Bovine hypodermosis—a global aspect

Cattle hypodermosis (warble fly infestation) is a notorious veterinary problem throughout the world. Larvae of Hypoderma species cause a subcutaneous myiasis of domesticated and wild ruminants. This disease is caused by, Hypoderma bovis, Hypoderma lineatum in cattle whereas, Hypoderma diana, Hypoderma actaeon, and Hypoderma tarandi, affect roe deer, red deer, and reindeer, respectively. Adults of the cattle grub are commonly known as heel flies, warble flies, bomb flies or gad flies. The biology of hypodermosis is complex because it passes through ecto- as well as endoparasitic stages in the life cycle. The parasitic stage of hypodermosis lasts about 1 year in domesticated as well as in the wild animals, while in the adult stage, a free-living fly lasts only for few days. The diagnosis of hypodermosis is of prime importance for planning treatment and the eradication program. Generally, there are two methods that are routinely used for diagnosis of hypodermosis, i.e., the direct clinical examination and immuno diagnosis by the use of pooled serum and/or milk sample. For the control of hypodermosis, different preparations are available and their use in most of the countries is limited to an individual level but never cover the whole cattle population of a country. Re-infestation in the herd occurs due to the untreated animals that remain the reservoir of the disease. The disease causes huge economic losses in animal production due to the effect of this disease on meat, milk, and the leather industry. It can also affect the general health status as well as the immune system of the body of the diseased animals. As regards the control measures of the disease, different methods have been efficiently practiced and consequently this disease is controlled at national level in many European countries.     

Bovine hypodermosis in north-eastern Algeria: prevalence and intensity of infestation]

Between 1989 and 1997 different factors related to warble fly infestation (prevalence, intensity, climate, breed) were studied in north-eastern Algeria. Mean prevalence during the period was 76%. This figure was obtained from a cattle market survey of four different regions (Jijel, Constantine, Guelma, and El Tarf). One-hundred percent of the herds were found to be infested in El Tarf and 61% of animals were infested. Within a herd, the intensity of infestation decreased with the age of the cattle. The mean number of warbles per animal decreased as reinfestations occurred. The peak of the emergence of warbles observed between January and March was progressively delayed in the older animals. Two species of Hypoderma were present in cattle in Algeria (H. bovis and H. lineatum) with a predominance of H. lineatum (63%) in the semi-arid area (Batna) and a majority of H. bovis (75%) in humid area (Jijel). Warbles appeared earlier in Batna (October) than in Jijel (November). The Prim'Holstein breed was more susceptible to the warble fly infestation than Montbeliard or local breeds. The implementation of a control programme for hypodermosis in Algeria is urgent. Control can be achieved through a mass treatment of cattle. This approach must take into account the factors described in this study which influence the epidemiology of the disease.     

Efficacy of moxidectin injectable and pour-on formulations in a pilot control program against bovine hypodermosis in Southern Italy

Bovine hypodermosis is a myiasis caused by Hypoderma bovis and Hypoderma lineatum (Diptera, Oestridae) larvae, which has a severe economic impact on the livestock industry. Though myiasis is widespread throughout Italy, no nationwide eradication program has ever been planned, unlike in other European Countries. With a view to setting up a national control program, a pilot study was carried out in Southern Italy on 9939 cattle bred in an area with a high prevalence of cattle hypodermosis, using moxidectin 0.5% pour-on (Cydectin, Fort Dodge) and 1% injectable (Cydectin, Fort Dodge) formulations. At the recommended dosage, moxidectin displayed efficacy levels of 99.9% in the pour-on and 100% in the injectable formulation, whereas the microdose (1 mg per head regardless of body weight) was less effective (65.7%). This trial contributed to a significant reduction in infestation rates in the study area and represented the first step through which a national program for eradicating warble fly infestation in Italy.     

Efficacy of injectable and pour-on microdose ivermectin in the treatment of goat warble fly infestation by Przhevalskiana silenus (Diptera, Oestridae)

The prophylactic efficacy of microdoses of injectable and pour-on ivermectin formulations against larval stages of Przhevalskiana silenus was assessed in naturally infected goats in the region of Calabria (southern Italy).Sixty-eight goats from two goat farms were divided into five groups: one group remained untreated, while the other four groups were treated with microdoses of ivermectin (5 and 10 microg/kg injectable formulation and 10 and 20 microg/kg pour-on formulation).The microdoses of ivermectin were fully effective in the treatment of goat warble fly infestation (GWFI) as no larvae emerged from the warbles in the treated groups, while all the larvae emerged in the control groups. Irrespective of the type of formulation used, the difference between the treated groups and the control group was statistically significant (P< 0.001). By contrast, no statistical differences were found between the goats treated with the injectable formulation and those receiving the pour-on applications, and between the two doses of the injectable and pour-on formulations used. Given the plasma concentrations it attains at its lowest dose (0.052 - 0.042 ng/ml for the injectable formulation and 0.030 ng/ml for the pour-on) the injectable formulation seems to offer the most reliable route for the administration of ivermectin microdoses and it is acceptable for milk consumption. The introduction of ivermectin in the early eighties and the use of microdoses in some cases have made it possible to control cattle hypodermosis in large areas of Europe. As with cattle hypodermosis, the administration of ivermectin microdoses in goats is particularly interesting because of the low costs involved and the low levels of residues found in goat milk; it may thus constitute the basis for GWFI control campaigns in areas where the disease is prevalent.     

Introduction of bovine hypodermiasis (Hypoderma bovis) with the importation of Hereford cattle from Canada

The infestation by warble-fly (Hypoderma bovis /De Geer/) larvae was observed in Hereford cattle imported from Canada to Czechoslovakia in the autumn 1974. A risk of introducing hypodermosis in the areas where it had been eradicated occurred after a several-year persistence of such foci of the disease. The original infestation of the imported cows corresponded to the invasion extensity of 22 to 45% and invasion intensity of 1.9 and 3.7 larvae. There were observed no differences in the degree of infestation in cattle from different regions of Canada. In the subsequent years the invasion extensity in heifers was 52% the invasion intensity was four larvae. To control hypodermosis, Czechoslovak chemicals Arpalit-Spray and Hypocide were applied to Hereford cattle. In the West Bohemian Region cattle was treated with the chemical Arpalit-Spray in spring for three years to eradicate hypodermosis in the Tachov and Susice districts. A good result was obtained after the treatment in May during the maximum occurrence of larvae in bulges under the skin, the treatment in June was late and inefficient. In the Central Slovakian Region, Dolny Kubín district, hypodermosis was eradicated in Hereford cattle by a repeated treatment with Hypocide in autumn. The control of hypodermosis in Hereford cattle in the Prievidza district failed. In 1979 the invasion extensity in heifers was 25-100%, the invasion intensity was 2 to 25 larvae. Cattle transferred from this herd to the Lucenec, Presov and Gottwaldov districts were also infested. In the Gottwaldov district in the South Moravian Region all infested cows were treated with Arpalit-Spray in the summer 1979.     

Migration of warble fly larvae in the yak and optimum timing of ivermectin treatment

Sixty yaks were autopsied to determine the migration pattern of warble fly larvae. In August, first instars were observed in the body of yak for the first time. These larvae peaked in number in October. From November to February, second instars were detected and their number peaked in January. Third instars appeared in January and peaked in March. Forty-five yaks were administered with ivermectin: 15 animals in September, 15 in October and 15 in November. Between December and June, the number of warbles was checked by palpation. Although some warbles were observed in the September- and November-treated groups, no warbles were detected in the October-treated group. Treatment of yaks with ivermectin was most effective for warble fly in October.     

Sero-epidemiological surveillance of hypodermosis in yaks and cattle in north China by ELISA

A large-scale serological surveillance was conducted for hypodermosis in the north of China. A total of 4175 sera samples of yaks and cattle were collected from five provinces in north China that included Xinjiang, Inner Mongolia, Heilongjiang, Jiling and Gansu provinces, between 2001 and 2002, and were examined for anti-hypoderma antibody by ELISA. The results indicate that the naturally infested positive rates of Hypoderma spp. in the above provinces were 51.77%, 27.02%, 13.00%, 6.03% and 44.41%, respectively. These results suggest a significant warble fly population in the north of China. Positive sera were collected from infested cattle in Pingliang county of the Gansu province monthly between August 2001 and July 2002. These sera were used to evaluate the seasonal kinetics of anti-hypoderma antibody. The kinetics demonstrated that anti-hypoderma antibody was elevated from October to December. Thus, serological surveillances associated with low infestation rates and chemical therapy would best be performed from October to December in the region.     

Emergence season of Hypoderma lineatum warbles in southern Punjab, Pakistan

The objective of the present study was to observe the seasonal pattern of the life cycle and the warble stage in bovines of Dera Ghazi Khan and Rajan Pur Districts of Southern‐Punjab, Pakistan. The study was conducted from July 2004 to June 2005. The association was studied between various climatic changes and the fly life cycle. The larvae of warble flies were extracted from the backs of naturally infested animals and identified. The adult fly laid eggs in June, and hatched larvae penetrated the skin and followed intensive internal migration to diaphragm, esophageal wall and subcutaneous connective tissue in the month of July. At the start of August they reached the subcutaneous tissue and emergence began. In both species, the maximum warble emergence was found in mid‐December and the lowest in mid‐March and mid‐August. It was concluded that preventive treatment should be adopted before the month of July to avoid carcass depreciation and decreased leather quality.     

Eradication of Hypoderma species in Northern Ireland

The field measures for the control and eradication of the warble fly in Northern Ireland are described. The level of infestation and the main economic losses before the introduction of these measures are indicated. The limitations of the control measures used before the introduction of systematic insecticides are discussed.A limited field trial with a systematic insecticide was conducted in 1964, but the main national programme for warble control was implemented in 1966 and 1967. Under the programme, the treatment of all cattle was compulsory.The nature and organization of the programme and its staffing and cost are described. The field monitoring, the extent and nature of adverse reactions in some of the treated animals, the effects on the rate of warble infestation, and the current status of “warbles” as a Notifiable Disease are discussed. Also described is the practicality of the eradication of cattle grubs from the Island of Ireland as a whole through synchronization of the warble control programmes in Northern Irelabnd and Eire.     

Effect of bovine hypodermosis on various health indicators of milk in first-calvers]

The effect of the last developmental phase of the warble fly (Hypoderma bovis de Greer) larvas was studied as exerted on some health indices of milk in 20 experimental (treated) and 18 control (untreated) first-calvers of the Pinzgau breed at two localities of an area affected by bovine hypodermosis in the period from May to June, 1975. The preparation Hypocid, at a dose of 15 ml per 100 kg of body weight, was applied externally in the lumbosacral region to the experimental animals in November, 1974. Throughout the experimental period (61 days) the milk was repeatedly examined bacteriologically and cytologically, the content of chlorides and the milk electric conductivity were determined. In none of the followed health indices of milk were significant differences in the values obtained from experimental and control first-calvers proved statistically.     

Durably controlling bovine hypodermosis

Cattle hypodermosis, due to insect larvae, is widely spread over the northern hemisphere. Very efficient insecticides are available and their use in most countries are done on an individual level but never cover the whole cattle population of a country. Untreated animals remain the reservoir of the disease and annually re-infest the cattle population. The economic effects of this disease on animal production (meat, milk and the leather industry) but also on the general cattle health status, have led many European countries to launch organised control programs. The first example of definitive hypodermosis control goes back one hundred years ago when Danish farmers eradicated hypodermosis from the Danish islands by manual elimination of the warbles. Since then, more and more European countries have considered the feasibility and economic returns of such programs. The various factors which foster these programs are related to (i) biological factors, (parasite cattle specificity, synchronous biological cycles of both species of insects involved), (ii) the development of more and more efficient insecticides used only once a year by systemic application, with high efficiency at very low dosages against the first larval stage of Hypoderma spp., (iii) the development of acute techniques of detection of the disease for the monitoring of hypodermosis free countries and (iv) the durable successful results obtained in more and more European countries. Although the programs were imposed by different partners of the livestock channel production (farmers, dairy industry, leather industry) and have been engaged within the last 50 years in many European countries (Denmark, The Netherlands, Ireland, the United Kingdom, the Czech Republic, Germany, France and Switzerland) common features have emerged among these different eradication programs. They all need a preliminary statement of the economic impact of this pest and the farmers' awareness of the economic returns of such programs. The programs' efficacy depends: (i) on a good knowledge ofthe epidemiology of the parasites, (ii) on the simultaneous implementation of the control program on the whole national cattle population whatever the structure monitoring the treatments (veterinary services, farmers association), (iii) on a national Warble fly legislation making the treatments compulsory and (iv) on an acute epidemiological survey as soon as the status of a hypodermosis free country is reached and the treatments are suspended. The sanitary and financial returns of such programs are a benefit to all the partners of livestock production, to the quality of the environment and to the consumers.     

Further evidence on the internal life cycle of Przhevalskiana silenus (Diptera, Oestridae)

Knowledge of the internal life cycle of goat warble fly infestation is scarce despite ample data available on the aetiology, epidemiology, immunodiagnosis and treatment of such infestations. This study was carried out at the slaughterhouse of Rossano Calabro (Cosenza, southern Italy) on 154 animals from 10 months to 6 years of age from May 1997 to June 1998. 1206 Przhevalskiana silenus larvae were collected during the trial period from the subcutaneous tissue of the slaughtered animals. The larval stage average size ranged from 4.7 mm, for first instar larvae (May), to 16.6 mm, for third instar larvae (February), in the first cycle of infestation. No larvae were found in March-April, coinciding with the pupation period. Small first instar larvae were found at the beginning of the second cycle of infestation (May-June). Necroscopic examinations were also carried out on internal organs and no larvae were found. The results pointed out that the internal life cycle of P. silenus is exclusively subcutaneous and there is no internal migration of the larvae.     

Assessment of cattle grub (Hypoderma spp.) prevalence in northeastern Italy: an immunoepidemiological survey on bulk milk samples using ELISA

Hypodermosis is a myiasis of cattle mainly found in the Northern Hemisphere. In Italy it has been reported primarily in southern regions with a farm prevalence reaching a peak of 85%, while few data are available in the north of the country.This paper reports the results of a serological survey carried out on hypodermosis in Vicenza province (northeastern Italy). During January and February 1999, bulk milk samples were collected from 224 dairy farms and tested, using an hypodermosis ELISA kit. Epidemiological data, such as farm location, herd size, number of cows, grazing management, treatments against Hypoderma larvae, presence of imported animals, were gathered and statistically analysed in relation to the serological results. In 15 farms the presence of warbles was monitored by manual palpation and larvae collected for identification.Ninety-seven (43.3%) samples were detected as positive, whereas 12 (5.4%) and 115 (51.3%) were inconclusive and negative, respectively.Thirteen farms were positive upon parasitological examination and the larvae collected were identified as Hypoderma bovis.Seroprevalence was highly correlated with the practice of free grazing and slightly, but significantly, correlated with the number of cows on the farm. The mean antibody level of positive herds was significantly higher on farms without imported animals. On farms with warbled animals there was a high inverse correlation between antibody level and quantity of milk in the tanks and the number of lactating cows.The ELISA test on bulk milk samples has been shown, under field conditions, to be a useful, cost-effective and easy test for the diagnosis of bovine hypodermosis.     

Serological survey of the incidence of Hypoderma bovis in cattle in 1988

Sera from 74,502 cattle from 3087 farms in England and Wales were tested for the presence of antibodies against Hypoderma bovis in the spring of 1988. Twenty-nine positive sera were identified on 18 premises and these animals were treated; an examination of 6030 sera taken from 108 neighbouring herds identified another 17 seropositive animals on 10 farms in Devon, Cornwall, Lancashire, Shropshire and Powys, indicating that these counties still harbour populations of warble fly.     

Towards a lower prevalence of Oestrus ovis infections in sheep in a temperate climate (south west France)

Oestrus ovis larvae are obligatory parasites of the nasal and sinus cavities of sheep and goats. In the temperate climate of western Europe, fly attacks occur between May and October and the first stage larvae arrest their development within the host between October and February. Oestrosis clinical signs such as nasal discharge and sneezing are well known by sheep breeders in southwest France. According to veterinarian recommendations, most of them treat their animals with long lasting fasciolicides once a year at least, mainly during the fly activity period and at the beginning of the hypobiotic period (when the parasitic population is only constituted of larvae). The consequences of these therapeutic programs were analysed in a local slaughterhouse by larval counts. Both prevalence and intensities of O. ovis infections decreased between 1989-1991 (before the use of systematic treatments) and 1996-1998 (after the spread of these treatments). The use of systematic treatments during the fly activity period and the beginning of the hypobiotic period seems to be very efficient in O. ovis control and could theoretically lead to a possible 'eradication' program as with cattle hypodermosis. Nevertheless the presence of parasites in apparently healthy goats, the possibility for a fly generation to develop before the first treatment in July-August and the succession of several fly generations all around the year in southern Mediterranean and tropical countries will maintain O. ovis infections. Furthermore, there are increased concerns about drug residues on consumer health and environment and this is the basis for the prospect of alternative strategies in O. ovis control.     

Progress in the British hypodermosis eradication programme: the role of serological surveillance.

The British warble fly eradication programme has resulted in the numbers of infested cattle falling from an estimated four million in 1978 to zero in 1991. In 1982, when about 705 herds were infested the disease was made notifiable, and serological surveillance was begun in 1988. In spring 1991, 227,000 blood samples were tested by using the ELISA technique and no warbled animals were found. In addition no clinical cases were reported during 1991.     

Prevalence and economic significance of bovine hypodermosis in Afyonkarahisar province of Turkey

This study was carried out to investigate the prevalence and economic losses due to in cattle of hypodermosis between May 2008 and April 2009 in Afyonkarahisar province of Turkey. A total of 6,598 cattle—3,498 in pasture and 3,100 in slaughterhouse—were examined for hypodermosis. One hundred ninety-five out of 6,598 cattle (2.96%) were found positive. Concerning this infestation rate, the prevalence of hypodermosis in field was 5.3%, whereas the prevalence was 0.3% in slaughter house. Hypoderma bovis and Hypoderma lineatum were recorded in slaughter house. First-stage Hypoderma spp. larvae weren’t found in cattle organs in slaughterhouse. The annual economic loss on skins is estimated to be about 18,288 TL (currency exchange rate is 1 USD:1.499 TL).     

Comparative study of strongyle infections of cattle and buffaloes in Mindanao, the Philippines

Faecal samples were collected from 500 cattle and 385 buffaloes belonging to backyard farmers from 24 villages in the province of Bukidnon, Mindanao, the Philippines. Strongyle nematode infections were studied on these samples by faecal egg counts and infective larvae differentiation. The effects of animal species and age on the prevalence and intensity of infections were studied. The overall prevalence of strongyle infection was 53% for cattle and 28% for buffaloes. The prevalence decreased with increasing age in both animal species. Faecal egg counts were significantly lower in buffaloes than in cattle. Adult animals had lower egg counts than calves. This age effect was most pronounced in buffaloes. Six genera of strongyle nematodes were identified from the faecal cultures in both animal species, Mecistocirrus, Haemonchus, Trichostrongylus, Cooperia, Bunostomum and Oesophagostomum. The distribution of larvae did not vary much with age.     

Horse infestation with the larva of the deer warble fly, Hypoderma diana Brauer, 1985 (Diptera, Hypodermatidae)

In South Bohemia a case was discovered of a yearling colt attacked by the larva of the IIIrd instar of the deer warble fly Hypoderma diana Brauer. The dead, almost mature larva of the fly was squeezed out of a subcutaneous lump above the shoulder in the first decade of April, 1985. The case is evaluated from the point of view of the possibility of the transition of specific parasites--warble flies--to another host. The attacking of a non-specific kind can occasionally occur only when there is a large number of the parasites and both kinds of host. At present the degree of attacking of deer by subcutaneous warble flies is high and therefore under favourable circumstances even domestic animals can be attacked by this type of warble fly. The above case is the first to be ascertained of a horse being attacked by a deer warble fly.     

Hypodermosis in cattle slaughtered in Nigde province,Turkey<Superscript>*</Superscript>

This study was carried out to investigate the prevalence of hypodermosis in cattle between January and June 2005 in Nigde province, which is located in the middle of Turkey. A total of 1336 cattle, which were slaughtered in Nigde, were investigated for Hypoderma larvae. The 68 out of 1336 cattle (%5.08) were found positive for Hypoderma larvae. A total of 536 Hypoderma larvae were found in the skin and subcutaneous tissue of the back of infested cattle. The 489 out of 536 larvae (%91.23) were identified as Hypoderma bovis and 47 out of 536 (%8.77) as H. lineatum. Number of Hypoderma larvae counted on single infested cattle varied between 1–45 and the mean number of Hypoderma larvae per cattle was 7.88 (536/68). Hypodermosis was recorded for the first time in cattle from Nigde. ^*This study was supported by the Scientific Research Projects Unit of Nigde University (FEB 2004/07).