---
title: "Reproductive factors and stromal fibroblast marker expression in benign breast biopsies"
id: "british-journal-of-cancer-0-reproductive-factors-and-the-expression-of-stromal-markers-in-benign-breast"
canonical_url: "https://medichelpline.com/clinical-feed/british-journal-of-cancer-0-reproductive-factors-and-the-expression-of-stromal-markers-in-benign-breast"
content_type: "clinical_feed_article"
specialty: "Oncology"
source_name: "British Journal of Cancer"
source_url: "https://www.nature.com/articles/s41416-026-03615-7"
published_at: "2026-09-22T12:00:00.000Z"
evidence_level: "Journal Feed"
license: "CC-BY-NC-4.0 / Informational Use"
---
# Reproductive factors and stromal fibroblast marker expression in benign breast biopsies
## Provenance & Clinical Metadata
- **Canonical URL:** https://medichelpline.com/clinical-feed/british-journal-of-cancer-0-reproductive-factors-and-the-expression-of-stromal-markers-in-benign-breast
- **Specialty:** [Oncology](https://medichelpline.com/clinical-feed/oncology.md)
- **Primary Source:** British Journal of Cancer
- **Source URL:** [Original Journal Publication](https://www.nature.com/articles/s41416-026-03615-7)
- **Published At:** 2026-09-22T12:00:00.000Z
- **Evidence Rating:** Journal Feed
## Executive GIST (TL;DR)
- This study assessed associations between reproductive factors and expression of stromal fibroblast activation markers in benign breast tissue from women with biopsy-confirmed benign breast disease in the Nurses’ Health Study II (NHSII). - Stromal markers evaluated were **αSMA**, **TNC**, **FAP**, **S100A6**, and **MMP14**, measured by immunofluorescence on tissue microarrays with percent positivity quantified per core. - Reproductive exposures examined included parity (including nulliparity), number of children, age at first birth, breastfeeding, age at menarche (continuous and categorical), time between menarche and first birth, and time since last birth; these were obtained from biennial NHSII questionnaires. - Statistical analysis used generalized linear regression on log-transformed marker positivity; models adjusted for covariates in multivariate analyses (specific covariates and full model specification were not reported in the provided source text). - Key findings reported in the abstract: a suggestive positive association between **nulliparous** status and **TNC** expression (β = 0.79, 95% CI −0.10 to 1.68, p = 0.08). No associations with nulliparity were observed for the other markers (all p > 0.10). - No statistically significant associations were observed between number of children, age at first birth, breastfeeding, continuous age at menarche, time between menarche and first birth, or time since last birth and any marker expression. - Categorical age at menarche showed a suggestive positive trend for **MMP14** expression (p-trend = 0.07). - The authors conclude that **nulliparity** and **age at menarche** may be related to expression of stromal activation markers **TNC** and **MMP14**, respectively, but emphasize that further studies are needed to confirm these findings. - Background context: parity, age at first birth, breastfeeding, and age at menarche are established reproductive influences on breast cancer risk and mammographic density; the study explored whether these factors relate to stromal biomarker expression as a potential pathway affecting risk. - Note: the provided source text is truncated and does not include full details of sample selection numbers beyond the 694 participants in the abstract, complete covariate lists, full methods, or extended results and discussion; those details were not reported in the source excerpt available here.
## Clinical Analysis & Structured Key Points
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[nature](https://www.nature.com/) 2. [british journal of cancer](https://www.nature.com/bjc) 3. [articles](https://www.nature.com/bjc/articles?type=article) 4. article Reproductive factors and the expression of stromal markers in benign breast biopsy samples [ Download PDF ](https://www.nature.com/articles/s41416-026-03615-7.pdf) [ Download PDF ](https://www.nature.com/articles/s41416-026-03615-7.pdf) * Article * [Open access](https://www.springernature.com/gp/open-science/about/the-fundamentals-of-open-access-and-open-research) * Published: 22 September 2026 Epidemiology # Reproductive factors and the expression of stromal markers in benign breast biopsy samples * [Maisey Ratcliffe](https://www.nature.com/articles/s41416-026-03615-7#auth-Maisey-Ratcliffe-Aff1)[1](https://www.nature.com/articles/s41416-026-03615-7#Aff1), * [Yujing J. Heng](https://www.nature.com/articles/s41416-026-03615-7#auth-Yujing_J_-Heng-Aff2) [ORCID: orcid.org/0000-0002-8930-817X](https://orcid.org/0000-0002-8930-817X)[2](https://www.nature.com/articles/s41416-026-03615-7#Aff2), * [Yaileen D. Guzman-Arocho](https://www.nature.com/articles/s41416-026-03615-7#auth-Yaileen_D_-Guzman_Arocho-Aff2)[2](https://www.nature.com/articles/s41416-026-03615-7#Aff2), * [Bernard Rosner](https://www.nature.com/articles/s41416-026-03615-7#auth-Bernard-Rosner-Aff3) [ORCID: orcid.org/0000-0001-6907-0056](https://orcid.org/0000-0001-6907-0056)[3](https://www.nature.com/articles/s41416-026-03615-7#Aff3), * [Rulla M. Tamimi](https://www.nature.com/articles/s41416-026-03615-7#auth-Rulla_M_-Tamimi-Aff4) [ORCID: orcid.org/0000-0003-2306-8668](https://orcid.org/0000-0003-2306-8668)[4](https://www.nature.com/articles/s41416-026-03615-7#Aff4) & * … * [Lusine Yaghjyan](https://www.nature.com/articles/s41416-026-03615-7#auth-Lusine-Yaghjyan-Aff1) [ORCID: orcid.org/0000-0002-1626-5340](https://orcid.org/0000-0002-1626-5340)[1](https://www.nature.com/articles/s41416-026-03615-7#Aff1) Show authors [_British Journal of Cancer_](https://www.nature.com/bjc) (2026) [Cite this article](https://www.nature.com/articles/s41416-026-03615-7#citeas) [ Save article ](https://www.nature.com/articles/s41416-026-03615-7/save-research?_csrf=xfzOWA6T75vXA20J9pRVaMo9jL_Jy6ib) [ View saved research ](https://www.nature.com/saved-research) ## Abstract ### Background We examined the associations of several reproductive factors with expression of stromal fibroblast markers αSMA, TNC, FAP, S100A6, and MMP14. ### Methods We included 694 cancer-free women with biopsy-confirmed incident benign breast disease within the Nurses’ Health Study II. Breast cancer risk factor data were obtained from biennial questionnaires. Immunofluorescence of stromal markers was completed on tissue microarrays. For each core, % positivity was quantified with inForm v2.6.0. Generalized linear regression was used to examine the associations of reproductive factors with log-transformed positivity for each marker. ### Results In multivariate analysis, nulliparous status showed a suggestive positive association with TNC expression (β = 0.79, 95% CI −0.10, 1.68, _p_ = 0.08) but was not associated with the other stromal markers (all _p_ > 0.10). No associations were seen for number of children, age at 1st birth, breastfeeding, continuous age at menarche, time between menarche and age at first birth, and time since last birth with any of the markers’ expression. Categorical age at menarche showed a suggestive positive association with MMP14 (_p_ -trend = 0.07). ### Conclusion Our findings suggest that nulliparous status and age at menarche may be associated with the expression of stromal fibroblast activation markers TNC and MMP14, respectively. Further studies are needed to confirm these findings. ### Explore related subjects Discover the latest articles and news in related subjects. * [Breast cancer](https://www.nature.com/subjects/breast-cancer) * [Epidemiology](https://www.nature.com/subjects/epidemiology) ## Introduction Reproductive factors are known to influence breast cancer risk. Notably, parity has been consistently associated with a reduced breast cancer risk [[1](https://www.nature.com/articles/s41416-026-03615-7#ref-CR1 "Woolcott CG, Koga K, Conroy SM, Byrne C, Nagata C, Ursin G, et al. Mammographic density, parity and age at first birth, and risk of breast cancer: an analysis of four case-control studies. Breast Cancer Res Treat. 2012;132:1163–71."),[2](https://www.nature.com/articles/s41416-026-03615-7#ref-CR2 "Ramon JM, Escriba JM, Casas I, Benet J, Iglesias C, Gavalda L, et al. Age at first full-term pregnancy, lactation and parity and risk of breast cancer: a case-control study in Spain. Eur J Epidemiol. 1996;12:449–53."),[3](https://www.nature.com/articles/s41416-026-03615-7#ref-CR3 "Britt K, Ashworth A, Smalley M. Pregnancy and the risk of breast cancer. Endocr Relat Cancer. 2007;14:907–33.")] and decreased mammographic breast density [[4](https://www.nature.com/articles/s41416-026-03615-7#ref-CR4 "Modugno F, Ngo DL, Allen GO, Kuller LH, Ness RB, Vogel VG, et al. Breast cancer risk factors and mammographic breast density in women over age 70. Breast Cancer Res Treat. 2006;97:157–66."),[5](https://www.nature.com/articles/s41416-026-03615-7#ref-CR5 "Yaghjyan L, Mahoney MC, Succop P, Wones R, Buckholz J, Pinney SM. Relationship between breast cancer risk factors and mammographic breast density in the Fernald Community Cohort. Br J Cancer. 2012;106:996–1003."),[6](https://www.nature.com/articles/s41416-026-03615-7#ref-CR6 "Vachon CM, Kuni CC, Anderson K, Anderson VE, Sellers TA. Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer \(United States\). Cancer Causes Control. 2000;11:653–62."),[7](https://www.nature.com/articles/s41416-026-03615-7#ref-CR7 "Yaghjyan L, Colditz GA, Rosner B, Bertrand KA, Tamimi RM. Reproductive factors related to childbearing and mammographic breast density. Breast Cancer Res Treat. 2016;158:351–9.")], with a recent meta-analysis suggesting approximately 3% and 12% breast cancer risk reduction with each additional full-term pregnancy in pre- and postmenopausal women, respectively [[8](https://www.nature.com/articles/s41416-026-03615-7#ref-CR8 "Clavel-Chapelon F, Gerber M. Reproductive factors and breast cancer risk. Do they differ according to age at diagnosis? Breast Cancer Res Treat. 2002;72:107–15.")]. Younger age at first birth and longer breastfeeding have been reported to reduce breast cancer risk [[9](https://www.nature.com/articles/s41416-026-03615-7#ref-CR9 "Stordal B. Breastfeeding reduces the risk of breast cancer: a call for action in high-income countries with low rates of breastfeeding. Cancer Med. 2023;12:4616–25."),[10](https://www.nature.com/articles/s41416-026-03615-7#ref-CR10 "Lord SJ, Bernstein L, Johnson KA, Malone KE, McDonald JA, Marchbanks PA, et al. Breast cancer risk and hormone receptor status in older women by parity, age of first birth, and breastfeeding: a case-control study. Cancer Epidemiol Biomark Prev. 2008;17:1723–30."),[11](https://www.nature.com/articles/s41416-026-03615-7#ref-CR11 "MacMahon B, Cole P, Lin TM, Lowe CR, Mirra AP, Ravnihar B, et al. Age at first birth and breast cancer risk. Bull World Health Organ. 1970;43:209–21.")] with ~3–5% reduction per year for age at first birth[[8](https://www.nature.com/articles/s41416-026-03615-7#ref-CR8 "Clavel-Chapelon F, Gerber M. Reproductive factors and breast cancer risk. Do they differ according to age at diagnosis? Breast Cancer Res Treat. 2002;72:107–15.")] and on average, 4% reduction per 12 months of breastfeeding [[12](https://www.nature.com/articles/s41416-026-03615-7#ref-CR12 "Breast cancer and breastfeeding: collaborative reanalysis of individual data from 47 epidemiological studies in 30 countries, including 50302 women with breast cancer and 96973 women without the disease. Lancet. 2002;360:187–95."), [13](https://www.nature.com/articles/s41416-026-03615-7#ref-CR13 "Islami F, Liu Y, Jemal A, Zhou J, Weiderpass E, Colditz G, et al. Breastfeeding and breast cancer risk by receptor status-a systematic review and meta-analysis. Ann Oncol. 2015;26:2398–407.")]. Later age at menarche has been associated with a 4–9% reduction in breast cancer risk per each additional year [[8](https://www.nature.com/articles/s41416-026-03615-7#ref-CR8 "Clavel-Chapelon F, Gerber M. Reproductive factors and breast cancer risk. Do they differ according to age at diagnosis? Breast Cancer Res Treat. 2002;72:107–15.")] whereas a longer interval between menarche and first pregnancy was associated with approximately 50% increased breast cancer risk for those with ≥16 vs ≤5 years in between the two dates [[14](https://www.nature.com/articles/s41416-026-03615-7#ref-CR14 "Li CI, Malone KE, Daling JR, Potter JD, Bernstein L, Marchbanks PA, et al. Timing of menarche and first full-term birth in relation to breast cancer risk. Am J Epidemiol. 2008;167:230–9.")]. The reproductive factors related to childbearing have also been linked to mammographic breast density, a well-established breast cancer risk factor reflective of the relative proportion of fibroglandular and adipose tissue in the breast [[4](https://www.nature.com/articles/s41416-026-03615-7#ref-CR4 "Modugno F, Ngo DL, Allen GO, Kuller LH, Ness RB, Vogel VG, et al. Breast cancer risk factors and mammographic breast density in women over age 70. Breast Cancer Res Treat. 2006;97:157–66."),[5](https://www.nature.com/articles/s41416-026-03615-7#ref-CR5 "Yaghjyan L, Mahoney MC, Succop P, Wones R, Buckholz J, Pinney SM. Relationship between breast cancer risk factors and mammographic breast density in the Fernald Community Cohort. Br J Cancer. 2012;106:996–1003."),[6](https://www.nature.com/articles/s41416-026-03615-7#ref-CR6 "Vachon CM, Kuni CC, Anderson K, Anderson VE, Sellers TA. Association of mammographically defined percent breast density with epidemiologic risk factors for breast cancer \(United States\). Cancer Causes Control. 2000;11:653–62."),[7](https://www.nature.com/articles/s41416-026-03615-7#ref-CR7 "Yaghjyan L, Colditz GA, Rosner B, Bertrand KA, Tamimi RM. Reproductive factors related to childbearing and mammographic breast density. Breast Cancer Res Treat. 2016;158:351–9.")]. Further, we recently showed that some of the reproductive factors are associated with the proportion of epithelium and stroma in the breast tissue, potentially suggesting their effect on epithelial-stromal interactions [[15](https://www.nature.com/articles/s41416-026-03615-7#ref-CR15 "Yaghjyan L, Austin-Datta RJ, Oh H, Heng YJ, Vellal AD, Sirinukunwattana K, et al. Associations of reproductive breast cancer risk factors with breast tissue composition. Breast Cancer Res. 2021;23:70.")]. The breast is a dynamic organ that undergoes extensive structural changes in response to various influences. The breast stroma consists of cellular components and extracellular matrix that are essential for maintaining tissue structure and function via a variety of mechanisms that could potentially modulate cancer risk [[16](https://www.nature.com/articles/s41416-026-03615-7#ref-CR16 "Conklin MW, Keely PJ. Why the stroma matters in breast cancer: insights into breast cancer patient outcomes through the examination of stromal biomarkers. Cell Adh Migr. 2012;6:249–60.")]. Of the cellular components of the stroma, normal (resident) fibroblasts are the most abundant and are involved in the regulation of various downstream pathways relevant to breast cancer etiology. Some studies suggest possible activation of fibroblasts during postpartum involution [[17](https://www.nature.com/articles/s41416-026-03615-7#ref-CR17 "O’Brien J, Lyons T, Monks J, Lucia MS, Wilson RS, Hines L, et al. Alternatively activated macrophages and collagen remodeling characterize the postpartum involuting mammary gland across species. Am J Pathol. 2010;176:1241–55."),[18](https://www.nature.com/articles/s41416-026-03615-7#ref-CR18 "Schedin P, O’Brien J, Rudolph M, Stein T, Borges V. Microenvironment of the involuting mammary gland mediates mammary cancer progression. J Mammary Gland Biol Neoplasia. 2007;12:71–82."),[19](https://www.nature.com/articles/s41416-026-03615-7#ref-CR19 "Lyons TR, O’Brien J, Borges VF, Conklin MW, Keely PJ, Eliceiri KW, et al. Postpartum mammary gland involution drives progression of ductal carcinoma in situ through collagen and COX-2. Nat Med. 2011;17:1109–15.")], but whether reproductive factors can have long-lasting effects on normal fibroblast activity in the breast tissue is unknown. To fill this knowledge gap, we examined the associations of several reproductive factors with the expression of stromal markers in non-malignant breast tissue from benign breast biopsy samples using prospective data from the Nurses’ Health Study II (NHSII). We included several stromal markers that capture fibroblast activation and have been linked to more aggressive tumor features in studies utilizing tumor tissue: alpha-smooth muscle actin (αSMA) [[20](https://www.nature.com/articles/s41416-026-03615-7#ref-CR20 "Yamashita M, Ogawa T, Zhang X, Hanamura N, Kashikura Y, Takamura M, et al. Role of stromal myofibroblasts in invasive breast cancer: stromal expression of alpha-smooth muscle actin correlates with worse clinical outcome. Breast Cancer. 2012;19:170–6.")], tenascin-C (TNC) [[21](https://www.nature.com/articles/s41416-026-03615-7#ref-CR21 "Chen W, Wu Y, Wang J, Yu W, Shen X, Zhao K, et al. Clinical advances in TNC delivery vectors and their conjugate agents. Pharmacol Therapeutics. 2024;253:108577.")], fibroblast activation protein (FAP) [[22](https://www.nature.com/articles/s41416-026-03615-7#ref-CR22 "Fitzgerald AA, Weiner LM. The role of fibroblast activation protein in health and malignancy. Cancer Metastasis Rev. 2020;39:783–803.")], calcyclin (S100A6) [[23](https://www.nature.com/articles/s41416-026-03615-7#ref-CR23 "Kuźnicki J, Kordowska J, Puzianowska M, Woźniewicz BM. Calcyclin as a marker of human epithelial cells and fibroblasts. Exp Cell Res. 1992;200:425–30.")], and matrix metallo-proteinase (MMP14) [[24](https://www.nature.com/articles/s41416-026-03615-7#ref-CR24 "Di D, Chen L, Guo Y, Wang L, Wang H, Ju J. Association of BCSC-1 and MMP-14 with human breast cancer. Oncol Lett. 2018;15:5020–6.")]. We hypothesized that protective reproductive factors are inversely associated with the expression of these markers, while reproductive factors that were positively associated with breast cancer risk are associated with increased expression of these markers. ## Materials and methods ### Study population We included women with incident biopsy-confirmed BBD within the Nurses’ Health Study II (NHSII) cohort that recruited registered nurses in the United States who were 25–42 years old [[25](https://www.nature.com/articles/s41416-026-03615-7#ref-CR25 "Bao Y, Bertoia ML, Lenart EB, Stampfer MJ, Willett WC, Speizer FE, et al. Origin, methods, and evolution of the three nurses’ health studies. Am J Public Health. 2016;106:1573–81.")]. The initial NHS II questionnaire in 1989, along with subsequent biennial questionnaires, requested participants to report any BBD diagnosis and to indicate whether this was confirmed through a biopsy or aspiration. The biennial questionnaires collected information on breast cancer risk factors, including reproductive history, exogenous hormone use, and disease diagnoses [[26](https://www.nature.com/articles/s41416-026-03615-7#ref-CR26 "Farland LV, Tamimi RM, Eliassen AH, Spiegelman D, Collins LC, Schnitt SJ, et al. A prospective study of endometriosis and risk of benign breast disease. Breast Cancer Res Treat. 2016;159:545–52.")]. All participants eligible for this study had a first diagnosis of BBD confirmed by biopsy. After obtaining consent, pathology slides were retrieved and reviewed by study pathologists [[27](https://www.nature.com/articles/s41416-026-03615-7#ref-CR27 "Su X, Colditz GA, Willett WC, Collins LC, Schnitt SJ, Connolly JL, et al. Genetic variation and circulating levels of IGF-I a
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