Mechanical Transmission of Disease Agents by Arthropods Professor Lane Foil

Mechanical Transmission of Disease Agents by Arthropods

Professor Lane Foil Department of Entomology Louisiana State University 1

Biological vs. Mechanical transmission

• Biological transmission: agent develops and or propagates within the vector • Mechanical transmission: transfer of agents from an infected host or a contaminated substrate to a susceptible host – Direct mechanical transmission: agents transferred directly between two hosts – Indirect or contaminative mechanical transmission: arthropods transmit pathogens picked up from contaminated sources

• Historically mechanical transmission studies conducted when associations of arthropods and disease were made • Even when experimental evidence is obtained, vehicles of mechanical transmission other than arthropods often exist • Feces source and fly vector; Fecal oral, food handlers, farm workers, etc. • Lesion source and fly vector; Direct contact • Blood source and fly vector; Multiple use needles, etc. • The relative importance of mechanical transmission of agents by arthropods in epidemiology is often situational 3

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Factors that influence indirect (contaminative) mechanical transmission

• Insect behavior; Dispersal, regurgitation (flies), defecation (flies and roaches) • Survival of agents; Within the environment and within and on arthropp(ods (enteric diseases associated with arthro pods usually are bacteria - facultative anaerobic gram-negative rods (Pseudomonas, Salmonella, Staphylococcus, Klebsiella, Escherichia, Campylobacter, etc.; But certain stable (rotaviruses) viruses with high numbers are described • Host factors; Crowding in unsanitary conditions (military, refugee, nosocomial, confined animals (poultry in particular) 4

Indirect mechanical transmission

• Viruses; Poliomyelitis and other enteroviruses (isolated but not important), rotavirus possible •Bacteria • Protozoa • Viruses • Helminths •Bacteria •Protozoa • Helminths

• Polio season often coincided with the fly season • Poliomyelitis virus experimental transmission with filth flies and cockroaches in the 1940’s • Coxsackieviruses and Echoviruses also isolated from flies • Ultimately MT fo und to be minimal at best • Greenburg B., 1971 & 1973; Flies and disease; Vols. 1 & 2; Princeton Press

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Indirect mechanical transmission

• Viruses • Bacteria; Enteric = the important group, also can multiply in environments before or after transfer •Protozoa • Helminths

Enteric bacteria

• Exposed human feces and frequent exposure of food • Escherichia coli, Vibrio cholerae, Salmonella and Shigella frequently isolated from filth flies • Role of arthropods compared to direct fecal-oral (food handlers) or consumption of contaminated water

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Indirect mechanical transmission

• Viruses •Bacteria • PtProtozoa; C Ctysts of EtEntomoeb a hi hitltistolytica andthd others survive passage through flies • Helminths

Indirect mechanical transmission

• Viruses •Bacteria •Protozoa • Helminths; Eggs of 17 species recovered from flies, but epidemiological studies do not support a role for MT by insects

Contaminative mechanical transmission

Events followed by ingestion of contaminated vector or food

Agents Sources Vectors Botulism Carcasses Maggots Enteric pathogens Offal Flies feeding on carcasses Enteric pathogens Offal Flies feeding on animal food Enteric pathogens Feces Flies feeding on human food Enteric pathogens Feces Flies feeding on animal food Marek's Carcasses Beetles Enteric pathogens Feces Flies feeding on oral mucosa Nosocomial Off host Ants, roaches , flies infections secretions/fomites 12

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Direct mechanical transmission

• Helminths: filarids all require a biological vector •Protozoa • Bacteria • Viruses

Agents of disease with demonstrated direct mechanical transmission by haematophagous arthropods

• Over 50 with mechanical transmission as a major transmission mechanism • Over 35 associated with tabanids • Equine infectious anemia, anaplasmosis and trypanosomiasis

Feeding behavior favoring direct mechanical transmission

• Solenophagy vs. Telmophagy • Pain resulting in interrupted bloodmeals • Mobility (ticks vs. flies) transfer to a second host following and interrupted feeding • Secondary blood feeding

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Direct MT between 2 hosts

•Protozoa – Skin - Besnoitiosis – Blood - Trypanosomes, T. evansi and T. vivax

Besnoitiosis

• Etiology is the sporozoan Isospora besnoiti • Skin disease of cattle with thickened skin and oozing fissures • Africa, Europe, Asia, and South America • Millions of cysts in the dermis • Mechanical transmission by tabanids and stable flies

Sole mechanical transmission of blood-borne protozoans

• None for humans • Livestock; Trypanosoma evansi and T. vivax in the New World

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The horse strain of Trypanosoma evansi in the blood of a rat (photograph by Roberto A.M.S. Silva) 19

Trypanosomes

• T. evansi mechanically transmitted worldwide (tabanids and stable flies) • Wide host range: camels, equids and bovids • High mortality, anemia and ataxia • T. vivax mechanically transmitted in the New World (tabanids) but biologically by tsetse in Africa

Direct mechanical transmission

• Helminths •Protozoa •Bacteria • Viruses

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Direct MT between 2 hosts

•Bacteria

– Host secretions to wounds; Treponema pertenue (yaws)

– Host secretions to wounds made by other insects

– EibddEye secretions to abraded cornea

–Skin

– Blood

An early disseminated yaws lesion on a young boy (photograph by Leo Lanoie, courtesy of Wayne M. Meyers and Armed Forces Institute of Pathology) 23

Yaws

• Yaws is a common disease of children in the tropics caused by the spirochete Treponema pertenue • For centuries, flies (particularly eye gnats) have been implicated in transmission by first feeding on lesions and then at the sites of cuts or abrasions • Transmission can also be by direct skin-to-skin contact but the spirochete cannot penetrate normal skin • Yaws is promoted by overcrowding and poor hygiene • Yaws can be cured by a single shot of penicillin

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Direct MT between 2 hosts •Bacteria – Host secretions to wounds; Treponema pertenue (yaws) – Host secretions to wounds made by other insects; Summer mastitis – Eye secretions to abraded cornea; IBK-face flies, Chlamydia trachomatis- Musca and Hippelates, Haemophilus influenza - eye gnats several spp. of chloropids –Skin -Dermatophilus (ticks and biting flies) – Blood, anthrax, borreliosis, tularemia (tabanids)

Summer mastitis

• Combination of anaerobic bacteria, e.g. Actinomyces and Fusobacterium • Requires and entry portal - bite of horn fly or Hydrotea spp. • Then either direct transmission or secondary with non-biters

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Direct MT between 2 hosts

•Bacteria – Host secretions to wounds; Treponema pertenue (yaws) – Host secretions to wounds made by other insects; Summer mastitis – Eye secretions to abraded cornea; Infectious bovine keratitis - face flies, Trachoma - Musca and Hippelates –Skin -Dermatophilus (ticks and biting flies) – Blood, anthrax, borreliosis, tularemia, (tabanids)

Infectious bovine keratitis (pinkeye)

• Etiology Moraxella bovis often with concurrent infections • Highly contagious disease of cattle worldwide causing economic losses and potential blindness of cattle • M. bovis cannot penetrate the intact conjunctiva • The portal of entry can be caused by mechanical factors such as dust and insect feeding

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Trachoma

• Etiology Chlamydia trachoma • Affects over 400 million people worldwide • Conjunctivitis and potential blindness • Spread by direct contact or by Musca sorbens, M. domestica, and eye gnats

Direct MT between 2 hosts

•Bacteria – Host secretions to wounds; Treponema pertenue (yaws) – Host secretions to wounds made by other insects; Summer mastitis – Eye secretions to abraded cornea –Skin -Dermatophilus congolensis (biting flies) – Blood - tularemia, anaplasmosis, anthrax (tabanids)

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Tularemia (rabbit fever)

• Etiology Francisella tularensis • Zoonosis infecting wild and domestic animals • Humans fever, chills, respiratory symptoms and often an ulcer at the site of infection • Transmission direct contact with animals (particularly rabbit hunters), biological transmission by ticks in the south-central U.S., and mechanically transmitted by tabanids (Chrysops spp.) in the western U.S. but possibly by mosquitoes in Russia and Sweden • Reaches 107 bacteria per ml and shown to survive on mouthparts for over 24 hours; High potential for mechanical transmission by arthropods 34

Anaplasmosis

• Etiology Anaplasma marginale • Causes anemia, weakness, and high mortality in older cattle worldwide • Biological transmission by ticks in many areas leads to enzootic stability but mechanical transmission leading to disease outbreaks in the absence of tick vectors • High blood titers in acute cases with demonstration of transmission by a single tabanid

Anthrax

• Etiology Bacillus anthracis • Endospores endemic in many areas of the world ingestion is the route of infection for most herbivores • Bacteremia can exceed 108 per ml and mechanical transmission to susceptible hosts ()(including humans) resulting in cutaneous anthrax, pruritic vesicle and necrosis • Transmission demonstrated with tabanids, stable flies, horn flies and mosquitoes

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Direct MT between 2 hosts

• Viruses – Skin - poxviruses; Myxoma, fowlpox, capripox; Viruses stable on insect mouthparts so interrupted meals not required – Blood - Retroviruses, etc. - the model for interrupted/mixed meals

Fowlpox viruses

• Fowlpox viruses cause papules and scabs on both domestic and wild birds worldwide and can be fatal • Transmission within flocks directly between birds occurs due to pecking but insect transmission between flocks of both wild and domestic birds is important • Fowlpox viruses- stable on mouthparts of mosquitoes for 210 days • Primary vectors mosquitoes in many areas but biting midges (Culicoides spp.) also have been shown to be vectors

Myxoma virus

• Myxoma virus is maintained in the natural host population of rabbits of the genus Sylvilagus in the Americas by mechanical transmission by insects • Recognized as a highly contagious, fatal disease of domestic rabbits in the 1800’s • Introduced into Australia in the 1950’s to helppp in the control of feral European rabbit populations; Control was successful only in areas with mosquitoes • Accidentally introduced into Europe in 1952 with an epizootic with the European rabbit flea as the vector • European rabbit fleas later introduced into Australia which resulted in range expansion • Myxoma virus-vectors are mosquitoes, fleas, etc.; Stable on mouthparts up to 220 days; Virus titers are high within pox inclusion bodies in localized skin tumors which is not the case for smallpox virus 39

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Sole mechanical transmission of blood-borne viruses (1)

• None for humans • Livestock; Retroviruses are the primary ones • Can be demonstrated when viremia high for flaviviruses (Hog cholera virus), bunyaviruses (RVF), togaviruses (VEE), etc.; The importance has to be evaluated by each situation

Sole mechanical transmission of blood-borne viruses (2)

• Retroviruses of livestock: –EIAV – BLV –BIV

Bovine leukemia virus

• Onchovirus which are generally associated with chronic lymphomas and leukemia • BLV persistent lymphocytosis due to proliferation of lymphocyte clones, up to 104 per ml of blood • BLV, chronic disease of cattle, particularly dairy cattle • Transmission, horizontal via iatrogenic transmission associated with tattooing and the multiple use of needles and surgical instruments • Experimental transmission with groups of tabanids 42

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Equine infectious anemia virus

• Lentivirus associated with immunodeficiency, inflammatory and hemolytic diseases • EIAV infects equids worldwide and is transmitted by the horizontal transfer of blood iatrogenically or by insects • Infection can result in an acute fatal febrile, anemic disease in which the virus reaches 106 per ml of blood; A chronic disease with recurrent fevers and virus levels approaching 104 per ml lasting up to 1 year • There also are inapparent carriers that harbor the virus at low levels for long periods • Experimental transmission of the virus has repeatedly been demonstrated with a single tabanid 43

Mechanically transmitted pathogens

• High levels in the environment (enteric bacteria) or in the infected host (EIAV) • Stable in the environment or on or within arthropods (poxviruses)

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Hosts susceptible for mechanically transmitted diseases

• Indirect mechanical transmission - crowded hosts (displaced humans and confined animals) and exposed feces • Direct mechanical transmission hosts without shelter exposed to large populations of insects (livestock and impoverished humans)

Efficient arthropod vectors

• Indirect mechanical transmission – feed on contaminated wastes and highly mobile (filth flies) • Direct mechanical transmission – feed on host secretions (eye gnats) or blood (tabanids) and highly mobile

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Probability of a transmission event for a blood-borne pathogen

• Infected host: 1 infectious dose per ml - transfusion 106 infectious dose per ml - needles

• Arthropods (number and percent that have mixed meals) • Susceptible host

• Desquesnes, M., F. Biteau-Coroller, J. Bouyer, M.L. Dia, and L.D. Foil; 2009; Development of a mathematical model for mechanical transmission trypanosomes and other pathogens of cattle transmitted by tabanids; Int J Parasitol. 39 (3): 333-346

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53 rn to host Percent retu Percent

Distance between hosts (meters) 54

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Infectivity of donor blood

Practical applications

• Other than vector control: – For EIAV - reduce the reuse of needles and separate infected horses from susceptible horses by at least 200 yards – For BLV - eliminate animals with PL – For HIV - mechanical transmission by insects not important

The screen versions of these slides have full details of copyright and acknowledgements 20 Mechanical Transmission of Disease Agents by Arthropods Professor Lane Foil

Legend Host factors

Vector factors Agent factors

Acknowledgements

Colleagues, students, and technical support Charles Issel and W. V. Adams

• Foil, L.D. 1989; Tabanids as vectors of disease agents; Parasitol. Today; 5: 88-96 • Foil, L.D. and C.J. Issel; 1991; Transmission of retroviruses by arthropods; Annual Review of Entomology; 36: 355-381 • Foil, L.D. and J.R. Gorham; 2000; Mechanical transmission of disease agents by arthropods, In Medical Entomology: A textbook on public health and veterinary problems caused by arthropods; Kluwer Acedemic Publishers. Pp. 461-514

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