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Table 1 Characteristics of the included studies

From: Screening for cervical cancer: a systematic review and meta-analysis

Randomized (cluster) controlled trial

Study

Location

Number of participants

Ages (years)

Screening exposure

Disease definition

Participant eligibility

Post screening treatment

Follow-up

Intervention

Control

Sankaranarayanan et al. [20]

India

HPV: 34,126 Cytology: 32,058

31,488

30 to 59

Only 8 (<0.007%) of the eligible women had ever been screened

Invasive cervical cancer; FIGO stages I+

No history of cervical cancer

Cryotherapy, LEEP, conization offered for CIN; invasive cancer referred for treatment (surgery, radiotherapy)

8 years 2000 to 2007

Cohort studies

Study

Location

Number of participants

Ages (years)

Screening exposure

Disease definition

Participant eligibility

Post screening treatment

Follow-up

Herbert et al.[21]

UK

116,022 (four groups based on screening history)

25 to 69

Interval since last smear: <3.5 y, 3.5 to 5.5 y, >5.5 y, no record

Invasive cervical cancer; FIGO stages I+

No hysterectomy

NR

3 years 1991 to 1993

Excluded: smears to investigate symptoms, referral smears in screen-detected cases

Rebolj et al. [22]

Netherlands

Cohort 1: 445,382 Cohort 2: 218,847

C1: 30 to 44 C2: 45 to 54

Mean interval between three consecutive negative results

Invasive cervical cancer; FIGO stages NR

Three consecutive negative smears in age interval; no history of CIN or cytological abnormalities

NR

10 years 1994 to 2002

C1: 39 m

C2: 40 m

Case control studies

Study

Location

Number of participants

Ages (years)

Screening exposure/history

Case/disease definition

Control eligibility

Post screening treatment

Case diagnosis dates

Cases

Controls

Andrae et al.[24]

Sweden

1,230

6,124

20 to 99

Interval since last smear: 6 to 42 m (ages <53), 6 to 66 m (ages 54 to 65), 6 to 78 m (ages ≥66), not screened during interval

Invasive cervical cancer; FIGO stages 1+

No history of cervical cancer; alive on case diagnosis date

NR

1999 to 2001

Excluded: smears <6 m prior to case diagnosis

Aristizabal et al. [15]

Colombia

277

554

16 to 60

Interval since last smear: 12 to 72 m prior to case diagnosis

Invasive cervical cancer; excluded in situ

Out-patient services from same clinic where case diagnosed or reside in same area as case

NR

1977 to 1981

Excluded: smears <12 m prior to diagnosis/index date

Berrino et al.[16]

Italy

121

350

NR

Interval since last negative smear: 0 to 11 m, 12 to 23 m, 24 to 35 m, 36 to 47 m, 48+ m, no prior negative smear

Invasive cervical cancer; FIGO stages I+

Married women hospitalized for and diagnosed with non-gynecological diseases; no history of breast cancer or hysterectomy

Two controls had been treated for carcinoma in situ after a positive smear result

1978

Included: smears prior to symptoms (cases), smears prior to study mid-point (controls)

Clarke and Anderson [17]

Canada

212

1,060

Mean 52

Interval since last smear: <5 y prior to case diagnosis

Invasive cervical cancer; most <6 m post diagnosis

No exclusion for hysterectomy

NR

1973 to 1976

Included: non-symptomatic, routine examination smears

Decker et al.[25]

Canada

666

3,343

≥18 Mean 50

Interval since last smear: <5 y prior to case diagnosis

Invasive cervical cancer; FIGO stages I+

No history of cervical cancer or malignant neoplasms (excluding non-melanoma skin cancer); no hysterectomy

NR

1989 to 2001

Excluded: smears <6 m prior to case diagnosis

Hernández-Avila et al. [26]

Mexico

397

1,005

25 to 80 Mean 48

Exposure: any lifetime smear(s), no history

Invasive cervical cancer

Eligibility limited only by age and area of residence

NR

1990 to 1992

Excluded: smears <12 m prior to case diagnosis or control interview

Herrero et al.[18]

Latin America

759

1,430

<70

Interval since last smear: 12 to 23 m, 24 to 47 m, never screened

Invasive cervical cancer; FIGO stages I+

No history of psychiatric diagnoses, hysterectomy, cancer, or diseases related to exposures of interest; history of sexual intercourse

NR

1986 to 1987

Excluded: smears <1 y prior to interview (mean interval between case diagnosis and: case interview 1 m; control interview 2.3 m)

Hoffman et al.[27]

South Africa

524

1,540

<60

Interval since last smear: <5 y, 5 to 9 y, 10 to 14 y, ≥15 y, unknown, never

Invasive cervical cancer; FIGO stages IB to IV; diagnosed ≤6 m prior to study enrollment

Hospital admission not related to risk of cervical cancer

NR

NR late 1990s

Analysis excluding smears in prior 12 m showed no difference in findings

Jiménez-Pérez and Thomas [28]

Mexico

143

311

Mean 49

Interval since last smear: 1 to 12 m, 13 to 60 m, >60 m, unknown, never

Invasive cervical cancer; FIGO stages IB to IV

No hysterectomy; not attending clinic for cervical screening, or any gynecologic or obstetric conditions; history of sexual intercourse

NR

1991 to 1994

Excluded: smears ≤12 m prior to diagnosis/index date

Kasinpila et al.[38]

Thailand

130

260

Mean 48

Interval since last smear: <6 m, 6 to 11 m, 12 to 35 m, 36+ m, never

Invasive cervical cancer; diagnosed ≤3 m prior to interview

No evidence of cervical disease or any other gynecological disease

Cryotherapy and LEEP offered for confirmed abnormalities

2009

Excluded: smears in previous 6 m

La Vecchia et al.[19]

Italy

191

191

22 to 74

Interval since last smear: <3 y, 3 to 5 y, >5 y, never

Invasive cervical cancer; FIGO Stages 1+

Admitted and diagnosed with acute non-malignant, non-hormonal, non-gynecological problems <1 y prior to interview

NR

1981 to 1983

Excluded: smears to investigate symptoms; cases with positive smear <1 y prior to diagnosis

Makino et al. [29]

Japan

129

396

35 to 79

Interval since last negative smear to diagnosis/index date: 1 y, 2 y, 3 y, 4 y, ≥5 y

Invasive cervical cancer; diagnosed <6 m after abnormal smear result

No invasive cervical cancer; no hysterectomy; no previous abnormal cytology results; participated in mass screening

NR

1984 to 1990

Exposure: any lifetime smear(s), no history

Excluded: smears to investigate symptoms or taken at time of diagnosis

Miller et al.[31]

USA

482

934

Mean 49

Interval from last negative smear to diagnosis/index date: 1 y (0 to 18 m), 2 y (19 to 30 m), 3 y (31 to 42 m), 3 to 5 y (42 to 66 m), 5 to 10 y (67 to 126 m), >10 y (>126 m)

Invasive squamous cell cervical cancer

No prior hysterectomy or radiation to the pelvis

NR

1983 to 1995

Nieminen et al.[23]

Finland

179

1,507

30 to 91 Mean 60

Exposure: any lifetime smear(s), no history

Invasive cervical cancer

Eligibility limited only by catchment (reside in area served by case treatment hospital)

Organized screening program provides colposcopy examinations and treatment for mild abnormalities

1987 to 1994

Excluded: smears <1 y prior to diagnosis/index date

Sasieni et al.[32]

UK

348

677

≥20

Interval since last negative smear (not immediately following a test showing abnormal results): 0 to 11 m, 12 to 23 m, 24 to 35 m, 36 to 47 m, 48 to 65 m, >66 m, no history

Invasive cervical cancer; FIGO stages IB+

No hysterectomy

NR

1992

Sasieni et al.[33]

UK

1,305

2,532

20 to 69

Interval since last negative smear (no abnormal smear in prior 12 m): <3 y, 3<5 y, 5+ y, no history of a negative smear

Invasive cervical cancer; FIGO stages IB+

No hysterectomy

NR

1990 to 2001

Sasieni et al.[34]

UK

4,012

7,889

20 to 69

Exposure: screening or no screening during specific age bands (for example, 20 to 21, 22 to 24, 20 to 24) related to cancers diagnosed in specific and imminent age bands (for example, 25 to 29)

Invasive cervical cancer; FIGO stages I+

No hysterectomy; registered with a National Health Services general practitioner, still alive, not emigrated

NR

1990 to 2008

Sasieni et al.[35]

UK

3,305

6,516

20 to 69

Maximum interval between smears: <3.5 y, 3.5 to 5.5 y, >5.5 y or no smear history

Invasive cervical cancer; FIGO stages I+

No hysterectomy

NR

1990 to 2008

Talbott et al.[30]

USA

143

143

Mean 45

Exposure: smear <3 y prior to case diagnosis or control interview

Invasive cervical cancer (localized, regional or distant); excluded in situ

No hysterectomy

NR

1984 to 1985

Diagnostic smears: any positive result <12 m prior to diagnosis

Yang et al.[36]

Australia

877

2,614

20 to 69

Exposure: 0, 1 or 2+ smears in last 4 y

Invasive cervical cancer (localized and non-localized)

No invasive cervical cancer diagnosis 1996 to 2003; alive at case diagnosis; no hysterectomy before end point

NR

2000 to 2003

Excluded: smears <3 m prior to case diagnosis

Zappa et al.[37]

Italy

208

832

<70

Interval since last smear (prior to index date): ≤3 y, 3 to 6 y, 6+ y, no record

Fully invasive cervical cancer; excluded micro-invasive

No hysterectomy prior to index date; alive at index date

NR

1994 to 1999

Excluded: smears <12 m prior to diagnosis/index date

  1. CIN, Cervical intraepithelial neoplasia; FIGO, International Federation of Gynecology and Obstetrics; LEEP, loop electrosurgical excision procedure; NR, not reported; m, months; y, years.