Evidence map›Paper›PMID 32437829›Full record

ArticleJournal of hepatology2020

Associations between reproductive factors and biliary tract cancers in women from the Biliary Tract Cancers Pooling Project.

Sarah S Jackson, Hans-Olov Adami, Gabriella Andreotti, Laura E Beane-Freeman, Amy Berrington de González, Julie E Buring, Gary E Fraser, Neal D Freedman, Susan M Gapstur, Gretchen Gierach and 33 more

Open access · greenAbstract readMulticenter Study
PubMed Full text at PMC Publisher
In one paragraph

Article in Journal of hepatology, 2020. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 25 papers.

0numbers the graph read from it
0cells of the map it votes in
25citing papers in PubMed
2.2field-weighted citation impact, top 12% of its field
1 · What the graph read from it

What it found

Each row is one number read from the abstract, on the scale the paper reported it, with its interval. Left of the dashed line favours the treatment, right favours the comparator. Under each row is the sentence it came from. New to these charts? A ten-minute tutorial.

The abstract states no effect estimate the extractor could read, or names no intervention and outcome on the map, so this paper lights no cell and moves no belief. It is still indexed, cited and linked below.

2 · The registry

The trial behind it

Trials whose registry record cites this paper, or whose number appears in the abstract. A trial that started after this paper was published is citing it as background, not reporting it.

Neither the registry nor the abstract names a trial number. If this is a trial report, that itself is worth knowing.

3 · Its place in the literature

Who cites it

25 citing papers in PubMed, 33 citations in OpenAlex.

  1. Article
  2. Sexual dimorphism in the liver.Nature reviews. Gastroenterology & hepatology · 2026
    Review
  3. Review
  4. Article
  5. Article
  6. Gastrointestinal cancers in women: The role of sex hormones.Indian journal of gastroenterology : official journal of the Indian Society of Gastroenterology · 2026
    Review
  7. Article
  8. Article
  9. Article
  10. Review
  11. Article
  12. Review
  13. Article
  14. Article
  15. Article
  16. Article
  17. Article
  18. Review
  19. Gallbladder cancer.Nature reviews. Disease primers · 2022
    Review
  20. Article
4 · The record

Corrections and comments

PubMed lists nothing against this paper. Absence here is not a guarantee, only a check that was made.

5 · Who and what money

Authors and funding

43 authors at 19 institutions in 6 countries.

Sarah S JacksonDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA. Electronic address: sarah.jackson@nih.gov.
Hans-Olov AdamiDepartment of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
Gabriella AndreottiDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Laura E Beane-FreemanDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Amy Berrington de GonzálezDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Julie E BuringDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA; Division of Preventive Medicine, Department of Medicine, Brigham and Women's Hospital, Boston, MA, USA.
Gary E FraserSchool of Public Health, Loma Linda University, Loma Linda, CA, USA.
Neal D FreedmanDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Susan M GapsturBehavioral and Epidemiology Research Group, American Cancer Society, Inc., Atlanta, GA, USA.
Gretchen GierachDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Graham G GilesCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Australia; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Parkville, Victoria, Australia; Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
Francine GrodsteinDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
Patricia HartgeDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Mazda JenabSection of Nutrition and Metabolism, International Agency for Research on Cancer (IARC-WHO), Lyon, France.
Victoria KirshOntario Institute for Cancer Research, Toronto, Ontario, Canada; Dalla Lana School of Public Health, University of Toronto, Toronto, Ontario, Canada.
Synnove F KnutsenSchool of Public Health, Loma Linda University, Loma Linda, CA, USA.
Qing LanDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Susanna C LarssonUnit of Cardiovascular and Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
I-Min LeeDepartment of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA; Division of Preventive Medicine, Department of Medicine, Brigham and Women's Hospital, Boston, MA, USA.
Mei-Hsuan LeeInstitute of Clinical Medicine, National Yang-Ming University, Taipei, Taiwan.
Linda M LiaoDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Roger L MilneCancer Epidemiology Division, Cancer Council Victoria, Melbourne, Australia; Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Parkville, Victoria, Australia; Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, Victoria, Australia.
Kristine R MonroeDepartment of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
Marian L NeuhouserCancer Prevention Program, Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
Katie M O'BrienEpidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
Jessica L PetrickSlone Epidemiology Center, Boston University, Boston, MA, USA.
Mark P PurdueDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Thomas E RohanDepartment of Epidemiology and Population Health, Albert Einstein College of Medicine, Bronx, NY, USA.
Sven SandinDepartment of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
Dale P SandlerEpidemiology Branch, National Institute of Environmental Health Sciences, Research Triangle Park, NC, USA.
Norie SawadaEpidemiology and Prevention Group, Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
Aladdin H ShadyabDepartment of Family Medicine and Public Health, University of California San Diego School of Medicine, La Jolla, CA, USA.
Tracey G SimonDivision of Gastroenterology, Department of Medicine, Massachusetts General Hospital, Boston, MA, USA; Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical, Boston, MA, USA.
Rashmi SinhaDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Rachael Stolzenberg-SolomonDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Shoichiro TsuganeEpidemiology and Prevention Group, Center for Public Health Sciences, National Cancer Center, Tokyo, Japan.
Elisabete WeiderpassInternational Agency for Research on Cancer (IARC), Lyon, France.
Alicja WolkUnit of Cardiovascular and Nutritional Epidemiology, Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Department of Surgical Sciences, Uppsala University, Uppsala, Sweden.
Hwai-I YangGenomics Research Center, Academia Sinica, Taipei, Taiwan; Institute of Clinical Medicine, National Yang-Ming University, Taipei, Taiwan.
Wei ZhengDivision of Epidemiology, Department of Medicine, Vanderbilt Epidemiology Center, Vanderbilt-Ingram Cancer Center, Vanderbilt University, Nashville, TN, USA.
Katherine A McGlynnDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
Peter T CampbellBehavioral and Epidemiology Research Group, American Cancer Society, Inc., Atlanta, GA, USA.
Jill KoshiolDivision of Cancer Epidemiology and Genetics, National Cancer Institute, Rockville, MD, USA.
National Cancer Institute · USAmerican Cancer Society · USBrigham and Women's Hospital · USCentre international de recherche sur le cancer · FRKarolinska Institutet · SELoma Linda University · USNational Institute of Environmental Health Sciences · USNational Yang Ming Chiao Tung University · TWThe University of Melbourne · AUUppsala University · SEAlbert Einstein College of Medicine · USBoston University · USFred Hutch Cancer Center · USHarvard University · USMassachusetts General Hospital · USOntario Institute for Cancer Research · CAUniversity of California San Diego · USUniversity of Southern California · USVanderbilt University · US

Funding

Statistical MethodsP01CA087969 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI TWOROGER, SHELLEY S · 2000 to 2019
$77.8M
Understanding Population Differences in Cancer: The MEC StudyU01CA164973 · NCI · UNIVERSITY OF HAWAII AT MANOA · PI HAIMAN, CHRISTOPHER ALAN, LE MARCHAND, LOIC · 2015 to 2025
$37.4M
Etiology of Biliary Tract CancerZIACP010218 · NCI · DIVISION OF CANCER EPIDEMIOLOGY AND GENETICS · PI KOSHIOL, JILL · 2011 to 2025
$30.4M
Women's Health Study: Continued Follow-upR01CA047988 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI BURING, JULIE E., LEE, I-MIN · 1991 to 2014
$28.2M
Environmental and Genetic Risk Factors For Breast Cancer: The Sister StudyZIAES044005 · NIEHS · NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES · PI SANDLER, DALE P · 2009 to 2025
$22.7M
Long Term Multidisciplinary Study of Cancer in Women: The Nurses Health StudyUM1CA186107 · NCI · BRIGHAM AND WOMEN'S HOSPITAL · PI ELIASSEN, A. HEATHER, STAMPFER, MEIR · 2014 to 2023
$22.3M
VALIDATION OF A DIET HISTORY METHOD FOR EPIDEMIOLOGIC STUDIES OF CANCERP01CA033619 · NCI · UNIVERSITY OF HAWAII AT MANOA · PI KOLONEL, LAURENCE N. · 1985 to 2010
$18.5M
Health Effects Of Exposures In AgricultureZIAES049030 · NIEHS · NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES · PI SANDLER, DALE P · 2009 to 2025
$11.2M
Cohort Study of Cancer inhibitory Factors in MenR01CA082729 · NCI · VANDERBILT UNIVERSITY · PI SHU, XIAO-OU · 2001 to 2011
$6.3M
Plant-based diets and risk of cancerU01CA152939 · NCI · LOMA LINDA UNIVERSITY · PI FRASER, GARY E. · 2011 to 2015
$5.7M
Shanghai Men's Health StudyUM1CA173640 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI SHU, XIAO-OU · 2013 to 2017
$4.9M
Cancer Risk Reduction and Diet: A Cohort Study of WomenR37CA070867 · NCI · VANDERBILT UNIVERSITY MEDICAL CENTER · PI ZHENG, WEI · 2009 to 2013
$4.7M
British Heart FoundationCancer Research UKDepartment of HealthIntramural NIH HHS Z01 ES044005Intramural NIH HHS Z01 ES049030Intramural NIH HHS Z99 CA999999Intramural NIH HHS ZIA CP010218Medical Research CouncilNCI NIH HHS P01 CA033619NCI NIH HHS P01 CA087969NCI NIH HHS R01 CA047988NCI NIH HHS R01 CA082729NCI NIH HHS R37 CA070867NCI NIH HHS U01 CA152939NCI NIH HHS U01 CA164973NCI NIH HHS U01 CA182913NCI NIH HHS UM1 CA173640NCI NIH HHS UM1 CA182913NCI NIH HHS UM1 CA186107NHLBI NIH HHS HHSN268201600001CNHLBI NIH HHS HHSN268201600002CNHLBI NIH HHS HHSN268201600003CNHLBI NIH HHS HHSN268201600004CNHLBI NIH HHS HHSN268201600018CNHLBI NIH HHS R01 HL043851NHLBI NIH HHS R01 HL080467NHLBI NIH HHS RC1 HL099355Wellcome TrustWorld Health Organization 001
6 · The paper itself

Abstract

BACKGROUND &

aimsGallbladder cancer (GBC) is known to have a female predominance while other biliary tract cancers (BTCs) have a male predominance. However, the role of female reproductive factors in BTC etiology remains unclear.

methodsWe pooled data from 19 studies of >1.5 million women participating in the Biliary Tract Cancers Pooling Project to examine the associations of parity, age at menarche, reproductive years, and age at menopause with BTC. Associations for age at menarche and reproductive years with BTC were analyzed separately for Asian and non-Asian women. Hazard ratios (HRs) and 95% CIs were estimated using Cox proportional hazards models, stratified by study.

resultsDuring 21,681,798 person-years of follow-up, 875 cases of GBC, 379 of intrahepatic bile duct cancer (IHBDC), 450 of extrahepatic bile duct cancer (EHBDC), and 261 of ampulla of Vater cancer (AVC) occurred. High parity was associated with risk of GBC (HR ≥5 vs. 0 births 1.72; 95% CI 1.25-2.38). Age at menarche (HR per year increase 1.15; 95% CI 1.06-1.24) was associated with GBC risk in Asian women while reproductive years were associated with GBC risk (HR per 5 years 1.13; 95% CI 1.04-1.22) in non-Asian women. Later age at menarche was associated with IHBDC (HR 1.19; 95% CI 1.09-1.31) and EHBDC (HR 1.11; 95% CI 1.01-1.22) in Asian women only.

conclusionWe observed an increased risk of GBC with increasing parity. Among Asian women, older age at menarche was associated with increased risk for GBC, IHBDC, and EHBDC, while increasing reproductive years was associated with GBC in non-Asian women. These results suggest that sex hormones have distinct effects on cancers across the biliary tract that vary by geography. LAY SUMMARY: Our findings show that the risk of gallbladder cancer is increased among women who have given birth (especially women with 5 or more children). In women from Asian countries, later age at menarche increases the risk of gallbladder cancer, intrahepatic bile duct cancer and extrahepatic bile duct cancer. We did not see this same association in women from Western countries. Age at menopause was not associated with the risk of any biliary tract cancers.

Indexed as

RegistriesAdultAgedBiliary Tract NeoplasmsFemaleFollow-Up StudiesGlobal HealthHumansIncidenceMiddle AgedProspective StudiesReproductionRisk AssessmentRisk FactorsSex FactorsSurvival RateBiliary tract cancerGallbladder cancerParityReproductive factors

Identifiers

PMID32437829
PMCPMC7901003
OpenAlexW3022888652

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Registered trials

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Read under generation 80e0d062 · epoch 390. Bibliography from PubMed, PubMed Central and OpenAlex; grants from NIH RePORTER; trial links from ClinicalTrials.gov; estimates, votes and beliefs from the OpenQuestion graph.