COVID-19 morbidity in lower versus higher income populations underscores the need to restore lost biodiversity of eukaryotic symbionts
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
36785786
PubMed Central
PMC9908430
DOI
10.1016/j.isci.2023.106167
PII: S2589-0042(23)00244-4
Knihovny.cz E-zdroje
- Klíčová slova
- Biological sciences, Health sciences, Virology,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
The avoidance of infectious disease by widespread use of 'systems hygiene', defined by hygiene-enhancing technology such as sewage systems, water treatment facilities, and secure food storage containers, has led to a dramatic decrease in symbiotic helminths and protists in high-income human populations. Over a half-century of research has revealed that this 'biota alteration' leads to altered immune function and a propensity for chronic inflammatory diseases, including allergic, autoimmune and neuropsychiatric disorders. A recent Ethiopian study (EClinicalMedicine 39: 101054), validating predictions made by several laboratories, found that symbiotic helminths and protists were associated with a reduced risk of severe COVID-19 (adjusted odds ratio = 0.35; p<0.0001). Thus, it is now apparent that 'biome reconstitution', defined as the artificial re-introduction of benign, symbiotic helminths or protists into the ecosystem of the human body, is important not only for alleviation of chronic immune disease, but likely also for pandemic preparedness.
Zobrazit více v PubMed
Rook G.A.W., Raison C.L., Lowry C.A. Microbial 'old friends', immunoregulation and socioeconomic status. Clin. Exp. Immunol. 2014;177:1–12. doi: 10.1111/cei.12269. PubMed DOI PMC
Maizels R.M. Infections and allergy - helminths, hygiene and host immune regulation. Curr. Opin. Immunol. 2005;17:656–661. PubMed
Parker W., Sarafian J.T., Broverman S.A., Laman J.D. Between a hygiene rock and a hygienic hard place: avoiding SARS-CoV-2 while needing environmental exposures for immunity. Evol. Med. Public Health. 2021;9:120–130. doi: 10.1093/emph/eoab006. PubMed DOI PMC
Sher A., Gazzinelli R.T., Oswald I.P., Clerici M., Kullberg M., Pearce E.J., Berzofsky J.A., Mosmann T.R., James S.L., Morse H.C., 3rd Role of T-cell derived cytokines in the downregulation of immune responses in parasitic and retroviral infection. Immunol. Rev. 1992;127:183–204. PubMed
Maizels R.M., Bundy D.A., Selkirk M.E., Smith D.F., Anderson R.M. Immunological modulation and evasion by helminth parasites in human populations. Nature. 1993;365:797–805. PubMed
Rook G.A.W. Review series on helminths, immune modulation and the hygiene hypothesis: the broader implications of the hygiene hypothesis. Immunology. 2009;126:3–11. PubMed PMC
Rook G.A.W. The hygiene hypothesis and the increasing prevalence of chronic inflammatory disorders. Trans. R. Soc. Trop. Med. Hyg. 2007;101:1072–1074. PubMed
Bickler S.W., DeMaio A. Western diseases: current concepts and implications for pediatric surgery research and practice. Pediatr. Surg. Int. 2008;24:251–255. PubMed
Hays R., Pierce D., Giacomin P., Loukas A., Bourke P., McDermott R. Helminth coinfection and COVID-19: an alternate hypothesis. PLoS Negl. Trop. Dis. 2020;14:e0008628. doi: 10.1371/journal.pntd.0008628. PubMed DOI PMC
Cepon-Robins T.J., Gildner T.E. Old friends meet a new foe: a potential role for immune-priming parasites in mitigating COVID-19 morbidity and mortality. Evol. Med. Public Health. 2020;2020:234–248. doi: 10.1093/emph/eoaa037. PubMed DOI PMC
Parker W., Laman J.D., Wolday D., Rinke de Wit T.F. The Evolution and Medicine Review. 2021. Evolutionary medicine helps explain pandemic dynamics: predictions regarding clinical impact of COVID-19 borne out.
Fonte L., Acosta A., Sarmiento M.E., Ginori M., García G., Norazmi M.N. COVID-19 lethality in sub-saharan Africa and helminth immune modulation. Front. Immunol. 2020;11:574910. doi: 10.3389/fimmu.2020.574910. PubMed DOI PMC
Siles-Lucas M., González-Miguel J., Geller R., Sanjuan R., Pérez-Arévalo J., Martínez-Moreno Á. Potential influence of helminth molecules on COVID-19 pathology. Trends Parasitol. 2021;37:11–14. doi: 10.1016/j.pt.2020.10.002. PubMed DOI PMC
Wolday D., Tasew G., Amogne W., Urban B., Schallig H.D., Harris V., Rinke de Wit T.F. Interrogating the impact of intestinal parasite-microbiome on pathogenesis of COVID-19 in sub-saharan Africa. Front. Microbiol. 2021;12:614522. doi: 10.3389/fmicb.2021.614522. PubMed DOI PMC
Paniz-Mondolfi A.E., Ramírez J.D., Delgado-Noguera L.A., Rodriguez-Morales A.J., Sordillo E.M. COVID-19 and helminth infection: beyond the Th1/Th2 paradigm. PLoS Negl. Trop. Dis. 2021;15:e0009402. doi: 10.1371/journal.pntd.0009402. PubMed DOI PMC
Kircheis R., Schuster M., Planz O. COVID-19: mechanistic model of the African paradox supports the central role of the NF-κB pathway. Viruses. 2021;13:1887. doi: 10.3390/v13091887. PubMed DOI PMC
Parker W., Sarafian J.T., Broverman S.A., Laman J.D. Authors' response to Graham Rook's commentary. Evol. Med. Public Health. 2021;9:206–207. doi: 10.1093/emph/eoab012. PubMed DOI PMC
Rook G.A.W. Comment on Parker et al. (Evolution, Medicine and Public Health 2021;9:120-30) Evol. Med. Public Health. 2021;9:192–193. doi: 10.1093/emph/eoab011. PubMed DOI PMC
Wolday D., Gebrecherkos T., Arefaine Z.G., Kiros Y.K., Gebreegzabher A., Tasew G., Abdulkader M., Abraha H.E., Desta A.A., Hailu A., et al. Effect of co-infection with intestinal parasites on COVID-19 severity: a prospective observational cohort study. EClinicalMedicine. 2021;39:101054. doi: 10.1016/j.eclinm.2021.101054. PubMed DOI PMC
Walker P.G.T., Whittaker C., Watson O.J., Baguelin M., Winskill P., Hamlet A., Djafaara B.A., Cucunubá Z., Olivera Mesa D., Green W., et al. The impact of COVID-19 and strategies for mitigation and suppression in low- and middle-income countries. Science. 2020;369:413–422. doi: 10.1126/science.abc0035. PubMed DOI PMC
Pal R., Yadav U. COVID-19 pandemic in India: present scenario and a steep climb ahead. J. Prim. Care Community Health. 2020;11 doi: 10.1177/2150132720939402. 2150132720939402. PubMed DOI PMC
Mallapaty S. Scientists fear coronavirus spread in countries least able to contain it. Nature. 2020;578:348. doi: 10.1038/d41586-020-00405-w. PubMed DOI
Ntoumi F., Velavan T.P. COVID-19 in Africa: between hope and reality. Lancet Infect. Dis. 2021;21:315. doi: 10.1016/s1473-3099(20)30465-5. PubMed DOI PMC
Ssentongo P., Fronterre C., Geronimo A., Greybush S.J., Mbabazi P.K., Muvawala J., Nahalamba S.B., Omadi P.O., Opar B.T., Sinnar S.A., et al. Tracking and predicting the African COVID-19 pandemic. medRxiv. 2020 doi: 10.1101/2020.11.13.20231241. Preprint at. PubMed DOI
Lone S.A., Ahmad A. COVID-19 pandemic - an African perspective. Emerg. Microbes Infect. 2020;9:1300–1308. doi: 10.1080/22221751.2020.1775132. PubMed DOI PMC
Cardoso E.H.S., Silva M.S.D., De Albuquerque Felix Junior F.E., De Carvalho S.V., De Carvalho A., Vijaykumar N., Frances C.R.L. Characterizing the impact of social inequality on COVID-19 propagation in developing countries. IEEE Access. 2020;8:172563–172580. doi: 10.1109/ACCESS.2020.3024910. PubMed DOI PMC
Dahab M., van Zandvoort K., Flasche S., Warsame A., Ratnayake R., Favas C., Spiegel P.B., Waldman R.J., Checchi F. COVID-19 control in low-income settings and displaced populations: what can realistically be done? Confl. Health. 2020;14:54. doi: 10.1186/s13031-020-00296-8. PubMed DOI PMC
Halpert G., Shoenfeld Y. SARS-CoV-2, the autoimmune virus. Autoimmun. Rev. 2020;19:102695. doi: 10.1016/j.autrev.2020.102695. PubMed DOI PMC
Preston P.J. The biology of the atopic response. J. R. Nav. Med. Serv. 1970;56:229–235. PubMed
Greenwood B.M. Autoimmune disease and parasitic infections in Nigerians. Lancet. 1968;2:380–382. doi: 10.1016/s0140-6736(68)90595-3. PubMed DOI
Greenwood B.M., Herrick E.M., Voller A. Can parasitic infection suppress autoimmune disease? Proc. R. Soc. Med. 1970;63:19–20. PubMed PMC
Greenwood B.M., Herrick E.M., Voller A. Suppression of autoimmune disease in NZB and (NZB x NZW) F1 hybrid mice by infection with malaria. Nature. 1970;226:266–267. doi: 10.1038/226266a0. PubMed DOI
Greenwood B.M., Voller A., Herrick E.M. Suppression of adjuvant arthritis by infection with a strain of the rodent malaria parasite Plasmodium berghei. Ann. Rheum. Dis. 1970;29:321–323. doi: 10.1136/ard.29.3.321. PubMed DOI PMC
Parker W., Ollerton J. Evolutionary biology and anthropology suggest biome reconstitution as a necessary approach toward dealing with immune disorders. Evol. Med. Public Health. 2013;2013:89–103. doi: 10.1093/emph/eot008. PubMed DOI PMC
Bilbo S.D., Wray G.A., Perkins S.E., Parker W. Reconstitution of the human biome as the most reasonable solution for epidemics of allergic and autoimmune diseases. Med. Hypotheses. 2011;77:494–504. doi: 10.1016/j.mehy.2011.06.019. PubMed DOI
Parker W., Perkins S.E., Harker M., Muehlenbein M.P. A prescription for clinical immunology: the pills are available and ready for testing. Curr. Med. Res. Opin. 2012;28:1193–1202. doi: 10.1185/03007995.2012.695731. PubMed DOI
Pearson, L.A., and Neilan, B.A. Protozoan diversity and biogeography. In eLS, pp. 1-7. 10.1002/9780470015902.a0029329
Yatsunenko T., Rey F.E., Manary M.J., Trehan I., Dominguez-Bello M.G., Contreras M., Magris M., Hidalgo G., Baldassano R.N., Anokhin A.P., et al. Human gut microbiome viewed across age and geography. Nature. 2012;486:222–227. http://www.nature.com/nature/journal/v486/n7402/abs/nature11053.html#supplementary-information PubMed PMC
You C., Jirků M., Corcoran D.L., Parker W., Jirků-Pomajbíková K. Altered gut ecosystems plus the microbiota's potential for rapid evolution: a recipe for inevitable change with unknown consequences. Comput. Struct. Biotechnol. J. 2021;19:5969–5977. doi: 10.1016/j.csbj.2021.10.033. PubMed DOI PMC
Venkatakrishnan A., Holzknecht Z.E., Holzknecht R., Bowles D.E., Kotzé S.H., Modliszewski J.L., Parker W. Evolution of bacteria in the human gut in response to changing environments: an invisible player in the game of health. Comput. Struct. Biotechnol. J. 2021;19:752–758. doi: 10.1016/j.csbj.2021.01.007. PubMed DOI PMC
Sonnenburg E.D., Smits S.A., Tikhonov M., Higginbottom S.K., Wingreen N.S., Sonnenburg J.L. Diet-induced extinctions in the gut microbiota compound over generations. Nature. 2016;529:212–215. doi: 10.1038/nature16504. PubMed DOI PMC
Atta A.M., D'Oliveira, Correa J., Atta M.L., Almeida R.P., Carvalho E.M. Anti-leishmanial IgE antibodies: a marker of active disease in visceral leishmaniasis. Am. J. Trop. Med. Hyg. 1998;59:426–430. doi: 10.4269/ajtmh.1998.59.426. PubMed DOI
Lu F., Huang S. The roles of mast cells in parasitic Protozoan infections. Front. Immunol. 2017;8:363. doi: 10.3389/fimmu.2017.00363. PubMed DOI PMC
O'Connell E.M., Nutman T.B. Eosinophilia in infectious diseases. Immunol. Allergy Clin. North Am. 2015;35:493–522. doi: 10.1016/j.iac.2015.05.003. PubMed DOI PMC
Denkers E.Y., Schneider A.G., Cohen S.B., Butcher B.A. Phagocyte responses to protozoan infection and how Toxoplasma gondii meets the challenge. PLoS Pathog. 2012;8:e1002794. doi: 10.1371/journal.ppat.1002794. PubMed DOI PMC
Manfredi A.A., Ramirez G.A., Rovere-Querini P., Maugeri N. The neutrophil's choice: phagocytose vs make neutrophil extracellular traps. Front. Immunol. 2018;9:288. doi: 10.3389/fimmu.2018.00288. PubMed DOI PMC
Yassour M., Jason E., Hogstrom L.J., Arthur T.D., Tripathi S., Siljander H., Selvenius J., Oikarinen S., Hyöty H., Virtanen S.M., et al. Strain-level analysis of mother-to-child bacterial transmission during the first few months of life. Cell Host Microbe. 2018;24:146–154.e4. doi: 10.1016/j.chom.2018.06.007. PubMed DOI PMC
Turnbaugh P.J., Ridaura V.K., Faith J.J., Rey F.E., Knight R., Gordon J.I. The effect of diet on the human gut microbiome: a metagenomic analysis in humanized gnotobiotic mice. Sci. Transl. Med. 2009;1:6ra14. doi: 10.1126/scitranslmed.3000322. PubMed DOI PMC
Heisel T., Montassier E., Johnson A., Al-Ghalith G., Lin Y.-W., Wei L.-N., Knights D., Gale C.A. High-fat diet changes fungal microbiomes and interkingdom relationships in the murine gut. mSphere. 2017;2:00351-17. doi: 10.1128/mSphere.00351-17. PubMed DOI PMC
Jeziorek M., Frej-Mądrzak M., Choroszy-Król I. The influence of diet on gastrointestinal Candida spp. colonization and the susceptibility of Candida spp. to antifungal drugs. Rocz. Panstw. Zakl. Hig. 2019;70:195–200. doi: 10.32394/rpzh.2019.0070. PubMed DOI
Yazdanbakhsh M., Kremsner P.G., van Ree R. Allergy, parasites, and the hygiene hypothesis. Science. 2002;296:490–494. PubMed
Helmby H. Helminths and our immune system: friend or foe? Parasitol. Int. 2009;58:121–127. PubMed
Weinstock J.V., Elliott D.E. Helminth infections decrease host susceptibility to immune-mediated diseases. J. Immunol. 2014;193:3239–3247. doi: 10.4049/jimmunol.1400927. PubMed DOI PMC
Versini M., Jeandel P.Y., Bashi T., Bizzaro G., Blank M., Shoenfeld Y. Unraveling the Hygiene Hypothesis of helminthes and autoimmunity: origins, pathophysiology, and clinical applications. BMC Med. 2015;13:81. doi: 10.1186/s12916-015-0306-7. PubMed DOI PMC
Smallwood T.B., Giacomin P.R., Loukas A., Mulvenna J.P., Clark R.J., Miles J.J. Helminth immunomodulation in autoimmune disease. Front. Immunol. 2017;8:453. doi: 10.3389/fimmu.2017.00453. PubMed DOI PMC
Liu J., Morey R.A., Wilson J.K., Parker W. Practices and outcomes of self-treatment with helminths based on physicians' observations. J. Helminthol. 2016;91:267–277. PubMed
Kou H.H., Parker W. Intestinal worms eating neuropsychiatric disorders? Brain Res. 2018;1693:218–221. doi: 10.1016/j.brainres.2018.01.023. PubMed DOI
Williamson L.L., McKenney E.A., Holzknecht Z.E., Belliveau C., Rawls J.F., Poulton S., Parker W., Bilbo S.D. Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection. Brain Behav. Immun. 2016;51:14–28. doi: 10.1016/j.bbi.2015.07.006. PubMed DOI
Blecharz-Klin K., Świerczyńska M., Piechal A., Wawer A., Joniec-Maciejak I., Pyrzanowska J., Wojnar E., Zawistowska-Deniziak A., Sulima-Celińska A., Młocicki D., Mirowska-Guzel D. Infection with intestinal helminth (Hymenolepis diminuta) impacts exploratory behavior and cognitive processes in rats by changing the central level of neurotransmitters. PLoS Pathog. 2022;18:e1010330. doi: 10.1371/journal.ppat.1010330. PubMed DOI PMC
Noel S.C., Fortin-Hamel L., Haque M., Scott M.E. Maternal gastrointestinal nematode infection enhances spatial memory of uninfected juvenile mouse pups. Sci. Rep. 2022;12:9796. doi: 10.1038/s41598-022-13971-y. PubMed DOI PMC
Ehrenfeld M., Tincani A., Andreoli L., Cattalini M., Greenbaum A., Kanduc D., Alijotas-Reig J., Zinserling V., Semenova N., Amital H., Shoenfeld Y. Covid-19 and autoimmunity. Autoimmun. Rev. 2020;19:102597. doi: 10.1016/j.autrev.2020.102597. PubMed DOI PMC
Adjobimey T., Meyer J., Terkeš V., Parcina M., Hoerauf A. Helminth antigens differentially modulate the activation of CD4+ and CD8+ T lymphocytes of convalescent COVID-19 patients in vitro. BMC Med. 2022;20:241. doi: 10.1186/s12916-022-02441-x. PubMed DOI PMC
Kalinkovich A., Weisman Z., Greenberg Z., Nahmias J., Eitan S., Stein M., Bentwich Z. Decreased CD4 and increased CD8 counts with T cell activation is associated with chronic helminth infection. Clin. Exp. Immunol. 1998;114:414–421. doi: 10.1046/j.1365-2249.1998.00736.x. PubMed DOI PMC
Rolot M., Dougall A.M., Chetty A., Javaux J., Chen T., Xiao X., Machiels B., Selkirk M.E., Maizels R.M., Hokke C., et al. Helminth-induced IL-4 expands bystander memory CD8(+) T cells for early control of viral infection. Nat. Commun. 2018;9:4516. doi: 10.1038/s41467-018-06978-5. PubMed DOI PMC
Lin J.S., Mohrs K., Szaba F.M., Kummer L.W., Leadbetter E.A., Mohrs M. Virtual memory CD8 T cells expanded by helminth infection confer broad protection against bacterial infection. Mucosal Immunol. 2019;12:258–264. doi: 10.1038/s41385-018-0100-x. PubMed DOI PMC
Samaddar A., Gadepalli R., Nag V.L., Misra S. The enigma of low COVID-19 fatality rate in India. Front. Genet. 2020;11:854. doi: 10.3389/fgene.2020.00854. PubMed DOI PMC
Jain V.K., Iyengar K., Vaish A., Vaishya R. Differential mortality in COVID-19 patients from India and western countries. Diabetes Metab. Syndr. 2020;14:1037–1041. doi: 10.1016/j.dsx.2020.06.067. PubMed DOI PMC
Chinnaswamy S. SARS-CoV-2 infection in India bucks the trend: trained innate immunity? Am. J. Hum. Biol. 2021;33:e23504. doi: 10.1002/ajhb.23504. PubMed DOI PMC
Chibwana M.G., Jere K.C., Kamng'ona R., Mandolo J., Katunga-Phiri V., Tembo D., Mitole N., Musasa S., Sichone S., Lakudzala A., et al. High SARS-CoV-2 seroprevalence in Health Care Workers but relatively low numbers of deaths in urban Malawi. medRxiv. 2020 doi: 10.1101/2020.07.30.20164970. Preprint at. DOI
Chatterjee B K.R., Mande S.C. The mortality due to COVID-19 in different nations is associated with the demographic character of nations and the prevalence of autoimmunity. medRxiv. 2020 doi: 10.1101/2020.07.31.20165696. Preprint at. DOI
Mbow M., Lell B., Jochems S.P., Cisse B., Mboup S., Dewals B.G., Jaye A., Dieye A., Yazdanbakhsh M. COVID-19 in Africa: dampening the storm? Science. 2020;369:624–626. doi: 10.1126/science.abd3902. PubMed DOI
Chatterjee B., Karandikar R.L., Mande S.C. Mortality due to COVID-19 in different countries is associated with their demographic character and prevalence of autoimmunity. Curr. Sci. 2021;120:501–508.
Chatterjee P. Is India missing COVID-19 deaths? Lancet. 2020;396:657. doi: 10.1016/S0140-6736(20)31857-2. PubMed DOI PMC
Correale J., Farez M., Razzitte G. Helminth infections associated with multiple sclerosis induce regulatory B cells. Ann. Neurol. 2008;64:187–199. PubMed
Correale J., Farez M. Association between parasite infection and immune responses in multiple sclerosis. Ann. Neurol. 2007;61:97–108. PubMed
Correale J., Farez M.F. The impact of parasite infections on the course of multiple sclerosis. J. Neuroimmunol. 2011;233:6–11. PubMed
Cheng A.M., Jaint D., Thomas S., Wilson J.K., Parker W. Overcoming evolutionary mismatch by self-treatment with helminths: current practices and experience. J. Evol. Med. 2015;3:1–22.
Smyth K., Morton C., Mathew A., Karuturi S., Haley C., Zhang M., Holzknecht Z.E., Swanson C., Lin S.S., Parker W. Production and use of Hymenolepis diminuta cysticercoids as anti-inflammatory therapeutics. J. Clin. Med. 2017;6:98. doi: 10.3390/jcm6100098. PubMed DOI PMC
Medeiros M., Jr., Figueiredo J.P., Almeida M.C., Matos M.A., Araújo M.I., Cruz A.A., Atta A.M., Rego M.A.V., de Jesus A.R., Taketomi E.A., Carvalho E.M. Schistosoma mansoni infection is associated with a reduced course of asthma. J. Allergy Clin. Immunol. 2003;111:947–951. doi: 10.1067/mai.2003.1381. PubMed DOI
Leonardi-Bee J., Pritchard D., Britton J. Asthma and current intestinal parasite infection: systematic review and meta-analysis. Am. J. Respir. Crit. Care Med. 2006;174:514–523. doi: 10.1164/rccm.200603-331OC. PubMed DOI
Broadhurst M.J., Leung J.M., Kashyap V., McCune J.M., Mahadevan U., McKerrow J.H., Loke P. IL-22+ CD4+ T cells are associated with therapeutic Trichuris trichiura infection in an ulcerative colitis patient. Sci. Transl. Med. 2010;2:60ra88. doi: 10.1126/scitranslmed.3001500. PubMed DOI
Wolff M.J., Broadhurst M.J., Loke P. Helminthic therapy: improving mucosal barrier function. Trends Parasitol. 2012;28:187–194. doi: 10.1016/j.pt.2012.02.008. PubMed DOI PMC
Croese J., O'Neil J., Masson J., Cooke S., Melrose W., Pritchard D., Speare R. A proof of concept study establishing Necator americanus in Crohn's patients and reservoir donors. Gut. 2006;55:136–137. PubMed PMC
Feary J., Venn A., Brown A., Hooi D., Falcone F.H., Mortimer K., Pritchard D.I., Britton J. Safety of hookworm infection in individuals with measurable airway responsiveness: a randomized placebo-controlled feasibility study. Clin. Exp. Allergy. 2009;39:1060–1068. PubMed PMC
Feary J.R., Venn A.J., Mortimer K., Brown A.P., Hooi D., Falcone F.H., Pritchard D.I., Britton J.R. Experimental hookworm infection: a randomized placebo-controlled trial in asthma. Clin. Exp. Allergy. 2010;40:299–306. PubMed PMC
Daveson A.J., Jones D.M., Gaze S., McSorley H., Clouston A., Pascoe A., Cooke S., Speare R., Macdonald G.A., Anderson R., et al. Effect of hookworm infection on wheat challenge in celiac disease--a randomised double-blinded placebo controlled trial. PLoS One. 2011;6:e17366. doi: 10.1371/journal.pone.0017366. PubMed DOI PMC
Turton J.A. IgE, parasites, and allergy. Lancet. 1976;2:686. PubMed
Summers R.W., Elliott D.E., Urban J.F., Jr., Thompson R., Weinstock J.V. Trichuris suis therapy in Crohn's disease. Gut. 2005;54:87–90. doi: 10.1136/gut.2004.041749. PubMed DOI PMC
Huang X., Zeng L.-R., Chen F.-S., Zhu J.-P., Zhu M.-H. Trichuris suis ova therapy in inflammatory bowel disease: a meta-analysis. Medicine. 2018;97:e12087. doi: 10.1097/MD.0000000000012087. PubMed DOI PMC
Helmby H. Human helminth therapy to treat inflammatory disorders- where do we stand? BMC Immunol. 2015;16:12. doi: 10.1186/s12865-015-0074-3. PubMed DOI PMC
Summers R.W., Elliott D.E., Urban J.F., Jr., Thompson R.A., Weinstock J.V. Trichuris suis therapy for active ulcerative colitis: a randomized controlled trial. Gastroenterology. 2005;128:825–832. PubMed
Fleming J., Hernandez G., Hartman L., Maksimovic J., Nace S., Lawler B., Risa T., Cook T., Agni R., Reichelderfer M., et al. Safety and efficacy of helminth treatment in relapsing-remitting multiple sclerosis: results of the HINT 2 clinical trial. Mult. Scler. 2019;25:81–91. doi: 10.1177/1352458517736377. PubMed DOI PMC
Voldsgaard A., Bager P., Garde E., Åkeson P., Leffers A.M., Madsen C.G., Kapel C., Roepstorff A., Thamsborg S.M., Melbye M., et al. Trichuris suis ova therapy in relapsing multiple sclerosis is safe but without signals of beneficial effect. Mult. Scler. 2015;21:1723–1729. doi: 10.1177/1352458514568173. PubMed DOI
Hollander E., Uzunova G., Taylor B.P., Noone R., Racine E., Doernberg E., Freeman K., Ferretti C.J. Randomized crossover feasibility trial of helminthic Trichuris suis ova versus placebo for repetitive behaviors in adult autism spectrum disorder. World J. Biol. Psychiatry. 2020;21:291–299. doi: 10.1080/15622975.2018.1523561. PubMed DOI
Mahajan N.N., Gajbhiye R.K., Bahirat S., Lokhande P.D., Mathe A., Rathi S., Warty N., Mahajan K.N., Srivastava V., Kuppusamy P., Mohite S.C. Co-infection of malaria and early clearance of SARS-CoV-2 in healthcare workers. J. Med. Virol. 2021;93:2431–2438. doi: 10.1002/jmv.26760. PubMed DOI
Achan J., Serwanga A., Wanzira H., Kyagulanyi T., Nuwa A., Magumba G., Kusasira S., Sewanyana I., Tetteh K., Drakeley C., et al. Current malaria infection, previous malaria exposure, and clinical profiles and outcomes of COVID-19 in a setting of high malaria transmission: an exploratory cohort study in Uganda. Lancet. Microbe. 2022;3:e62–e71. doi: 10.1016/s2666-5247(21)00240-8. PubMed DOI PMC
Bamorovat M., Sharifi I., Aflatoonian M.R., Karamoozian A., Tahmouresi A., Jafarzadeh A., Heshmatkhah A., Sharifi F., Salarkia E., Khaleghi T., et al. Prophylactic effect of cutaneous leishmaniasis against COVID-19: a case-control field assessment. Int. J. Infect. Dis. 2022;122:155–161. doi: 10.1016/j.ijid.2021.09.050. PubMed DOI PMC
Sobotková K., Parker W., Levá J., Růžková J., Lukeš J., Jirků Pomajbíková K. Helminth therapy - from the parasite perspective. Trends Parasitol. 2019;35:501–515. doi: 10.1016/j.pt.2019.04.009. PubMed DOI
Whitehead B., Christiansen S., Østergaard L., Nejsum P. Helminths and COVID-19 susceptibility, disease progression, and vaccination efficacy. Trends Parasitol. 2022;38:277–279. doi: 10.1016/j.pt.2022.01.007. PubMed DOI PMC
Levin A.T., Owusu-Boaitey N., Pugh S., Fosdick B.K., Zwi A.B., Malani A., Soman S., Besançon L., Kashnitsky I., Ganesh S., et al. Assessing the burden of COVID-19 in developing countries: systematic review, meta-analysis and public policy implications. BMJ Glob. Health. 2022;7:e008477. doi: 10.1136/bmjgh-2022-008477. PubMed DOI PMC
Makram A.M., Alied M., Khan Z.A., Huy N.T. Parasites protect from severe COVID-19. Myth or reality? Int. J. Infect. Dis. 2022;119:117–118. doi: 10.1016/j.ijid.2022.03.027. PubMed DOI PMC
Areru H.A., Dangisso M.H., Lindtjørn B. Low and unequal use of outpatient health services in public primary health care facilities in southern Ethiopia: a facility-based cross-sectional study. BMC Health Serv. Res. 2021;21:776. doi: 10.1186/s12913-021-06846-x. PubMed DOI PMC
Chelkeba L., Mekonnen Z., Emana D., Jimma W., Melaku T. Prevalence of soil-transmitted helminths infections among preschool and school-age children in Ethiopia: a systematic review and meta-analysis. Glob. Health Res. Policy. 2022;7:9. doi: 10.1186/s41256-022-00239-1. PubMed DOI PMC
Alemu G., Aschalew Z., Zerihun E. Burden of intestinal helminths and associated factors three years after initiation of mass drug administration in Arbaminch Zuria district, Southern Ethiopia. BMC Infect. Dis. 2018;18:435. doi: 10.1186/s12879-018-3330-3. PubMed DOI PMC
Phillips S.R., Goldberg T.L., Muller M.N., Machanda Z.P., Otali E., Friant S., Carag J., Langergraber K.E., Mitani J.C., Wroblewski E.E., et al. Faecal parasites increase with age but not reproductive effort in wild female chimpanzees. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2020;375:20190614. doi: 10.1098/rstb.2019.0614. PubMed DOI PMC
Akinyi M.Y., Jansen D., Habig B., Gesquiere L.R., Alberts S.C., Archie E.A. Costs and drivers of helminth parasite infection in wild female baboons. J. Anim. Ecol. 2019;88:1029–1043. doi: 10.1111/1365-2656.12994. PubMed DOI PMC
Habig B., Doellman M.M., Woods K., Olansen J., Archie E.A. Social status and parasitism in male and female vertebrates: a meta-analysis. Sci. Rep. 2018;8:3629. doi: 10.1038/s41598-018-21994-7. PubMed DOI PMC
El-Sherbini G.T., Abosdera M.M. Risk factors associated with intestinal parasitic infections among children. J. Egypt. Soc. Parasitol. 2013;43:287–294. doi: 10.12816/0006385. PubMed DOI
Panda A.K., Tripathy R., Das B.K. Plasmodium falciparum infection may protect a population from severe acute respiratory syndrome coronavirus 2 infection. J. Infect. Dis. 2020;222:1570–1571. doi: 10.1093/infdis/jiaa455. PubMed DOI PMC
Parker W. EvMed Review; 2010. Reconstituting the Depleted Biome to Prevent Immune Disorders.
Venkatakrishnan A., Sarafian J.T., Jirků-Pomajbíková K., Parker W. Socio-medical studies of individuals self-treating with helminths provide insight into clinical trial design for assessing helminth therapy. Parasitol. Int. 2022;87:102488. doi: 10.1016/j.parint.2021.102488. PubMed DOI
Lukeš J., Stensvold C.R., Jirků-Pomajbíková K., Wegener Parfrey L. Are human intestinal eukaryotes beneficial or commensals? PLoS Pathog. 2015;11:e1005039. doi: 10.1371/journal.ppat.1005039. PubMed DOI PMC
Bono-Lunn D., Villeneuve C., Abdulhay N.J., Harker M., Parker W. Policy and regulations in light of the human body as a ‘superorganism’ containing multiple, intertwined symbiotic relationships. Clin. Res. Regul. Aff. 2016;33:39–48. doi: 10.1080/10601333.2016.1210159. DOI
Villeneuve C., Kou H.H., Eckermann H., Palkar A., Anderson L.G., McKenney E.A., Bollinger R.R., Parker W. Evolution of the hygiene hypothesis into biota alteration theory: what are the paradigms and where are the clinical applications? Microbes Infect. 2018;20:147–155. doi: 10.1016/j.micinf.2017.11.001. PubMed DOI
Okada H., Kuhn C., Feillet H., Bach J.F. The 'hygiene hypothesis' for autoimmune and allergic diseases: an update. Clin. Exp. Immunol. 2010;160:1–9. doi: 10.1111/j.1365-2249.2010.04139.x. PubMed DOI PMC
Haahtela T., Holgate S., Pawankar R., Akdis C.A., Benjaponpitak S., Caraballo L., Demain J., Portnoy J., von Hertzen L., WAO Special Committee on Climate Change and Biodiversity The biodiversity hypothesis and allergic disease: world allergy organization position statement. World Allergy Organ. J. 2013;6:3. doi: 10.1186/1939-4551-6-3. PubMed DOI PMC
Borkow G., Leng Q., Weisman Z., Stein M., Galai N., Kalinkovich A., Bentwich Z. Chronic immune activation associated with intestinal helminth infections results in impaired signal transduction and anergy. J. Clin. Invest. 2000;106:1053–1060. PubMed PMC
Chabé M., Lokmer A., Ségurel L. Gut Protozoa: friends or foes of the human gut microbiota? Trends Parasitol. 2017;33:925–934. doi: 10.1016/j.pt.2017.08.005. PubMed DOI
Billy V., Lhotská Z., Jirků M., Kadlecová O., Frgelecová L., Parfrey L.W., Pomajbíková K.J. Blastocystis colonization alters the gut microbiome and, in some cases, promotes faster recovery from induced colitis. Front. Microbiol. 2021;12:641483. doi: 10.3389/fmicb.2021.641483. PubMed DOI PMC
Stauffer W.M., Alpern J.D., Walker P.F. COVID-19 and dexamethasone: a potential strategy to avoid steroid-related Strongyloides hyperinfection. JAMA. 2020;324:623–624. doi: 10.1001/jama.2020.13170. PubMed DOI
Ademe M., Girma F. The influence of helminth immune regulation on COVID-19 clinical outcomes: is it beneficial or detrimental? Infect. Drug Resist. 2021;14:4421–4426. doi: 10.2147/idr.s335447. PubMed DOI PMC
Awasthi S., Peto R., Read S., Richards S.M., Pande V., Bundy D., DEVTA Deworming and Enhanced Vitamin A team Population deworming every 6 months with albendazole in 1 million pre-school children in North India: DEVTA, a cluster-randomised trial. Lancet. 2013;381:1478–1486. PubMed PMC
Liu C., Lu L., Zhang L., Luo R., Sylvia S., Medina A., Rozelle S., Smith D.S., Chen Y., Zhu T. Effect of deworming on indices of health, cognition, and education among schoolchildren in rural China: a cluster-randomized controlled trial. Am. J. Trop. Med. Hyg. 2017;96:1478–1489. doi: 10.4269/ajtmh.16-0354. PubMed DOI PMC
Jirků M., Kašparová A., Lhotská Z., Oborník M., Brožová K., Petrželková K.J., Samaš P., Kadlecová O., Stensvold C.R., Jirků K. A cross-sectional study on the occurrence of the intestinal protist, dientamoeba fragilis, in the gut-healthy volunteers and their animals. Int. J. Mol. Sci. 2022;23:15407. PubMed PMC
Abdoli A. Helminths and COVID-19 Co-infections: a neglected critical challenge. ACS Pharmacol. Transl. Sci. 2020;3:1039–1041. doi: 10.1021/acsptsci.0c00141. PubMed DOI PMC
Naidoo P., Ghazi T., Chuturgoon A.A., Naidoo R.N., Ramsuran V., Mpaka-Mbatha M.N., Bhengu K.N., Nembe N., Duma Z., Pillay R., et al. SARS-CoV-2 and helminth co-infections, and environmental pollution exposure: an epidemiological and immunological perspective. Environ. Int. 2021;156:106695. doi: 10.1016/j.envint.2021.106695. PubMed DOI PMC
Pi C., Allott E.H., Ren D., Poulton S., Lee S.Y.R., Perkins S.E., Everett M.L., Holzknecht Z.E., Lin S.S., Parker W. Increased biodiversity in the environment improves the humoral response of rats. PLoS One. 2015;10:e0120255. PubMed PMC
Mastrangelo A., Bonato M., Cinque P. Smell and taste disorders in COVID-19: from pathogenesis to clinical features and outcomes. Neurosci. Lett. 2021;748:135694. doi: 10.1016/j.neulet.2021.135694. PubMed DOI PMC
Barker D.J., Morris J. Acute appendicitis, bathrooms, and diet in Britain and Ireland. Br. Med. J. 1988;296:953–955. PubMed PMC
Barker D.J., Morris J.A., Simmonds S.J., Oliver R.H. Appendicitis epidemic following introduction of piped water to Anglesey. J. Epidemiol. Community Health. 1988;42:144–148. PubMed PMC
Strachan D.P. Hay fever, hygiene, and household size. Brit Med J. 1989;299:1259–1260. PubMed PMC
Gale E.A.M. A missing link in the hygiene hypothesis? Diabetologia. 2002;45:588–594. doi: 10.1007/s00125-002-0801-1. PubMed DOI
Tilp C., Kapur V., Loging W., Erb K.J. Prerequisites for the pharmaceutical industry to develop and commercialise helminths and helminth-derived product therapy. Int. J. Parasitol. 2013;43:319–325. doi: 10.1016/j.ijpara.2012.12.003. PubMed DOI
Zardecki C., Dutta S., Goodsell D.S., Lowe R., Voigt M., Burley S.K. PDB-101: educational resources supporting molecular explorations through biology and medicine. Protein Sci. 2022;31:129–140. doi: 10.1002/pro.4200. PubMed DOI PMC
Seyer A., Karasartova D., Ruh E., Güreser A.S., Turgal E., Imir T., Taylan-Ozkan A. Epidemiology and prevalence of Blastocystis spp. in North Cyprus. Am. J. Trop. Med. Hyg. 2017;96:1164–1170. doi: 10.4269/ajtmh.16-0706. PubMed DOI PMC
Scanlan P.D., Knight R., Song S.J., Ackermann G., Cotter P.D. Prevalence and genetic diversity of Blastocystis in family units living in the United States. Infect. Genet. Evol. 2016;45:95–97. doi: 10.1016/j.meegid.2016.08.018. PubMed DOI
Lhotská Z., Jirků M., Hložková O., Brožová K., Jirsová D., Stensvold C.R., Kolísko M., Jirků Pomajbíková K. A study on the prevalence and subtype diversity of the intestinal protist Blastocystis sp. in a gut-healthy human population in the Czech republic. Front. Cell. Infect. Microbiol. 2020;10:544335. doi: 10.3389/fcimb.2020.544335. PubMed DOI PMC
Lohiya G.S., Tan-Figueroa L., Crinella F.M., Lohiya S. Epidemiology and control of enterobiasis in a developmental center. West. J. Med. 2000;172:305–308. doi: 10.1136/ewjm.172.5.305. PubMed DOI PMC
McKenna M.L., McAtee S., Bryan P.E., Jeun R., Ward T., Kraus J., Bottazzi M.E., Hotez P.J., Flowers C.C., Mejia R. Human intestinal parasite burden and poor sanitation in rural Alabama. Am. J. Trop. Med. Hyg. 2017;97:1623–1628. doi: 10.4269/ajtmh.17-0396. PubMed DOI PMC