Waste Management & Research (1984) 2, 163-168
CYSTICERCOSIS AND SALMONELLOSIS IN CATTLE CAUSED BY SEWAGE SLUDGE ON DANISH FARMLAND Per Haugaard* (Received 5 April 1984) Three cases of infection in which beef tapeworms were transferred to cattle exposed to sewage sludge or septage applied to grass fields are reviewed together with an epizooty of salmonellosis, caused by infected latrine tankwagon used to irrigate a field. Mention is made of proposals on Danish regulations concerning the application of sewage sludge to agricultural soils, and the preventive measures with regard to epidemiological risks which are being discussed . It is concluded that it is possible to apply sewage sludge to agricultural soils without serious infection risks when appropriate preventive measures are taken . In particular raw latrine contents and septage from septic tanks appear to be particularly dangerous when spread on agricultural land . Key Words-Sludge, septage, land application, infection risk, cysticercosis, salmonellosis, cattle, Denmark, beef tapeworm.
1 . Agricultural use of sludge When considering resources and ecology problems it seems attractive to continue to use farm land as a recipient for sludge and maybe even to extend this method of disposal . Due to rising prices for phosphorus, which makes up approximately 2% of the sludge dry matter, there is increasing interest in utilizing this component . The results of several years of research on land application of sludge and farm wastes in Denmark have been published (Hansen & Tjell 1981 ; Errebo Larsen & Munch 1982) . It may, therefore, be useful to evaluate the infection risk of applying sludge on farm land and to give advice on, how to take precautions against this risk in order to eliminate or reduce it .
1 .1 . The infection risk Sludge may contain large numbers of pathogens, i .e . bacteria, viruses and parasites infectious to both animal and man . When applying sludge on farm land the most probable risk is that cattle will contract parasitic diseases . The reason is that a single egg is sufficient to cause disease, whereas the infective dose in for instance salmonellosis often may exceed several million bacteria . The beef tapeworm (Taenia saginata) is a parasite found in cattle muscles as bladderworms (cysticerci) . Heavy infestation of cattle flocks has occurred in Denmark following application of sludge to pastures resulting in considerable economic losses for the farmers . The frequency of salmonellosis in Danish livestock is increasing . This fact has attracted much attention and the possibility of transmitting salmonellosis with sewage sludge will also be mentioned .
*Municipal Food Control, I Engelshejgade, DK-6400 Senderborg . Denma 0734--242X/84/020163 + 06 $03 .00/0
Telephone : 454 429300 . r
1984 ISWA
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2 . Bladderworms (cysticerci) in cattle 2 .1 . The life cycle of the beef tapeworm The beef tapeworm is the most common tapeworm in Denmark . The adult worms live in the human small intestine, where it can reach a length of several metres . The eggs leave with the faeces and may be transported to pastures, where they are picked up by the cattle . In the intestines of cattle onchospheres emerge from the eggs, penetrate the intestinal wall, and are carried to all parts of the body via the lymphatic and venous system . The onchospheres undergo a metamorphosis in striate and cardiac muscle and develop into the fluid filled bladderworms or cysticerci, which are approximately the size of a pea . If beef meat, which has not been thoroughly cooked or frozen at a minimum of 10 ° C for at least 10 days, is consumed by humans, the cysticerci can develop into tapeworms, which attach to the intestinal wall and the life cycle is completed .
2 .2 . Cysticercosis caused by application of sludge on pastures The first case in Denmark, where sludge application on grassland resulted in cysticercosis in cattle has been reported previously and will be briefly described below together with two other cases .
2 .2 .1 . Cysticercosis cases on the island Als (South Jutland) 1972-73 (Haugaard 1975) During the summer 1972 a farmer agreed, that a public treatment plant could apply their aerobic stabilized sludge from activated sludge treatment to a pasture of his . A couple of months later 50 bull-calves were allowed to graze on the area . When they were slaughtered cysticerci were found in seven bulls . Four of them were condemned by the meat inspector due to a heavy infestation with cysticerci, whereas the remaining three bulls were approved for human consumption on the condition that the carcasses were frozen as previously described . As the treatment plant receives wastewater from a typical recreational area visited by numerous tourists, especially from the Federal Republic of Germany, it is very likely, that the tapeworm eggs in the sludge originated from this area . Tapeworms in humans are far more common in Central and Southern Europe than they are in Denmark . One or some tourists from abroad could therefore be the primary source of infection for this outbreak of cysticercosis . The farmer brought action against the responsible municipality, which was ordered to pay compensation to the farmer . The court found that the employees of the municipality ought to have known the risk of cattle infection with cysticerci by such application of sludge on pastures . 2 .2 .2 . Cysticercosis cases by Varde (Southwest Jutland) 1976-77 During 1976-77 28 head of cattle from one herd were condemned at slaughter due to infestation with cysticerci . An investigation showed that the pastures had been infected with tapeworm eggs . The farmer had an agreement with an agricultural contractor to spread farm slurry once every month . On one occasion the agricultural contractor had emptied the septic tanks at an international scout camp and instead of bringing the content of the septic tanks (septage) to a treatment plant, he had mixed it with the farm
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slurry and spread it onto the pastures of the farm . The insurance company of the agricultural contractor covered the farmer's losses, which were extensive (Westergaard 1982) . 2 .2 .3 . Cysticercosis cases at Esbjerg (Southwest Jutland) 1981-82 Due to infection with cysticerci in 1981-82 14 young bull-calves were condemned and six conditionally approved after having been frozen . The reason for this infestation has not yet been fully explained, but the farmer has brought action against the municipality, claiming that the maintenance of the sewerline has been insufficient, that his grassland had been flooded with sewage and his cattle thus been exposed to infection . A more likely explanation could be that an agricultural contractor has emptied a septic tank contaminated with tapeworm eggs and then used the vacuum wagon for spreading of liquid manure without cleaning it sufficiently inbetween . The farmer suffered an economic loss of Dkr . 85,000 and had to sell his farm by order of the court to pay his debts . 3 . Salmonellosis in cattle Intestinal infections with Salmonellae is commonly seen among animal and man all over the world . Salmonellosis is, therefore, an universal problem in connection with disposal of wastewater, sludge and farm manure . 3 .1 . The increase infrequency of salmonellosis in cattle In Switzerland, the Federal Republic of Germany and the Netherlands an increase in the occurrence of subclinical salmonellosis among adult cattle on grass has been noted . This fact has been linked to the application of sludge on farm land (Hess & Beer 1975 ; Strauch & Parrakova 1979) . In Scotland 26 incidents of salmonellosis occurred between 1973 and 1979 attributed to environmental pollution . The apparent sources were sewage effluents (ten incidents), septic tank effluents (eight), sewage sludge (three), seagulls (three) and abattoir effluents (two) . There were also five known outbreaks of cysticercosis in cattle attributed to the use of sludge in Scotland during 1973-79 (Reilly et al. 1981) . Having mentioned the risk of infection by the spreading of sludge on agricultural soils one should also consider the corresponding conditions connected with the spreading of farm slurry on soils . In several countries the number of salmonellosis cases in cattle herds has increased during the past decades (Veterinary Record 1978) . Among other things this increase might be caused by the industrialization of cattle farming . Epidemiological investigations made by Thunegard (1975) have proved that cattle on farms provided with farm yard slurry systems are far more exposed to nfections with Salmonellae than other stocks of cattle . In Denmark, too, there has been a considerable increase in cases of salmonella infections (Errebo Larsen 1980 ; Brest Nielsen 1984) . A survey made in 1980 revealed that two-thirds of the infected herds of cattle raised on split floors could come into contact with manure cellars or slurry tanks . This figure exceeds considerably the Danish average, which is 25-30% (Danish State Veterinary Serum Laboratory 1980) . In 1980 salmonellosis was found in 315 herds of cattle (Danish State Veterinary Service 1980) . Approximately 60% of the cases were found in the county of Ringkobing (West Jutland), where the number of livestock and the number of animals per herd is the largest in Denmark .
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Berthelsen (1982) has described cases of cattle salmonellosis in an area in West Jutland and he points out, that no less than 16 out of 25 infected herds of cattle had either contact to slurry from another herd through the use of a common slurry tankwagon or contact through the use of the same agricultural contractor for spreading the liquid manure . 3 .2 . Cattle salmonellosis near Aabenraa (South Jutland) 1975 In July 1975 a farmer borrowed a vacuum tank, which had been used to empty the collection tank of a camp site . He wanted to use the vacuum tank to irrigate a drought-stricken grass field . It was brought to a water hole, where the contents were diluted with water and then spread on to the grass field . Shortly afterwards his 18 cows were put out to graze on the field, and they contracted salmonellosis (Salmonella typhi murium) . In August 1975 the adjoining livestock caught salmonellosis . Two cows died, and also two persons on the farm were infected with salmonellosis . In October 1975 a third herd was infected with salmonellosis, here one cow died . Epidemiological investigations proved that these three outbreaks of salmonellosis were all caused by the camp latrine by way of the vacuum tanker (Hage & Brest Nielsen 1977) . 4 . Prevention of the risk of infection
4 .1 . What mistakes have been made in the four cases referred to? In the four outbreaks of disease some mistakes in the planning of spreading of a sludge are common :
• insufficient or no treatment of the sludge or septage prior to application ; • sludge was spread on grass areas ; • no or very short period from the spreading of sludge until cattle was put out to graze ;
• insufficient cleaning of tank wagons used for the transport of sludge after their use for other purposes or application of mixtures of sludge, slurry and liquid manure . 4 .2 . How could this have been avoided? One cannot expect to completely eliminate all pathogens in sludge by conventional treatment or by inactivation in the environment . However, the following methods will reduce the risk considerably . Treatment of sludge with quicklime, thermophilic digestion, composting, heat and a reasonable storage period after the treatment minimize the infection risks . A study by Strauch & Schreiber-Rothschild (1980) has demonstrated, that it is not possible to detect salmonellae in digested sludge after addition of a minimum of 7 kg quicklime m -3 (pH = 12) . The same negative result was achieved in salmonella studies of sludge from a local sewage plant in Sonderborg, where 10 kg quicklime m -3 was added . The risk of infection caused by spreading insufficiently treated sludge on pastures is so great that even with a long waiting period after spreading the idea should be rejected . It is very important that the transport wagons used for liquid manure, slurry etc . are thoroughly cleaned before they are used for other purposes . The spreading of both sludge and slurry is often carried out by an agricultural contractor which means, that the possibility of mixing sludge and slurry is obvious .
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4 .3 . Proposal for Danish legislation on the application of sludge in agriculture For several years the Danish Agency for Environmental Protection has been working on regulations for the use of sludge on agricultural soils, and according to their latest publication (Miljostyrelsen 1982) sludge can be applied on agricultural soils, provided certain demands on quality of the sludge, storage, transport and spreading are observed . The main points are : (i) There should be restrictions on the concentrations of cadmium, mercury, lead and nickel in sludge . (ii) When storing, transporting and spreading sludge unhygienic conditions and ould be avoided . (iii) Tools and tank wagons used for transport, handling and spreading should be cleaned immediately after the use and prior to the use for other purposes . (iv) Sludge may be spread on agricultural soils, provided they are dug in within 48 h . (v) Untreated sludge (including sludge from septic tanks) may be spread on agricultural soils if it is dug in . (vi) For at least half a year after an area has received sludge only grain or industrial crops may be grown and ripened on the area . (vii) The concentration of cadmium applied to the fields must not exceed 200 g ha - t (viii) There should be requirements for analysis of sludge and the municipal should make sure that the prescriptions of the legislation are observed . The proposed Danish regulations are primarily concerned with the effects of cad on human health and make little or no reference to the possible risk of infection from sludge spread on pasture or crop land . While this may be appropriate from the standpoint of human health it does not face the potential economic consequences of infection in cattle herds for the farmers .
5. Conclusions Under the prevailing conditions in Denmark the application of sludge on agricultural soils is a question of risks to animals rather than that of a risk to human health . However, the risk of infection should be reduced as much as possible by appropriate treatment of the sludge in sewage plants . If the storage, handling, transport and spreading is carefully planned, as suggested in the Danish draft for legislation about the application of sludge in agriculture, the risk of infection will be negligible . Experiences referred to in the literature and the cases described in this paper indicate that the application of raw sludge or septage on pastures constitute a great risk of infection for cattle and if not properly carried out this way to apply sludge should be banned . The cases described here have shown, that the cleaning of tank wagons used for liquid manure and slurry should be very thoroughly carried out to avoid infection of cattle .
References Berthelsen, G . (1982), En Salmonella dublin epidemi blandt kalve, (Salmonella dublin epidemic among calves), Dansk Veterintertidsskrift, 65, 262-269 . Brest Nielsen, B . (1984), Kvxgsalmonellosens bakteriologi og udbredelse, (The bacteriology and extension of salmonellosis in cattle), Dansk Veterinartidsskrift, 67, 77-81 . Danish State Veterinary Serum Laboratory (Statens Veterinxre Serumlaboratorium) (1980) . SVSinformation, 3, Copenhagen . Danish State Veterinary Service (Veterinxrdirektoratet 1980) Arsberetning fra Veterinaer-
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direktoratet . for drei 1980 . (The annual report from the Danish State Veterinary Service for the year 1980) . Copenhagen . Errebo Larsen, H . (1980), Communicable diseases among danish farm livestock . Proceedings C.E.C . scientific workshop on communicable diseases resulting from storage, handling, transport and landspreading of manures. Hannover 5-6 November 1980 . Errebo Larsen, H . & Munch, B . (1982), Sygdoms : og miljemiessige problemer i forbindelse med behandling og spreadning of flydende husdyrgodning (gylle), (Disease and environmental problems related to treatment and land application of farm slurry) . DSR forlag, Bülowsvej, DK-1871 Copenhagen . Hage, L . & Brest Nielsen, B . (1977), Latrinbeholder som ärsag til udbrud of kvaegsalmonellose (Latrinetank caused outbreaks of salmonellosis in cattle), Dansk Veterintertidsskrift, 60, 657-659 . Hansen, J . Aa . & Tjell, J . C . (1981), Slammets jordbrugsanvendelse (Land application of sludge) . Polyteknisk forlag, Anker Engelundsvej, DK-2800 Lyngby. Haugaard, P . (1975), Tinter og slutdisponering of slam, (Cysticerci and the final disposal of sludge), Dansk Veterinœrtidsskrift, 58, 541-546 . Hess, E . & Breed, C . (1975), Salmonellaepidemiologie und Grünlandsdüngung mit Kläschlam, (The epidemiology of salmonellosis and spreading of sludge on pastures), Zentralblatt für Bakteriologie, Mikrobiologie und Hygiene, I . Abteilung Originale Reihe B, 161, 54-60 . Miljestyrelsen (Danish Agency of Environmental Protection) (1982), Udkast til bekendtgorelse om anvendelse of slam i jordbruget (Draft for legislation about application of sludge in agriculture), dated 8 November 1982 . Reilly, W . J ., Forbes, G . I ., Paterson, G . M . & Sharp, J . C . M . (1981), Human and animal salmonellosis in Scotland associated with environmental contamination 1973-79, The Veterinary Record. 108, 553-555 . Strauch, D . & Parrâkovâ, E . (1979), Gefährdung des Weideviehs bei der Landwirtschaftlichen Verwertung von Klärschlam . (The danger to cattle arising from the use of sludge on farm land) . Städtehygiene, 21, 195-198 . Strauch, D . & Schreiber-Rothschild, R . (1980), Mikrobiologische Untersuchungen zur Hygienisierung von Klärschlamm . 8 . Mitteilung: Der Einfluss von Kalk als Konditionirungsmittel bei Kammerfilterpressen, (Microbiological investigations of sewage sludge desinfection . 8th communication : The significance of lime as condition material in chamber filterpresses), Gwf- Wasser/Abwasser, 121, 607, 611 . Thunegard, E . (1975), On the persistence of bacteria in manure . A field study with special reference to Salmonella in liquid manure . Acta veterinaria Scandinavica, Suppl. 56, 1-56 . Veterinary Record (1978), Salmonellosis increases in humans and livestock, Veterinary Record 102, 271-272 . Westergaard, J . M . (1982), Veterinary inspector, Danish State Veterinary Service pers . comm .