Bile Acids Impair Vaccine Response in Children With Biliary Atresia

Overview

Journal Front Immunol

Specialty Allergy & Immunology

Date 2021 May 3

PMID 33936059

Citations 5

Authors

Jinchuan Liu

Yi Fei

Tao Zhou

Hao Ji

Ji Wu

Xiangqian Gu

Yi Luo

Jianjun Zhu

Mingxuan Feng

Ping Wan

Bijun Qiu

Yefeng Lu

Tian Yang

Pengfei Deng

Cuiping Zhou

Dongcheng Gong

Jun Deng

Feng Xue

Qiang Xia

Affiliations

Soon will be listed here.

Abstract

Background: Vaccination is the best way to protect children under 5 years from death or disability. Children with biliary atresia (BA), which is the most common pediatric cholestatic end-stage liver disease (PELD), are more vulnerable to infectious diseases. However, the vaccination coverage and factors modulating vaccine responses in children with BA are largely unknown.

Methods: In this study, 288 children (median age: 7 months) diagnosed with BA before liver transplantation were enrolled for the evaluation of vaccination status and the factors affecting the immune response to the hepatitis B (HBV) vaccine. Moreover, 49 BA children (median age: 4 months) were enrolled for flow cytometric analysis of CD4 T cells and CD19 B cell subsets and correlations with serum bile acid levels.

Results: Generally, these children had very low routine vaccination rates for the meningococcal serogroup AC (Men AC) (41.2%), measles-mumps-rubella (MMR) (31.3%), poliomyelitis (Polio) (25.3%), hepatitis A (HAV) (25.0%), Japanese encephalitis (JE) (15.0%), diphtheria-tetanus-pertussis (DTP) (14.2%), meningococcal serogroup A (Men A) (13.5%) and varicella (VAR) (10.8%) vaccines, but not for the HBV (96.2%) and bacillus Calmette-Guérin (BCG) (84.7%) vaccines. Remarkably, 19.8% (57/288) of the patients had HBV infection. Out of 220 patients vaccinated for HBV, 113 (51.4%), 85 (38.6%) and 22 (10%) had one, two or three doses of the HBV vaccine, respectively. Furthermore, logistic regression analysis revealed that the bile acid level was an independent factor associated with poor HBV vaccine response ( = 0.03; OR = 0.394; 95% CI = 0.170-0.969). Immunophenotyping showed that bile acids were only negatively correlated with the CD19CD27IgG post-class-switched memory B cell ratio ( = 0.01).

Conclusion: This study reveals the overall vaccination rates of routine vaccines in Chinese BA children are very low and the poor HBV vaccine responses are associated with bile acids, possibly the inhibition of CD19CD27IgG post-class-switched memory B cell response.

Clinical Trial Registration: http://www.chictr.org.cn, identifier ChiCTR1800019165.

Citing Articles

A pre-vaccination immune metabolic interplay determines the protective antibody response to a dengue virus vaccine.

Pelletier A, Pacheco Sanchez G, Izmirly A, Watson M, Di Pucchio T, Carvalho K Cell Rep. 2024; 43(7):114370.

PMID: 38900640 PMC: 11404042. DOI: 10.1016/j.celrep.2024.114370.

Vaccine Responses in Patients with Liver Cirrhosis: From the Immune System to the Gut Microbiota.

Airola C, Andaloro S, Gasbarrini A, Ponziani F Vaccines (Basel). 2024; 12(4).

PMID: 38675732 PMC: 11054513. DOI: 10.3390/vaccines12040349.

Bile acids regulate MAdCAM-1 expression to link the gut microbiota to cancer immunosurveillance.

Fidelle M, Tian A, Zitvogel L, Kroemer G Oncoimmunology. 2023; 12(1):2224672.

PMID: 37405191 PMC: 10316723. DOI: 10.1080/2162402X.2023.2224672.

Gut microbiota derived bile acid metabolites maintain the homeostasis of gut and systemic immunity.

Su X, Gao Y, Yang R Front Immunol. 2023; 14:1127743.

PMID: 37256134 PMC: 10225537. DOI: 10.3389/fimmu.2023.1127743.

Neonatal Hepatic Myeloid Progenitors Expand and Propagate Liver Injury in Mice.

Alkhani A, Korsholm C, Levy C, Mohamedaly S, Duwaerts C, Pietras E J Clin Med. 2023; 12(1).

PMID: 36615137 PMC: 9821039. DOI: 10.3390/jcm12010337.

References

Cui F, Shen L, Li L, Wang H, Wang F, Bi S . Prevention of Chronic Hepatitis B after 3 Decades of Escalating Vaccination Policy, China. Emerg Infect Dis. 2017; 23(5):765-772. PMC: 5403029. DOI: 10.3201/eid2305.161477. View

Fiorucci S, Biagioli M, Zampella A, Distrutti E . Bile Acids Activated Receptors Regulate Innate Immunity. Front Immunol. 2018; 9:1853. PMC: 6099188. DOI: 10.3389/fimmu.2018.01853. View

Zimmermann P, Curtis N . Factors That Influence the Immune Response to Vaccination. Clin Microbiol Rev. 2019; 32(2). PMC: 6431125. DOI: 10.1128/CMR.00084-18. View

Kikuchi K, Hsu W, Hosoya N, Moritoki Y, Kajiyama Y, Kawai T . Ursodeoxycholic acid reduces CpG-induced IgM production in patients with primary biliary cirrhosis. Hepatol Res. 2009; 39(5):448-54. DOI: 10.1111/j.1872-034X.2008.00474.x. View

Greene S, Ahmed J, Datta S, Burns C, Quddus A, Vertefeuille J . Progress Toward Polio Eradication - Worldwide, January 2017-March 2019. MMWR Morb Mortal Wkly Rep. 2019; 68(20):458-462. PMC: 6532951. DOI: 10.15585/mmwr.mm6820a3. View

Osterholm M, Kelley N, Sommer A, Belongia E . Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis. 2011; 12(1):36-44. DOI: 10.1016/S1473-3099(11)70295-X. View

Tarlinton D, Good-Jacobson K . Diversity among memory B cells: origin, consequences, and utility. Science. 2013; 341(6151):1205-11. DOI: 10.1126/science.1241146. View

. Progress in hepatitis B prevention through universal infant vaccination--China, 1997-2006. MMWR Morb Mortal Wkly Rep. 2007; 56(18):441-5. View

Hang S, Paik D, Yao L, Kim E, Trinath J, Lu J . Bile acid metabolites control T17 and T cell differentiation. Nature. 2019; 576(7785):143-148. PMC: 6949019. DOI: 10.1038/s41586-019-1785-z. View

10.

Mieli-Vergani G, Vergani D . Biliary atresia. Semin Immunopathol. 2009; 31(3):371-81. DOI: 10.1007/s00281-009-0171-6. View

11.

Pol S . Hepatitis: HBV vaccine--the first vaccine to prevent cancer. Nat Rev Gastroenterol Hepatol. 2015; 12(4):190-1. DOI: 10.1038/nrgastro.2015.28. View

12.

Dehghani S, Shakiba M, Ziaeyan M, Imanieh M, Haghighat M, Sedaghat M . Evaluation of immunity status to routine vaccination in pediatric liver transplant candidates. Turk J Gastroenterol. 2015; 25 Suppl 1:26-31. DOI: 10.5152/tjg.2014.5139. View

13.

Poland G, Ovsyannikova I, Kennedy R . Personalized vaccinology: A review. Vaccine. 2017; 36(36):5350-5357. PMC: 5792371. DOI: 10.1016/j.vaccine.2017.07.062. View

14.

Wu J, Ni Y, Chen H, Hsu H, Lai H, Chang M . Humoral immunogenicity to measles, rubella, and varicella-zoster vaccines in biliary atresia children. Vaccine. 2009; 27(21):2812-5. DOI: 10.1016/j.vaccine.2009.02.094. View

15.

Dehghani S, Shakiba M, Ziaeyan M, Imanieh M, Haghighat M, Bahador A . Vaccination status in pediatric liver transplant candidates. Pediatr Transplant. 2009; 13(7):820-2. DOI: 10.1111/j.1399-3046.2009.01177.x. View

16.

Balistreri W, Heubi J, Suchy F . Immaturity of the enterohepatic circulation in early life: factors predisposing to "physiologic" maldigestion and cholestasis. J Pediatr Gastroenterol Nutr. 1983; 2(2):346-54. View

17.

Verkade H, Bezerra J, Davenport M, Schreiber R, Mieli-Vergani G, Hulscher J . Biliary atresia and other cholestatic childhood diseases: Advances and future challenges. J Hepatol. 2016; 65(3):631-42. DOI: 10.1016/j.jhep.2016.04.032. View

18.

Yaghobi R, Didari M, Gramizadeh B, Rahsaz M, Heidari T, Banihashemi M . Study of viral infections in infants with biliary atresia. Indian J Pediatr. 2010; 78(4):478-81. DOI: 10.1007/s12098-010-0309-5. View

19.

. Global prevalence, treatment, and prevention of hepatitis B virus infection in 2016: a modelling study. Lancet Gastroenterol Hepatol. 2018; 3(6):383-403. DOI: 10.1016/S2468-1253(18)30056-6. View

20.

Akkaya M, Kwak K, Pierce S . B cell memory: building two walls of protection against pathogens. Nat Rev Immunol. 2019; 20(4):229-238. PMC: 7223087. DOI: 10.1038/s41577-019-0244-2. View