Skip to main content

Advertisement

Log in

Risk of breast cancer and adipose tissue concentrations of polychlorinated biphenyls and organochlorine pesticides: a hospital-based case-control study in Chinese women

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Polychlorinated biphenyls (PCBs), dichlorodiphenyltrichloroethane (DDT), and dichlorodiphenyldichloroethylene (DDE) are suspected to be associated with breast cancer risk, but the results are controversial. This study was performed to evaluate the associations between adipose tissue PCB, DDT, and DDE concentrations and breast cancer risk. Two hundred and nine pathologically diagnosed breast cancer cases and 165 controls were recruited from three local hospitals in Shantou city, China, from 2014 to 2016. Concentrations of 7 PCB congeners, p,p′-DDT, and p,p′-DDE were measured in adipose tissues obtained from the breast for cases and the breast/abdomen for controls during surgery. Clinicopathologic information and demographic characteristics were collected from medical records. PCBs, p,p′-DDT, and p,p′-DDE concentrations in adipose tissues were compared between cases and controls. Multivariate logistic regression model was used to analyze the risk of breast cancer by PCBs, p,p′-DDT, and p,p′-DDE concentrations in adipose tissues. Breast cancer cases have relatively higher menarche age, higher breastfeeding and postmenopausal proportion than controls. Levels of PCB-52, PCB-101, PCB-118, PCB-138, PCB-153, PCB-180, total PCBs (∑PCBs), and p,p′-DDE were relatively higher in breast cancer cases than controls. Breast cancer risk was increased in the third tertile of PCB-101, PCB-118, PCB-138, PCB-153, PCB-180, ∑PCBs, and p,p′-DDE as compared with the first tertile in both adjusted and unadjusted logistic regression models (odds ratios [ORs] were from 1.58 to 7.88); and increased linearly across categories of PCB-118 and p,p′-DDE in unadjusted model, and PCB-118 and PCB-153 in the adjusted model with trend (all P < 0.01). While breast cancer risk was declined in the second tertile of PCB-28, PCB-52, and PCB-101 in both unadjusted and adjusted models, also second tertile of p,p′-DDT and third tertile of PCB-28 in the adjusted models. This study suggests associations between the exposure of PCBs, p,p′-DDT, and p,p′-DDE and breast cancer risk. Based on adjusted models, PCB-118, PCB-138, PCB-153, PCB-180, ∑PCBs, and p,p′-DDE exposures increase breast cancer risk at current exposure levels, despite existing inconsistent even inverse results in PCB-28, PCB-52, PCB-101, and p,p′-DDT. More epidemiological studies are still needed to verify these findings in different populations.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Aronson KJ, Miller AB, Woolcott CG, Sterns EE, McCready DR, Lickley LA et al (2000) Breast adipose tissue concentrations of polychlorinated biphenyls and other organochlorines and breast cancer risk. Cancer Epidemiol Biomark Prev 9:55–63

    CAS  Google Scholar 

  • Arrebola JP, Martin-Olmedo P, Fernandez MF, Sanchez-Cantalejo E, Jimenez-Rios JA, Torne P et al (2009) Predictors of concentrations of hexachlorobenzene in human adipose tissue: a multivariate analysis by gender in southern Spain. Environ Int 35:27–32

    CAS  Google Scholar 

  • Arrebola JP, Belhassen H, Artacho-Cordon F, Ghali R, Ghorbel H, Boussen H et al (2015) Risk of female breast cancer and serum concentrations of organochlorine pesticides and polychlorinated biphenyls: a case-control study in Tunisia. Sci Total Environ 520:106–113

    CAS  Google Scholar 

  • Arrebola JP, Fernandez-Rodriguez M, Artacho-Cordon F, Garde C, Perez-Carrascosa F, Linares I et al (2016) Associations of persistent organic pollutants in serum and adipose tissue with breast cancer prognostic markers. Sci Total Environ 566-567:41–49

    CAS  Google Scholar 

  • ATSDR (2000) Toxicological profile for polychlorinated biphenyls. US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta

    Google Scholar 

  • ATSDR (2002) Toxicological profile for DDT, DDE, and DDD. US Department of Health and Human Services, Public Health Service, Agency for Toxic Substances and Disease Registry, Atlanta

    Google Scholar 

  • Aube M, Larochelle C, Ayotte P (2011) Differential effects of a complex organochlorine mixture on the proliferation of breast cancer cell lines. Environ Res 111:337–347

    CAS  Google Scholar 

  • Barnard ME, Boeke CE, Tamimi RM (2015) Established breast cancer risk factors and risk of intrinsic tumor subtypes. Biochim Biophys Acta 1856:73–85

    CAS  Google Scholar 

  • Brauner EV, Raaschou-Nielsen O, Gaudreau E, Leblanc A, Tjonneland A, Overvad K et al (2012) Predictors of adipose tissue concentrations of organochlorine pesticides in a general Danish population. J Expo Sci Environ Epidemiol 22:52–59

    Google Scholar 

  • Campeau PM, Foulkes WD, Tischkowitz MD (2008) Hereditary breast cancer: new genetic developments, new therapeutic avenues. Hum Genet 124:31–42

    CAS  Google Scholar 

  • Chen W, Zheng R, Zeng H, Zhang S (2016) The incidence and mortality of major cancers in China, 2012. Chin J Cancer 35:73

    Google Scholar 

  • Cohn BA, Wolff MS, Cirillo PM, Sholtz RI (2007) DDT and breast cancer in young women: new data on the significance of age at exposure. Environ Health Perspect 115:1406–1414

    CAS  Google Scholar 

  • Cohn BA, Terry MB, Plumb M, Cirillo PM (2012) Exposure to polychlorinated biphenyl (PCB) congeners measured shortly after giving birth and subsequent risk of maternal breast cancer before age 50. Breast Cancer Res Treat 136:267–275

    CAS  Google Scholar 

  • Cohn BA, La Merrill M, Krigbaum NY, Yeh G, Park JS, Zimmermann L et al (2015) DDT exposure in utero and breast cancer. J Clin Endocrinol Metab 100:2865–2872

    CAS  Google Scholar 

  • Covaci A, Voorspoels S, Roosens L, Jacobs W, Blust R, Neels H (2008) Polybrominated diphenyl ethers (PBDEs) and polychlorinated biphenyls (PCBs) in human liver and adipose tissue samples from Belgium. Chemosphere 73:170–175

    CAS  Google Scholar 

  • Demers A, Ayotte P, Brisson J, Dodin S, Robert J, Dewailly E (2002) Plasma concentrations of polychlorinated biphenyls and the risk of breast cancer: a congener-specific analysis. Am J Epidemiol 155:629–635

    Google Scholar 

  • Dickerson SM, Gore AC (2007) Estrogenic environmental endocrine-disrupting chemical effects on reproductive neuroendocrine function and dysfunction across the life cycle. Rev Endocr Metab Disord 8:143–159

    CAS  Google Scholar 

  • Dorgan JF, Brock JW, Rothman N, Needham LL, Miller R, Stephenson HE Jr et al (1999) Serum organochlorine pesticides and PCBs and breast cancer risk: results from a prospective analysis (USA). Cancer Causes Control 10:1–11

    CAS  Google Scholar 

  • Dubey AK, Gupta U, Jain S (2015) Breast cancer statistics and prediction methodology: a systematic review and analysis. Asian Pac J Cancer Prev 16:4237–4245

    Google Scholar 

  • Ferlay J, Soerjomataram I, Dikshit R, Eser S, Mathers C, Rebelo M, Parkin DM, Forman D, Bray F (2015) Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer 136:E359–E386

    CAS  Google Scholar 

  • Floehr T, Xiao H, Scholz-Starke B, Wu L, Hou J, Yin D, Zhang X, Ji R, Yuan X, Ottermanns R, Roß-Nickoll M, Schäffer A, Hollert H (2013) Solution by dilution?--a review on the pollution status of the Yangtze River. Environ Sci Pollut Res Int 20:6934–6971

    CAS  Google Scholar 

  • Gatto NM, Longnecker MP, Press MF, Sullivan-Halley J, McKean-Cowdin R, Bernstein L (2007) Serum organochlorines and breast cancer: a case-control study among African-American women. Cancer Causes Control 18:29–39

    Google Scholar 

  • Gaudet MM, Press MF, Haile RW, Lynch CF, Glaser SL, Schildkraut J, Gammon MD, Douglas Thompson W, Bernstein JL (2011) Risk factors by molecular subtypes of breast cancer across a population-based study of women 56 years or younger. Breast Cancer Res Treat 130:587–597

    Google Scholar 

  • Goldsmith DF (2000) Linking environmental cancer with occupational epidemiology research: the role of the International Agency for Research on Cancer (IARC). J Environ Pathol Toxicol Oncol 19:171–175

    CAS  Google Scholar 

  • Gu MB, Min J, Kim EJ (2002) Toxicity monitoring and classification of endocrine disrupting chemicals (EDCs) using recombinant bioluminescent bacteria. Chemosphere 46:289–294

    CAS  Google Scholar 

  • Hall P, Easton D (2013) Breast cancer screening: time to target women at risk. Br J Cancer 108:2202–2204

    CAS  Google Scholar 

  • He Y, Peng L, Huang Y, Peng X, Zheng S, Liu C, Wu K (2017) Association of breast adipose tissue levels of polychlorinated biphenyls and breast cancer development in women from Chaoshan. China Environ Sci Pollut Res Int 24:4778–4790

    CAS  Google Scholar 

  • He Y, Peng L, Zhang W, Liu C, Yang Q, Zheng S, Bao M, Huang Y, Wu K (2018) Adipose tissue levels of polybrominated diphenyl ethers and breast cancer risk in Chinese women: a case–control study. Environ Res 167:160–168

    CAS  Google Scholar 

  • Helzlsouer KJ, Alberg AJ, Huang HY, Hoffman SC, Strickland PT, Brock JW et al (1999) Serum concentrations of organochlorine compounds and the subsequent development of breast cancer. Cancer Epidemiol Biomark Prev 8:525–532

    CAS  Google Scholar 

  • Hernandez F, Portoles T, Pitarch E, Lopez FJ (2009) Searching for anthropogenic contaminants in human breast adipose tissues using gas chromatography-time-of-flight mass spectrometry. J Mass Spectrom 44:1–11

    CAS  Google Scholar 

  • Ho ML, Hsiao YH, Su SY, Chou MC, Liaw YP (2015) Mortality of breast cancer in Taiwan, 1971-2010: temporal changes and an age-period-cohort analysis. J Obstet Gynaecol 35:60–63

    Google Scholar 

  • Holmes AK, Koller KR, Kieszak SM, Sjodin A, Calafat AM, Sacco FD, Varner DW, Lanier AP, Rubin CH (2014) Case-control study of breast cancer and exposure to synthetic environmental chemicals among Alaska native women. Int J Circumpolar Health 73:25760

    Google Scholar 

  • Ingber SZ, Buser MC, Pohl HR, Abadin HG, Murray HE, Scinicariello F (2013) DDT/DDE and breast cancer: a meta-analysis. Regul Toxicol Pharmacol 67:421–433

    CAS  Google Scholar 

  • Itoh H, Iwasaki M, Hanaoka T, Kasuga Y, Yokoyama S, Onuma H, Nishimura H, Kusama R, Tsugane S (2009) Serum organochlorines and breast cancer risk in Japanese women: a case-control study. Cancer Causes Control 20:567–580

    Google Scholar 

  • Iwasaki M, Inoue M, Sasazuki S, Kurahashi N, Itoh H, Usuda M, Tsugane S (2008) Plasma organochlorine levels and subsequent risk of breast cancer among Japanese women: a nested case-control study. Sci Total Environ 402:176–183

    CAS  Google Scholar 

  • Johnson NA, Ho A, Cline JM, Hughes CL, Foster WG, Davis VL (2012) Accelerated mammary tumor onset in a HER2/Neu mouse model exposed to DDT metabolites locally delivered to the mammary gland. Environ Health Perspect 120:1170–1176

    CAS  Google Scholar 

  • Knower KC, To SQ, Leung YK, Ho SM, Clyne CD (2014) Endocrine disruption of the epigenome: a breast cancer link. Endocr Relat Cancer 21:T33–T55

    CAS  Google Scholar 

  • Kraugerud M, Zimmer KE, Dahl E, Berg V, Olsaker I, Farstad W, Ropstad E, Verhaegen S (2010) Three structurally different polychlorinated biphenyl congeners (Pcb 118, 153, and 126) affect hormone production and gene expression in the human H295R in vitro model. J Toxicol Environ Health A 73:1122–1132

    CAS  Google Scholar 

  • Laden F, Hankinson SE, Wolff MS, Colditz GA, Willett WC, Speizer FE, Hunter DJ (2001) Plasma organochlorine levels and the risk of breast cancer: an extended follow-up in the Nurses’ Health Study. Int J Cancer 91:568–574

    CAS  Google Scholar 

  • Lee HR, Hwang KA, Nam KH, Kim HC, Choi KC (2014) Progression of breast cancer cells was enhanced by endocrine-disrupting chemicals, triclosan and octylphenol, via an estrogen receptor-dependent signaling pathway in cellular and mouse xenograft models. Chem Res Toxicol 27:834–842

    CAS  Google Scholar 

  • Li C, Yu C, Wang P (2015) An age-period-cohort analysis of female breast cancer mortality from 1990-2009 in China. Int J Equity Health 14:76

    Google Scholar 

  • Lin CH, Huang CL, Chuang MC, Wang YJ, Chen DR, Chen ST, Lin PH (2009) Protective role of estrogen receptor-alpha on lower chlorinated PCB congener-induced DNA damage and repair in human tumoral breast cells. Toxicol Lett 188:11–19

    CAS  Google Scholar 

  • Lopez-Cervantes M, Torres-Sanchez L, Tobias A, Lopez-Carrillo L (2004) Dichlorodiphenyldichloroethane burden and breast cancer risk: a meta-analysis of the epidemiologic evidence. Environ Health Perspect 112:207–214

    CAS  Google Scholar 

  • Martin AM, Weber BL (2000) Genetic and hormonal risk factors in breast cancer. J Natl Cancer Inst 92:1126–1135

    CAS  Google Scholar 

  • Muscat JE, Britton JA, Djordjevic MV, Citron ML, Kemeny M, Busch-Devereaux E et al (2003) Adipose concentrations of organochlorine compounds and breast cancer recurrence in Long Island, New York. Cancer Epidemiol Biomark Prev 12:1474–1478

    CAS  Google Scholar 

  • Pahwa M, Harris SA, Hohenadel K, McLaughlin JR, Spinelli JJ, Pahwa P et al (2012) Pesticide use, immunologic conditions, and risk of non-Hodgkin lymphoma in Canadian men in six provinces. Int J Cancer 131:2650–2659

    CAS  Google Scholar 

  • Parada H Jr, Wolff MS, Engel LS, Eng SM, Khankari NK, Neugut AI, Teitelbaum SL, Gammon MD (2016) Polychlorinated biphenyls and their association with survival following breast cancer. Eur J Cancer 56:21–30

    CAS  Google Scholar 

  • Park JH, Cha ES, Ko Y, Hwang MS, Hong JH, Lee WJ (2014) Exposure to dichlorodiphenyltrichloroethane and the risk of breast cancer: a systematic review and meta-analysis. Osong Public Health Res Perspect 5:77–84

    Google Scholar 

  • Petreas M, Smith D, Hurley S, Jeffrey SS, Gilliss D, Reynolds P (2004) Distribution of persistent, lipid-soluble chemicals in breast and abdominal adipose tissues: lessons learned from a breast cancer study. Cancer Epidemiol Biomark Prev 13:416–424

    CAS  Google Scholar 

  • Ptak A, Mazur K, Gregoraszczuk EL (2011) Comparison of combinatory effects of PCBs (118, 138, 153 and 180) with 17 beta-estradiol on proliferation and apoptosis in MCF-7 breast cancer cells. Toxicol Ind Health 27:315–321

    CAS  Google Scholar 

  • Radice S, Chiesara E, Fucile S, Marabini L (2008) Different effects of PCB101, PCB118, PCB138 and PCB153 alone or mixed in MCF-7 breast cancer cells. Food Chem Toxicol 46:2561–2567

    CAS  Google Scholar 

  • Ramos JJ, Huetos O, Gonzalez S, Esteban M, Calvo E, Perez-Gomez B et al (2017) Organochlorinated pesticides levels in a representative sample of the Spanish adult population: the Bioambient.es project. Int J Hyg Environ Health 220:217–226

    CAS  Google Scholar 

  • Ritter R, Scheringer M, MacLeod M, Hungerbuhler K (2011) Assessment of nonoccupational exposure to DDT in the tropics and the north: relevance of uptake via inhalation from indoor residual spraying. Environ Health Perspect 119:707–712

    CAS  Google Scholar 

  • Rubin CH, Lanier A, Kieszak S, Brock JW, Koller KR, Strosnider H, Needham L, Zahm S, Harpster A (2006) Breast cancer among Alaska native women potentially exposed to environmental organochlorine chemicals. Int J Circumpolar Health 65:18–27

    Google Scholar 

  • Rudolph A, Chang-Claude J, Schmidt MK (2016) Gene-environment interaction and risk of breast cancer. Br J Cancer 114:125–133

    CAS  Google Scholar 

  • Salehi F, Turner MC, Phillips KP, Wigle DT, Krewski D, Aronson KJ (2008) Review of the etiology of breast cancer with special attention to organochlorines as potential endocrine disruptors. J Toxicol Environ Health B Crit Rev 11:276–300

    CAS  Google Scholar 

  • Sifakis S, Androutsopoulos VP, Tsatsakis AM, Spandidos DA (2017) Human exposure to endocrine disrupting chemicals: effects on the male and female reproductive systems. Environ Toxicol Pharmacol 51:56–70

    CAS  Google Scholar 

  • Stellman SD, Djordjevic MV, Britton JA, Muscat JE, Citron ML, Kemeny M et al (2000) Breast cancer risk in relation to adipose concentrations of organochlorine pesticides and polychlorinated biphenyls in Long Island, New York. Cancer Epidemiol Biomark Prev 9:1241–1249

    CAS  Google Scholar 

  • Trichopoulos D, Adami HO, Ekbom A, Hsieh CC, Lagiou P (2008) Early life events and conditions and breast cancer risk: from epidemiology to etiology. Int J Cancer 122:481–485

    CAS  Google Scholar 

  • van Duursen MB, Sanderson JT, van der Bruggen M, van der Linden J, van den Berg M (2003) Effects of several dioxin-like compounds on estrogen metabolism in the malignant MCF-7 and nontumorigenic MCF-10A human mammary epithelial cell lines. Toxicol Appl Pharmacol 190:241–250

    Google Scholar 

  • Wang H, He M, Lin C, Quan X, Guo W, Yang Z (2007) Monitoring and assessment of persistent organochlorine residues in sediments from the Daliaohe River watershed, northeast of China. Environ Monit Assess 133:231–242

    CAS  Google Scholar 

  • Wielsoe M, Kern P, Bonefeld-Jorgensen EC (2017) Serum levels of environmental pollutants is a risk factor for breast cancer in Inuit: a case control study. Environ Health 16:56

    Google Scholar 

  • Xing P, Li J, Jin F (2010) A case-control study of reproductive factors associated with subtypes of breast cancer in Northeast China. Med Oncol 27:926–931

    Google Scholar 

  • Zheng T, Holford TR, Tessari J, Mayne ST, Owens PH, Ward B, Carter D, Boyle P, Dubrow R, Archibeque-Engle S, Zahm SH (2000) Breast cancer risk associated with congeners of polychlorinated biphenyls. Am J Epidemiol 152:50–58

    CAS  Google Scholar 

Download references

Acknowledgments

We thank all the volunteers for participating in the present study.

Funding

This study was supported by the National Natural Science Foundation of China (No. 81470152).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Kusheng Wu.

Ethics declarations

Ethical approval was obtained from the Human Ethical Committee of Shantou University Medical College. All participants gave their informed written consent before enrollment.

Conflict of interest

The authors declare that they have no competing interests.

Additional information

Responsible editor: Philippe Garrigues

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 22 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Huang, W., He, Y., Xiao, J. et al. Risk of breast cancer and adipose tissue concentrations of polychlorinated biphenyls and organochlorine pesticides: a hospital-based case-control study in Chinese women. Environ Sci Pollut Res 26, 32128–32136 (2019). https://doi.org/10.1007/s11356-019-06404-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-019-06404-3

Keywords

Navigation