The Influence of Helminth Immune Regulation on COVID-19 Clinical Outcomes: Is it Beneficial or Detrimental?

References

• Yang P, Wang X. COVID-19: a new challenge for human beings. Cell Mol Immunol. 2020;17(5):555–557. doi:10.1038/s41423-020-0407-x32235915
   PubMed Web of Science ®Google Scholar
• 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(8):1–3. doi:10.1371/journal.pntd.0008628
   Web of Science ®Google Scholar
• Ssebambulidde K, Segawa I, Abuga KM, et al. Parasites and their protection against COVID-19- Ecology or Immunology? medRxiv. 2020. doi:10.1101/2020.05.11.20098053
   Google Scholar
• Masaku J, Mutungi F, Gichuki PM, Okoyo C, Njomo DW, Njenga SM. High prevalence of helminths infection and associated risk factors among adults living in a rural setting, central Kenya: a cross-sectional study. Trop Med Health. 2017;45(1):1–9. doi:10.1186/s41182-017-0055-828077924
   PubMedGoogle Scholar
• Geng JS, Yu XL, Bao HN, et al. Chronic diseases as a predictor for severity and mortality of COVID-19: a systematic review with cumulative meta-analysis. Front Med. 2021;8(September):1–16. doi:10.3389/fmed.2021.588013
   Web of Science ®Google Scholar
• Lake MA. What we know so far: COVID-19 current clinical knowledge and research. Clin Med. 2020;20(2):124–127. doi:10.7861/clinmed.2019-coron
   PubMed Web of Science ®Google Scholar
• Wang C, Horby PW, Hayden FG, Gao GF. A novel coronavirus outbreak of global health concern. Lancet. 2020;395(10223):470–473. doi:10.1016/S0140-6736(20)30185-931986257
   PubMed Web of Science ®Google Scholar
• de Wit E, van Doremalen N, Falzarano D, Munster VJ. SARS and MERS: recent insights into emerging coronaviruses. Nat Rev Microbiol. 2016;14(8):523–534. doi:10.1038/nrmicro.2016.8127344959
   PubMed Web of Science ®Google Scholar
• Cucinotta D, Vanelli M. WHO declares COVID-19 a pandemic. Acta Biomed. 2020;91(1):157–160.32191675
   PubMedGoogle Scholar
• World Health Organization. Coronavirus disease (COVID-19) weekly epidemiological update and weekly operational update [Internet]; 2021. Available from: https://www.who.int/emergencies/diseases/novel-coronavirus-2019/situation-reports. Accessed October 19, 2021.
   Google Scholar
• Stringhini S, Wisniak A, Piumatti G, et al. Seroprevalence of anti-SARS-CoV-2 IgG antibodies in Geneva, Switzerland (SEROCoV-POP): a population-based study. Lancet. 2020;396(10247):313–319. doi:10.1016/S0140-6736(20)31304-032534626
   PubMed Web of Science ®Google Scholar
• Havers FP, Reed C, Lim T, et al. Seroprevalence of antibodies to SARS-CoV-2 in 10 sites in the United States, March 23-May 12, 2020. JAMA Intern Med. 2020;180(12):1576. doi:10.1001/jamainternmed.2020.4130
   Web of Science ®Google Scholar
• Derbie A, Mekonnen D, Woldeamanuel Y, Abebe T. No TitWhy has Africa reported relatively few COVID-19 cases so far? A web-based survey. Ethiop J Heal Dev. 2020;34(4):313–316.
   Web of Science ®Google Scholar
• Dente MG, Resti CV, Declich S, Putoto G. The reported few cases and deaths of covid-19 epidemic in Africa are still data too questionable to reassure about the future of this continent. Front Public Heal. 2021;9:10–13.
   Web of Science ®Google Scholar
• Welker C, Huang J, Gil IJN, Ramakrishna H. Acute respiratory distress syndrome update, with coronavirus disease 2019 focus. J Cardiothorac Vasc Anesth. 2021. doi:10.1053/j.jvca.2021.02.053
   Web of Science ®Google Scholar
• Brindley PJ, Mitreva M, Ghedin E, Lustigman S. Helminth genomics: the implications for human health. PLoS Negl Trop Dis. 2009;3(10):e538. doi:10.1371/journal.pntd.000053819855829
   PubMed Web of Science ®Google Scholar
• Karin N, Miles JJ. Helminth immunomodulation in autoimmune disease. Front Immunol. 2017;8(April):453.28484453
   PubMed Web of Science ®Google Scholar
• Gazzinelli-Guimaraes PH, Nutman TB. Helminth parasites and immune regulation. F1000Research. 2018;7:1685. doi:10.12688/f1000research.15596.1
   Google Scholar
• Si H. Global, regional, and national disability-adjusted life-years (DALYs) for 333 diseases and injuries and healthy life expectancy (HALE) for 195 countries and territories, 1990–2016: a systematic analysis for the Global Burden of Disease Study 2016. Lancet. 2017;390(10100):1260–1344.28919118
   PubMed Web of Science ®Google Scholar
• Hotez PJ, Brooker S, Bethony JM, Bottazzi ME, Loukas A, Xiao S. Hookworm infection. N Engl J Med. 2004;351(8):799–807. doi:10.1056/NEJMra03249215317893
   PubMed Web of Science ®Google Scholar
• Maizels RM, Yazdanbakhsh M. Immune regulation by helminth parasites: cellular and molecular mechanisms. Nat Rev Immunol. 2003;3(9):733–744. doi:10.1038/nri118312949497
   PubMed Web of Science ®Google Scholar
• Dixon MA, Braae UC, Winskill P, et al. Strategies for tackling Taenia solium taeniosis/cysticercosis: a systematic review and comparison of transmission models, including an assessment of the wider Taeniidae family transmission models. PLoS Negl Trop Dis. 2019;13(4):e0007301. doi:10.1371/journal.pntd.000730130969966
   PubMed Web of Science ®Google Scholar
• Mostafa MH, Sheweita SA, O’Connor PJ. Relationship between schistosomiasis and bladder cancer. Clin Microbiol Rev. 1999;12(1):97–111.9880476
   PubMed Web of Science ®Google Scholar
• Schluth CG, Standley CJ, Bansal S, Colin J. Mapping the human helminthiases: advances and gaps in neglected disease surveillance. MedRxiv. 2020;1–26. doi:10.1101/2020.10.30.20223529
   Google Scholar
• Pabalan N, Singian E, Tabangay L, Jarjanazi H, Boivin MJ, Ezeamama AE. Soil-transmitted helminth infection, loss of education and cognitive impairment in school-aged children: a systematic review and meta-analysis. PLoS Negl Trop Dis. 2018;12(1):e0005523. doi:10.1371/journal.pntd.000552329329288
   PubMed Web of Science ®Google Scholar
• Mbabazi PS, Andan O, Fitzgerald DW, Chitsulo L, Engels D, Downs JA. Examining the relationship between urogenital schistosomiasis and HIV infection. PLoS Negl Trop Dis. 2011;5(12):e1396. doi:10.1371/journal.pntd.000139622163056
   PubMed Web of Science ®Google Scholar
• van Riet E, Hartgers FC, Yazdanbakhsh M. Chronic helminth infections induce immunomodulation: consequences and mechanisms. Immunobiology. 2007;212(6):475–490. doi:10.1016/j.imbio.2007.03.00917544832
   PubMed Web of Science ®Google Scholar
• Allen JE, Maizels RM. Diversity and dialogue in immunity to helminths. Nat Rev Immunol. 2011;11(6):375–388. doi:10.1038/nri299221610741
   PubMed Web of Science ®Google Scholar
• Finlay CM, Walsh KP, Mills KHG. Induction of regulatory cells by helminth parasites: exploitation for the treatment of inflammatory diseases. Immunol Rev. 2014;259(1):206–230. doi:10.1111/imr.1216424712468
   PubMed Web of Science ®Google Scholar
• Zakeri A. Helminth-induced apoptosis: a silent strategy for immunosuppression. Parasitology. 2017;144(13):1663–1676. doi:10.1017/S003118201700084128659212
   PubMed Web of Science ®Google Scholar
• Oliveira SC, Figueiredo BC, Cardoso LS, Carvalho EM. A double edged sword: schistosoma mansoni Sm29 regulates both Th1 and Th2 responses in inflammatory mucosal diseases. Mucosal Immunol. 2016;9(6):1366–1371. doi:10.1038/mi.2016.6927554296
   PubMed Web of Science ®Google Scholar
• Zakeri A, Hansen EP, Andersen SD, Williams AR, Nejsum P. Immunomodulation by helminths: intracellular pathways and extracellular vesicles. Front Immunol. 2018;9:2349. doi:10.3389/fimmu.2018.0234930369927
   PubMed Web of Science ®Google Scholar
• Riganò R, Buttari B, Profumo E, et al. Echinococcus granulosus antigen B impairs human dendritic cell differentiation and polarizes immature dendritic cell maturation towards a Th2 cell response. Infect Immun. 2007;75(4):1667–1678. doi:10.1128/IAI.01156-0617210662
   PubMed Web of Science ®Google Scholar
• Klaver EJ, van der Pouw Kraan TCTM, Laan LC, et al. Trichuris suis soluble products induce Rab7b expression and limit TLR4 responses in human dendritic cells. Genes Immun. 2015;16(6):378–387. doi:10.1038/gene.2015.1825996526
   PubMed Web of Science ®Google Scholar
• Laan LC, Williams AR, Stavenhagen K, et al. The whipworm (Trichuris suis) secretes prostaglandin E2 to suppress proinflammatory properties in human dendritic cells. FASEB J off Publ Fed Am Soc Exp Biol. 2017;31(2):719–731.
   PubMed Web of Science ®Google Scholar
• Summan A, Nejsum P, Williams AR. Modulation of human dendritic cell activity by Giardia and helminth antigens. Parasite Immunol. 2018;40(5):e12525. doi:10.1111/pim.1252529574798
   PubMed Web of Science ®Google Scholar
• Pineda MA, Eason RJ, Harnett MM, Harnett W. From the worm to the pill, the parasitic worm product ES-62 raises new horizons in the treatment of rheumatoid arthritis. Lupus. 2015;24(4–5):400–411. doi:10.1177/096120331456000425801883
   PubMed Web of Science ®Google Scholar
• Almeida S, Nejsum P, Williams AR. Modulation of human macrophage activity by Ascaris antigens is dependent on macrophage polarization state. Immunobiology. 2018;223(4–5):405–412. doi:10.1016/j.imbio.2017.11.00329162324
   PubMed Web of Science ®Google Scholar
• Midttun HLE, Acevedo N, Skallerup P, et al. Ascaris suum infection downregulates inflammatory pathways in the pig intestine in vivo and in human dendritic cells in vitro. J Infect Dis. 2018;217(2):310–319. doi:10.1093/infdis/jix58529136163
   PubMed Web of Science ®Google Scholar
• Harris NL, Loke P. Recent advances in type-2-cell-mediated immunity: insights from helminth infection. Immunity. 2017;47(6):1024–1036. doi:10.1016/j.immuni.2017.11.01529262347
   PubMed Web of Science ®Google Scholar
• Brosschot TP, Reynolds LA. The impact of a helminth-modified microbiome on host immunity. Mucosal Immunol. 2018;11(4):1039–1046. doi:10.1038/s41385-018-0008-529453411
   PubMed Web of Science ®Google Scholar
• Kruse RL. Therapeutic strategies in an outbreak scenario to treat the novel coronavirus originating in Wuhan, China. F1000Research. 2020;9:72. doi:10.12688/f1000research.22211.232117569
   PubMedGoogle Scholar
• Huang C, Wang Y, Li X, et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet. 2020;395(10223):497–506. doi:10.1016/S0140-6736(20)30183-531986264
   PubMed Web of Science ®Google Scholar
• Çakır Edis E. Chronic pulmonary diseases and COVID-19. Turkish Thorac J. 2020;21(5):345–349. doi:10.5152/TurkThoracJ.2020.20091
   PubMed Web of Science ®Google Scholar
• Nishiga M, Wang DW, Han Y, Lewis DB, Wu JC. COVID-19 and cardiovascular disease: from basic mechanisms to clinical perspectives. Nat Rev Cardiol. 2020;17(9):543–558. doi:10.1038/s41569-020-0413-932690910
   PubMed Web of Science ®Google Scholar
• Bitencourt L, Pedrosa AL, de Brito SBCS, et al. COVID-19 and renal diseases: an update. Curr Drug Targets. 2021;22(1):52–67. doi:10.2174/138945012199920101315130033050860
   PubMed Web of Science ®Google Scholar
• Yanai H. Metabolic Syndrome and COVID-19. Cardiol Res. 2020;11(6):360–365. doi:10.14740/cr118133224380
   PubMed Web of Science ®Google Scholar
• Bornstein SR, Rubino F, Ludwig B, et al. Consequences of the COVID-19 pandemic for patients with metabolic diseases. Nat Metab. 2021;Mar(3):289–292. doi:10.1038/s42255-021-00358-y
   Google Scholar
• Tracey EF, McDermott RA, McDonald MI. Do worms protect against the metabolic syndrome? A systematic review and meta-analysis. Diabetes Res Clin Pract. 2016;120:209–220. doi:10.1016/j.diabres.2016.08.01427596058
   PubMed Web of Science ®Google Scholar
• Rajamanickam A, Munisankar S, Dolla C, et al. Helminth infection modulates systemic pro-inflammatory cytokines and chemokines implicated in type 2 diabetes mellitus pathogenesis. PLoS Negl Trop Dis. 2020;14(3):e0008101. doi:10.1371/journal.pntd.000810132126084
   PubMed Web of Science ®Google Scholar
• Rolot M, Dougall AM, Chetty A, et al. Helminth-induced IL-4 expands bystander memory CD8(+) T cells for early control of viral infection. Nat Commun. 2018;9(1):4516. doi:10.1038/s41467-018-06978-530375396
   PubMed Web of Science ®Google Scholar
• Chowaniec W, Wescott RB, Congdon LL. Interaction of Nematospiroides dubius and influenza virus in mice. Exp Parasitol. 1972;32(1):33–44. doi:10.1016/0014-4894(72)90007-05065669
   PubMed Web of Science ®Google Scholar
• Gebrecherkos T, Gessesse Z, Kebede Y, Gebreegzabher A, Wit TRD, Wolday D. Effect of co-infection with parasites on severity of COVID-19. medRxiv. 2021;267:1–15.
   Google Scholar
• Bradbury RS, Piedrafita D, Greenhill A, Mahanty S. Will helminth co-infection modulate COVID-19 severity in endemic regions? Nat Rev Immunol. 2020;20(6):342. doi:10.1038/s41577-020-0330-532358579
   PubMed Web of Science ®Google Scholar
• Oliveira RA, Gurgel-gonçalves R, Machado ER. Intestinal parasites in two indigenous ethnic groups in northwestern Amazonia. Acta Amaz. 2016;46(3):241–246. doi:10.1590/1809-4392201505883
   Web of Science ®Google Scholar
• Ramírez JD, Sordillo EM, Gotuzzo E, et al. SARS-CoV-2 in the Amazon region: a harbinger of doom for Amerindians. PLoS Negl Trop Dis. 2020;14(10):e0008686. doi:10.1371/journal.pntd.000868633119616
   PubMed Web of Science ®Google Scholar
• Nastasi-Miranda J. Prevalence of intestinal parasites in educational units from Ciudad Bolı´var, Venezuela. Rev Cuid. 2015;6(2):1077–1084. doi:10.15649/cuidarte.v6i2.181
   Google Scholar
• Paniz-Mondolfi AE, Ramírez JD, Delgado-Noguera LA, Rodriguez-Morales AJ, Sordillo EM. Covid-19 and helminth infection: beyond the th1/th2 paradigm. PLoS Negl Trop Dis. 2021;15(5):10–12. doi:10.1371/journal.pntd.0009402
   Web of Science ®Google Scholar
• Su C, Cao Y, Zhang M, et al. Helminth infection impairs autophagy-mediated killing of bacterial enteropathogens by macrophages. J Immunol. 2012;189(3):1459–1466. doi:10.4049/jimmunol.120048422732589
   PubMed Web of Science ®Google Scholar
• Reese TA, Wakeman BS, Choi HS, et al. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science. 2014;345(6196):573–577. doi:10.1126/science.125451724968940
   PubMed Web of Science ®Google Scholar
• Osborne LC, Monticelli LA, Nice TJ, et al. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science (80-). 2014;345(6196):578–582. doi:10.1126/science.1256942
   PubMed Web of Science ®Google Scholar
• Nayak D, Kelley G. Synergistic effect of Ascaris migration and influenza infection in mice. J Parasitol. 1965;51(2):297–298. doi:10.2307/327610314275227
   PubMed Web of Science ®Google Scholar
• Abdoli A. Helminths and COVID-19 co-infections: a neglected critical challenge. ACS Pharmacol Transl Sci. 2020;3:1039–1041.33073203
   PubMedGoogle Scholar
• Chacin-Bonilla L, Chacón-Fonseca N, Rodriguez-Morales AJ. Emerging issues in COVID-19 vaccination in tropical areas: impact of the immune response against helminths in endemic areas. Travel Med Infect Dis. 2021;42:2.
   Web of Science ®Google Scholar
• Liao M, Liu Y, Yuan J, et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat Med. 2020;26(6):842–844. doi:10.1038/s41591-020-0901-932398875
   PubMed Web of Science ®Google Scholar