The author is Senior Officer (Veterinary Services Group) of the Animal Production and Health Division, FAO, Rome.
The occurrence in North Africa of the New World screwworm (NWS), Cochliomyia hominivorax, its first establishment outside its home range in tropical and subtropical America, has caused renewed interest in and concern about this most serious insect pest of livestock of the western hemisphere. The purpose of this article is to review the most important features of the NWS and its effect on its hosts and the livestock industry of the Americas as background information on possible consequences of its spread-to other areas of the eastern hemisphere. Measures and programmes are also described on how this pest was controlled and then eradicated in Mexico and the United States of America, as well as the efforts made so far to control and prevent NWS spread in North Africa.
Close-up of screwworm larva showing hook-like mouthparts - Détail d'une larve de lucilie bouchère montrant les pièces buccales en forme de crochet - Primer piano de una larva de gusano barrenador, con las piezas bucales en forma de gancho
Except where it is now eradicated, the NWS occurs throughout tropical and subtropical America and also in adjacent temperate climate areas seasonally. The first reported case of screwworm was made by Coquerel in 1858, from a human sample collected on Devil's Island, off the shore of Guiana.
Although identified early, NWS was only recognized as a serious livestock problem in the southern part of the United States of America as the livestock industry there became more developed. Infestation occurred in subtropical areas of the southwestern United States all year round, spreading northward with warmer weather. Outbreaks also occurred sporadically in other areas of the United States to which infested animals had been transported during periods when the weather was suitable for the parasite's reproduction. In temperate areas, the onset of winter brought an end to these infestations. In 1933 infestation spread from the southwest to the southeastern United States, adding the southern part of the state of Florida to the overwintering areas from where, during spring and summer, infestation spread northward along the eastern part of the country.
With the exception of Mexico, some Caribbean Islands and Central America, losses due to NWS elsewhere in the Americas have been less well documented than in the United States. Because there are no official programmes for control in these countries, the presence of the parasite is not normally notifiable, and prevention and treatment of NWS is considered the responsibility of the individual livestock owner.
When the presence of NWS was confirmed in the Libyan Arab Jamahiriya in 1989, countries of the region and FAO became concerned that the parasite, if it should spread, could, in the words of the Director-General "have disastrous consequences to livestock, wildlife and even perhaps to human populations of Africa, the Near East and southern Europe".
Since breeding populations that overwinter have been established in North Africa, there is little reason for optimism that the NWS could not also establish itself in other areas of the eastern hemisphere with suitable climatic conditions, causing damage to the livestock industry equivalent to, or possibly even more severe than, that caused in the Americas.
The larval stage of the NWS is an obligate parasite of living flesh of warm-blooded animals. Gravid female flies are attracted to wound sites, even those as small as tick bites. As many as 400 eggs are laid in and on the edges of these wounds. These eggs hatch into small larvae approximately 12 hours later and invade the wound. With their hook-like mouth parts, larvae rasp the living tissue and feed on the resulting secretions, growing quickly. The wound is enlarged and deepened as a result, attracting more female flies which in turn lay more eggs. Multiple infestations, often complicated by secondary infections of wounds, lead to sickness and frequently death of the host animal.
Worms feed from the wound for an average of one week before the mature larvae, approximately 1.5 cm in length, drop to the ground to burrow into the soil arid pupate. The length of this pupal stage of the life cycle in the ground is temperature-dependent. During ideal conditions, it can be as brief as seven days, and during cool weather can exceed one month. Neither pupae nor other stages of the parasite survive freezing weather a feature determining its geographical distribution during the winter.
Emerging flies quickly mature. Males mate several times, commencing 24 hours after emergence. The female mates about two days after emergence and four days later she is ready to lay her first batch of eggs. Several batches, at three-day intervals, may be laid where the opportunity occurs. She may-travel long distances in search of wounds - up to 200 km have been recorded with marked sterile flies, although such distances may be exceptional. Distances travelled depend on the local availability of hosts, mates and vegetation upon which adult flies feed. Adult flies are rarely seen. It is the larval "worm" that causes the damage and is easily seen by the livestock keeper.
In warm weather, ideal conditions for screwworm reproduction, the complete life cycle can be less than three weeks; during cooler weather it can be prolonged to up to two months. Characteristics of screwworm biology relevant to prevention, control and eradication will be described as these topics are presented.
Where it occurred in the United States and Mexico, NWS was a major animal health constraint to production and careful ranch management was necessary. Breeding was frequently scheduled to avoid calving during heavy fly seasons, with the subsequent risk of infestation of umbilical wounds. Surgical intervention and branding of herds were similarly scheduled. Those ranchers with the resources to do so employed cowboys to "ride the range" to treat wounds either prophylactically or curatively during the height of infestation. Small or part-time livestock raisers made similar efforts to avoid losses, or were forced to give up keeping animals if they were unable to treat them. The development of modern insecticides with residual effect significantly improved both preventive and curative treatment. With continuous surveillance and treatment of all wounds detected, livestock losses could be reduced but not without considerable expense and effort.
In most countries of the Americas, evidence of the importance of the parasite is found in discussions with livestock owners and by observing the predominance of NWS medications in veterinary pharmacies throughout the region. By making a projection of studies made in North and Central America, losses to the livestock industry throughout the hemisphere including the cost of constant surveillance and treatment can be estimated to amount to several hundred million dollars annually.
The economic consequences of the NWS can perhaps best be indicated by the results of the pressures by the United States and Mexican livestock industries affected by this pest to have programmes - implemented for screwworm eradication when the technology became available. The first programme began in Florida, United States, in 1958. A series of programmes, strongly promoted by and with the participation of livestock producers, eradicated screwworms to a specifically chosen barrier in the relatively narrow Isthmus of Tehuantepec in southern Mexico, by 1984. The cost of these programmes, met by governments and cooperating producer groups in the United States and Mexico, exceeded US$500 million. Costs for similar programmes would, of course, be significantly higher today.
In 1935, a USDA study estimated costs of that year of severe screwworm infestation in the country's largest cattle state, Texas, at US$10 million. By 1960, costs of the infestation to the United States were conservatively estimated at US$80 million annually. This occurred after the screwworm had been eradicated in the southeastern states, where losses had been estimated at US$20 million a year. In 1976, a screwworm outbreak in the State of Texas was estimated to have caused losses to the livestock industry and to consumers of between US$283 million and US$375 million in that year. Recent estimates of losses to the United States if screwworm were to become enzootic in that country again range as high as US$ 1 000 million per year.
In 1984, by the time screwworm infestation had been eradicated as far as the sterile fly barrier in southern Mexico, giving protection to most of the country, annual benefits to the livestock industry of that country were estimated at US$130 million.
A study carried out in 1977 in Jamaica estimated annual losses due to screwworm infestation at US$3 million. Belize, with a small livestock population, currently estimates losses at US$1.25 million/year.
Losses caused by screwworm infestation are not only those resulting from morbidity and mortality of livestock but also from the costs of continuous surveillance and treatment of animals. Increased costs of livestock management practices, dictated by NWS presence, are difficult to estimate. If the infestation were to spread to most-countries of Africa there would clearly be concern about the foreign exchange costs required to employ insecticides continuously to control the parasite effectively. If the infestation should reach sub-Saharan Africa, there is also concern that in some areas the tradition of scarring livestock for therapeutic purposes would produce an additional source of manmade wounds for the parasite.
Human hosts. Like other warm-blooded animals, humans too are subject to NWS infestation. As shown by the name of the species, hominivorax, or "eater of man", the original diagnoses were made in humans. Hundreds of human cases of this condition have been documented in the Americas. As might be expected, the infestation which seems to predominate is that in cavities not easily observed, such as nasal sinuses, and in severely debilitated people. In the most traditionally affected areas of tropical America, the population is aware of the parasite and takes precautions. The spread to areas where NWS has not previously occurred also presents risks that people will not protect themselves because of lack of knowledge and experience.
Animal movement control is vital to prevent spread of infestation - Le contrôle des déplacements des animaux est indispensable pour empêcher la propagation de l'infestation - El control de los movimientos de animales es vital pare impedir la propagación de la infestación
Progress in screwworm eradication in the United States and Mexico - Evolution de l'éradication de la lucilie bouchère aux Etats-Unis et au Mexique - Avances en la erradicación del gusano barrenador del ganado en los Estados Unidos y México
Large sterile screwworm fly plant in southern Mexico - Grande installation du sud du Mexique produisant des lucilies bouchères stériles - Grandes instalaciones pare la obtención de moscas gusaneras estériles en el sur de México
Preventive larvacide treatment of flock. Small wounds are difficult to see - Traitement préventif des troupeaux aux larvicides. Les petites plates vent difficiles a repérer - Tratamiento preventivo de un rebano con larvicida. Las pequeñas heridas son difíciles de ver
Wildlife hosts. The wide host range of NWS infestation includes the expected variety of mammalian wildlife, seen more easily in captivity, but also observed in nature under difficult circumstances. Most American observations and reflections about wildlife have been made on North America's major ungulates, the indigenous deer. In normally enzootic areas, the whitetail deer (Odocoileus virginianus) population increased rapidly after the eradication of the pest. Hitherto there had been many observed cases of infestation in deer, particularly death by infestation of the umbilicus of newborn fawns.
One type of ranching, that of game animals, where routine preventive treatment is difficult for the owner and traumatic for the animals, is said to have been made possible by the eradication of screwworm. Game ranching is a growing activity, particularly in areas of the United States previously enzootic for NWS.
Latin America has few of the large herds of ungulates with seasonal breeding similar to those found in parts of sub-Saharan Africa. Where such herds are found in Africa, there is concern that the spread of infestation to these areas could cause explosive outbreaks with significant loss to fauna due, among other things, to the simultaneous availability of umbilical wounds of newborn animals.
To the general public the image of the sterile insect technique (SIT), which interrupts the fly's life cycle by mass rearing, sterilization and aerial dispersion of NWS, is appealing. Livestock owners in Mexico and the United States, however, are aware of the equally massive ground efforts that were required by them and their governments to control, contain and eventually eradicate this pest. Such elements required for prevention and control of NWS are indeed also essential for eradication. Those described here, it is believed, have particular relevance to the present situation in North Africa.
Although the insect is a strong flier, the transport of infested animals is the most important means of long-distance spread of this parasite. The larval stage of the parasite within the host animal is approximately one week. In this time, wherever animals are transported or walk, mature larvae drop to the ground to pupate and cause new outbreaks.
Most of the far-flung Caribbean Islands were presumably infested as a result of infested animal shipment. A NWS-infested dog originating from Latin America was found in France; and since eradication in the United States and neighbouring Mexico, two similar incidents have also occurred in the United States. It is thought that the most likely means of introduction of NWS into North Africa was by importation of an infested animal, or animals, from Latin America.
During the first eradication programme, in the southeastern United States, a quarantine line was established all along the Mississippi river to ensure that infested animals transported from the southwestern United States would not cause new outbreaks.
When self-sustaining NWS populations were eradicated from the southwestern United States, livestock imported from Mexico were dipped not only for NWS but for other parasites. As the campaign progressed southward in Mexico, it became evident that freed areas were being constantly reinfested by the shipment of livestock from still enzootic areas. Inspection points on roads, in cooperation with other government agencies, were originally inadequate to inspect all animals, but enough infested animals were intercepted to confirm that animal movement was indeed reinfesting areas. Epidemiological investigation of outbreaks confirmed the same.
Public information campaigns on the dangers of moving uninspected and untreated animals were intensified. Permanent quarantine stations at the Isthmus of Tehuantepec were established where all animals were individually inspected, and quarantined if required. Since small wounds are not readily visible, all animals on vehicles were dipped before passing through the Isthmus, even when no wounded animals were observed in the shipment. Establishment of the stations helped accelerate eradication and ensure that, once free, areas remained free of screwworms.
Long experience has demonstrated that, particularly for areas and countries far from those infested, the most effective way of preventing NWS introduction is by controlling animal importation. This has led to FAO recommendations that for importation of animals from infested countries and territory, there should be official certification that:
- animals did not originate from infested herds;
- before being transported, animals were individually inspected and those with visible wounds excluded from exportation;
- unwounded animals to be transported were dipped or sprayed with an officially approved organophosphate insecticide, and floors of transport units were also sprayed.
At the point of importation and during quarantine, animals should be examined and wounds treated with an organophosphate insecticide.
It is evident that for areas and countries closer to those infested, difficulties in carrying out these measures will arise, but every possible effort should be made to contain this serious pest. Public information campaigns aimed particularly at the farmer and transporter should promote voluntary cooperation.
Although a certain amount of restriction of animal movement is necessary for international and national prevention and control, animal product restrictions have not been employed nor are they recommended because of the living flesh requirements of the parasite.
Small wounds become enlarged causing sickness or death of the animal - Les petites plates s'agrandissent, provoquant la maladie, voire la mort de l'animal - Las pequeñas heridas aumentan de tamaño, ocasionando al animal la enfermedad o la muerte
Wound treatment is important to prevent losses in both control and eradication programmes - Le traitement des plates dans le cadre des programmes de lutte et d'éradication est important pour éviter les pertes d'animaux - El tratamiento de las heridas es importante pare prevenir las perdidas de animales en los programas de lucha y erradicación
Larval sampling is essential for surveillance for prevention, control and eradication programmes - Le prélèvement des larves dans le cadre des programmes de lutte et d'éradication est essentiel pour la surveillance et la prévention - El muestreo de larvae es esencial pare la vigilancia y la prevención en los programas de lucha y erradicación
The programme in the United States and Mexico evolved with strong support and promotion by livestock owners and succeeded because of their active participation. Programme personnel were continuously publicizing the fact that if all animal wounds were treated, populations of this parasite which are dependent on wounds for the completion of their life cycle would be eliminated. Traditional wound smears had been widely used by most livestock producers to reduce the damaging worm population and promote healing. These, however, seldom killed all the larvae in a wound but the advent of modem insecticides with residual effect increased the effectiveness of treatment. Cooperating livestock owners carrying out this treatment not only protected their own animals but helped advance the programme.
Veterinary services cannot be staffed for preventive treatment of all wounds, nor of surveillance of all wounds for parasites. To overcome this, in both the United States and Mexico, millions of combined treatment/sampling kits were continuously distributed free to livestock owners, together with inspection and public information campaigns. The objective was to have as near as possible to 100 percent of wounds prophylactically treated so as to deny the NWS opportunities for its propagation. As the results of this campaign were obvious to the livestock owner, a high degree of participation was achieved. The benefit of dipping or spraying for NWS, similar to that for other ectoparasites, was also promoted.
With each presentation of wound-treatment packets, a sampling tube containing larval preservative and a questionnaire were supplied. The role of the screwworm inspector was accurately viewed as an information: representative, with his periodic visits to farms, interviews of cooperating officials, and attendance at all gatherings of livestock owners.
The inspector promoted wound treatment and the collection of larvae for immediate identification of NWS. These activities preceded, and were carried out both during, and subsequent to, control and eradication campaigns. Owners were asked to sample larvae from the deepest part of the wound so as not to send as samples the: frequently seen, non-malignant secondary blowflies which may accompany NWS infestation. Similarly, sampling of maggots found on long-dead animals was not solicited as NWS, unlike other maggots, would be found only or. animals where infestation originated prior to death. Data were recorded and analysed. Programme personnel continuously studied the ratio of NWS to other blowfly samples as a measure of cooperation and of programme progress. Both the limits and the intensity of infestation were measurable. A continuous submission of negative samples gave officials assurance that areas thought to be free were indeed free.
Positive NWS samples submitted by stock owners led to action by the inspectors in spraying infested and adjacent herds and flocks, in addition to sterile fly dispersion. This immediate response was fully appreciated by the livestock owners. The use of these treatment/sampling kits was an invaluable tool for both control and continuous epizootological surveillance of the parasite.
Efforts are being made by FAO to assist the North African countries to establish these necessarily livestock-owner oriented programmes for prevention, surveillance and control of NWS. Substantial public information programmes at the grassroots level are essential to convince the livestock owner to avoid wounds where possible, and prophylactically treat all wounds, with special attention during the lambing and shearing seasons. The livestock owner should be convinced not to move untreated wounded animals, and to collect worm samples for immediate identification when they are seen. By August 1989, 1.75 million wound treatment and sampling kits were en route to the countries at most immediate risk, accompanied by an additional half million extra individual wound treatment - packets.
Programme elements familiar to veterinary services worldwide - surveillance, epizootiology, preventive and curative measures, animal movement control - referred to above, are required to control and eradicate NWS as for other animal diseases.
Control and eradication of the NWS also employed, for the first time, the sterile insect technique (SIT). In 1950, Muller had demonstrated induction of sterility in the fruitfly, Drosophila, by exposure to x-rays. In the light of the severe economic effects of the NWS parasite, entomologists Knipling and Bushland (Knipling, 1985) chose NWS to field test the former's earlier theory of autocidal control, suppression of pest populations by genetic altering of a stage of the life cycle.
A trial on a small island off the coast of Florida showed promising results, and in 1954 eradication was achieved on the Caribbean Island of Curaçao. An article (Williams, Gartman and Hourrigan, 1977) in World Animal Review described the successful application-of the SIT as well as the status of NWS in the Americas at that time. The parasite had been eradicated in the southeastern United States and Puerto Rico and overwintering populations were eradicated in the southwestern United States. An attempt was made to maintain the United States and northern Mexico screwworm-free by employing a massive sterile-fly barrier on both sides of the 3 000 km Mexico-United States border.
However, in years with conditions favouring the fly, infestation continued to penetrate this barrier from enzootic areas further south in Mexico. Foreseeing this, in 1972 livestock owners of both Mexico and the United States joined forces to convince their governments to eradicate screwworms up to the Isthmus of Tehuantepec in southern Mexico, by creation of the Mexico-USA Screwworm Eradication Commission. This was patterned after a similar commission that had eradicated foot-and-mouth disease (FMD) from Mexico and, as a result, the North American continent by the early 1950s.
A large sterile fly production plant in the State of Chiapas in southern Mexico began production in 1976. As a result of programme progress, in 1981 the southern Texas plant which had provided sterile-flies for the southwestern United States and for northern Mexico was closed, leaving the Chiapas plant the only one functioning in the world.
Production in the Mexican plant increased to 500 million per week in 1982. Sixty aircraft were required to fly daily to disperse these numbers of flies. The map on p. 43 shows progress of the eradication campaign up to 1984 when the screwworm was eradicated as far as the programmed area at the relatively narrow Isthmus of Tehuantepec. As many as 2 800 full-time employees had worked in the campaign. Programme costs exceeded US$50 million per year. At the peak of its activities, the Mexico-USA screwworm eradication programme was the largest international animal health campaign and the most ambitious user of SIT employed against any kind of pest then in operation in the world.
The NWS eradication programme continues to progress southward in the western hemisphere with the objective of eradicating NWS from Central America to the even narrower Darien Isthmus in southern Panama, the present foot-and-mouth disease barrier adjacent to the FMD-free area in Colombia between the two American continents. Another NWS sterile fly production plant will be built near the future barrier zone.
Since 1984, permanent populations of NWS in the remaining areas of Mexico have been eradicated, and there exists animal movement control, treatment of animals and sterile fly dispersion in neighbouring Guatemala and Belize.
After confirmation of the presence of NWS, the Government of the Libyan Arab Jamahiriya began a large-scale programme for its control, based on surveillance, animal treatment and livestock movement control. Consultants from Mexico with programme experience in screwworm eradication advised the National Screwworm Committee. Up to September 1989, reported cases were confined to coastal areas on both sides of the national capital, Tripoli. FAO and UNDP have complemented Government resources for the programme.
After being alerted, those countries at immediate risk reacted quickly. FAO initiated a variety of measures with those most directly threatened. Experts were sent to suggest programmes for prevention and surveillance. A series of emergency projects were begun using Technical Cooperation Programme (TCP) funds.
In addition to TCP projects in the Libyan Arab Jamahiriya, Tunisia, Algeria, Egypt, the Niger and Chad, a regional project sought to coordinate international strategy. Objectives were to determine the extent of screwworm infestation, prevent spread to unaffected areas and bordering countries, and to control NWS in infested areas.
Training of national staff was one of the first steps. The Government of the Libyan Arab Jamahiriya hosted an FAO-sponsored training course in July. In addition to several participants from Libya, neighbouring countries were invited to send two specialists, one whose responsibilities include NWS identification and another who would be-responsible for surveillance, prevention and control. A draft of an FAO manual on these subjects was distributed. Consultants were sent to participating countries and resources were made available for beginning national surveillance and prevention programmes.
In cooperation with the Mexican Government a study tour was organized in Mexico for North African specialists to acquaint them with screwworm eradication activities there.
A proposal for including screwworm myiasis caused by Cochliomyia hominivorax on the list of internationally notifiable diseases was approved by the General Session of the International Office of Epizootics in Paris in May 1989. Recommendations for export and import of animals in respect of this disease will be included in the OIE International Zoo-sanitary Code.
Following recommendations of an FAO preparatory meeting to formulate a Regional Strategy for the Control and Eradication of Screwworm in North Africa, Rome, 5-6 June 1989, FAO together with IAEA, in coordination with governments and donors, began preparation for the application of SIT, which with surveillance, treatment and animal movement control proved to be effective in eradicating NWS from the United States and Mexico.
Gabaj, M.M., Wyatt, N.P., Pont, A.C., Beesley, W.N., Awan, M.A.Z., Gusby A.M. & Benhat, K.M. 1989. The SW fly in Libya: a threat to the livestock industry of the Old World. Veterinary Record, 125: 347-349.
Graham O.M. 1979. The chemical control of screwworm: a review. The Southwestern Entomologist, 4(4).
Graham, O.M., ed. 1985. Symposium on Eradication of the Screwworm from: the United States and Mexico. Miscellaneous Publication, No. 62. Hyattsville, Entomological Society of America.
Knipling, E.F. 1985. Symposium on Eradication of the Screwworm from the United States and Mexico. Miscellaneous Publication, No. 62. Hyattsville,- Entomological Society of America.
Texas Agriculture Extension Service. 1985. Evaluation of the Mexican / American Screwworm Eradication Programme in Mexico. Vol. 1. Economic Impact from SW Eradication in Mexico
USDA. 1981. Annotated Bibliography of the Screwworm, C. hominivorax. Science and Education Administration Agricultural Reviews and Manuals ARM-S-14.
Williams, D.L., Gartman, S.C. & Hourrigan, J.L. 1977. Screwworm eradication in Puerto Rico and the Virgin Islands. Wld Anim. Rev., 21: 31.