Soil-transmitted helminth infections are associated with an increase in human papillomavirus prevalence and a T-helper type 2 cytokine signature in cervical fluids

Journal of Infectious Diseases

Volumn 212, Issue 11, 2015, Pages 723-730

  Gravitt, Patti E ^a,b   Marks, Morgan ^b,d   Kosek, Margaret ^c,f   Huang, Christine ^g   Cabrera, Lilia ^f   Olortegui, Maribel Paredes ^f   Medrano, Alberto Mejia ^g   Trigoso, Dixner R ^f   Qureshi, Sarah ^c   Bardales, Gustavo S ^h   Manrique Hinojosa, Javier ^h   Cardenas, Albert Z ^h   Larraondo, Manuel A ^h   Cok, Jaime ⁱ   Qeadan, Fares ^a   Siracusa, Mark ^e   Gilman, Robert H ^c  

^a UNIVERSITY OF NEW MEXICO SCHOOL OF MEDICINE   (United States)

^b University of New Mexico ^*  (United States)

^c JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^d MERCK RESEARCH LABORATORIES   (United States)

^e RUTGERS NEW JERSEY MEDICAL SCHOOL   (United States)

^f ASOCIACIÓN BENÉFICA PRISMA   (Peru)

^g Hospital Regional de Loreto   (Peru)

^h INSTITUTO NACIONAL DE ENFERMEDADES NEOPLÁSICAS   (Peru)

ⁱ UNIVERSIDAD PERUANA CAYETANO HEREDIA   (Peru)

Author keywords

Age; Cervical cancer; Human papillomavirus; Parasite; Prevalence; Soil transmitted helminth

Indexed keywords

CYTOKINE; DRINKING WATER; SOIL;

ADULT; ARTICLE; BUILDING; COMPARATIVE STUDY; CONTROLLED STUDY; COOKING; DISEASE ASSOCIATION; FEMALE; GEOGRAPHIC DISTRIBUTION; HELMINTHIASIS; HUMAN; PARASITOSIS; PERU; PREVALENCE; PRIORITY JOURNAL; PROTOZOAL INFECTION; SANITATION; SEWER; SEXUAL BEHAVIOR; SOIL TRANSMITTED HELMINTH INFECTION; TH2 CELL; UTERINE CERVIX CANCER; UTERINE CERVIX MUCUS; WART VIRUS; COMPLICATION; GENE EXPRESSION REGULATION; HELPER CELL; IMMUNOLOGY; ISOLATION AND PURIFICATION; METABOLISM; MIDDLE AGED; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PARASITOLOGY; PILOT STUDY; SOIL; TRANSMISSION; UTERINE CERVIX;

ADULT; CERVIX UTERI; CYTOKINES; FEMALE; GENE EXPRESSION REGULATION; HELMINTHIASIS; HUMANS; MIDDLE AGED; PAPILLOMAVIRIDAE; PAPILLOMAVIRUS INFECTIONS; PERU; PILOT PROJECTS; SOIL; T-LYMPHOCYTES, HELPER-INDUCER;

EID: 84958659010     PISSN: 00221899     EISSN: 15376613     Source Type: Journal    
DOI: 10.1093/infdis/jiv498     Document Type: Article

References (35)

1. Peto J, Gilham C, Fletcher O, Matthews FE. The cervical cancer epidemic that screening has prevented in the UK. Lancet 2004; 364:249-56
2. Drain PK, Holmes KK, Hughes JP, Koutsky LA. Determinants of cervical cancer rates in developing countries. Int J Cancer 2002; 100:199-205
3. Maucort-Boulch D, Franceschi S, Plummer M. IARC HPV Prevalence Surveys Study Group. International correlation between human papillomavirus prevalence and cervical cancer incidence. Cancer Epidemiol Biomarkers Prev 2008; 17:717-20
4. Bruni L, Diaz M, Castellsague X, Ferrer E, Bosch FX, de Sanjose S. Cervical human papillomavirus prevalence in 5 continents: meta-analysis of 1 million women with normal cytological findings. J Infect Dis 2010; 202:1789-99
5. Osborne LC, Monticelli LA, Nice TJ, et al. Coinfection. Virus-helminth coinfection reveals a microbiota-independent mechanism of immunomodulation. Science 2014; 345:578-82
6. Reese TA, Wakeman BS, Choi HS, et al. Coinfection. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science 2014; 345:573-7
7. Fakhry C, Marks MA, Gilman RH, et al. Comparison of the immune microenvironment of the oral cavity and cervix in healthy women. Cytokine 2013; 64:597-604
8. Marks MA, Eby Y, Howard R, Gravitt PE. Comparison of normalization methods for measuring immune markers in cervical secretion specimens. J Immunol Methods 2012; 382:211
9. Yori PP, Kosek M, Gilman RH, et al. Seroepidemiology of strongyloidiasis in the Peruvian Amazon. Am J Trop Med Hyg 2006; 74:97-102
10. Ahmadi NA, Damraj FA. A field evaluation of formalin-gasoline technique in the concentration of stool for detection of intestinal parasites. Parasitol Res 2009; 104:553-7
11. Gravitt PE, Peyton CL, Alessi TQ, et al. Improved amplification of genital human papillomaviruses. J Clin Microbiol 2000; 38:357-61
12. Gravitt PE, Peyton CL, Apple RJ, Wheeler CM. Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by a single hybridization, reverse line blot detection method. J Clin Microbiol 1998; 36:3020-7
13. Hernan MA, Hernandez-Diaz S,Werler MM, Mitchell AA. Causal knowledge as a prerequisite for confounding evaluation: an application to birth defects epidemiology. Am J Epidemiol 2002; 155:176-84
14. Gravitt PE. The known unknowns of HPV natural history. J Clin Invest 2011; 121:4593-9
15. Stanley M, Pinto LA, Trimble C. Human papillomavirus vaccines - immune responses. Vaccine 2012; 30(suppl 5):F83-7
16. Scott ME, Ma Y, Farhat S, Shiboski S, Moscicki AB. Covariates of cervical cytokine mRNA expression by real-time PCR in adolescents and young women: effects of Chlamydia trachomatis infection, hormonal contraception, and smoking. J Clin Immunol 2006; 26:222-32
17. Poppe WA, Ide PS, Drijkoningen MP, Lauweryns JM, Van Assche FA. Tobacco smoking impairs the local immunosurveillance in the uterine cervix. An immunohistochemical study. Gynecol Obstet Invest 1995; 39:34-8
18. Chappell CA, Isaacs CE, Xu W, et al. The effect of menopause on the innate antiviral activity of cervicovaginal lavage. Am J Obstet Gynecol 2015; 213:204.e1-6
19. Fallon PG, Ballantyne SJ, Mangan NE, et al. Identification of an interleukin (IL)- 25-dependent cell population that provides IL-4, IL-5, and IL-13 at the onset of helminth expulsion. J Exp Med 2006; 203:1105-16
20. Moro K, Yamada T, Tanabe M, et al. Innate production of TH2 cytokines by adipose tissue-associated c-Kit+ Sca-1+ lymphoid cells. Nature 2010; 463:540-6
21. Price AE, Liang H-E, Sullivan BM, et al. Systemically dispersed innate IL-13- expressing cells in type 2 immunity. Proc Natl Acad Sci U S A 2010; 107: 11489-94
22. Saenz SA, Siracusa MC, Monticelli LA, et al. IL-25 simultaneously elicits distinct populations of innate lymphoid cells and multipotent progenitor type 2 (MMPtype2) cells. J Exp Med 2013; 210:1823-37
23. Saenz SA, Siracusa MA, Perrigoue JG, et al. IL25 elicits a multipotent progenitor cell population that promotes TH2 cytokine responses. Nature 2010; 464:1362-7
24. King IL, Mohrs K, Mohrs M. A nonredundant role for IL-21 receptor signaling in plasma cell differentiation and protective type 2 immunity against gastrointestinal helminth infection. J Immunol 2010; 185:6138-45
25. Pesce J, Kaviratne M, Ramalingam TR, et al. The IL-21 receptor augments Th2 effector function and alternative macrophage activation. J Clin Invest 2006; 116:2044-55
26. Mahanty S, Abrams JS, King CL, Limaye AP, Nutman TB. Parallel regulation of IL- 4 and IL-5 in human helminth infections. J Immunol 1992; 148:3567-71
27. Figueiredo CA, Barreto ML, Rodrigues LC, et al. Chronic intestinal helminth infections are associated with immune hyporesponsiveness and induction of a regulatory network. Infect Immun 2010; 78:3160-7
28. Facciloli LH, Medeiros AI, Malheiro A, Pietro RCLR, Januario A, Vargaftig BB. Interleukin-5 modulates interleukin-8 secretion in eosinophilic inflammation. Med Inflamm 1998; 7:41-7
29. Perrigoue JG, Li J, Zaph C, et al. IL-31-IL31R interactions negatively regulate type 2 inflammation in the lung. J Exp Med 2007; 204:481-7
30. Vaccarella S, Franceschi S, Clifford GM, et al. Seroprevalence of antibodies against human papillomavirus (HPV) type 16 and 18 in four continents: the International Agency for Research on Cancer HPV Prevalence Surveys. Cancer Epidemiol Biomarkers Prev 2010; 19:2379-88
31. Veldhoen M, Heeney JL. A helminth-mediated viral awakening. Trends Immunol 2014; 35:452-3
32. Damania B, Dittmer DP. What lies within: coinfection and immunity. Cell Host Microbe 2014; 16:145-7
33. Bedoya AM, Tate DJ, Baena A, et al. Immunosuppression in cervical cancer with specific reference to arginase activity. Gynecol Oncol 2014; 135:74-80
34. Kobayashi A, Weinberg V, Darragh T, Smith-McCune K. Evolving immunosuppressive microenvironment during human cervical carcinogenesis. Mucosal Immunol 2008; 1:412-20
35. Hotez P, Whitham M. Helminth infections: a new global women's health agenda. Obstet Gynecol 2014; 123:155-60