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Control of Dermatobia hominis larvae by manual extraction is effective and does not cause abscess.

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Summary
In order to study alternative ways of control of Dermatobia hominis fly larvae, we tested: T1, cypermethrin 5% + chlorpyrifos 7% + citronellal 0.5% (Pour on); T2, trichlorphon powder dissolved at 2% in burnt oil passed on the nodules; T3, manual larva extraction. The study was conducted at Instituto de Zootecnia, located in Nova Odessa, São Paulo State, Brazil. In a dairy herd of 176 animals, we found 29 with at least one larvae that were distributed in the three treatments. The percentage of efficacy of each treatment was based on the numbers of live botflies that were before and after 14 days. The animals were observed on days +4, +7, +14 and +21 and new botflies and abscesses related to treated botflies in these animals were annotated. All treatments presented high effectiveness (above 98%). New botflies were already seen in the first week after the application of the three treatments and in the 21 day we observed two abscesses in each chemical treatment. Larva extraction was 100% effective, no originating abscesses, and should be encouraged in organic properties, or not, and in those with larval resistance to chemical products.

Keywords: botfly, cattle, dairy herd, chemical control, alternative control, abscess

Controle da larva de Dermatobia hominis com extração manual é efetivo e não causa abscesso.

PORTUGUÊS (PTBR)

Resumo
Com a finalidade de estudar formas alternativas de controle de larvas da mosca Dermatobia hominis, foram testados: T1, cipermetrina 5% + clorpirifós 7% + citronelal 0,5% (Pour on); T2, triclorfon em pó, dissolvido a 2% em óleo queimado, passado sobre o nódulo; T3, extração manual das larvas. O estudo foi realizado no Instituto de Zootecnia, localizado em Nova Odessa, Estado de São Paulo, Brasil. Em um rebanho leiteiro de 176 animais, encontramos 29 com pelo menos uma larva, que foram distribuíram nos três tratamentos. O percentual de eficácia foi baseado no número de bernes vivos antes e depois de 14 dias da aplicação dos tratamentos. Os animais foram observados nos dias +4, +7, +14 e +21 e foram anotados novos bernes e abcessos relacionados a bernes tratados. Todos os tratamentos apresentam alta eficácia (acima de 98%). Logo na primeira semana, foram observados novos bernes em todos os tratamentos, e no 21º dia observamos dois abcessos em cada tratamento químico. A extração da larva foi 100% eficaz, não originando abscessos, devendo ser incentivada nas propriedades orgânicas, ou não, e naquelas com resistência da larva a produtos químicos.
Palavras-chave: berne, gado, rebanho leiteiro, controle químico, controle alternativo, abscesso

TEXTO COMPLETO:

Control of Dermatobia hominis larvae by manual extraction is effective and does not cause abscess.

Introduction
In recent years, research has sought sustainable development and the world is interested in health and environmental concerns, mainly in relation to less contamination by agrochemicals (Azevedo et al., 2011). There is a great demand for organic food, which requires producers to search for parasite control that does not harm the quality of the meat or milk and the environment. Controlling the diseases and parasites that cause great losses in cattle farming at the lowest cost, having a more resistant herd and working with a lower risk of environmental contamination are goals of great relevance to cattle farmers (Pinto et al., 2005).
Dermatobia hominis is a fly that lays its eggs on another insect, usually another diptera, that, by landing on the bovine, or other warm-blooded animal, releases the larvae that promptly begin their insertion into the subcutaneous tissue. In cattle, the larvae go through three stages , L1, L2 and L3, in a period of 31 to 69 days , depending on the animal (Ribeiro and Oliveira, 1983). When the L3 is mature, it spontaneously leaves the host, usually at night (Ribeiro and Oliveira, 1983), actively seeking to bury itself in the ground , where it will pupate and turn into a new fly in 26 to 31 days (25oC, UR 70 %) (Barbosa et al., 2002). Its control is usually done with chemicals, and those based on macrocyclic lactones have been used successfully ( Roncalli and Benitez Usher, 1988; Moya-Borja et al., 1993; Silva Netto et al., 2001); nevertheless, there have been reports of failure in the control of this myiasis with the use of these products (Neves et al., 2015). Berne does not seem to do much harm from a clinical point of view, to the point of impairing the weight gain of the animals that harbor them ( Magalhães and Lesskiu, 1982; Barbosa et al., 2002), however, the damage is great when the quality of the leather for the industry is taken into consideration (Magalhães and Lesskiu, 1982; Marques et al., 2000). In Brazil, the losses caused by Berne have been estimated at more than 380 million dollars annually (Grisi et al., 2014). As the larvae develop, a nodule forms, which can reach 2-3 cm in diameter at the end of the cycle (Barbosa et al., 2002). In addition, the nodules are usually infected by bacteria (Sancho et al., 1996), some with lethal potential to cattle ( Pereira et al., 2000; Ladeira et al., 2010).
The oldest method of D. hominis control is manual extraction of the larvae , used in both animals and humans , where they are expelled through the abscess hole , however, there are few scientific papers that address this form of Berne control (Roncalli, 1984; Villarino et al, 2003).
Due to the current need to search for alternatives to control this parasite, the objective of this study was to evaluate the control provided by the extraction of larvae, compared to two other chemical control methods: commercial chemical in a Pour on formulation and another commercial chemical in powder form, mixed with burnt oil applied directly to the nodules, both methods widely applied in Brazil.
Material and methodsThe study was carried out with dairy animals from the Institute of Zootechnics, located in the city of Nova Odessa (latitude 22º 46' 40" south; length 47º 17' 45" west), and was approved by the Ethics Committee of this institution (protocol number 281/19). Of a total of 176 animals, 29 with the presence of at least one Berne were distributed in the treatments; the animals were of varying ages, most being adults. The assignment lasted 21 days of observation, beginning in March 2019. The herd was meticulously inspected for the presence of Berne, and immobilized in a containment trunk. The treatments were:T1 - Chemical in Pour on form (formula based on cypermethrin 5 g, chlorpyrifos 7 g, and citronellal 0.5 g, Colosso Pour on ®), N=9;T2 - Chemical in powder form (triclorfon, Neguvon®), by applying a mixture of 20 g of the product in 1 liter of reused car engine oil, directly on each lump, using a 5 cm wide brush, N=10;T3 - Extraction of the larvae, pressing the nodule, between thumb and index finger, from bottom to top; when the larva was small, and difficult to get out, tweezers were used to help in the extraction , N=10.The experimental period accounted for five observations, i.e. on days 0, +4, +7, +14 and +21 post-treatment. On the day of treatment (day 0), the location of each Berne nodule was marked as a dot on drawings representing the right and left side of the animal. Subsequently, the location of each Berne was defined according to the figure proposed by Cardoso et al. (2014), which divided the bovine body into seven regions, namely: head, cervical region (neck and shoulder), thoracic limb, rib, flank, pelvic limb, and tail/croup. Each day of observation, the treated nodules were evaluated for abscess formation, or disappearance of the nodule, whether the Berne would be dead or alive, considering as alive those with an intact orifice through which they breathe, The larvae were found to be viable after the 14th day of treatment, and live larvae were extracted.Extracted larvae were stored in jars labeled with the animal number and included in 70% alcohol, to later be evaluated as to the larval stage they were in by the number of respiratory stigmata.New nodules with D. hominis larvae that appeared during the study were noted, but no treatment has been done for these new hornworms; only after the 14th day of the experiment were these new roundworms extracted. The coloration of the animal and the location of the Berne on the black or white coat were also noted, in the case of Holstein cattle, and which side they were on, right or left.         After the treatment, each animal stayed in its original paddock. To evaluate the effectiveness of each treatment the formula was used: % Effectiveness = [(Total hornworms before treatment - Total hornworms surviving treatment) / Total hornworms before treatment)] x 100 Results  The distribution of Berne nodules in the herd animals can be seen in Figure 1. The distribution of Berne-parasitized animals fits a negative binomial model curve, Where the majority of the herd (83.5%) was free of Berne's disease on the day the evaluation was done to apply the treatments and the number of animals with more than 10 hornworms was very small, The maximum number found was 17 hornworms in 1 animal; most of the parasitized animals, 20 animals (69%), had between 1 and 4 hornworms.      Figure 1 - Distribution of animals with zero, 1 and 2, 3 and 4, 6 to 8, and more than 10 nodules of roundworms in a dairy herd (Nova Odessa, SP, 19/03/2019).The results of the effectiveness of each treatment, new hornworms and abscesses observed over a 21-day period are shown in Table 1. All treatments were found to have high efficacy on roundworms (98 - 100%). New hornworms were observed at T1 already in the first week post-treatment; At T2, new hornworms were also observed from the first week post-treatment; at T3, the first new Berne was observed on day +4, that, It probably went unnoticed on day zero, since it was located on the inside of the left hand, in a place that was difficult to see. All the new hornworms (37) were manually extracted once they were noticed.  Table 1 - Number of hornworm nodules observed immediately before the application of treatments and 14 days later; efficacy of treatments; new hornworms and number of abscesses resulting from dead hornworms observed in the 21-day post-treatment period.  T1T2T3Hornworms nodules before treatment 495229Live hornworms nodules 14 days post-treatment010Treatment Effectiveness %10098100New hornworms52210Abscesses220T1 - Pour on product based on cypermethrin 5 g, chlorpyrifos 7 g, and citronellal 0.5 gT2 - Triclorfon (2 %) mixed with burnt oil brushed over the noduleT3 - Manual larval extractionAs for the larval stage of the recovered roundworms, 76 % were in the L2 stage and 24 % in the L3 stage.A total of 113 hornworms were observed on the day of treatment, and 37 more were observed over the 21-day observation period, totaling 150 hornworms, 90 on the right side (60%) and 60 on the left side (40%). Table 2 includes the percentage distribution of larvae in the animal's body, according to body regions, by Cardoso et al. (2014). Table 2. Percentage of larvae found in the regions, according to division of the bovine body proposed by Cardoso et al. (2014).
HeadNeckThoracic LimbRibsFlankPelvicLimbTail/Rump%1,927,6921,1559,623,853,851,92
DiscussionInfestation by D. hominis larvae varies among animals of the same breed, crossbreed, herd and management (Maia and Guimarães, 1985; Oliveira and Alencar, 1990). This could be verified, since of the 176 animals evaluated on day Zero, only 29 were parasitized, with very few having more than 10 hornworms (Figure 1).In the present study, all treatments were more than 90% effective, However, none of the chemical treatments tested prevented reinfestation of the animals with new Berne larvae within 21 days. The lower number of new hornworms observed in the animals that received T1 indicates that this product offered greater protection to the animals. At T2, the highest number of new hornworms was observed and a single live hornworm was found that survived the treatment. In both chemical treatments abscess formation was observed; some formed soon after treatment, but disappeared over the course of weeks, and at 21 days of observation, There remained 2 closed nodules with abscesses in each of these chemical treatments. Abscess formation was not seen in the treatment with larval extraction, which controlled 100% of the hornworms, without the need to apply any product. Larval extraction can be easily done on small and medium farms, because not all animals in the herd are parasitized, and most of them have few parasites present in the body (Moya-Borja, 2003; Cardoso et al., 2014), which was confirmed in this study, since only 16 % of the herd was parasitized. Roncalli (1984) reports that manual extraction is possibly the oldest method of dermatobiosis control. The verification of nodules is performed by visual and tactile inspection (Gomes et al., 1996), and especially the mature larvae (L3) can be easily extracted just by pressing the fingers from below upwards, or with the aid of anatomical forceps if they are in younger forms (L2). It is also recommended to eliminate the larvae extracted from the animal to interrupt the biological cycle, and thereby decrease the Dermatobia hominis fly population at the site.
Next to the D. hominis larvae, many bacteria live in the subcutaneous tissue (Sancho et al., 1996), some very harmful to cattle (Pereira et al., 2000). When the larva dies within the subcutaneous tissue, the follicle through which it breathes heals quickly, preventing necrotic material from being expelled naturally, forming abscesses, which, depending on the size they reach, may not be reabsorbed by the body, becoming a problem for the animals. One example is the pathology caused by the bacteria Mannheimia granulomatis, one of the bacteria that can be isolated from D. hominis larvae (Pereira et al., 2000) and that can lead a bovine to death (Ladeira et al., 2010). First stage larvae were not observed in the study, probably because they are very small, making them imperceptible on the body, some very harmful to cattle.
In 2003, Moya-Borja said that pyrethroids, commonly used as tick and mosquito killers, have little lethal action against the second and third stages of Berne, but are excellent repellents of the carrier insects and were able to control the early stage of the larva when it penetrated the host's skin. In Brazil, in the 1990s, a study evaluated a pyrethroid-based product (alfamethrin 0.005 %), applied as a spray to control Berne disease, was 100 % effective up to 18 days after treatment (Sanavria and Grisi, 1991). Kasai et al. (1997), working in the region of Pirassununga, SP, with a formulation cypermethrin 4.5% + DDVP 50%, via spraying, found bernicidal efficacy of 65% (day 3) to 72% (day 21 after spraying). The explanation for the low effectiveness obtained, according to the authors, was because it is a product that acts by contact, and not in a systemic way, with limited effect on the larvae present in the subcutaneous tissue of cattle. Valencia et al. (2007), using a spray-on product based on 15% cypermethrin + 25% chlorpyrifos, in a city in Colombia, observed a bernicidal efficacy of 96.3% three days after treatment, with a residual effect up to 28 days after treatment (82.7% efficacy on day +28). According to Correa (2011), the combination cypermethrin 15% + chlorpyrifos 30% + fenthion 15% achieved a tick control efficacy of more than 95% on dates 7, 14 and 21 after treatment, starting to decline on day 28 to 74.97% efficacy. Now for mosquicidal efficacyThe author found 99% in the first three days after treatment and anti-hematobic efficacy of 60% on the fourteenth day after treatment. For the evaluation of Dermatobia hominis larvae, he found a repellency of 100 percent, up to the seventh day after treatment.
The organophosphates are a group of chemical compounds widely used in agriculture and cattle raising as acaricides and insecticides (Cavaliere et al., 1996). In this study, one product from this group, Triclorfon, was used in treatment 2, mixed with already used automotive oil, brushed onto each Berne nodule. This way of diluting and applying the product with burning oil is very popular among small and medium-sized homeowners. According to Moya-Borja (2003), the use of trichlorfon stands out as the active ingredient most used to control infestations by D. hominis larvae in small properties in Brazil, due to its efficacy and low cost, however, literature on the effectiveness of this treatment is scarce. In a survey, Villarino et al. (2003) found that the most commonly used method of Berne control in Nicaragua was ivermectin (43%), followed by dichlorvos with burnt oil brushed on the nodules (40%) and trichlorfon with burnt oil, also brushed on the nodules (19%); only 2% used manual larval extraction. In a study of popular knowledge with producers in Formosa, MG, Cansi (2012) reports that the medication most commonly used by farmers to combat Berne was Neguvon® (Triclorfon) mixed with burning oil. The results obtained in this experiment showed that while achieving 98% efficacy, there was one live larva, survived this treatment, in addition to abscess formation, as it was noted that in most of the nodules, the larvae die inside the skin without being expelled, which triggers the inflammatory process in the host.
Until the year 2003, when Moya-Borja published his considerations on eradication or integrated management of Neotropical myiases of the Americas, there were no reports of D. hominis resistance to any chemical group of insecticidal drugs. However, the existence of drug-resistant organisms is a reality nowadays, and a big problem in the agricultural and livestock sector, Therefore, the empirical perception of loss or decrease in efficacy of insecticides against D. hominis larvae has often been attributed to the emergence of resistant parasites by cattle farmers. However, many homeowners choose to discontinue the use of certain insecticides in order to employ more broad-spectrum drugs. (Oliveira-Sequeira et al., 2014). Regarding injectable endectocidal products, ivermectin and moxidectin, launched in the 1980s and 1990s (Roncalli and Benitez Usher, 1988; Silva Netto et al., 2001), and still widely used in our environment for Berne control, there are reports of resistance of this parasite to products of these chemical groups (Neves et al., 2015). Not to mention that injectable endectocides and other chemical groups in the Pour on formulation cause negative environmental impacts by reducing the coprophagous fauna, which causes a delay in manure decomposition (Bang et al., 2007), and the possibility of inducing resistance to other parasite species, such as nematodes, ticks and other flies, by the amount or by unnecessary exposure to these products (Alegría-López et al., 2015).
Regarding coat coloration, Gomes et al. (1996), evaluating animals of different beef cattle breeds in Mato Grosso do Sul, identified that the infestation was related to the coat coloration of the animals: those with dark coats had more hornworms, because dark coats attract hornworm-vectoring flies more intensely (Guimarães and Papavero, 1999). The same was observed by Cardoso et al. (2014), who found that darker animals were more parasitized than lighter ones. In this experiment, this characteristic was noticeable: as the vast majority of the animals were of the Holsteins breed, it was easy to notice that 100% of the nodules were present in the black patches of the coat.
As for the location of the Berne nodules on the animals' bodies, our data corroborate most of the works that have made this type of annotation ( Pinto et al., 2002; Mozzaquatro and Sanavria, 2003; Cardoso et al., 2014), Most of them, 90.38%, are located in the anterior region, from the rib to the head, since the movements provided by the animal's tail broom are able to scare away the D. hominis egg vectors from the posterior region (Oliveira, 1991). The skin surface of 8,124 cattle slaughtered in a slaughterhouse in the state of Rio de Janeiro over a one-year period was examined by Sanavria et al. (2002), who found a higher incidence in the anterior quadrants, more on the left side, in dark-haired animals; in 84.8% of the hides no typical lesion caused by D. hominis larvae was detected.
In this study, some animals had pecks, but none was directly related to the Berne hole. Maia e Guimarães (1985), observing 10 Nellore cows in a one-year experiment, also found no relationship between Dermatobia and Cochliomyia parasitism, but found an association of Berne with abscesses, and cite 3 other authors who also found this association.
Conclusions  The mechanical extraction of larvae is an excellent alternative for the control of dermatobiosis caused by the fly Dermatobia hominis in small and medium farms. Although it requires more attention and labor, it does not need chemicals, bringing savings to the production system. In addition, using this method reduces the likelihood of the development of resistance to ectoparasites and prevents abscess formation, contamination of the environment, the animals, and their products, and is perfect for organic or non-organic production systems and for farms where chemical products are no longer effective against this parasite. It is recommended that the larvae removed from the animals be properly destroyed so that they cannot complete the parasitic cycle, thus reducing the population of flies of the genus Dermatobia on the property.
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