By Allie Neill
Edited by Kyle Lesack
Introduction
If you’ve ever heard of botflies, you’ve probably seen them in gruesome videos or blog posts describing them as “human flesh-eating parasites”. Most of this is true. They are in fact flesh eating parasites. Humans, however, have little to do with it. Their parasitism of people is accidental and infrequent with very mild symptoms. Despite this, most people know very little about botflies besides those interactions with humans. In this blog post we’re going to discuss what are botflies really all about and where their real impact on human lives is.
Backgrounds
Botflies are obligate parasites of mammals and belong to the Dipteran family Oestridae. Botflies can parasitize a large range of mammalian species – even within subfamilies – with rodents, ungulates, canids, and felids being among the most common (Scholl et al., 2019). They are endemic to lower latitude regions across the globe. There are four subfamilies: Oestrinae which parasitize nasopharyngeal regions, Gasterophilinae which parasitize the gastrointestinal organs, and Hypodermatinae and Cuterebrinae which both parasitize the subdermal skin regions (Scholl et al., 2019). The pupa and adult life stages are free-living in all four subfamilies. Eggs are deposited by the adult fly directly on the host or in soil or vegetation in the environment to be picked up by the intended host. The exception is members of the Oestrinae subfamily that deposit already-hatched larvae directly onto the host. In all subfamilies the three larval instars are parasitic and rely on the mammalian hosts for survival, feeding on their tissues to grow and develop (Colwell, 2006). The larvae burrow into the host and consume its tissues from within. Upon reaching the end of the third larval instar they will either erupt from the host’s skin and fall to the soil or, in the case of Gasterophilinae, they will pass in the feces. From here the larvae burrow into the soil to pupate and undergo metamorphosis, emerging as the adult fly and begin the process of locating a mate to continue the life cycle once more. The infection of a given host with botfly larvae is known as myiasis (Colwell, 2006; Scholl et al., 2019).
Source: https://www.cdc.gov/parasites/myiasis/biology.html
Summary of scientific literature
The largest focus in the scientific literature surrounding botflies is related to livestock and veterinary medicine. Despite claims in popular culture that botflies exist to feed on human flesh, humans are not the intended host of any species of botfly since they are usually noticed and removed by people before they can complete larval development (Scholl et al., 2019). When humans appear in the literature it’s in human myiasis case reports. The scientific source of the (WSFA, 2018) article regarding a Florida woman infected with human botfly larva in Belize explored her case in great detail. The case report discusses the human botfly life cycle, the process of diagnosis, the benign nature of human infection, methods of possible extraction, and difficulty that often comes with diagnosing a botfly infection due to nonspecific symptoms similar to many common skin conditions (Shenouda, 2018). By contrast, livestock are among the intended targets of various botfly species within all four Oestridae subfamilies (Colwell, 2006; Scholl et al., 2019). Botfly infection has been documented in livestock populations of ancient Roman, Egyptian, and Grecian societies (Amci, 2006). The stress that excessive myiasis puts on livestock is known to reduce milk, fur, and meat yields (Toure, 1994). For these reasons, the scientific literature centers around researching host-parasite relationships and metamorphosis of botflies as it relates to developing treatments and preventative measures for infected livestock.
Investigating the host-parasite relationship is the biggest theme within the literature. When newly hatched larvae are first deposited on the host’s skin, they require a method of breaking past the outer layers and into the subdermal tissues. It was confirmed by (Boulard, 1969) that cattle botfly larvae use a series of collagenases to break down skin and tissues for burrow creation and feeding. Collagenases also facilitate migration through the host’s internal tissues to target organs or tissues during the first larval instar (Boulard, 1969). They continue to use collagenases to dissolve tissues for consumption throughout the second and third larval instars and additional types of proteolytic enzymes produced by later stage larvae are still being discovered (Angulo-Valadez et al., 2007). To avoid the host’s immune system, botfly larvae produce immunomodulatory enzymes that decrease the scale of the host immune response. Botfly larvae will secrete proteolytic enzymes that target the complement-complex system involved in innate immunity (Boulard, 1989). They are also capable of secreting enzymes that decrease the production and recruitment of lymphocytes through degradation or inactivation of interleukins and cytokines (Moire, 1997; Panadero, 2009). Strength of host immune response also depends on the number of larvae present. In cases of severe infection (>100 larvae) the host immune response results in a larval mortality rate of up to 99%. In cases of moderate infection (<20 larvae) the host immune response results in a larval mortality rate as low as 50% (Breev, 1967). While inside the burrow – which is essentially an open wound – they’re able to keep the surrounding tissue free of infection by secreting large amounts of antibiotic products (Scholl et al., 2019).
Source: Shenouda, M. et al. 2018. Human Botfly: A Case Report and Overview of Differential Diagnosis. SAGE Publications Ltd. Journal of Investigative Medicine High Impact Case Reports 6: 1-4.
The study of the botfly pupae metamorphosis is also a current topic of interest in scientific research. Understanding the detailed complexities involved in metamorphosis is very valuable to the development of possible treatments for soils in livestock pastures that would prevent the pupae from completing metamorphosis. In a species of nasal botfly, Oestrus ovis, that parasitizes sheep it was recently discovered that there exists a key difference in the developmental process during metamorphosis that results in a vestigial adult digestive tract that is distinct from other closely related Dipteran taxa (Martin-Vega et al., 2020). This could be indicative of chemical signalling processes unique to groups of Oesterid flies that could be specifically targeted with future treatments.
Interestingly, there also exists discussion and evidence within the literature that botflies aren’t a significant health threat to hosts in non-domesticated mammal populations. Wild white-footed mice populations were surveyed in Williamsburg, Ohio where rodent botflies are common. Uninfected and infected mice were trapped, weighed, and tagged during the warmer months when botflies are active for two years from 2002-2003. Researchers found no correlation between botfly infection and weight or infection and survival. Mice who were re-trapped and previously recorded as being parasitized displayed healthy weights just as often as previously unparasitized mice (Cramer and Cameron, 2006). This subverted the researcher’s expectations that botflies would have a negative impact on survivorship in wild mammalian host populations.
Closing
The scientific literature focuses on livestock, the aspect of human lives where botfly parasitism can cause serious problems. It heavily explores topics of metamorphic development and host-parasite interactions with livestock in various host species. The angle of approach is one with the goal of understanding these parasites and their physiology. A greater physiological understanding of parasites is required if we are to create effective and efficient treatments and controls. The literature aims to increase physiological knowledge of botflies so that we can improve and develop new measures to prevent and treat botfly infection of livestock. It also includes research on botfly impacts in wild mammal populations. Contrary to what might be expected, this research indicates that botflies aren’t a significant health concern and that the host populations are very tolerant of infection. Since botflies don’t cause long-lasting or serious symptoms it’s possible that launching a severe immune response would cost more energy and cause more damage than it would be worth, so the host simply tolerates the parasite as long as the parasite load is low enough. This is supported by (Breev, 1967) and the differential larval mortality seen in cattle infected with high parasite loads vs. low parasite loads. This begs one to question why botflies have been such a historical and continued concern for livestock. The likely answer is that since livestock are contained to specific fields year-round and botflies mate and lay their eggs in areas near where they pupate, a resident population of botflies could establish itself and grow exponentially in livestock pastures, resulting in damaging levels of parasitism. Scientific literature aims to increase knowledge and understanding involving botfly physiology and host-parasite relationships to better manage livestock health.
Upcoming Blog Post
Now that we’ve discussed how botflies are treated in the scientific world, how does pop-culture stack up?
Citations
Amci, R. R. 2006. Historical Perspectives on the Importance and Impact of Oestrids. In The oestrid flies: Biology, host-parasite relationships, impact and management. CABI Publishing, Wallingford, 8–19 p.
Angulo-Valadez, C. E. et al. 2007. Proteolytic activity in salivary gland products of sheep bot fly (Oestrus ovis) larvae. Elsevier. Veterinary Parasitology 149: 117–125.
Boulard, C. 1969. Anatomy and histology of the digestive system of Hypoderma bovis larva (Diptera, Oestriformes). Annales de la Société Entomologique de France. 5: 371-387.
Boulard, C. 1989. Degradation of bovine C3 by serine proteases from parasites Hypoderma lineatum (Diptera: Oestridae). Veterinary Immunology and Immunopathology. 20: 387- 398.
Breev, K. A. 1967. New data on the migration of instar-I larvae of Hypoderma bovis De Geer in the host organism. Parazitologicheskii sbornik 23: 191-221.
Colwell, D. D. 2006. Life Cycle Strategies. In The oestrid flies: Biology, host-parasite relationships, impact and management. CABI Publishing, Wallingford, 67–77 p.
Cramer, M. J., and Cameron, G. N. 2006. Effects of bot fly (Cuterebra fontinella) parasitism on a population of white-footed mice (Peromyscus leucopus). Journal of Mammology. 87(6): 1103-1111.
Martín-Vega, D. et al. 2020. Internal morphological changes during metamorphosis in the sheep nasal bot fly, Oestrus ovis. Medical and Veterinary Entomology 34: 476–487.
Moiré, N. et al. 1997. Enzymatic effect of hypodermin A, a parasite protease, on bovine lymphocyte membrane antigens. Blackwell Publishing Ltd. Parasite Immunology 19: 21–27.
Panadero, R. et al. 2009. Immunomodulatory effect of Hypoderma lineatum antigens: In vitro effect on bovine lymphocyte proliferation and cytokine production. Parasite Immunology 31: 72–77.
Scholl, P. J. et al. 2019. Myiasis (Muscoidea, Oestroidea). In Medical and Veterinary Entomology, 3rd edition. Academic Press, London, 383–419 p.
Shenouda, M. et al. 2018. Human Botfly: A Case Report and Overview of Differential Diagnosis. SAGE Publications Ltd. Journal of Investigative Medicine High Impact Case Reports 6: 1-4.
Toure´, S.M., 1994. Myiases of economic importance. Revue Scientifique et Technique. 3, 1053–1073.
WSFA 12 News Staff. 2018. Deeply embedded maggot found in Florida woman’s groin. NBC. https://www.wsfa.com/2018/10/31/deeply-embedded-maggot-found-florida-womans-groin/
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