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Table 1 Epidemiologic Studies of the Association Between Tubal Ligation and Risk of Ovarian Cancer

From: Tubal ligation, hysterectomy and ovarian cancer: A meta-analysis

Author (Country)

Study Design

Case definition

Covariates

OR, RR, or SIR (95%CI)

Comments

NECC 2012 (USA) [personal communication with Dr. Daniel Cramer]

Case-control

Borderline or invasive epithelial ovarian cancer N=2076

age, study center, BMI , study phase, smoking, family history of ovarian and breast cancers, talc use, OC use, parity, breast feeding, age at menarche, post-menopausal status, use of post-menopausal hormones, hysterectomy

0.79 (0.66-0.94)

 

Ness et al. 2011 (USA) [11]

Case-control

Invasive or borderline epithelial ovarian cancer

Age, number of pregnancies, race, infertility, family history of

0.63 (0.51-0.77)

 
  

N=867

ovarian cancer, ever use of oral contraceptives, ever use of IUDs, ever use of barriers, vasectomy

  

Moorman et al. 2009 (USA) [12]

Case-control North Carolina Ovarian Cancer Study

Invasive epithelial ovarian cancer

Age, parity, age at menarche, duration of OC use, family history of breast/ovarian cancer, BMI

Whites: 0.74 (0.58, 0.94)

 

African-Americans: 0.43 (0.24, 0.80)

N=746 White cases

N=111 African-American cases

Antoniou et al. 2009 (Europe and Canada) [13]

Retrospective Cohort

Ovarian cancer (only BRCA 1/2 carriers)

Age, duration of OC use, parity

BRCA 1/2: 0.43 (0.24, 0.75)

Includes prevalent and incident cases.

BRCA1: 0.42 (0.22, 0.80)

N=201 BRCA1 cases

BRCA2: 0.47 (0.18, 1.21)

Mean difference between age at diagnosis and interview: 6.7 years

N=52 BRCA2 cases

Wu et al. 2009 (USA) [37]

Case-control

Invasive and borderline ovarian cancer

Race/ethnicity, age, education, family history of ovarian cancer, menopausal status, use of oral contraceptives, parity

0.66 (0.47, 0.93)

 
  

N=609 cases

   

Dorjgochoo T. et al. 2009 (China) [14]

Prospective cohort

Ovarian cancer

Age, education, age at menarche, parity, breastfeeding, BMI, physical activity, smoking, menopausal status, family history of cancer, other contraceptive methods.

1.17 (0.62, 2.26)

Cohort N=66,661

N=94 cases

76.1% participation rate

Nagle et al. 2008 (Australia) [15]

Case-control

Invasive epithelial endometrioid and clear cell ovarian cancer

Age, education, parity, and hormone contraceptive use

Endometrioid: 0.4 (0.3, 0.7)

47% participation rate in controls

Clear cell: 0.7 (0.4, 1.2)

N=142 endometrioid cases

N=90 clear cell cases

Jordan et al. 2008 (Australia) [10]

Case-control

Invasive epithelial serous ovarian cancer

Parity, hormonal contraceptive use, history of breast or ovarian cancer, age, education

Serous (invasive): 0.87 (0.69-1.09)

 

N=627 cases

Jordan et al. 2007 (Australia) [16]

Case-control

Epithelial benign serous tumors (N=230) and benign mucinous tumors (N=133)

Age, state of residence, education, parity, hormonal contraceptive use, hysterectomy, smoking status

Combined: 1.04 (0.76-1.44)

65% participation rate in cases, 47% in controls.

Mucinous: 1.00 (0.61-1.64)

Serous: 1.08 (0.75-1.57)

 

Tworoger et al. 2007 (USA) [17]

Prospective cohort

Incident invasive epithelial ovarian cancer

Age, BMI, parity, smoking history, age at menarche, age at menopause, duration of postmenopausal hormone use, duration of oral contraceptive use

0.66 (0.50, 0.87)

Update of Hankinson et al. 1993

N=612 cases

McLaughlin JR et al. 2007 (International) [18]

Case-control

Invasive ovarian cancer (only BRCA 1/2 carriers)

Age, mutation type, country of residence, parity, breastfeeding, oral contraceptive use, ethnicity.

BRCA1+2 carriers: 0.78 (0.60, 1.00)

Includes prevalent and incident cases. Results similar when restricted to women interviewed within 3 years of diagnosis.

BRCA1: 0.80 (0.59, 1.08)

N=799 cases

BRCA2: 0.63 (0.34, 1.15)

BRCA1 N=670 BRCA2 N=128

BRCA1/2 N=1

Modugno et al. 2004 (USA) [9]

Pooled case-control

Epithelial ovarian cancer

Study site, age, family history, duration of oral contraceptive use, parity

0.63 (0.54, 0.73)

Pooled analysis from four studies.

N=2098 cases

Kjaer et al. 2004 (Denmark) [19]

Population-based follow-up study

Invasive ovarian cancer and borderline ovarian tumor

Age and calendar year

Invasive: 0.82 (0.6, 1.0)

Observed number of cancer cases in cohort of women who underwent tubal ligation was compared to the expected number of cases based on the age and calendar year specific rates from the Danish Cancer Registry.

Borderline: 0.82 (0.5, 1.3)

N=75 invasive cases

N=21 borderline cases

McGuire et al. 2004 (USA) [20]

Case-control

Invasive epithelial ovarian cancer

Age, parity, duration of OC use, race/ethnicity

BRCA 1 carriers: 0.68 (0.25, 1.90)

 

Noncarriers: 0.65 (0.45, 0.95)

N=36 BRCA1 cases

N=381 noncarrier cases

Pike et al. 2004 (Los Angeles, USA) [21]

Case-control

Invasive ovarian cancer

Age, ethnicity, SES, education, family history of ovarian cancer, use of talc, BMI, parity, age at last birth, number of incomplete pregnancies, OC use, menopausal status, age at menopause, hormone replacement therapy

0.82 (0.53-1.26)

 

N=477 cases

Rutter et al. 2003 (Israel) [23]

Case-control

Invasive epithelial ovarian cancer or primary peritoneal cancer

Age, ethnicity, parity, years of oral contraceptive use

0.70 (0.42, 1.18)

Participation rate was 79% for case patients and 66% for controls.

N=1124 cases

Wittenberg et al. 1999 (USA) [24]

Case-control

Mucinous and non-mucinous epithelial ovarian cancer

Age at diagnosis, parity, duration of OC use

Mucinous: 0.4 (0.1, 1.9)

64% participation rate in cases, 72% in controls. Included both borderline and invasive.

Non-mucinous: 0.6 (0.3, 1.1)

N=43 mucinous cases

N=279 non-mucinous cases

Kreiger et al, 1997 (Canada) [25]

Historical cohort study

Invasive and borderline ovarian cancer

Age, calendar year, length of follow-up

0.57 p<0.001

Calculated observed over expected events.

N=108 observed cases in tubal ligation subcohort

Sensitivity analysis excluding borderline malignancies similar.

Green, Purdie, et al. 1997 (Australia) [26]

Case-control

Incident, primary epithelial ovarian cancer

Age, education, BMI, parity, OC duration, smoking, family history of ovarian cancer

0.61 (0.46, 0.85)

90% participation rate in cases, 73% in controls.

N=824 cases

Cornelison et al 1997 (USA) [27]

Case-control

Ovarian cancer N=300 cases

Age , SES, marital status, parity, age at first pregnancy, age at menarche, age at menopause, irregular menses, breast-feeding duration, BMI, OC use

0.52 (0.31,0.85)

Patient controls with no malignancy or ovarian disease.

Miracle-McMahill, et al. 1997 (USA) [28]

Prospective Cohort Study

Ovarian cancer mortality

Age, race, BMI, education, family history of ovarian cancer, family history of breast ca, parity, marital status, age at menarche, OC use, ERT, age at menopause, miscarriages smoking status

0.68 (0.45, 1.03)

 

N=799 ovarian cancer deaths

Rosenblatt, et al. 1996 (International) [29]

Case-control

Borderline or malignant epithelial ovarian cancer

Age, hospital, year of interview, parity OC use

0.71 (0.47, 1.08)

No differences observed for borderline and malignant tumors.

N=385 cases

Risch et al. 1996 (Canada) [22]

Case-control

Epithelial ovarian cancer

Age, parity, years of OC use, average lactation/pregnancy, total years of ERT, hysterectomy, family history of breast cancer

0.67 (0.47-0.94)

Invasive and borderline tumors included.

N=450 cases Borderline

N=83 Invasive N=376

Nandakumar et al. 1995 (India) [30]

Case-control

Ovarian cancer

Age, residential area, parity, age at first birth

0.25 (0.08, 0.78)

Restricted to ever-married women. Hospital-based controls.

N=97 cases

Whittemore et al 1992 (USA) [31]

Pooled case-control

Invasive epithelial ovarian cancer

Age, study, parity, OC use

Hospital-based studies:

Restricted to white women. 6 hospital based studies and 6 population-based studies.

0.59 (0.38, 0.93) Population-based studies: 0.87 (0.62, 1.20)

N=2197 cases

Booth et al 1989 (England) [32]

Case-control

Epithelial ovarian cancer

Age, social class, gravidity, unprotected intercourse

0.2 (0.1, 0.6)

Cases were less than 65 years old and interviewed within 2 years of diagnosis. Age-matched hospital-based controls.

N=235 cases

Shu et al 1989 (China) [33]

Case-control

Invasive epithelial ovarian cancer

Age, education, parity, age at menarche, ovarian cyst

0.8 (0.4, 1.6)

89% participation rate in cases, 100% in controls. All <70 years of age.

N=172 cases

Koch et al 1988 (Canada) [34]

Case-control

Epithelial ovarian cancer

None

0.8 (0.5, 1.3)

47% participation rate in controls. Age-matched, but did not control for age in analyses.

N=200 cases

Mori et al 1988 (Japan) [36]

Case-control

Primary epithelial ovarian cancer

Age, parity, marital status, number of induced abortions

0.5 (0.25, 1.00)

Controls were hospital in-patients with gynecological complaints other than ovarian cancer and OB/GYN outpatients without a malignant ovarian disorder. 100% participation rate in cases and controls.

N=110 cases

Koch et al. 1984 (Canada) [35]

Retrospective cohort

Ovarian cancer N=4 cases

Age, nulliparity

2.4 (0.9, 6.7)

Population who underwent tubal ligation were mental patients. 34% were lost to follow-up. Many underwent the procedure at young ages (i.e. 10-19). Expected rates calculated from a previous retrospective study. Incomplete adjustment for parity.

  1. Abbreviations: OR, odds ratio; RR, relative risk; SIR, standardized incidence ratio; OC, oral contraceptive; BMI, body mass index; SES, socio-economic status; ERT, estrogen replacement therapy.