Surveillance of Echinococcus granulosus in dogs with arecoline hydrobromide

Bull. Org. mond. Santi 1 1973, 48, 649-652 Bull. Wld Hlth Org. j Surveillance of Echinococcus granulosus in dogs with arecoline hydrobromide M. A. GEMMELL1 Arecoline hydrobromide has been used for almost half a century for the treatment of Echinococcus granulosus in dogs. Trials in New Zealand showed that it had real limitations for this purpose. Its main value lies in its use as a diagnostic agentfor detecting infections in dogs on a group basis. The data so obtained can be used in educating dog owners as well as for providing base-line data and an index ofprogress in a continuing controlprogramme. The drug's limitations for treatment and value as a diagnostic agent in a field trial are assessed. For many years New Zealand has had a strong programme for the evaluation of arecoline hydro- bromide in the treatment of infections of Echino- coccus granulosus and other taeniid tapeworms such as Taenia hydatigena and T. ovis in dogs. More recently, studies have centred on its use for the detection of such infections. A brief review is given here of the principal findings of research work in New Zealand regarding the drug's value and limita- tions for both treatment and diagnosis. TREATMENT Studies with arecoline hydrobromide have con- cerned its efficiency in worm removal (Batham, 1946), speed of action (Forbes & Whitten, 1961), and use as an enema (Forbes, 1961). Limitations A comprehensive study on arecoline hydrobro- mide was carried out by Batham (1946). She found that this substance was about 90% effective in removing E. granulosus from some dogs, but that others retained worms even after 6 consecutive treat- ments. A prime factor in the failure to remove worms was the compound's failure to induce purgation. Increasing the dose rate above 3.5 mg per kg body weight did not increase the number of dogs that reacted unfavourably to treatment. Purgation Forbes & Whitten (1961) recognized that a practi- cal method was needed for treating dogs en masse, 1 Director, Hydatid Research Unit, Medical Research Council of New Zealand, University of Otago Medical School, Dunedin, New Zealand. particularly with regard to reducing the time interval between treatment and purgation. They found that this interval was decreased if arecoline hydrobromide was given in liquid rather than solid form. Forbes (1961), confirming the earlier work on purgation, studied the possibility of increasing the effectiveness of the drug by giving an arecoline hydrobromide enema to dogs that were not purged by an oral treatment. He found that the proportion of dogs that failed to be purged could be reduced dramatically by using the enema. Mode of action Progress was made towards defining the factors responsible for the drug's erratic behaviour by exam- ining its effect on the dog and on the worm (Forbes, 1964a, 1964b; Bell & Bennett, 1970). The studies showed that arecoline hydrobromide given per os acts locally on the gut wall to induce purgation, and that the liver is the principal site for detoxification of the drug. In direct contact with the worm, arecoline hydrobromide was found to inhibit neuromuscular activity, thereby causing paralysis but not death. DIAGNOSIS Evidence that arecoline hydrobromide, if used for detecting tapeworm infections in dogs and combined with appropriate measures to prevent dogs gaining access to raw offal, could reduce the prevalence of E. granulosus more effectively than a control pro- gramme based solely on anthelmintic treatment was reported from the Styx field trial (Gemmell, 1958, 1968b). In the first 9 years of the trial, farm dogs were regularly treated every 3 months with arecoline 3062 649 - M. A. GEMMELL hydrobromide by a trained worker. During that period diagnosis was not undertaken. The trial was continued for a further 6 years, during which time the dogs were treated at irregular intervals by the owners. Again, no diagnosis was made of tapeworm infections. Progress was assessed, however, by exam- ining sheep for larval tapeworms at slaughter. Throughout this period it was found that there was no way for the control authority or the owners to determine whether or not dogs were gaining access to raw and infective offal. In addition, it was difficult to account for the continued high infection rate in the sheep. In other words, progress could not be mea- sured adequately and correlations could not be made between infections in dogs and those in sheep. Any field trial or control scheme that fails to produce reasonable evidence of progress must in the end fail. As a result of this experience, it was decided to evaluate arecoline hydrobromide in the diagnosis of tapeworm infections, both for epidemiological stu- dies and for educational purposes. Before the method could be applied, it was necessary (a) to develop practical methods for separating worms from dog faeces; (b) to define safety precautions; (c) to determine the limitations of arecoline hydro- bromide in expelling worms. Methods for separating worms from faeces Small tapeworms are difficult to detect in faeces. Two techniques were developed to isolate the worms, the details of which were reported by Gemmell (1968b). The first-the salt flotation technique-was intended for making an immediate diagnosis in the presence of the owner. The second-sieving under pressure-was designed for large-scale diagnostic operations in the laboratory. It was concluded, after assessment of their limitations, that both methods, although less accurate than the more costly sedimen- tation and dilution technique, separated worms from faeces adequately. When microscopy was not used, the size of the worms, rather than their number, was a limiting factor in detecting organisms. Health precautions There are obvious health risks in handling dogs infected or faeces contaminated with eggs of E. gran- ulosus. A number of studies were undertaken to define these risks and thereby determine the precau- tions that should be taken to reduce health hazards to a minimum (Gemmell, 1968c). It was observed that the normal method of transmission is by inges- tion of eggs, but hydatid cysts can develop if eggs are inhaled directly into the lungs (Borrie et al., 1965). The eggs can survive for long periods in a wide range of chemicals, including formalin (Hercus et al., 1962). Although the eggs can be killed by heat, heat penetrates dog faeces slowly; hence the faeces should be boiled for no less than 5 minutes before examina- tion or disposal (Gemmell, 1968b). If the general precautions used for handling infectious diseases are applied, the risk of technicians contracting hydatid disease appears to be small (Gemmell, 1968c). Limitations for diagnosis An assessment was made of the value and limita- tions of field and laboratory diagnosis of tapeworm infections in dogs over a period of 6 years during the Styx field trial (Gemmell, 1968a, 1968b). Among the more important findings, it was noted that under field conditions a high proportion (about 20%) of dogs failed to be purged, whether the drug was given in solid or liquid form. Even when purgation was induced, a negative result at 2 or more treatments could not be regarded as proof that a dog was free from tapeworms. Treatment with an arecoline hydro- bromide enema, although it increased the number of dogs successfully purged, decreased the accuracy of the test by increasing the number of false negatives. At any time during the trial a proportion of the dogs was not available for treatment because of pregnancy or other reasons. Moreover, it was possible for a tapeworm to reach patency and be naturally elimi- nated, perhaps 2 years later, without being detected, even when an attempt was made to treat the available dogs every 3 months. It was concluded that surveys of tapeworm popu- lations in dogs cannot replace those of cyst popula- tions in food animals as the major criterion for assessing progress in control. With care, however, data of epizootiological and educational value can be obtained by using arecoline hydrobromide as a diagnostic agent. Backed by a strong follow-up programme directed at dog control, diagnosis is considered more likely to reduce the prevalence of echinococcosis than treating dogs regularly without diagnosis. When diagnosis is undertaken, a greater educational advantage may be achieved by using salt flotation in the presence of the dog owner than by collecting samples and performing the diagnosis later in the laboratory. Validity of data A number of factors tended to reduce the efficiency of the salt flotation method for diagnosis. Apart 650 SURVEILLANCE OF ECHINOCOCCUS GRANULOSUS IN DOGS from gross deficiencies in worm removal by treat- ment with arecoline hydrobromide, it was possible to double or halve the apparent incidence of infections by varying the testing procedure. For survey data to be meaningful they should be accompanied inter alia by information on the following points: the method used for treating the dogs; the interval between treatments; the thoroughness with which doubtful samples were eliminated from the analysis; the amount and type of material examined; the method used for separating worms from faeces; and the use of visual aids for examining samples. CONCLUSIONS With regard to treatment, it seems clear from the data obtained in New Zealand that arecoline hydro- bromide is highly erratic in its action on both dogs and worms, and all practical attempts to improve its efficiency have been unsuccessful. It is difficult to see how any improvements can be made until further basic information on the mode of action of this class of parasympathomimetic compound on the dog and worm is available. On the other hand, despite its limitations for treatment, arecoline hydrobromide used as a diag- nostic agent to detect the presence of E. granulosus and other taeniid tapeworms in dogs on a group or farm basis has three useful roles. Firstly, the method can be employed to obtain base-line data on the prevalence of these organisms in a particular region. Secondly, in association with studies on infection rates in food animals, the data can provide valuable epizootiological information. Finally, following the initiation of a control programme, the method pro- vides the control authority with immediate informa- tion on the success or failure of measures taken by the owner to prevent his dogs gaining access to raw and infective offal. A further benefit is that if the data on infections obtained by diagnosis are intelligently fed back to the owner, particularly if the diagnosis is made in his presence, they provide a stimulus that will usually lead to a genuine attempt by him to prevent his dogs gaining access to raw offal. In the case of those who remain unimpressed by the repeated demonstration of worms, diagnosis provides the information re- quired by the control authority to take any steps necessary (e.g., quarantine) to ensure compliance with the regulations. It is emphasized, however, that if such surveillance is to be carried out successfully, very high standards of training and supervision of technical personnel must be maintained. This means that the diagnostic programme must be designed, organized and financed in such a way that it can be continued indefinitely. SUMIt CONTROLE DE L'INFECTION A ECHINOCOCCUS GRANULOSUS CHEZ LE CHIEN PAR LE BROMHYDRATE D'ARECOLINE Les resultats d'un essai sur le terrain, qui est toujours en cours, indiquent qu'un programme de lutte contre Echinococcus granulosus axe sur l'emploi du brom- hydrate d'arecoline fait preuve du maximum d'efficacite lorsque le depistage des infections est directement associe a des mesures visant i empecher les chiens de se nourrir d'abats de mouton crus. On a constate que 6 traitements ou plus sont neces- saires pour eliminer les tenias chez le chien. Des methodes ont ete mises au point pour recolter les 6chantillons de feces apres administration du m6dicament et pour isoler les vers. Le tamisage sous pression, pour le diagnostic de masse au laboratoire, et la flottation en solution salee, pour le depistage immediat sur place, se sont reveles efficaces. On recommande de st6riliser les feces par ebullition avant toute manipulation. L'identification des parasites en presence du proprie- taire du chien a un effet certain de persuasion en ce qui concerne l'adoption de mesures propres a pr6venir la reinfection des animaux. S'il fait preuve d'une activite therapeutique ikreguliere, le bromhydrate d'ar6coline s'avere en revanche tres utile pour le diagnostic. II permet de recueillir des informations sur la prevalence de l'infec- tion a E. granulosus dans une region donn6e et de suivre les progres de la lutte contre la maladie. 2 651 652 M. A. GEMMELL REFERENCES Batham, E. J. (1946) Parasitology, 37, 185 Bell, M. E. & Bennett, E. W. (1970) Proc. Univ. Otago med. Sch., 48, 3 Borfe, J. et al. (1965) Brit. J. Surg., 52, 876 Forbes, L. S. (1961) N.Z. vet. J., 9, 105 Forbes, L. S. (1964a) Ann. trop. Med. Parasit., 58, 116 Forbes, L. S. (1964b) Ann. trop. Med. Parasit., 58, 119 Forbes, L. S. & Whitten, L. K. (1961) N.Z. vet. J., 9, 101 Gemmell, M. 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