodiagnosis of bovine cysticercosis and the application of sewage sludge to pasture, in: Block J.C., Havelaar A.H., L'Hermite P. (Eds.), Epidemiological studies of risks associated with the agricultural use of sewage sludge: knowledge and needs, Elsevier Applied Science Publishers, London, UK, 1986, pp. 102-105.
89. Sinnecker H., The epidemiological significance of urban sewage sludge in the spread of possible zooparasitic infections, Z. Ges. Hyg. 4 (1958) 98-115.
90. Slifko T.R., Smith H.V, Rose J.B., Emerging parasite zoonoses associated with water and food, Int. J. Parasitol. 30 (2000) 1379-1393.
91. Slonka G.F., Matulich W., Morphet E., An outbreak of bovine cysticercosis in California, Am. J. Trop. Med. Hyg. 27 (1978) 101-105.
92. Smith C.T., Sylvicultural use of municipal and industrial biosolids: overview of USA research programs and research priorities. Biosolids utilization in forestry, Bordeaux, 29-30 March 2000, ADEME-INRA, Abstracts of communications, p. 4.
93. Stevenson P., Observations on the hatching and activation of fresh Taenia saginata eggs, Ann. Trop. Med. Parasitol. 77 (1983) 399-404.
94. Swiss Government, Ordonnance sur les substances dangereuses pour l'environnement, Journal Officiel, ordonnance sur les substances dangereuses Osubst., Modification du 16 septembre 1992, 16 p.
95. Thomaz-Soccol V., Paulino R., Castro E.A., Andreoli C.V., Helminth eggs viability in sewage and biosolid sludge in Curitiba, Parana, Brazil, Arq. Biol. Tecnol. 40 (1997) 829-836.
96. Thornton I., Abraham P., Soil ingestion as a pathway of metal intake in a grazing livestock, in: Proc. Int. Conf. Heavy metals in the environment, Edinburgh, Scotland, 1981, CEP consultants.
97. US Government, Part 503, Standards for the use or disposal of sewage sludge, 40CFRCh1 (7-1-93 edition), Washington DC, USA, 1993.
98. Walther M., Koske J.K., Taenia saginata cysticercosis: a comparison of routine meat inspection and carcass dissection results in calves, Vet. Rec. 106 (1980) 401-402.
99. Wang I.C., Ma Y.X., Kuo C.H., Fan P.C., A comparative study on egg hatching methods and onchosphere viability determination for Taenia solium eggs, Int. J. Parasitol. 27 (1997) 1311-1314.
100. Watson D.C., Satchwell M., Jones C.E., A study of the prevalence of parasitic helminth eggs and cysts in sewage sludges disposed of to agricultural land, Water Pollut. Control 82 (1983) 285-289.
101. Wouters G., Geerts S., Brandt J., Kumar V, Calus A., Meriones unguiculatus as an experimental host for Taenia saginata metacestodes, Int. J. Parasitol. 18 (1988) 129-131.