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Treatment and control of bovine hypodermosis with ivermectin long-acting injection (IVOMEC® GOLD)

Abstract

Background

The studies reported here were conducted to assess the efficacy of ivermectin long-acting injection (IVM LAI; IVOMEC® GOLD, Merial; 3.15 % w/v ivermectin) for the treatment and control of natural infestations of cattle by Hypoderma bovis and Hypoderma lineatum, which are the most economically important oestrid flies of cattle in the northern hemisphere.

Methods

Cattle selected from herds with a history of Hypoderma infestation were grouped into blocks of three (Italy, 33 cattle; Germany, 30 cattle) or two (USA, 16 cattle) animals each, on the basis of positivity at the pre-treatment anti-Hypoderma antibody titres. Within each block, animals were randomly allocated to one of the following treatment regimens: saline (control); IVM LAI, administered at the predicted time of occurrence of first-instar larvae (Italy, Germany, USA); IVM LAI, administered at the predicted time of occurrence of second- and/or third-instar larvae (Italy, Germany). All treatments were administered by subcutaneous injection in correspondence of the area anterior to the shoulder at 1 ml/50 kg body weight, which corresponds to 630 mcg IVM/kg for IVM LAI.

Results

No Hypoderma larvae emerged from animals treated with IVM LAI, whereas live H. lineatum (Italy) or H. bovis (Germany, USA) larvae were collected from saline-treated animals (P < 0.01). No adverse reactions to treatments were in any of the animals enrolled in the study.

Conclusions

The results from this study demonstrate that ivermectin in a long-acting formulation is 100 % efficacious in the treatment of cattle naturally infested by H. bovis and H. lineatum larvae at all stages of development. IVM LAI can, therefore, be used as ‘prophylactic’ treatment for Hypoderma spp. infestations in absence of external evidence of their presence and thus prior to skin and carcass damage, and as ‘therapeutic’ treatment, when warbles are already present.

Background

The family Oestridae includes some 150 species of dipteran flies whose larvae are obligate parasites living, over weeks to months, in the tissues or organs of domestic and wild animals and causing obligate myiases [1, 2]. The oestrid genus Hypoderma includes seven species of flies, of which three are known to cause bovine hypodermosis (also known as cattle grub or warble fly infestation) in the northern hemisphere, i.e. Hypoderma bovis, H. lineatum and H. sinense. During the summer season, female flies lay eggs; from these, first-instar larvae hatch to then migrate over several months through the somatic tissues of the animals via the oesophagus (H. lineatum, H. sinense) or the perirachidian tissues (H. bovis). Larvae moult into second- and third-instar larvae and form the typical subcutaneous nodules under the skin in the dorsal and lumbar regions of cattle (warbles) in late winter and spring [3, 4].

Though bovine hypodermosis does not induce significant mortality and morbidity, this infestation affects the productivity and welfare of animals, thus resulting in considerable losses to the livestock industry arising from a number of causes [2, 5, 6]. In addition, bovine Hypoderma species may accidentally infest humans and seldom cause severe conditions [79].

Administration of systemically active insecticides, i.e. topical formulations of organophosphates and products with macrocyclic lactone compounds, kill Hypoderma larvae during their migration through the animal’s body. Since the early 1980s, the widespread use of broad-spectrum parasiticides, particularly macrocyclic lactones, led to a marked decrease in the prevalence of bovine hypodermosis in many developed countries of the northern hemisphere [10]. This resulted in successful area-wide or national control programs. However, despite the extensive control measures undertaken, surveillance studies based on serum and milk serology, as well as reports on clinical infestation of cattle and parasiticide efficacy studies and/or description of human cases published over the past 15 years, provide evidence that residual populations of Hypoderma spp. are still present in cattle in North America including Canada and the USA, as well as in Europe, e.g. in Portugal, Spain, France, Italy, Belgium, Switzerland, Germany, Poland, Slovakia and Estonia [1124]. In addition, bovine hypodermosis is prevalent in several countries in eastern and south eastern Europe including Belarus, Russia, Romania, Serbia, Bosnia and Herzegovina, Kosovo, Albania and Greece [2533], and it is still endemic in resource-limited countries in northern Africa and Asia [3441].

Macrocyclic lactones are characterized by excellent efficacy against a broad spectrum of nematode endo- and arthropod ectoparasites, including infestation with myiasis causing larvae of oestrid flies [42]. More recently, injectable long-action macrocyclic lactone formulations were authorized for use in cattle in several countries including ivermectin long-acting injection (IVM LAI; IVOMEC® GOLD, Merial) [43].

Earlier studies that reported IVM LAI is highly efficacious in the control of cattle infestations by larvae of the neotropical oestrid fly, Dermatobia hominis [44, 45]. The studies reported here were conducted to assess the efficacy of IVM LAI for the treatment and control of natural infestations of cattle by H. bovis and H. lineatum, the economically most important oestrid flies of cattle in the northern hemisphere.

Methods

The studies were designed in accordance with and consistent to the World Association for the Advancement of Veterinary Parasitology guidelines for evaluating the efficacy of ectoparasiticides against myiasis causing parasites [46]. The studies were conducted in compliance with VICH GL9, entitled Good Clinical Practice and with the local legislation for animal welfare. The studies were performed as blinded studies, i.e. all personnel involved in collecting efficacy data were masked as to the assignment of each animal to treatment groups.

Experimental animals

A total of 79 healthy beef cattle, weighing 121.5 to 386 kg at the start of the study (day -1 or day 0), and aging approximately 5–21 months, were included in three studies, conducted in Italy (Study 1), Germany (Study 2) and the USA (Study 3). Animal descriptions and details are presented in Table 1. The animals were sourced from herds with a history of Hypoderma spp. in the Basilicata region, Italy, Rhine Palatinate, Germany or Wisconsin, USA. Animals had not been previously treated with a macrocyclic lactone product and they were previously exposed to Hypoderma spp. as confirmed by the presence of anti-Hypoderma antibodies prior to treatment.

Table 1 Animal description and details

All animals were handled with due regard to their welfare and in compliance with Merial Institutional Animal Care and Use Committee (IACUC) approvals, any applicable local regulations, and requirements of any local IACUC.

Experimental design

A randomized block design based on pre-treatment anti-Hypoderma antibody levels was used; each individual animal represented the experimental unit in each study. Eleven or ten blocks of three (Studies 1 and 2) or eight blocks of two (Study 3) cattle each were formed sequentially based on decreasing pre-treatment anti-Hypoderma antibody level results (Studies 1 and 2: Pourquier® ELISA Bovine Hypodermosis/Hypo Serums; Montpellier, France; Study 3: ELISA test as described by Colwell et al. [47]. Within each block, animals were randomly allocated to 1 of the following treatments: saline (control) (Studies 1, 2 and 3); IVM LAI (3.15 % w/v ivermectin in a LAI formulation; IVOMEC® GOLD, Merial), administered in correspondence of the predicted occurrence of first-instar larvae (Studies 1, 2 and 3); IVM LAI, administered in correspondence of the predicted occurrence of second- and/or third-instar larvae (Studies 1 and 2).

Cattle were either kept indoors and housed in loose-pens (Study 1) or individually stanchioned (Study 2) per block, or were kept as one group in a fenced dry lot (Study 3). Animals were fed as per local practice and were water was provided ad libitum.

The studies commenced either in November (Study 1) or in December (Studies 2 and 3). Treatments, saline as well as IVM LAI, were administered at 1 ml/50 kg bodyweight once in correspondence of the predicted occurrence of Hypoderma spp. first-instar larvae (day 0: all studies) or once in correspondence of the predicted occurrence of second- and third-instar larvae (day 84: Study 1; day 125: Study 2) by subcutaneous injection in an area anterior to the shoulder using commercial disposable syringes and needles. All cattle were observed hourly for 4 h post-treatment and thereafter once daily throughout the course of the studies for health problems or adverse drug reactions. Animals were weighed prior to treatments (days -1 and 84: Study 1; days 0 and 125: Study 2; day -1: Study 3) for dose calculation. Cattle were inspected for warbles starting 40 (Studies 1 and 2) or 28 (Study 3) days following day 0 treatment and then at intervals no greater than every 2 weeks until sufficient warbles were detected to warrant a second treatment in correspondence of the predicted occurrence of second- and third-instar larvae. Thereafter, cattle were inspected, and mature Hypoderma spp. larvae were collected, viability was determined and larvae were identified to species according to published keys [48, 49], unless identification was impossible because of decomposition prior to collection. Cattle were examined until the end of the studies, i.e. emergence of larvae could no longer be detected.

Data analysis

Hypoderma live larval counts were transformed to the natural logarithm of (count + 1) for calculation of geometric means. IVM LAI treatment groups were compared (separately) to the saline-treated (control) group using the Wilcoxon rank sum test. A 2-sided test was used at the significance level of 0.05. Analyses were performed using SAS® Version 8.2. Efficacy was calculated as 100[(C-T)/C], where C is the geometric mean for the saline-treated (control) group and T is the geometric mean for the IVM LAI treated group.

Results

All identifiable larvae collected in Study 1 were identified as H. lineatum, whereas all larvae collected in Studies 2 and 3 were identified as H. bovis.

Sufficient warbles to warrant treatment against second- and third-instar Hypoderma larvae were detected on study days 84 (Study 1: 3 to 49 warbles in 10/11 animals) and 125 (Study 2: 1 to 16 warbles in 8/10 animals), respectively. In correspondence of these days, 3 to 41 warbles were counted on 9/11 control animals in Study 1, and 1 to 14 warbles on 7/10 control animals in Study 2.

Following treatments against second- and third-instar larvae appearance, the number of warbles regressed to one warble each within 6 or 10 weeks in Study 2 and Study 1, respectively. At the inspection, the warbles contained a dead third-instar Hypoderma larva (Study 1) or granulomatous tissue (Study 2). No Hypoderma spp. larvae emerged from any of the cattle treated in correspondence to the predicted occurrence of first-instar larvae or when the Hypoderma spp. larvae were in the second and/or third stage.

Forty-nine live H. lineatum larvae and 23 and 66 live H. bovis larvae were collected from the saline-treated (control) animals in Studies 1, 2 and 3, respectively, emergence of larvae could no longer be observed (study days 158, 168, or 183 in Studies 1, 2 and 3, respectively).

Cattle treated with IVM LAI in correspondence to the predicted occurrence of Hypoderma spp. first or second and third-instar larvae had significantly fewer H. lineatum or H. bovis larvae emerging and/or expressed than the saline-treated (control) animals (Table 2). The efficacy of IVM LAI against larval stages of H. lineatum or H. bovis was 100 % (Table 2).

Table 2 Therapeutic efficacy of IVM LAI against natural infestations of first-stage and second- and third-stage larvae of Hypoderma spp

Animals were reported as normal during hourly observations for 4 h post-treatment, indicating that the treatment (either IVM LAI or saline) was well accepted. There were no drug related health problems or adverse drug events observed at any time during the studies.

Discussion

The results presented herein demonstrate that ivermectin in a long-acting formulation is 100 % efficacious in the treatment of cattle naturally infested with H. bovis and H. lineatum larvae. IVM LAI can, therefore, be used as ‘prophylactic’ treatment for Hypoderma spp. infestations, i.e. in absence of external evidence of their presence and prior to carcass and skin damage, and as ‘therapeutic’ treatment, e.g. when warbles are already present. Similar results were reported previously by several authors who tested other commercial formulations containing ivermectin and other compounds of the macrocyclic lactone family (reviewed by [23, 42]).

Serodiagnosis of hypodermosis was used to select the study animals, as this is the only way to detect infested animals well before the appearance of the warbles; however, there is no correlation between titer levels and intensity of infestation [5052]. Although anti-Hypoderma antibody positive animals were enrolled in the studies, warbles were only detected in 80 % of the saline-treated animals (Studies 1, 2 and 3; n = 29), as well as in the animals subjected to treatment in correspondence of the predicted occurrence of second- and/or third-instar larvae (Studies 1 and 2; n = 21), with infestation rates of 86.4, 75 and 75 % in Studies 1, 2 and 3, respectively. The 80 % overall infestation rate is consistent with observations from previous studies where the development of warbles was recorded in 81.4 % of the animals which had tested positive for anti-Hypoderma antibodies [23]. Similarly, numbers of warbles on the animals and numbers of Hypoderma larvae collected from the control animals in this study were similar to those reported in the same studies [23]. As discussed earlier, these findings are in line with the predictive value of the available ELISAs but may also reflect, at least in part, the high mortality of larvae in Hypoderma spp. infestations [23]. Although ELISA serology may over-estimate the percentage of cattle that develop warbles (clinical hypodermosis), it is considered to be a sensitive indication of exposure of cattle to grub infestation and thus a suitable measure for detection of low level, persistent bovine Hypoderma spp. populations [22].

Conclusions

With respect to the efficacy profile of IVM LAI, which provides effective control of nematode infections in cattle for up three months [53, 54] and the high sensitivity of Hypoderma spp. to macrocyclic lactones in general [42] and ivermectin in particular [55, 56], it can be assumed that IVM LAI while the flies are at the adult developmental stage will also provide protection against cattle Hypoderma spp. larval infestation. Hypoderma spp. populations are known to (re)generate promptly if eradication or control measures are incomplete or if re-introduction occurs [5760]. Thus, these parasites should not be ignored and further attention should be paid to cattle parasite management programs not only in regions where bovine hypodermosis is widespread and an important economic burden for the cattle industry, but also in regions where these parasites occur (currently) at very low prevalence with patchy distribution.

Abbreviations

IACUC:

Merial Institutional Animal Care and Use Committee

IVM LAI:

Ivermectin long-acting injection

References

  1. Zumpt F. Myiasis in man and animals in the old world. London: Butterworth’s; 1965.

    Google Scholar 

  2. Hall MJR, Wall R. Myiasis in humans and domestic animals. Adv Parasitol. 1995;35:257–334.

    Article  CAS  PubMed  Google Scholar 

  3. Scholl PJ. Biology and control of cattle grubs. Ann Rev Entomol. 1993;39:53–70.

    Article  Google Scholar 

  4. Otranto D, Paradies P, Testini G, Lia RP, Giangaspero A, Traversa D, et al. First description of the endogenous life cycle of Hypoderma sinense affecting yaks and cattle in China. Med Vet Entomol. 2006;20:325–8.

    Article  CAS  PubMed  Google Scholar 

  5. Reist M, Medjitna TD, Braun U, Pfister K. Effect of a treatment with eprinomectin or trichlorfon on the yield and quality of milk produced by multiparous cows. Vet Rec. 2002;151:377–80.

    Article  CAS  PubMed  Google Scholar 

  6. Hassan M, Khan MN, Abubakar M, Waheed HM, Iqbal Z, Hussain M. Bovine hypodermosis - a global aspect. Trop Anim Health Prod. 2010;42:1615–25.

  7. Anderson JR. Oestrid myiasis of humans. In: Colwell DD, Hall MJR, Scholl PJ, editors. The oestrid flies: biology, host-parasite relationships, impact and management. Wallingford: CABI Publishing; 2006. p. 201–9.

    Chapter  Google Scholar 

  8. Puente S, Otranto D, Panadero R, Herrero MD, Rivas P, Ramírez-Olivencia G, et al. First diagnosis of an imported human myiasis caused by Hypoderma sinense (Diptera: Oestridae), detected in an European traveler returning from India. J Travel Med. 2010;17:419–23.

    Article  PubMed  Google Scholar 

  9. Panadero-Fontán R, Otranto D. Arthropods affecting the human eye. Vet Parasitol. 2015;208:84–93.

    Article  PubMed  Google Scholar 

  10. Boulard C. Durably controlling bovine hypodermosis. Vet Res. 2002;33:455–64.

    Article  PubMed  Google Scholar 

  11. Minář J. Results of the monitoring of cattle hypodermosis in the Czech and Slovak Republics in the period 1998–2002. In: Good M, Hall MJ, Losson B, O’Brien D, Pithan K, Sol J, editors. COST Action 833: Mange and Myiasis of Livestock. Brussels: European Commission; 2003. p. 144–9.

    Google Scholar 

  12. Haine D, Boelaert F, Pfeiffer DU, Saegerman C, Lonneux J-F, Losson B, et al. Herd-level seroprevalence and risk-mapping of bovine hypodermosis in Belgian cattle herds. Prev Vet Med. 2004;65:93–104.

    Article  CAS  PubMed  Google Scholar 

  13. Citterio CV, Marconi P, Timini M. Esperienze di monitoraggio su alcune parassitosi nei bovini della montagna lombarda. Quaderno SOZOOALP. 2005;2:127–9.

    Google Scholar 

  14. Otranto D, Lia RP, Agostini A, Traversa D, Milillo P, Capelli G. Efficacy of moxidectin injectable and pour-on formulations in a pilot control program against bovine hypodermosis in southern Italy. Prev Vet Med. 2005;69:153–9.

    Article  PubMed  Google Scholar 

  15. Panadero R, Sánchez-Andrade R, Morrondo P, López C, Paz A, Suarez JL, et al. Estado actual de las miasis que afectan a los ruminates domesticos en la Península Ibérica. Actas del XIV Congreso Internacional de la Federación Mediterránea de Sanidad y Producción de Rumiantes, 12–15 de Julio 2006, Lugo-Santiago de Compostela, España, p. 461–6. (in Spanish)

  16. Panadero R, Fernandez M, Vazquez L, López C, Dacal V, Cienfuegos S, et al. Occurrence and larval growth of Hypoderma lineatum in the oesophagi of cattle from northwest Spain: influence of geographical and climatic conditions. Med Vet Entomol. 2007;21:225–30.

    Article  CAS  PubMed  Google Scholar 

  17. Panadero R, Vazquez L, Colwell DD, López C, Dacal V, Morrondo P, et al. Evaluation of an antigen capture ELISA for the early diagnosis of Hypoderma lineatum in cattle under field conditions. Vet Parasitol. 2007;147:297–302.

    Article  CAS  PubMed  Google Scholar 

  18. Rambozzi L, Rimella R, Curcio A, Sala L, Rossi L. Field efficacy of minidosed eprinomectin against Hypoderma spp. in dairy cattle. Vet Parasitol. 2006;135:89–91.

    Article  CAS  PubMed  Google Scholar 

  19. Zygutiene M, Narkeviciute I, Mudeniene V, Ziliukiene J. A case of myiasis due to Hypoderma bovis, Lithuania, 2004. Euro Surveill. 2006;11:E1–2.

    CAS  PubMed  Google Scholar 

  20. Mémeteau S, Bronner A, Erimund S. Report on surveillance of bovine hypodermosis in 2010: detection of two outbreaks associated with neighbouring countries. Bulletin Epidémiologique, Santé Animale Alimentation. 2010;46:21–3.

    Google Scholar 

  21. Bednarko-Młynarczyk E, Szetyn J, Białobrzewski I, Wiszniewska-Łaszczych A, Liedtke K. The presence of anti-Hypoderma antibodies in udder milk samples, and correlation with selected parameters of dairy performance. Polish J Vet Sci. 2012;15:487–91.

    Google Scholar 

  22. Colwell DD. Out of sight but not gone: sero-surveillance for cattle grubs, Hypoderma spp., in western Canada between 2008 and 2010. Vet Parasitol. 2013;197:297–303.

    Article  PubMed  Google Scholar 

  23. Rehbein S, Holste JE, Smith LL, Lloyd LJ. The efficacy of eprinomectin extended-release injection against Hypoderma spp. (Diptera: Oestridae) in cattle. Vet Parasitol. 2013;192:353–8.

    Article  CAS  PubMed  Google Scholar 

  24. Pfister K, Charbon J-L. Die erfolgreiche Bekämpfung der Hypodermose in der Schweiz: ein Blick zurück. Schweiz Arch Tierheilk. 2014;156:39–43.

    Article  CAS  Google Scholar 

  25. Papadopoulos E. Hypodermosis in Greece. Chin J Vet Parasitol. 2004;12:20–3.

    Google Scholar 

  26. Otranto D, Zalla P, Testini G, Zanaj S. Cattle grub infestation by Hypoderma sp. in Albania and risk for European countries. Vet Parasitol. 2005;128:157–62.

    Article  PubMed  Google Scholar 

  27. Stepanova EA, Yakubovskij MV. Gipodermatoz krupnogo rogatogo skota. Epizootol Immunobiol Farmakol Sanit. 2009;1:4–9 (in Russian).

    Google Scholar 

  28. Zalla P, Shoshi N, Bizhga B, Postoli R, Rapti D. Impact of the management system on the presence of hypodermosis in cattle. Macedonian J Anim Sci. 2012;2:235–40.

    Google Scholar 

  29. Gorcea FC, Călescu N, Gherman CM, Mihalca AD, Cozma V. Diagnostic values of clinical, pathological and serological findings in cattle hypodermosis in Peştişani, Gorj County Romania. Sci Parasitol. 2011;12:173–6.

    Google Scholar 

  30. Nepoklonov AA, Prohorova IA, Mavrin NA. Control of prophylaxis of bovine hypodermosis in Russia and in the world. 2011. http://vetkuban.com/num5_20117.html. Accessed 22 May 2016 (in Russian).

    Google Scholar 

  31. Sylejmani D, Robaj A, Ismalji A. Incidenca e hipodermozës në kushte ambulatore në disa rrethe të Kosovës. Aktet. 2012;3:84–8 (in Albanian).

    Google Scholar 

  32. Zuko A. Ectoparasitoses in ruminants in Bosnia-Herzegovina. Proceedings of the 3rd International Epizootiological Days & 15th Serbian Epizootiological Days, 8–11 May 2013, Niš, Serbia, p. 204–8.

  33. Becskei Z, Ilić T, Pavlićević N, Kiskároly F, Petrović T, Dimitrijević S. Hypodermosis in northern Serbia (Vojvodina). Macedonian Vet Rev. 2016;3:129–33.

    Google Scholar 

  34. Otranto D, Traversa D, Colwell DD, Guan G, Giangaspero A, Traversa D, et al. A third species of Hypoderma (Diptera: Oestridae) affecting cattle and yaks in China: molecular and morphological evidence. J Parasitol. 2004;90:958–65.

    Article  CAS  PubMed  Google Scholar 

  35. Guan G, Luo J, Ma M, Yang D, Wang Y, Gao J, et al. Sero-epidemiological surveillance of hypodermosis in yaks and cattle in northern China. Vet Parasitol. 2005;129:133–7.

    Article  PubMed  Google Scholar 

  36. Saidani K, Benakala A, Díez-Baños P, Panadero R. Chronobiology of Hypoderma spp. in north-central Algeria as a basis to establish a control program. Rev Ibero-Latinoam Parasitol. 2011;70:157–62.

    Google Scholar 

  37. Dheghani R, Sedaghar MM, Esmaeli N, Ghasemi A. Myiasis among slaughtered animals in Kashan, Iran. Iranian J Vet Sci Techn. 2012;4:19–28.

    Google Scholar 

  38. Khan MQ, Irshad H, Jahangir M, Razzaq A. Studies on the biology, chemotherapy and distribution of warble fly in Pakistan. Rev Sci Techn, Off Int Epizoot. 2012;31:959–68.

    Article  Google Scholar 

  39. Karatepe M, Simsek S, Karatepe B, Cayvaz M, Sevgili M, Balkaya I. Seroprevalence of hypodermosis in cattle in Nigde province of Turkey by comparison of commercial and indirect-ELISA methods. Israel J Vet Med. 2013;68:38–42.

    Google Scholar 

  40. Yadav A, Katoch R, Khaiuria JK, Godara R, Agrawal R. Prevalence of Hypoderma lineatum in cattle in Jammu region. J Parasitol Dis. 2013;37:196–8.

    Article  Google Scholar 

  41. Jaiswal AK, Sudan V, Kumar P, Srivastava A, Shanker D. Bovine hypodermosis in indigenous cattle herd and its successful therapeutic management. J Parasitic Dis. 2016;40:166–8.

    Article  Google Scholar 

  42. Scholl PJ. Management and control of oestrid flies. In: Colwell DD, Hall MJR, Scholl PJ, editors. The oestrid flies: biology, host-parasite relationships, impact and management. Wallingford: CABI Publishing; 2006. p. 210–9.

    Chapter  Google Scholar 

  43. Cady SM, Cheifetz PM, Galeska I. Veterinary long-acting injections and implants. In: Rathbone MJ, McDowell A, editors. Long-acting animal health drug products. Fundamentals and applications. New York: Springer; 2013. p. 271–94.

    Chapter  Google Scholar 

  44. Cruz JB, Cox JL, Maciel AE, Barrick RA. Efficacy of ivermectin long-acting injection against Dermatobia hominis in cattle. In: Abstracts of the 44th Meeting of the American Association of Veterinary Parasitologists, 10–13 July 1999, New Orleans, LA, USA; 1999. p. 50.

  45. Serra-Freire MN, Lopes LM, Famadas KM, Cruz JB, Alva R, Barrick RA. Comparative efficacy of ivermectin long-acting injection against Dermatobia hominis in cattle. In: Abstracts of the 26th World Veterinary Congress, 23–26 September 1999, No. 635. Lyon, France; 1999.

  46. Holdsworth PA, Vercruysse J, Rehbein S, Peter RJ, De Bruin C, Letonja T, et al. World Association for the Advancement of Veterinary Parasitology (W.A.A.V.P.) guidelines for evaluating the efficacy of ectoparasiticides against myiasis causing parasites on ruminants. Vet Parasitol. 2006;136:15–28.

    Article  CAS  PubMed  Google Scholar 

  47. Colwell DD, Baron RW, Lysyk TJ. Influence of parasiticide treatment on kinetics of antigen specific antibody response in cattle infested with Hypoderma lineatum (Diptera, Oestridae). Vet Parasitol. 1997;68:175–86.

    Article  CAS  PubMed  Google Scholar 

  48. James MT. The flies that cause myiasis in man. USDA Misc Publ No 631, Washington, DC 1947.

  49. Grunin KJ. Hypodermatidae Teil. In: Lindner E, editor. Die Fliegen der paläarktischen Region. Stuttgart: Schweizerbarth’sche Verlagsbuchhandlung; 1965. p. 62.

    Google Scholar 

  50. Sinclair IJ, Tarry DW, Wassal DA. Persistence of antibody in calves after an infection with Hypoderma bovis. Res Vet Sci. 1984;37:383–4.

    CAS  PubMed  Google Scholar 

  51. Boulard C. Avantages de l’immunodiagnostic de l’hypodermose bovine établi par hémagglutination passive et par ELISA, à partir du sérum et du lactosérum, sur la numération des varons. Ann Rech Vét. 1985;16:335–43.

    CAS  PubMed  Google Scholar 

  52. Colwell DD, Baron RW. Early detection of cattle grub infestation (Hypoderma lineatum De Vill. and H. bovis L.) (Diperta: Oestridae) using ELISA. Med Vet Entomol. 1990;4:35–42.

    Article  CAS  PubMed  Google Scholar 

  53. Rehbein S, Knaus M, Visser M, Winter R, Yoon S, Anderson A, et al. Activity of ivermectin long-acting injectable (IVOMEC® Gold) in first-season grazing cattle exposed to natural challenge conditions in Germany. Parasitol Res. 2015;114:47–54.

    Article  CAS  PubMed  Google Scholar 

  54. Rehbein S, Knaus M, Visser M, Winter R, Yoon S. Control of parasitic infection with ivermectin long-acting injection (IVOMEC® GOLD) and production benefit in first-season grazing cattle facing a high level larval challenge in Germany. Parasitol Res. 2016. doi:10.1007/s00436-016-5256-2.

    Google Scholar 

  55. Drummond RO. Control of larvae of the common cattle grub with animal systemic insecticides. J Econ Entomol. 1984;77:402–6.

    Article  CAS  PubMed  Google Scholar 

  56. Boulard C, Alvinerie M, Argenté G, Languille J, Paget L, Petit E. A successful, sustainable and low cost control-programme for bovine hypodermosis in France. Vet Parasitol. 2008;158:1–10.

    Article  PubMed  Google Scholar 

  57. O’Brien DJ. Warble fly prevalence in Europe 1997 after COST 811. In: Boulard C, Sol J, O’Brien D, Webster K, Sampimon OC, editors. COST 811: Improvements in the Control Methods for Warble Fly in Livestock. Brussels: European Commission; 1998. p. 20–7.

    Google Scholar 

  58. Scholl PJ. The current situation of hypodermosis in North America. In: Boulard C, Sol J, O’Brien D, Webster K, Sampimon OC, editors. COST 811: Improvements in the Control Methods for Warble Fly in Livestock. Brussels: European Commission; 1998. p. 38–41.

    Google Scholar 

  59. Colwell DD. Persistence of hypodermosis in North America and prospects for the development of vaccines. In: Good M, Hall MJ, Losson B, O’Brien D, Pithan K, Sol J, editors. COST Action 833: Mange and Myiasis of Livestock. Brussels: European Commission; 2002. p. 7–15.

    Google Scholar 

  60. Colebrook E, Wall R. Ectoparasites of livestock in Europe and the Mediterranean region. Vet Parasitol. 2004;120:251–74.

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors thank Merial, Inc., Duluth, GA, US for sponsoring this multicentre study.

Funding

Studies were funded by Merial, Inc., Duluth, GA, USA.

Availability of data and material

All the data are contained within the article and its tables.

Authors’ contributions

SR conceived the study, participated in the data collection, analysis and developed the first draft manuscript. All other authors played a role in data collection (DO, GJ, KS, JSH, SR), data analysis (SY) and interpretation of findings (DO, GJ, KS, SY, JSH, SR). All authors read and approved the final manuscript.

Competing interests

Authors were contractors of Merial (DO, GJ, KS) or are current employees of Merial (JSH III, SY, SR) and assisted with the study design, conduct, data analysis and manuscript preparation. IVOMEC® is a registered trademark of Merial. All other marks are the property of their respective owners.

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All animals were handled with due regard to their welfare and in compliance with Merial Institutional Animal Care and Use Committee (IACUC) approvals, any applicable local regulations, and requirements of any local IACUC.

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Correspondence to Domenico Otranto.

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Otranto, D., Johnson, G., Syvrud, K. et al. Treatment and control of bovine hypodermosis with ivermectin long-acting injection (IVOMEC® GOLD). Parasites Vectors 9, 551 (2016). https://doi.org/10.1186/s13071-016-1823-8

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