The Interrelation Between Microbial Immunoglobulin Coating, Vaginal Microbiota, Ethnicity, and Preterm Birth

Overview

Journal Microbiome

Publisher Biomed Central

Specialties Genetics
Microbiology

Date 2024 May 27

PMID 38802950

Authors

H J Schuster

A C Breedveld

S P F Matamoros

R van Eekelen

R C Painter

M Kok

P J Hajenius

P H M Savelkoul

M van Egmond

R van Houdt

Affiliations

Soon will be listed here.

Abstract

Background: Vaginal microbiota composition is associated with spontaneous preterm birth (sPTB), depending on ethnicity. Host-microbiota interactions are thought to play an important underlying role in this association between ethnicity, vaginal microbiota and sPTB.

Methods: In a prospective cohort of nulliparous pregnant women, we assessed vaginal microbiota composition, vaginal immunoglobulins (Igs), and local inflammatory markers. We performed a nested case-control study with 19 sPTB cases, matched based on ethnicity and midwifery practice to 19 term controls.

Results: Of the 294 included participants, 23 pregnancies ended in sPTB. We demonstrated that Lactobacillus iners-dominated microbiota, diverse microbiota, and ethnicity were all independently associated with sPTB. Microbial Ig coating was associated with both microbiota composition and ethnicity, but a direct association with sPTB was lacking. Microbial IgA and IgG coating were lowest in diverse microbiota, especially in women of any ethnic minority. When correcting for microbiota composition, increased microbial Ig coating correlated with increased inflammation.

Conclusion: In these nulliparous pregnant women, vaginal microbiota composition is strongly associated with sPTB. Our results support that vaginal mucosal Igs might play a pivotal role in microbiota composition, microbiota-related inflammation, and vaginal community disparity within and between ethnicities. This study provides insight in host-microbe interaction, suggesting that vaginal mucosal Igs play an immunomodulatory role similar to that in the intestinal tract. Video Abstract.

Citing Articles

Vaginal and endometrial microbiome dysbiosis associated with adverse embryo transfer outcomes.

Su W, Gong C, Zhong H, Yang H, Chen Y, Wu X Reprod Biol Endocrinol. 2024; 22(1):111.

PMID: 39198832 PMC: 11351450. DOI: 10.1186/s12958-024-01274-y.

Vaginal microbiota and spontaneous preterm birth in pregnant women at high risk of recurrence.

Schuster H, Bos A, Himschoot L, van Eekelen R, Matamoros S, de Boer M Heliyon. 2024; 10(10):e30685.

PMID: 38803950 PMC: 11128838. DOI: 10.1016/j.heliyon.2024.e30685.

References

Breedveld A, van Egmond M . IgA and FcαRI: Pathological Roles and Therapeutic Opportunities. Front Immunol. 2019; 10:553. PMC: 6448004. DOI: 10.3389/fimmu.2019.00553. View

Green E, Arck P . Pathogenesis of preterm birth: bidirectional inflammation in mother and fetus. Semin Immunopathol. 2020; 42(4):413-429. PMC: 7508962. DOI: 10.1007/s00281-020-00807-y. View

Hansen I, Hoepel W, Zaat S, Baeten D, Dunnen J . Serum IgA Immune Complexes Promote Proinflammatory Cytokine Production by Human Macrophages, Monocytes, and Kupffer Cells through FcαRI-TLR Cross-Talk. J Immunol. 2017; 199(12):4124-4131. DOI: 10.4049/jimmunol.1700883. View

Kumar M, Murugesan S, Singh P, Saadaoui M, Elhag D, Terranegra A . Vaginal Microbiota and Cytokine Levels Predict Preterm Delivery in Asian Women. Front Cell Infect Microbiol. 2021; 11:639665. PMC: 7969986. DOI: 10.3389/fcimb.2021.639665. View

Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett W . Metagenomic biomarker discovery and explanation. Genome Biol. 2011; 12(6):R60. PMC: 3218848. DOI: 10.1186/gb-2011-12-6-r60. View

Nasioudis D, Forney L, Schneider G, Gliniewicz K, France M, Boester A . Influence of Pregnancy History on the Vaginal Microbiome of Pregnant Women in their First Trimester. Sci Rep. 2017; 7(1):10201. PMC: 5579028. DOI: 10.1038/s41598-017-09857-z. View

Breedveld A, Schuster H, van Houdt R, Painter R, Mebius R, van der Veer C . Enhanced IgA coating of bacteria in women with Lactobacillus crispatus-dominated vaginal microbiota. Microbiome. 2022; 10(1):15. PMC: 8787895. DOI: 10.1186/s40168-021-01198-4. View

Sterlin D, Fadlallah J, Adams O, Fieschi C, Parizot C, Dorgham K . Human IgA binds a diverse array of commensal bacteria. J Exp Med. 2020; 217(3). PMC: 7062531. DOI: 10.1084/jem.20181635. View

Soneji S, Beltran-Sanchez H . Association of Maternal Cigarette Smoking and Smoking Cessation With Preterm Birth. JAMA Netw Open. 2019; 2(4):e192514. PMC: 6481448. DOI: 10.1001/jamanetworkopen.2019.2514. View

10.

Peelen M, Moller Luef B, Lamont R, De Milliano I, Jensen J, Limpens J . The influence of the vaginal microbiota on preterm birth: A systematic review and recommendations for a minimum dataset for future research. Placenta. 2019; 79:30-39. DOI: 10.1016/j.placenta.2019.03.011. View

11.

Usala S, Usala F, Haciski R, Holt J, SCHUMACHER G . IgG and IgA content of vaginal fluid during the menstrual cycle. J Reprod Med. 1989; 34(4):292-4. View

12.

Borgdorff H, van der Veer C, van Houdt R, Alberts C, de Vries H, Bruisten S . The association between ethnicity and vaginal microbiota composition in Amsterdam, the Netherlands. PLoS One. 2017; 12(7):e0181135. PMC: 5507447. DOI: 10.1371/journal.pone.0181135. View

13.

Okai S, Usui F, Yokota S, Hori-I Y, Hasegawa M, Nakamura T . High-affinity monoclonal IgA regulates gut microbiota and prevents colitis in mice. Nat Microbiol. 2016; 1(9):16103. DOI: 10.1038/nmicrobiol.2016.103. View

14.

Petrova M, Reid G, Vaneechoutte M, Lebeer S . Lactobacillus iners: Friend or Foe?. Trends Microbiol. 2016; 25(3):182-191. DOI: 10.1016/j.tim.2016.11.007. View

15.

Callahan B, McMurdie P, Rosen M, Han A, Johnson A, Holmes S . DADA2: High-resolution sample inference from Illumina amplicon data. Nat Methods. 2016; 13(7):581-3. PMC: 4927377. DOI: 10.1038/nmeth.3869. View

16.

Fettweis J, Serrano M, Brooks J, Edwards D, Girerd P, Parikh H . The vaginal microbiome and preterm birth. Nat Med. 2019; 25(6):1012-1021. PMC: 6750801. DOI: 10.1038/s41591-019-0450-2. View

17.

Blencowe H, Cousens S, Oestergaard M, Chou D, Moller A, Narwal R . National, regional, and worldwide estimates of preterm birth rates in the year 2010 with time trends since 1990 for selected countries: a systematic analysis and implications. Lancet. 2012; 379(9832):2162-72. DOI: 10.1016/S0140-6736(12)60820-4. View

18.

Harmsen H, Pouwels S, Funke A, Bos N, Dijkstra G . Crohn's disease patients have more IgG-binding fecal bacteria than controls. Clin Vaccine Immunol. 2012; 19(4):515-21. PMC: 3318288. DOI: 10.1128/CVI.05517-11. View

19.

Ashford K, Chavan N, Wiggins A, Sayre M, McCubbin A, Critchfield A . Comparison of Serum and Cervical Cytokine Levels throughout Pregnancy between Preterm and Term Births. AJP Rep. 2018; 8(2):e113-e120. PMC: 5980496. DOI: 10.1055/s-0038-1656534. View

20.

Bayigga L, Kateete D, Anderson D, Sekikubo M, Nakanjako D . Diversity of vaginal microbiota in sub-Saharan Africa and its effects on HIV transmission and prevention. Am J Obstet Gynecol. 2018; 220(2):155-166. PMC: 10715630. DOI: 10.1016/j.ajog.2018.10.014. View