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Human behaviour and the epidemiology of parasitic zoonoses
Abstract
The behaviour of Homo sapiens has a pivotal role to play in the macro and microepidemiology of emerging or re-emerging parasitic zoonoses. Changing demographics and the concomitant alterations to the environment, climate, technology, land use and changes in human behavior, converge to favour the emergence and spread of parasitic zoonoses. The recent unprecedented movements of people, their animals and their parasites around the world, introduce and mix genes, cultural preferences, customs, and behavioral patterns. The increasing proclivity for eating meat, fish, crabs, shrimp, molluscs raw, undercooked, smoked, pickled or dried facilitates a number of protozoan (Toxoplasma), trematode (Fasciola sp., Paragonimus spp., Clonorchis sp., Opisthorchis spp., Heterophyes sp., Metagonimus sp., Echinostoma spp., Nanophyetus sp.) cestode (Taenia spp, Diphyllobothrum sp.) and nematode (Trichinella spp., Capillaria spp., Gnathostoma spp., Anisakis sp., Parastrongylus spp.) caused zoonoses. The increasing world population and the inability to keep pace with the provision of adequate sanitation and clean, safe drinking water, has led to an increased importance of waterborne zoonoses, such as those caused by Giardia, Cryptosporidium and Toxoplasma. Our close relationship with and the numerous uses to which we put companion animals and their ubiquitous distribution has resulted in dogs and cats unwitting participation in sharing over 60 parasite species including: Giardia, Cryptosporidium, Toxoplasma, most foodborne trematode species, Diphyllobothrum, Echinococcus spp., Ancylostoma and Toxocara. Changing human behaviour through education, to encourage the proper cooking of food, which may have cultural and social significance, will remain as challenging as controlling stray and feral pet populations, improving hygiene levels and the provision of safe drinking water and the proper use of sanctuary facilities. Long pre-patent periods and the normally insidious sub-clinical nature of most zoonoses makes advice requiring behavioural change for their control a difficult task. Our clearer understanding of the heterogeneity of susceptibility to infection, the complex genetic variations of people and parasite species and the development of molecular epidemiological tools is shedding more light on transmission routes and the spectrum of disease that is observed. Improved and new serological, molecular and imaging diagnostic tests and the development of broad spectrum chemotherapeutic agents has led to the attenuation of morbidity and mortality due to parasitic zoonoses in economically advantaged regions. Such advancements, in partnership with supportive behavioural change, has the potential for a sustainable global reduction in the burden of ill health due to parasitic zoonoses. Whether this will materialise is a challenge for us all.
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“but there is also a potential direct infection route to humans from raw meat (Macpherson 2005).”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Macpherson 2005
In the citing paper
“Several helminths and protozoa have been proposed as potential pathogenic risks for raw‐fed cats and dogs and/or for in‐contact owners and livestock.”
From Raw diets for dogs and cats: a review, with particular reference to microbiological hazards. (2019) · cites this paper as Macpherson 2005
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Human Waterborne Trematode and Protozoan Infections
Graczyk, T. K., & Fried, B. N. (2007) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(06)64002-5 · Cited by 54
“Currently, mammalian wildlife is recognized as a significant source of waterborne Cryptosporidium oocysts in a watershed (Macpherson, 2005).”
BackgroundTraversa, D., & Cesare, A. D. (2014) · Frontiers in Veterinary Science · doi:10.3389/fvets.2014.00011 · Cited by 53
Clinical Features of Bowel Anisakiasis in Japan
Yasunaga, H., Horiguchi, H., Kuwabara, K., Hashimoto, H., & Matsuda, S. (2010) · American Journal of Tropical Medicine and Hygiene · doi:10.4269/ajtmh.2010.09-0780 · Cited by 53
Knowledge and perceptions of dog-associated zoonoses: Brazos County, Texas, USA
Bingham, G. M., Budke, C. M., & Slater, M. R. (2009) · Preventive Veterinary Medicine · doi:10.1016/j.prevetmed.2009.09.019 · Cited by 53
Awadallah, M. A. I., & Salem, L. (2015) · Veterinary World · doi:10.14202/vetworld.2015.946-957 · Cited by 52
Saenna, P., Hurst, C. P., Echaubard, P., Wilcox, B. A., & Sripa, B. (2017) · Infectious Diseases of Poverty · doi:10.1186/s40249-017-0281-7 · Cited by 52
Genotyping of Giardia duodenalis from Southern Brown Howler Monkeys (Alouatta clamitans) from Brazil
Volotão, A. C. C., Júnior, J. C. S., Grassini, C. M., Peralta, J. M., & Fernandes, O. (2008) · Veterinary Parasitology · doi:10.1016/j.vetpar.2008.07.003 · Cited by 52
“Considering that monkeys and humans are both infected by the same genotypes of G. duodenalis, there is a potential public health risk for the traffic of G. duodenalis cysts to humans (Macpherson, 2005; Papini et al., 2007; Volotão et al., 2007).”
BackgroundHealth and the avoidance of macroparasites: a preliminary cross-cultural study
Prokop, P., Uşak, M., & Fančovičová, J. (2009) · Journal of Ethology · doi:10.1007/s10164-009-0195-3 · Cited by 52
“Parasites pose threats to the health of humans and cause serious disease problems or even deaths of millions of people a year (Macpherson 2005).”
BackgroundThe prevalence and intensity of gastrointestinal parasites of dogs in Ile-Ife, Nigeria
Sowemimo, O. A. (2008) · Journal of Helminthology · doi:10.1017/s0022149x08067229 · Cited by 50
Boylan, S. M. (2011) · Veterinary Clinics of North America Exotic Animal Practice · doi:10.1016/j.cvex.2011.05.003 · Cited by 51
“Cultural and socioeconomical factors predispose certain people to infection with the majority of fish-borne parasitic zoonoses occurring in lower-income countries.(18,20) The movement of aquaculture species has”
BackgroundEnes, J. E., Wages, A. J., Malone, J. B., & Tesana, S. (2010) · PubMed · Cited by 49
Molecular characterization of Toxocara spp. from soil of public areas in Ahvaz southwestern Iran
Khademvatan, S., Abdizadeh, R., & Tavalla, M. (2014) · Acta Tropica · doi:10.1016/j.actatropica.2014.03.016 · Cited by 49
A systematic review of zoonotic enteric parasitic diseases among nomadic and pastoral people
Barnes, A. N., Davaasuren, A., Baasandagva, U., & Gray, G. C. (2017) · PLoS ONE · doi:10.1371/journal.pone.0188809 · Cited by 49
Eiras, J. C., Pavanelli, G. C., Takemoto, R. M., & Nawa, Y. (2018) · Korean Journal of Parasitology · doi:10.3347/kjp.2018.56.3.215 · Cited by 49
“In addition to the cultural changes of eating habits, increase of global trading and traveling, expansion of fishing areas and development of cold transportation systems caused considerable changes in epidemiology of fish-borne parasitic zoonoses [40-44].”
BackgroundHost-parasite interactions under extreme climatic conditions
Martı́nez, J., & Merino, S. (2011) · Current Zoology · doi:10.1093/czoolo/57.3.390 · Cited by 51
Health Is Associated With Antiparasite Behavior and Fear of Disease-Relevant Animals in Humans
Prokop, P., Fančovičová, J., & Fedor, P. (2010) · Ecological Psychology · doi:10.1080/10407413.2010.496676 · Cited by 46
“Development of these items was based on the fact that poor hygiene and contact with companion animals or infected humans increases risk of parasite transmission (Hwang, Kiss, Ho, Leung, & Gundlapalli, 2008; Macpherson, 2005; Ramirez, Ward, & Sreevatsan, 2004).”
BackgroundFeline lungworms unlock a novel mode of parasite transmission
Colella, V., Giannelli, A., Brianti, E., Ramos, R. A. N., Cantacessi, C., Dantas‐Torres, F., & Otranto, D. (2015) · Scientific Reports · doi:10.1038/srep13105 · Cited by 46
Social Science Implications for Control of Helminth Infections in Southeast Asia
Vandemark, L. M., Jia, T.-W., & Zhou, X. (2010) · Advances in Parasitology/Advances in parasitology · doi:10.1016/s0065-308x(10)73006-2 · Cited by 46
Canine angiostrongylosis: recent advances in diagnosis, prevention, and treatment
Cesare, A. D., & Traversa, D. (2014) · Veterinary medicine · doi:10.2147/vmrr.s53641 · Cited by 41
Towards the comprehension of fasciolosis (re-)emergence: an integrative overview
Alba, A., Vázquez, A. A., & Hurtrez‐Boussès, S. (2020) · Parasitology · doi:10.1017/s0031182020002255 · Cited by 44
“Human behaviour is influenced by psycho-social factors such as ethnicity, culture and religion, which relate to every aspect of our lives including food choice and preparation, and determine the range and level of exposure to parasites (Macpherson, 2005).”
BackgroundInfluentialPennisi, M. G., Hartmann, K., Addie, D., Boucraut‐Baralon, C., Egberink, H. F., Frymus, T., Gruffydd-Jones, T., Horzinek, M. C., Hosie, M. J., Lloret, A., et al. (2015) · Journal of Feline Medicine and Surgery · doi:10.1177/1098612x15588455 · Cited by 47
Giraudet, C., Liu, K., McElligott, A. G., & Cobb, M. (2022) · PeerJ · doi:10.7717/peerj.14532 · Cited by 50
“Dog transmitted infections often go unnoticed ( Macpherson, 2005 ).”
BackgroundInfectious diseases in North Africa and North African immigrants to Europe
Khyatti, M., Trimbitas, R.-D., Zouheir, Y., Benani, A., Messaoudi, M. D. E., & Hemminki, K. (2014) · European Journal of Public Health · doi:10.1093/eurpub/cku109 · Cited by 42
The epidemiology and control of Toxocara canis in puppies
Schwartz, R., Bidaisee, S., Fields, P. J., Macpherson, M. L. A., & Macpherson, C. N. L. (2021) · Parasite Epidemiology and Control · doi:10.1016/j.parepi.2021.e00232 · Cited by 50
“This would require behavioral changes which have proven to be difficult for most parasitic disease control programs (Macpherson, 2005).”
BackgroundSelf-citationAlho, A. M., Lima, C., Colella, V., Madeira de Carvalho, L., Otranto, D., & Cardoso, L. (2018) · Parasites & Vectors · doi:10.1186/s13071-018-2720-0 · Cited by 57
“Known risk factors for infection include lack of regular and efficient application of endo- and ectoparasiticides, absence of routine vaccination programs, poor hygiene practices, low socio-economic factors and education, high animal density, improper cooking of food, geophagia (especially in children), failure to reg…”
BackgroundBorhani, M., Fathi, S., Harandi, M. F., Casulli, A., Ding, J., Liu, M., Zhang, W., & Wen, H. (2024) · Parasites & Vectors · doi:10.1186/s13071-024-06581-2 · Cited by 40
“To effectively evaluate the CE status in areas where it prevails, the utilization of portable ultrasound devices and hospital registry records can play a pivotal role in conducting regular and active mass screening surveys [161].”
Kong, Q., Fan, L., Zhang, J., Akao, N., Dong, K., Lou, D., Ding, J., Tong, Q., Zheng, B., Chen, R., et al. (2015) · International Journal of Food Microbiology · doi:10.1016/j.ijfoodmicro.2015.01.007 · Cited by 39
“Larvae belonging to the two latter genera are with weak invasive potential and case reports attributed to these two genera are rare (Macpherson, 2005).”
BackgroundA molecular survey on cystic echinococcosis in Sinnar area, Blue Nile state (Sudan).
Ibrahim, K. M., Romig, T., Kern, P., & Omer, R. A. (2011) · PubMed · Cited by 39
Existence of Angiostrongylus cantonensis in rats (Rattus norvegicus) in Grenada, West Indies
Chikweto, A., Bhaiyat, M. I., Macpherson, C. N. L., DeAllie, C., Pinckney, R., Richards, C., & Sharma, R. (2009) · Veterinary Parasitology · doi:10.1016/j.vetpar.2009.02.020 · Cited by 39
“This parasite has spread geographically in recent years with the dissemination of one of its intermediate hosts, the giant African land snail (Achatina fulica), which is a popular item of food in some countries (Macpherson, 2005) and by ships infested with rats (Wang et al.”
BackgroundSelf-citationProtozoa interaction with aquatic invertebrate: interest for watercourses biomonitoring
Ladeiro, M. P., Bigot‐Clivot, A., Aubert, D., Hohweyer, J., Favennec, L., Villena, I., & Geffard, A. (2012) · Environmental Science and Pollution Research · doi:10.1007/s11356-012-1189-1 · Cited by 38
“However, one in two person of the world was affected by waterborne or foodborne parasitic zoonoses (Macpherson 2005).”
BackgroundRibeiro, F. S., Nichols, E., Morato, R. G., Metzger, J. P., & Pardini, R. (2018) · Diversity and Distributions · doi:10.1111/ddi.12845 · Cited by 37
“…domestic/agropastoral areas and native forests, dogs may occupy a relatively unique role in disease transmission both to wildlife and to humans (Macpherson, 2005), particularly given the low rates of reported preventative (vaccination) and therapeutic (parasite treatment) care of dogs by…”
BackgroundProspects and Challenges towards Sustainable Liver Fluke Control
Sripa, B., & Echaubard, P. (2017) · Trends in Parasitology · doi:10.1016/j.pt.2017.06.002 · Cited by 36
“Human eating behavior is known to be influenced by a variety of factors, including ethnicity, culture, religion, age, and gender [41].”
Harvey, T. V., Tang, A., Sevá, A. D. P., dos Santos, C. A., Carvalho, S. M. S., da Rocha, C. M. B. M., Oliveira, B. C. M., & Albuquerque, G. R. (2020) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0008378 · Cited by 35
PARK, J.-K., Kim, K., Kang, S., Jeon, H.-K., KIM, J.-H., Littlewood, D. T. J., & Eom, K. S. (2006) · Parasitology · doi:10.1017/s003118200600206x · Cited by 36
“It is also rec- ognized as an emerging disease in some countries (e.g. in Brazil) (Sampaio et al. 2005), as develop- ments in mariculture, the world trade in fish and fish products, and the trend for humans to eat raw fish (e.g. see Macpherson, 2005), increases the incidence of diphyllobothriasis.”
BackgroundBurniston, S., Okello, A. L., Khamlome, B., Inthavong, P., Gilbert, J. R., Blacksell, S. D., Allen, J., & Welburn, S. C. (2015) · Infectious Diseases of Poverty · doi:10.1186/2049-9957-4-11 · Cited by 34
“infections [47,54-57].”
Hegglin, D., Bontadina, F., Gloor, S., Romig, T., Deplazes, P., & Kern, P. (2008) · BMC Public Health · doi:10.1186/1471-2458-8-247 · Cited by 34
Souza, J. B. B., de Assis-Silva, Z. M., Alves-Ribeiro, B. S., Moraes, I. D. S., Alves-Sobrinho, A. V., Saturnino, K. C., Ferraz, H. T., Machado, M. R. F., Braga, Í. A., & Ramos, D. G. D. S. (2023) · Veterinary Sciences · doi:10.3390/vetsci10080492 · Cited by 32
Urdaneta-Morales, S. (2014) · Frontiers in Public Health · doi:10.3389/fpubh.2014.00265 · Cited by 32
Synthesising 30 Years of Mathematical Modelling of Echinococcus Transmission
Occhipinti, J., Williams, G. M., Yakob, L., Clements, A., Barnes, T. S., McManus, D. P., Yang, Y. R., & Gray, D. J. (2013) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0002386 · Cited by 32
“granulosus, human behavioural factors play an important role in the exposure of dogs to infectious material, either through poor dog control and hence increased scavenging behaviour, or by deliberately feeding dogs the offal from infected intermediate hosts [60].”
Background
Metadata
- Authors
- Macpherson, C. N. L.
- Affiliations
- St. George's University (GD)
- Corresponding author
- Macpherson, Calum N.L.
- Venue
- International Journal for Parasitology
- Publisher
- Elsevier BV
- Published
- 2005-10
- Volume
- 35
- Issue
- 11-12
- Pages
- 1319-1331
- ISSN
- 0020-7519 (ISSN-L)
- OpenAlex
- W2120235087
- Cited by
- 431
- References
- 112
- Citations by year
- 2026: 15 · 2025: 15 · 2024: 19 · 2023: 26 · 2022: 44 · 2021: 21 · 2020: 21 · 2019: 21 · 2018: 18 · 2017: 22 · 2016: 23 · 2015: 29 · 2014: 26 · 2013: 19 · 2012: 15
- FWCI
- 2.41
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- International Journal for Parasitology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Immunology and Microbiology › Parasitology › Parasitic infections in humans and animals
- Health Sciences › Medicine › Public Health, Environmental and Occupational Health › Zoonotic diseases and public health
- Life Sciences › Immunology and Microbiology › Parasitology › Helminth infection and control
- Keywords
- parasitic zoonoses, human behavior, emerging infectious diseases, foodborne zoonoses, companion animals, Giardia, Cryptosporidium, Toxoplasma, trematodes, cestodes, nematodes, behavior change, molecular epidemiology, parasite transmission, zoonosis control, Trichinella
- MeSH terms
- Animals, Animals, Domestic, Behavior, Communicable Diseases, Humans, Parasitic Diseases, Parasitology, Plants, Zoonoses, Prevalence, Food Chain
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