Impact of Helminth Infections on Female Reproductive Health and Associated Diseases

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2020 Dec 17

PMID 33329545

Citations 13

Authors

Alisha Chetty

Millicent A Omondi

Claire Butters

Katherine Ann Smith

Gnatoulma Katawa

Manuel Ritter

Laura Layland

William Horsnell

Affiliations

Soon will be listed here.

Abstract

A growing body of knowledge exists on the influence of helminth infections on allergies and unrelated infections in the lung and gastrointestinal (GI) mucosa. However, the bystander effects of helminth infections on the female genital mucosa and reproductive health is understudied but important considering the high prevalence of helminth exposure and sexually transmitted infections in low- and middle-income countries (LMICs). In this review, we explore current knowledge about the direct and systemic effects of helminth infections on unrelated diseases. We summarize host disease-controlling immunity of important sexually transmitted infections and introduce the limited knowledge of how helminths infections directly cause pathology to female reproductive tract (FRT), alter susceptibility to sexually transmitted infections and reproduction. We also review work by others on type 2 immunity in the FRT and hypothesize how these insights may guide future work to help understand how helminths alter FRT health.

Citing Articles

Exploring microRNA-Mediated Immune Responses to Soil-Transmitted Helminth and Herpes Simplex Virus Type 2 Co-Infections.

Pillay R, Naidoo P, Mkhize-Kwitshana Z Diseases. 2025; 13(1).

PMID: 39851470 PMC: 11765296. DOI: 10.3390/diseases13010006.

Potential Interactions Between Soil-Transmitted Helminths and Herpes Simplex Virus Type II: Implications for Sexual and Reproductive Health in Sub-Saharan African.

Pillay R, Naidoo P, Duma Z, Bhengu K, Mpaka-Mbatha M, Nembe-Mafa N Biology (Basel). 2025; 13(12.

PMID: 39765717 PMC: 11673149. DOI: 10.3390/biology13121050.

Engineering nanosystems for regulating reproductive health in women.

Fu Q, Fu L Theranostics. 2025; 15(2):439-459.

PMID: 39744682 PMC: 11671389. DOI: 10.7150/thno.102626.

Herpes simplex virus type 2 in sub-Saharan Africa and the potential impact of helminth immune modulation.

Pillay R, Naidoo P, Mkhize-Kwitshana Z Front Cell Infect Microbiol. 2024; 14():1471411.

PMID: 39698320 PMC: 11652539. DOI: 10.3389/fcimb.2024.1471411.

Co-infection of and soil-transmitted helminth among pregnant women in Abaya district, South Ethiopia: A community-based study.

Gemechu T, Aliyo A, Husen O, Jarso H, Assefa L IJID Reg. 2024; 13:100475.

PMID: 39582882 PMC: 11582442. DOI: 10.1016/j.ijregi.2024.100475.

References

Zhou C, Tuong Z, Frazer I . Papillomavirus Immune Evasion Strategies Target the Infected Cell and the Local Immune System. Front Oncol. 2019; 9:682. PMC: 6688195. DOI: 10.3389/fonc.2019.00682. View

Nussbaum J, Van Dyken S, von Moltke J, Cheng L, Mohapatra A, Molofsky A . Type 2 innate lymphoid cells control eosinophil homeostasis. Nature. 2013; 502(7470):245-8. PMC: 3795960. DOI: 10.1038/nature12526. View

Straubinger K, Paul S, Prazeres da Costa O, Ritter M, Buch T, Busch D . Maternal immune response to helminth infection during pregnancy determines offspring susceptibility to allergic airway inflammation. J Allergy Clin Immunol. 2014; 134(6):1271-1279.e10. DOI: 10.1016/j.jaci.2014.05.034. View

Mkhize-Kwitshana Z, Taylor M, Jooste P, Mabaso M, Walzl G . The influence of different helminth infection phenotypes on immune responses against HIV in co-infected adults in South Africa. BMC Infect Dis. 2011; 11:273. PMC: 3213674. DOI: 10.1186/1471-2334-11-273. View

Ishida K, Hsieh M . Understanding Urogenital Schistosomiasis-Related Bladder Cancer: An Update. Front Med (Lausanne). 2018; 5:223. PMC: 6104441. DOI: 10.3389/fmed.2018.00223. View

Clerici M, Merola M, Ferrario E, Trabattoni D, Villa M, Stefanon B . Cytokine production patterns in cervical intraepithelial neoplasia: association with human papillomavirus infection. J Natl Cancer Inst. 1997; 89(3):245-50. DOI: 10.1093/jnci/89.3.245. View

Neill D, Wong S, Bellosi A, Flynn R, Daly M, Langford T . Nuocytes represent a new innate effector leukocyte that mediates type-2 immunity. Nature. 2010; 464(7293):1367-70. PMC: 2862165. DOI: 10.1038/nature08900. View

Bancroft A, Levy C, Jowitt T, Hayes K, Thompson S, Mckenzie E . The major secreted protein of the whipworm parasite tethers to matrix and inhibits interleukin-13 function. Nat Commun. 2019; 10(1):2344. PMC: 6538607. DOI: 10.1038/s41467-019-09996-z. View

Oh J, Oh D, Jung H, Lee H . A mechanism for the induction of type 2 immune responses by a protease allergen in the genital tract. Proc Natl Acad Sci U S A. 2017; 114(7):E1188-E1195. PMC: 5320955. DOI: 10.1073/pnas.1612997114. View

10.

Bernhard P, Makunde R, Magnussen P, Lemnge M . Genital manifestations and reproductive health in female residents of a Wuchereria bancrofti-endemic area in Tanzania. Trans R Soc Trop Med Hyg. 2000; 94(4):409-12. DOI: 10.1016/s0035-9203(00)90123-8. View

11.

Shea-Donohue T, Sullivan C, Finkelman F, Madden K, Morris S, Goldhill J . The role of IL-4 in Heligmosomoides polygyrus-induced alterations in murine intestinal epithelial cell function. J Immunol. 2001; 167(4):2234-9. DOI: 10.4049/jimmunol.167.4.2234. View

12.

Downs J, Mguta C, Kaatano G, Mitchell K, Bang H, Simplice H . Urogenital schistosomiasis in women of reproductive age in Tanzania's Lake Victoria region. Am J Trop Med Hyg. 2011; 84(3):364-9. PMC: 3042809. DOI: 10.4269/ajtmh.2011.10-0585. View

13.

Petrillo M, Zannoni G, Martinelli E, Pedone Anchora L, Ferrandina G, Tropeano G . Polarisation of Tumor-Associated Macrophages toward M2 Phenotype Correlates with Poor Response to Chemoradiation and Reduced Survival in Patients with Locally Advanced Cervical Cancer. PLoS One. 2015; 10(9):e0136654. PMC: 4559430. DOI: 10.1371/journal.pone.0136654. View

14.

Du Plessis N, Kleynhans L, Thiart L, Van Helden P, Brombacher F, Horsnell W . Acute helminth infection enhances early macrophage mediated control of mycobacterial infection. Mucosal Immunol. 2012; 6(5):931-41. DOI: 10.1038/mi.2012.131. View

15.

Grainger J, Smith K, Hewitson J, McSorley H, Harcus Y, Filbey K . Helminth secretions induce de novo T cell Foxp3 expression and regulatory function through the TGF-β pathway. J Exp Med. 2010; 207(11):2331-41. PMC: 2964568. DOI: 10.1084/jem.20101074. View

16.

Lee B, Follen M, Tortolero-Luna G, Eriksen N, Helfgott A, Hammill H . Synthesis of IFN-gamma by CD8(+) T cells is preserved in HIV-infected women with HPV-related cervical squamous intraepithelial lesions. Gynecol Oncol. 1999; 75(3):379-86. DOI: 10.1006/gyno.1999.5587. View

17.

Jordan S, Gupta K, Ogendi B, Bakshi R, Kapil R, Press C . The Predominant CD4 Th1 Cytokine Elicited to Chlamydia trachomatis Infection in Women Is Tumor Necrosis Factor Alpha and Not Interferon Gamma. Clin Vaccine Immunol. 2017; 24(4). PMC: 5382828. DOI: 10.1128/CVI.00010-17. View

18.

Doetze A, Satoguina J, Burchard G, Rau T, Loliger C, Fleischer B . Antigen-specific cellular hyporesponsiveness in a chronic human helminth infection is mediated by T(h)3/T(r)1-type cytokines IL-10 and transforming growth factor-beta but not by a T(h)1 to T(h)2 shift. Int Immunol. 2000; 12(5):623-30. DOI: 10.1093/intimm/12.5.623. View

19.

Darby M, Chetty A, Mrjden D, Rolot M, Smith K, Mackowiak C . Pre-conception maternal helminth infection transfers via nursing long-lasting cellular immunity against helminths to offspring. Sci Adv. 2019; 5(5):eaav3058. PMC: 6587632. DOI: 10.1126/sciadv.aav3058. View

20.

Geiger S, Alexander N, Fujiwara R, Brooker S, Cundill B, Diemert D . Necator americanus and helminth co-infections: further down-modulation of hookworm-specific type 1 immune responses. PLoS Negl Trop Dis. 2011; 5(9):e1280. PMC: 3167770. DOI: 10.1371/journal.pntd.0001280. View