Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress 2023 EHA Congress 2023 ASCO Annual Meeting
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
BMC Public Health
Published in: BMC Public Health 1/2015

Open Access 01-12-2015 | Research article

Multistage carcinogenesis and the incidence of thyroid cancer in the US by sex, race, stage and histology

Authors: Rafael Meza, Joanne T. Chang

Published in: BMC Public Health | Issue 1/2015

Login to get access

Abstract

Background

Thyroid cancer has the fastest growing incidence in the US. However, the underlying causes are still under debate.

Methods

We analyzed thyroid cancer incidence in the SEER-9 registry from 1973-2010 using multistage carcinogenesis and age-period-cohort models. Multistage models were used to investigate differences in initiation, promotion and malignant conversion rates of thyroid tumors by sex, race, stage, and histology. Models were adjusted for period and cohort trends to investigate the contributions of each factor, and determine whether birth- or diagnosis-year better correlate with observed incidence patterns.

Results

Significant increases in thyroid cancer incidence by period or calendar-year were found for all sex, race, stage and histology combinations, particularly for localized cases (a 3- and 4-fold increase from 1973-2010 for females and males, respectively). Multistage analyses suggest that the 3-fold higher incidence in women could be explained by 1.5-fold higher initiation and promotion rates. Analyses by race suggest that the lower incidence in blacks can be attributed to lower promotion rates versus whites. Analysis by histology showed considerable decreases in follicular cancer incidence by birth-cohort since the early 1900s.

Conclusions

Multistage modeling suggests that variations in thyroid cancer initiation and promotion can explain the observed differences in incidence by sex, race and histology. The consistent increases in incidence by calendar-year for all sex-race-histology-stage combinations suggest that the rise may be predominantly due to more intensive screening-diagnostics, although an environmental factor may be also at play. Our analyses constitute a first step towards the development of thyroid cancer natural history models.
Appendix
Available only for authorised users
Literature
1.
Kilfoy BA, Zheng T, Holford TR, Han X, Ward MH, Sjodin A, et al. International patterns and trends in thyroid cancer incidence, 1973-2002. Cancer Causes Control. 2009;20:525–31.CrossRefPubMed
2.
Zhu C, Zheng T, Kilfoy BA, Han X, Ma S, Ba Y, et al. A birth cohort analysis of the incidence of papillary thyroid cancer in the United States, 1973-2004. Thyroid. 2009;19:1061–6.CrossRefPubMedPubMedCentral
3.
Davies L, Welch HG. Increasing incidence of thyroid cancer in the United States, 1973-2002. JAMA. 2006;295:2164–7.CrossRefPubMed
4.
Roche LM, Niu X, Pawlish KS, Henry KA. Thyroid cancer incidence in New Jersey: time trend, birth cohort and socioeconomic status analysis (1979-2006). J Environ Public Health. 2011;2011:850105.CrossRefPubMedPubMedCentral
5.
Aschebrook-Kilfoy B, Sabra MM, Brenner A, Moore SC, Ron E, Schatzkin A, et al. Diabetes and thyroid cancer risk in the National Institutes of Health-AARP Diet and Health Study. Thyroid. 2011;21:957–63.CrossRefPubMedPubMedCentral
6.
Kitahara CM, Platz EA, Freeman LE, Hsing AW, Linet MS, Park Y, et al. Obesity and thyroid cancer risk among U.S. men and women: a pooled analysis of five prospective studies. Cancer Epidemiol. Biomarkers Prev. 2011;20:464–72.CrossRef
7.
Kitahara CM, Platz EA, Park Y, Hollenbeck AR, Schatzkin A, Berrington de Gonzalez A. Body fat distribution, weight change during adulthood, and thyroid cancer risk in the NIH-AARP Diet and Health Study. Int J Cancer. 2012;130:1411–9.CrossRefPubMed
8.
Weiss W. Changing incidence of thyroid cancer. J Natl Cancer Inst. 1979;62:1137–42.PubMed
9.
Pottern LM, Stone BJ, Day NE, Pickle LW, Fraumeni Jr JF. Thyroid cancer in Connecticut, 1935-1975: an analysis by cell type. Am J Epidemiol. 1980;112:764–74.PubMed
10.
Kent WD, Hall SF, Isotalo PA, Houlden RL, George RL, Groome PA. Increased incidence of differentiated thyroid carcinoma and detection of subclinical disease. CMAJ. 2007;177:1357–61.CrossRefPubMedPubMedCentral
11.
Davies L, Ouellette M, Hunter M, Welch HG. The increasing incidence of small thyroid cancers: where are the cases coming from? Laryngoscope. 2010;120:2446–51.CrossRefPubMed
12.
13.
Sadetzki S, Chetrit A, Lubina A, Stovall M, Novikov I. Risk of thyroid cancer after childhood exposure to ionizing radiation for tinea capitis. J Clin Endocrinol Metab. 2006;91:4798–804.CrossRefPubMed
14.
Spitz MR, Sider JG, Katz RL, Pollack ES, Newell GR. Ethnic patterns of thyroid cancer incidence in the United States, 1973-1981. Int J Cancer. 1988;42:549–53.CrossRefPubMed
15.
16.
Aschebrook-Kilfoy B, Ward MH, Sabra MM, Devesa SS. Thyroid cancer incidence patterns in the United States by histologic type, 1992-2006. Thyroid. 2011;21:125–34.CrossRefPubMedPubMedCentral
17.
Adami, HO, Hunter, DDJ, Trichopoulos, D 2008 Textbook Of Cancer Epidemiology Oxford University Press.
18.
Li N, Du XL, Reitzel LR, Xu L, Sturgis EM. Impact of enhanced detection on the increase in thyroid cancer incidence in the United States: review of incidence trends by socioeconomic status within the surveillance, epidemiology, and end results registry, 1980-2008. Thyroid. 2013;23:103–10.CrossRefPubMedPubMedCentral
19.
Calafat AM, Ye X, Wong LY, Reidy JA, Needham LL. Exposure of the U.S. population to bisphenol A and 4-tertiary-octylphenol: 2003-2004. EnvironHealth Perspect. 2008;116:39–44.
20.
Seaberg RM, Eski S, Freeman JL. Influence of previous radiation exposure on pathologic features and clinical outcome in patients with thyroid cancer. Arch Otolaryngol Head Neck Surg. 2009;135:355–9.CrossRefPubMed
21.
Aschebrook-Kilfoy B, Kaplan EL, Chiu BC, Angelos P, Grogan RH. The Acceleration in Papillary Thyroid Cancer Incidence Rates is Similar Among Racial and Ethnic Groups in the United States. Ann Surg Oncol. 2013;20:2746–53.CrossRefPubMed
22.
Enewold LR, Zhou J, Devesa SS, Berrington De Gonzalez A, Anderson WF, Zahm SH, et al. Thyroid cancer incidence among active duty U.S. military personnel, 1990-2004. Cancer EpidemiolBiomarkers Prev. 2011;20:2369–76.
23.
24.
Morris LG, Sikora AG, Myssiorek D, DeLacure MD. The basis of racial differences in the incidence of thyroid cancer. Ann Surg Oncol. 2008;15:1169–76.CrossRefPubMed
25.
Chen AY, Jemal A, Ward EM. Increasing incidence of differentiated thyroid cancer in the United States, 1988-2005. Cancer. 2009;115:3801–7.CrossRefPubMed
26.
Haselkorn T, Stewart SL, Horn-Ross PL. Why are thyroid cancer rates so high in southeast asian women living in the United States? The bay area thyroid cancer study. Cancer EpidemiolBiomarkers Prev. 2003;12:144–50.
27.
Moolgavkar SH, Knudson Jr AG. Mutation and cancer: a model for human carcinogenesis. J Natl Cancer Inst. 1981;66:1037–52.PubMed
28.
29.
Moolgavkar SH, Luebeck EG. Multistage carcinogenesis and the incidence of human cancer. Genes, Chromosomes Cancer. 2003;38:302–6.CrossRefPubMed
30.
Jeon J, Luebeck EG, Moolgavkar SH. Age effects and temporal trends in adenocarcinoma of the esophagus and gastric cardia (United States). Cancer Causes Control. 2006;17:971–81.CrossRefPubMed
31.
Meza R, Jeon J, Moolgavkar SH, Luebeck EG. Age-specific incidence of cancer: Phases, transitions, and biological implications. Proc Natl Acad Sci U S A. 2008;105:16284–9.CrossRefPubMedPubMedCentral
32.
Moolgavkar SH, Meza R, Turim J. Pleural and peritoneal mesotheliomas in SEER: age effects and temporal trends, 1973-2005. Cancer Causes Control. 2009;20:935–44.CrossRefPubMed
33.
Meza R, Jeon J, Renehan AG, Luebeck EG. Colorectal cancer incidence trends in the United States and United kingdom: evidence of right- to left-sided biological gradients with implications for screening. Cancer Res. 2010;70:5419–29.CrossRefPubMedPubMedCentral
34.
Surveillance, Epidemiology, and End Results (SEER) Program (www.​seer.​cancer.​gov) SEER*Stat Database: Incidence - SEER 9 Regs Research Data, Nov 2010 Sub (1973-2010) <Katrina/Rita Population Adjustment> - Linked To County Attributes - Total U.S., 1969-2013 Counties, National Cancer Institute, DCCPS, Surveillance Research Program, Surveillance Systems Branch, released April 2013, based on the November 2010 submission.
35.
World Health Organization. International Classification of Diseases for Oncology (2000) 3rd Edition ed. .
36.
Luebeck EG, Curtius K, Jeon J, Hazelton WD. Impact of tumor progression on cancer incidence curves. Cancer Res. 2013;73:1086–96.CrossRefPubMed
37.
R Development Core Team 2008 R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. ISBN 3-900051-07-0, URL http://​www.​R-project.​org.
38.
Kim HJ, Fay MP, Feuer EJ, Midthune DN. Permutation tests for joinpoint regression with applications to cancer rates. Stat Med. 2000;19:335–51.CrossRefPubMed
39.
Aiaike H. A new look at the statistical model identification. IEEE Transactions on Automatic Control. 1974;19:716–23.CrossRef
40.
Kilfoy BA, Devesa SS, Ward MH, Zhang Y, Rosenberg PS, Holford TR, et al. Gender is an age-specific effect modifier for papillary cancers of the thyroid gland. Cancer Epidemiol Biomarkers Prev. 2009;18:1092–100.CrossRefPubMedPubMedCentral
41.
Hollowell JG, Staehling NW, Hannon WH, Flanders DW, Gunter EW, Maberly GF, et al. Iodine nutrition in the United States. Trends and public health implications: iodine excretion data from National Health and Nutrition Examination Surveys I and III (1971-1974 and 1988-1994). J Clin Endocrinol Metab. 1998;83:3401–8.PubMed
42.
Holford TR. Analysing the temporal effects of age, period and cohort. Stat Methods Med Res. 1992;1:317–37.CrossRefPubMed
43.
Holford TR, Zhang Z, McKay LA. Estimating age, period and cohort effects using the multistage model for cancer. Stat Med. 1994;13:23–41.CrossRefPubMed
44.
Brito JP, Morris JC, Montori VM. Thyroid cancer: zealous imaging has increased detection and treatment of low risk tumours. BMJ. 2013;347:f4706.CrossRefPubMed
45.
Esserman LJ, Thompson Jr IM, Reid B. Overdiagnosis and overtreatment in cancer: an opportunity for improvement. JAMA. 2013;310:797–8.CrossRefPubMed
46.
de Koning, Harry J and Meza, Rafael and Plevritis, Sylvia K and ten Haaf, Kevin and Munshi, Vidit N and Jeon, Jihyoun and Erdogan, S Ayca and Kong, Chung Yin and Han, Summer S and van Rosmalen, Joost and others 2013 Benefits and Harms of Computed Tomography Lung Cancer Screening Programs for High-Risk Populations.
47.
Mandelblatt JS, Cronin KA, Bailey S, Berry DA, de Koning HJ, Draisma G, et al. Effects of mammography screening under different screening schedules: model estimates of potential benefits and harms. Ann Intern Med. 2009;151:738–47.CrossRefPubMedPubMedCentral
Metadata
Title
Multistage carcinogenesis and the incidence of thyroid cancer in the US by sex, race, stage and histology
Authors
Rafael Meza
Joanne T. Chang
Publication date
01-12-2015
Publisher
BioMed Central
Published in
BMC Public Health / Issue 1/2015
Electronic ISSN: 1471-2458
DOI
https://doi.org/10.1186/s12889-015-2108-4

Other articles of this Issue 1/2015

BMC Public Health 1/2015 Go to the issue

Research article

Prevalence and pattern of alcohol consumption during pregnancy in the Netherlands

Research article

Has the prevalence of stunting in South African children changed in 40 years? A systematic review

Research article

Early motherhood: a qualitative study exploring the experiences of African Australian teenage mothers in greater Melbourne, Australia

Research article

Long term trends in control of hypertension in the Northern Sweden MONICA study 1986–2009

Research article

Factors that challenge health for people involved in the compensation process following a motor vehicle crash: a longitudinal study

Research article

The association between the parental perception of the physical neighborhood environment and children’s location-specific physical activity