Review
A successful, sustainable and low cost control-programme for bovine hypodermosis in France

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Abstract

Bovine hypodermosis affecting livestock performance and the leather industry was still widespread in France up to the nineties despite successive directives from the Ministry of Agriculture since 1941, encouraging livestock owners to treat, on a voluntary basis. In 1969 the French Ministry of Agriculture, asked the national Farmers’ Animal Health Organisation (FAHO), to plan a durable hypodermosis control programme and a working group including all the partners in cattle production was set up, under the coordination of the national FAHO. Improved systems of hypodermosis control, including new treatment and surveillance methods were developed. Among the main benefits obtained from this original work, were (i) the identification of scientific data which allowed inexpensive and accurate immuno-surveillance procedures, and a highly effective low-cost treatment, Ivomec®, administered at the micro dose rate (2 μg/kg), which is environmentally non-threatening, and (ii) the development of a new strategy to manage the control programmes progressively, on a regional basis, in two to three concentric zones over three successive years at a maximum. The current programme, coordinated at the National level since 1998, has been implemented in each region of France. The compulsory systemic winter treatments directed against the endo-parasitic stage, carried out by technicians and veterinarians involved the entire bovine population in controlled zones. As each zone reached a hypodermosis herd prevalence of under 5%, usually after two years, the treatments were suspended. However treatments of the infected farms and contiguous farms were maintained. An immuno-survey was carried out, each winter, to evaluate the prevalence of the disease and detect any residual foci or re-infestations. Since 2002, bovine hypodermosis in France is under control with immuno-surveillance maintained at a very low cost. In 2006 hypodermosis became a notifiable disease.

Introduction

Bovine hypodermosis is still widely distributed all over the Northern hemisphere from Eastern and Southern Europe (O’Brien, 1998) to Eastern China (Yin et al., 2003), and in North America (Scholl, 1998). It is caused by the development of the larval stages of insects inducing myiasis (Diptera, Oestridae), belonging to the genus Hypoderma (H.). Two species are generally involved in bovine hypodermosis (H. lineatum and H. bovis), H. sinense is also encountered in China (Yin et al., 2003). They are strictly parasites of all the Bos genus species but may infect humans accidentally. These parasites have an annual synchronised biological cycle. The first endo-parasitic stage migrates in the deep connective tissues of their hosts, from summer to the following spring. In spring, the larvae reach the dorsal subcutaneous tissue of their hosts and moult into the second and the third larval stages, producing swellings on the skin along the back, called warbles. The mature third stages fall on the ground and pupate at the end of spring. After one month the adult stages emerge. These flies unable to feed have a short life of one week. They spread the disease, within a radius of 5 km, by laying their eggs on the hair of the cattle.

The larvae induce hypodermosis, a serious cattle disease (Tarry, 1998), affecting weight gain, welfare, bovine immune defence mechanisms (Boulard, 1989, Nicolas-Gaulard et al., 1995) and the leather industry. In consequence, many attempts to control these parasites have been made following different approaches. The control measures were generally directed towards the larvae, but also in one case against the adults. A joint US-Canada pilot cattle grub project was carried out for a period of four years (1982–1986) in a territory containing 72,000 bovines. This programme was based on the principle of massive releases of sterile flies of Hypoderma spp. into natural populations. Such methods had proved successful in the eradication of the screwworm, but the project failed to control hypodermosis in North America (Kunz et al., 1990). The main limiting factor was the absence of reliable techniques for mass production in vitro, of Hypoderma flies for sterilization.

So far, definitive hypodermosis control has been achieved only in Western European countries. The first example of bovine hypodermosis eradication occurred, one hundred years ago, in the Danish islands without any therapeutic agents. The farmers eliminated the pest with success, by a manual extraction, of all the grubs from the warbles of their cattle and it was maintained a hypodermosis-free territory for a few years (Boulard, 2002). This example demonstrates that definitive control of hypodermosis is strictly dependent on organisation and management.

Later successful control programmes have all been based on chemical control directed against the larvae of the first stage, the most sensitive to insecticides, using a single annual systemic drug administered in winter, when the cattle are housed. These programmes have been successful, whatever the molecule used (organo-phosphorus (OP) compounds or macrocyclic lactones) (Boulard, 2002).

The successes and the failures of each of these hypodermosis control programmes including those which finally succeeded, were examined by the European specialists on hypodermosis, between 1992 to 2002, in the framework of two European Cost (European cooperation in the field of scientific and technical research) actions (811 and 833).

The main success’ factors for hypodermosis control which were identified were: (i) the awareness of the stockowners of the economic effects of hypodermosis and the cost/benefit of a control programme, (ii) the need for a political commitment and the introduction of specific legislation for bovine hypodermosis, (iii) the organisation in each country of a coordinated, large scale, control scheme at national level, making compulsory the treatment of all cattle, (iv) the maintenance of warble free status, involving sensitive tools for hypodermosis surveillance and detection (Boulard, 2002).

Among the hypodermosis free European countries, France was the last one to reach this status. Up to the nineties, after successive attempts at hypodermosis control (Boulard, 2002), the overall results remained poor and the warbled herd prevalence stayed as high as 50% in some regions.

However, in 1969, the French Ministry of Agriculture, greatly concerned over this disease, invited the national Farmers’ Animal Health Organisations (FAHO) to become involved in the coordination of research into improving the methods required for an efficient management of the ongoing programmes. In France, twenty millions cattle (both beef and dairy cattle) needed to be treated simultaneously, all over the country. Under such a large project, the drugs available on the market were not satisfactory in terms of risks of environmental pollution, residues in milk, and financial cost. It was recognised that original solutions should be provided, taking into account the protection of the environment and the consumers and the cost of such programme. A working group was created, bringing together the national FAHO, the Veterinary Services (VS), the Veterinary Practitioners Organisation (VPO), the leather industry and the scientific community of the Ministry of Agriculture (INRA). Through sharing their experience and understanding of this disease, they built up, step by step, the basis of a new management regimen to achieve sustainable and durable results.

Section snippets

Preliminary assays on a communal and a departmental basis

One of the primary factors in the success demonstrated by the Irish and British hypodermosis control programmes in the seventies was the compulsory treatment, of the entire cattle population, in the regions involved in the programme.

In France, the first law aimed at stimulating hypodermosis control was introduced in 1941, making the treatment of warbled cattle compulsory. But the treatments were carried out on a voluntary basis by farmers and a survey carried out forty years later indicated

The national directives of the current French programme leading to a durable control of hypodermosis

Two directives of the Ministry of Agriculture, in 1969 and 1989 reinforced the legislative support for the departmental and regional pilot schemes launched during that period. They also raised awareness and created incentives to farmers to become more active in the control of hypodermosis.

Then, finally in November 1994 a definitive national hypodermosis control programme was announced by the Ministry of Agriculture. This statutory order set out the different steps in the implementation of the

Conclusion

The control measures and the management of the hypodermosis control programme developed in France in 1998, have proven their effectiveness since their implementation. The reduced cost of this programme, by the use of Ivomec® administered at the micro dose level (2 μg/kg), and by the reduction in the numbers of samples for the immuno-survey, has facilitated the recruitment of livestock owners to this programme. The French animal health structures and farmers’ organisations have been very

Acknowledgement

Dr. D. O’Brien president of the European Cost 833, is gratefully acknowledged for his helpful advice all during the evolution of this programme and for reviewing most of the related publications.

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