Night-Shift Work Duration and Risk of Colorectal Cancer According to IRS1 and IRS2 Expression

doi:10.1158/1055-9965.EPI-19-0325

. 2020 Jan;29(1):133-140.

doi: 10.1158/1055-9965.EPI-19-0325. Epub 2019 Oct 30.

Night-Shift Work Duration and Risk of Colorectal Cancer According to IRS1 and IRS2 Expression

Yan Shi^#^{1

2}, Li Liu^#^{1

3}, Tsuyoshi Hamada¹, Jonathan A Nowak⁴, Marios Giannakis^{5

6}, Yanan Ma^{7

8}, Mingyang Song^{9

10}, Daniel Nevo^{11

12}, Keisuke Kosumi¹, Mancang Gu¹, Sun A Kim¹³, Teppei Morikawa¹⁴, Kana Wu¹⁵, Jing Sui^{7

16}, Kyriaki Papantoniou¹⁷, Molin Wang^{11

12}, Andrew T Chan^{5

7

9

10}, Charles S Fuchs^{7

18

19

20}, Jeffrey A Meyerhardt⁶, Edward Giovannucci^{7

12

15}, Shuji Ogino^{1

4

5

12}, Eva S Schernhammer^#^{21

12

17}, Reiko Nishihara^#^{22

4

5

11

12}, Xuehong Zhang^#²¹

Affiliations

¹ Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
² Department of Medical Oncology, Chinese PLA General Hospital, Beijing, China.
³ Department of Epidemiology and Biostatistics, and the Ministry of Education Key Lab of Environment and Health, School of Public Health, Huazhong University of Science and Technology, Wuhan, China.
⁴ Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
⁵ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, Massachusetts.
⁶ Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
⁷ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
⁸ Department of Biostatistics and Epidemiology, School of Public Health, China Medical University, Shenyang, Liaoning, China.
⁹ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
¹⁰ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
¹¹ Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹² Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹³ Laboratory of Human Carcinogenesis, NCI, NIH, Bethesda, Maryland.
¹⁴ Department of Pathology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
¹⁵ Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹⁶ Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing, Jiangsu, China.
¹⁷ Department of Epidemiology, Center for Public Health, Medical University of Vienna, Vienna, Austria.
¹⁸ Yale Cancer Center, New Haven, Connecticut.
¹⁹ Department of Medicine, Yale School of Medicine, New Haven, Connecticut.
²⁰ Smilow Cancer Hospital, New Haven, Connecticut.
²¹ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts. xuehong.zhang@channing.harvard.edu reiko.nishihara@mail.harvard.edu eva.schernhammer@channing.harvard.edu.
²² Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts. xuehong.zhang@channing.harvard.edu reiko.nishihara@mail.harvard.edu eva.schernhammer@channing.harvard.edu.

^# Contributed equally.

PMID: 31666286
PMCID: PMC6954315
DOI: 10.1158/1055-9965.EPI-19-0325

Night-Shift Work Duration and Risk of Colorectal Cancer According to IRS1 and IRS2 Expression

Yan Shi et al. Cancer Epidemiol Biomarkers Prev. 2020 Jan.

. 2020 Jan;29(1):133-140.

doi: 10.1158/1055-9965.EPI-19-0325. Epub 2019 Oct 30.

Authors

Affiliations

¹ Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
² Department of Medical Oncology, Chinese PLA General Hospital, Beijing, China.
³ Department of Epidemiology and Biostatistics, and the Ministry of Education Key Lab of Environment and Health, School of Public Health, Huazhong University of Science and Technology, Wuhan, China.
⁴ Program in MPE Molecular Pathological Epidemiology, Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
⁵ Broad Institute of Massachusetts Institute of Technology (MIT) and Harvard, Cambridge, Massachusetts.
⁶ Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
⁷ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
⁸ Department of Biostatistics and Epidemiology, School of Public Health, China Medical University, Shenyang, Liaoning, China.
⁹ Clinical and Translational Epidemiology Unit, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
¹⁰ Division of Gastroenterology, Massachusetts General Hospital and Harvard Medical School, Boston, Massachusetts.
¹¹ Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹² Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹³ Laboratory of Human Carcinogenesis, NCI, NIH, Bethesda, Maryland.
¹⁴ Department of Pathology, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan.
¹⁵ Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
¹⁶ Key Laboratory of Environmental Medicine Engineering, Ministry of Education, School of Public Health, Southeast University, Nanjing, Jiangsu, China.
¹⁷ Department of Epidemiology, Center for Public Health, Medical University of Vienna, Vienna, Austria.
¹⁸ Yale Cancer Center, New Haven, Connecticut.
¹⁹ Department of Medicine, Yale School of Medicine, New Haven, Connecticut.
²⁰ Smilow Cancer Hospital, New Haven, Connecticut.
²¹ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts. xuehong.zhang@channing.harvard.edu reiko.nishihara@mail.harvard.edu eva.schernhammer@channing.harvard.edu.
²² Department of Oncologic Pathology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts. xuehong.zhang@channing.harvard.edu reiko.nishihara@mail.harvard.edu eva.schernhammer@channing.harvard.edu.

^# Contributed equally.

PMID: 31666286
PMCID: PMC6954315
DOI: 10.1158/1055-9965.EPI-19-0325

Abstract

Background: We hypothesized that the risk of colorectal cancer in night-shift workers might be different according to insulin receptor substrate status.

Methods: Among 77,470 eligible women having night work assessed in the Nurses' Health Study, we documented a total of 1,397 colorectal cancer cases, of which 304 or 308 had available data on IRS1 and IRS2, respectively. We used duplication-method Cox proportional hazards regression analysis for competing risks to calculate HRs and 95% confidence intervals (CI) for each colorectal cancer subtype. We measured tumor IRS1 or IRS2 expression by immunohistochemistry (IHC).

Results: Compared with women who never worked night shifts, those working ≥15 years night shifts had a marginal trend of increased overall risk of colorectal cancer (P _trend = 0.06; multivariable HR = 1.20; 95% CI, 0.99-1.45). Longer duration of night-shift work was associated with a higher risk of IRS2-positive tumors (multivariable HR = 2.69; 95% CI, 1.48-4.89; P _trend = 0.001, ≥15 years night shifts vs. never) but not with IRS2-negative tumors (multivariable HR = 0.90; 95% CI, 0.54-1.51; P _trend = 0.72; P _{heterogeneity} for IRS2 = 0.008). Similarly, the corresponding multivariable HRs were 1.81 for IRS1-positive tumors (95% CI, 0.94-3.48; P _trend = 0.06) and 1.13 for IRS1-negative tumors (95% CI, 0.71-1.80; P _trend = 0.56; P _{heterogeneity} for IRS1 = 0.02).

Conclusions: Our molecular pathologic epidemiology data suggest a potential role of IRS in mediating carcinogenesis induced by night-shift work.

Impact: Although these findings need validation, rotating night shift might increase colorectal cancer risk in women with abnormal insulin receptor pathways.

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Conflict of interest statement

Conflict of interest statement: None declared.

Figures

**Figure 1.**
Flow chart of the study population in the Nurses’ Health Study.

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References

1. Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Bouvard V, et al. Carcinogenicity of shift-work, painting, and fire-fighting. The Lancet Oncology 2007;8(12):1065–6 doi 10.1016/S1470-2045(07)70373-X. - DOI - PubMed
1. group IMV. Carcinogenicity of night shift work. The Lancet Oncology 2019. doi 10.1016/S1470-2045(19)30455-3. - DOI - PubMed
1. Papantoniou K, Castano-Vinyals G, Espinosa A, Turner MC, Alonso-Aguado MH, Martin V, et al. Shift work and colorectal cancer risk in the MCC-Spain case-control study. Scandinavian journal of work, environment & health 2017;43(3):250–9 doi 10.5271/sjweh.3626. - DOI - PubMed
1. Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, et al. Night-shift work and risk of colorectal cancer in the nurses’ health study. Journal of the National Cancer Institute 2003;95(11):825–8. - PubMed
1. Tsai RJ, Luckhaupt SE, Sweeney MH, Calvert GM. Shift work and cancer screening: do females who work alternative shifts undergo recommended cancer screening? Am J Ind Med 2014;57(3):265–75 doi 10.1002/ajim.22285. - DOI - PMC - PubMed

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[1] Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Bouvard V, et al. Carcinogenicity of shift-work, painting, and fire-fighting. The Lancet Oncology 2007;8(12):1065–6 doi 10.1016/S1470-2045(07)70373-X. - DOI - PubMed

[2] Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Bouvard V, et al. Carcinogenicity of shift-work, painting, and fire-fighting. The Lancet Oncology 2007;8(12):1065–6 doi 10.1016/S1470-2045(07)70373-X. - DOI - PubMed

[3] group IMV. Carcinogenicity of night shift work. The Lancet Oncology 2019. doi 10.1016/S1470-2045(19)30455-3. - DOI - PubMed

[4] group IMV. Carcinogenicity of night shift work. The Lancet Oncology 2019. doi 10.1016/S1470-2045(19)30455-3. - DOI - PubMed

[5] Papantoniou K, Castano-Vinyals G, Espinosa A, Turner MC, Alonso-Aguado MH, Martin V, et al. Shift work and colorectal cancer risk in the MCC-Spain case-control study. Scandinavian journal of work, environment & health 2017;43(3):250–9 doi 10.5271/sjweh.3626. - DOI - PubMed

[6] Papantoniou K, Castano-Vinyals G, Espinosa A, Turner MC, Alonso-Aguado MH, Martin V, et al. Shift work and colorectal cancer risk in the MCC-Spain case-control study. Scandinavian journal of work, environment & health 2017;43(3):250–9 doi 10.5271/sjweh.3626. - DOI - PubMed

[7] Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, et al. Night-shift work and risk of colorectal cancer in the nurses’ health study. Journal of the National Cancer Institute 2003;95(11):825–8. - PubMed

[8] Schernhammer ES, Laden F, Speizer FE, Willett WC, Hunter DJ, Kawachi I, et al. Night-shift work and risk of colorectal cancer in the nurses’ health study. Journal of the National Cancer Institute 2003;95(11):825–8. - PubMed

[9] Tsai RJ, Luckhaupt SE, Sweeney MH, Calvert GM. Shift work and cancer screening: do females who work alternative shifts undergo recommended cancer screening? Am J Ind Med 2014;57(3):265–75 doi 10.1002/ajim.22285. - DOI - PMC - PubMed

[10] Tsai RJ, Luckhaupt SE, Sweeney MH, Calvert GM. Shift work and cancer screening: do females who work alternative shifts undergo recommended cancer screening? Am J Ind Med 2014;57(3):265–75 doi 10.1002/ajim.22285. - DOI - PMC - PubMed

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Night-Shift Work Duration and Risk of Colorectal Cancer According to IRS1 and IRS2 Expression

Affiliations

Night-Shift Work Duration and Risk of Colorectal Cancer According to IRS1 and IRS2 Expression

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