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Table 1 Characteristics of studies included in the meta-analysis

From: Breastfeeding and the risk of childhood cancer: a systematic review and dose-response meta-analysis

First author, year, country

Data collection years

Design

No. of cases/controls1

Age (years)

Source of cases

Source of controls

Cancer type

Breastfeeding categories (months)

Method of assessing breastfeeding

Variables matched or adjusted

NOS

Risk of bias

Davis, 1988, USA [33]

1976–1983

PC-CS

201/181

1.5–15

Colorado Central Cancer Registry

Population

Leukemia (N = 63); brain tumors (N = 38); lymphoma (N = 26); STS (N = 15); other cancers (N = 59)

Never/≤ 6/> 6 (lymphoma); ≤ 6/> 6 (leukemia, brain tumors, STS)

Interview of parents

Matched: age (±3 years), sex, telephone exchange. Adjusted: none.

7

Moderate

Magnani, 1988, Italy [34]

1981–1984

HC-CS

182/307

NA

The main pediatric hospital of Turin

Hospital patients

Leukemia (N = 163); NHL (N = 19)

Never/1–6/> 7

Interview of parents

Matched: none. Adjusted: none.

5

Serious

Van Duijn, 1988, Netherlands [35]

1973–1979

PC-CS

492/480

1–15

The national registry of the Dutch Childhood Leukemia Study Group

Population

ALL (N = 492)

Never/≤ 6/> 6

Questionnaires mailed to parents

Matched: age (±3 years), sex. Adjusted: age, sex, birth order, social class, maternal education, and maternal factors (age, smoking, alcohol use in pregnancy).

7

Moderate

Shu, 1995, China [36]

1981–1991

PC-CS

241/241

1–15

Shanghai Cancer Registry

Population

Lymphoma (N = 82); leukemia (N = 159)

Never/1–6/> 6

Interview of parents

Matched: sex, year of birth. Adjusted: maternal age at birth, birthweight, maternal working status and occupational exposure to chemicals during infancy.

8

Moderate

Shu, 1995, USA and Canada [17]

1982–1989

PC-CS

105/639

0–15

The Children’s Cancer Group (CCG), 1982–1989

Population

Malignant germ cell tumors (N = 105)

Never/1–6/7–12/> 12

Self-administered questionnaire to mother

Matched: none. Adjusted: age, gender, gestational age, number of livebirths, maternal education, and smoking during pregnancy.

7

Moderate

Petridou, 1997, Greece [37]

1993–1994

HC-CS

153/300

0–14

A nationwide network of childhood hematologists/oncologists

Hospital patients

Leukemia (N = 153)

Ever vs. never

Interview of guardians

Matched: place of residence, gender and age. Adjusted: sex, age, place of residence, sociodemographic, lifestyle, environmental and biomedical variables.

7

Serious

Schüz, 1999, Germany [38]

1992–1997

PC-CS

1001/1001

0–14

German Children’s Cancer Registry (GCCR)

Population

Leukemia (N = 1001)

≤ 1/2–6/> 6

Questionnaire and telephone interview

Matched: gender, date of birth and district. Adjusted: socioeconomic status (SES).

7

Moderate

Shu, 1999, USA and Canada [39]

1989–1993

PC-CS

2200/2418

1–17

The Children’s Cancer Group (CCG), 1989–1993

Population

Leukemia (N = 2200)

Never/1–3/4–6/7–9/10–12/> 12; Ever vs. never

Interview of mothers

Matched: age, geographic location and ethnicity. Adjusted: maternal race, maternal education, and family annual income.

8

Moderate

Smulevich, 1999, Russia [40]

1986–1988

PC-CS

593/1181

0–14

Russian Cancer Research Center RAMS

Population

Lymphoma (N = 117); leukemia (N = 199); brain tumors (N = 57); neuroblastoma(N = 42); nephroblastoma (N = 48); STS (N = 53); other cancers (N = 77)

< 1/1–2/3–4/5–6/7–12/> 12 (leukemia, STS, neuroblastoma, nephroblastoma); ≤ 2/3–4/5–6/7–12/> 12 (lymphoma, brain tumors)

Interview of mothers

Matched: age, gender and residence. Adjusted: none.

7

Moderate

Dockerty, 1999, New Zealand [41]

1991–1995

PC-CS

97/303

0–14

National databases including the New Zealand Cancer Registry

Population

ALL (N = 97)

Never/≤6/> 6–12/> 12; Ever vs. never

Interview of mothers

Matched: age and sex.Adjusted: age, sex, child’s social class, mother’s education, household crowding, delay from reference date to interview.

8

Moderate

Infante-Rivard, 2000, Canada [42]

1980–1993

PC-CS

491/491

0–9

Tertiary care centers

Population

ALL (N = 491)

Never/≤ 3/> 3

Interview of mothers

Matched: age, sex, and region of residence at the time of diagnosis.Adjusted: none.

8

Moderate

UKCCS Investigators, 2001, UK [43]

1991–1996

PC-CS

3500/6964

1–14

UKCCS

Population

Lymphoma (N = 342); leukemia (N = 1637); other cancers (N = 1521)

Never/< 1/1–6/≥ 7; Ever vs. never

Interview of mothers

Matched: month and year of birth, sex and region of residence at diagnosis.Adjusted: age at diagnosis, sex, region, birth order and deprivation index.

7

Moderate

Hardell, 2001, Sweden [14]

1993–1996

PC-CS

835/860

0–14

Swedish Cancer Register

Population

Leukemia (N = 235); lymphoma (N = 99); brain tumors (N = 264); neuroblastoma (N = 34); retinoblastoma (N = 22); germ cell tumors (N = 21); STS(N = 37); other cancers (N = 123)

0– < 1/1– < 6/≥ 6;≥ 1 vs. 0- < 1

Routine child health records

Matched: age and sex.Adjusted: none.

8

Moderate

Schüz, 2001, Germany [44]

1988–1994

PC-CS

465/2442

0–14

German Children’s Cancer Registry (GCCR)

Population

Brain tumors (N = 281); other cancers (N = 184)

≤ 1/2–6/> 6

Questionnaire and telephone interview

Matched: gender and date of birth within 1 year.Adjusted: degree of urbanization and socioeconomic status.

7

Moderate

Daniels, 2002, USA and Canada [45]

1992–1994

PC-CS

393/376

0.5–19

The Children’s Oncology Group in the United States and Canada, 1992–1994

Population

Neuroblastoma (N = 393)

Never/0–3/4–6/7–9/9–12/≥ 13; Ever vs. never

Interview of mothers

Matched: date of birth.Adjusted: income and age.

6

Moderate

Murray, 2002, UK [46]

1975–1986

Historical cohort

178/409969

0–16

The Northern Ireland Cancer Registry

Population

ALL (N = 178)

Ever vs. never

Child health records

Matched: none.Adjusted: none.

6

Serious

Perrillat, 2002, France [47]

1995–1999

HC-CS

247/237

2–15

The hospitals of Lille, Lyon, Nancy and Paris

Hospital patients

Leukemia (N = 247)

Never/< 3/3–5/6–11/≥ 12; Ever vs. never

Interview of mothers

Matched: age, gender, hospital, hospital catchment area and ethnic origin.Adjusted: age, gender, hospital, ethnic origin, maternal educational level and parental socio professional category, birth weight, length of pregnancy and number of previous pregnancies

8

Moderate

Lancashire, 2003, UK [13]

1972–1981

PC-CS

3376/3376

1–14

The Oxford Survey of Childhood Cancers (OSCC)

Population

Leukemia (N = 1342); other cancers (N = 2034)

Never/< 1/1–6/≥ 7; Ever vs. never

Interview of parents

Matched: sex and date of birth.Adjusted: sex, age at death, father’s occupational social class, sibship position, maternal age at child’s birth.

7

Moderate

Jourdan-Da, 2004, France [48]

1995–1998

PC-CS

452/530

1–15

The National Registry of Childhood Leukemia and Lymphoma

Population

Leukemia (N = 452)

Never/< 3/3–6/> 6; Ever vs. never

Self-administered questionnaire to mother

Matched: age, sex and region.Adjusted: gender, age at diagnosis, region of residence at diagnosis.

7

Moderate

Altinkaynak, 2006, Turkey [49]

1990–2000

PC-CS

137/146

1–16

The Ataturk University Medicine Faculty

Population

Leukemia (N = 87); lymphoma(N = 50)

0–6 vs. > 6

Interview of mothers

Matched: sex and age.Adjusted: none.

7

Moderate

Saddlemire, 2006, USA and Canada [50]

1999–2002

PC-CS

461/443

0.5–16

The Children’s Oncology Group in the United States and Canada, 1999–2002

Population

Wilms tumor (N = 461)

Never/0–3/4–6/7–9/10–12/≥ 13; Ever vs. never

Telephone interviews of mothers

Matched: age strata and geographic region of residence.Adjusted: child’s age at reference date, geographic region of residence, household income and mother’s education.

7

Moderate

Shaw, 2006, Canada [51]

1980–1993;1995–1999

PC-CS

272/272

0–14

Tertiary care centers in the province of Quebec

Population

Brain tumors (N = 272)

Never/≤ 8 weeks/9-24 weeks/> 24 weeks; Ever vs. never

Interview of parents

Matched: sex and age at diagnosis.Adjusted: mother’s education level.

6

Moderate

Petridou, 2006, Greece [52]

1996–2002

HC-CS

71/71

0–14

A nationwide network of childhood hematologists/oncologists

Hospital patients

HD (N = 71)

Ever vs. never

Interview of guardians

Matched: gender and age (±6 months).Adjusted: demographic, socioeconomic, anthropometric and perinatal variables.

7

Serious

Bener, 2008, United Arab Emirates [53]

1983–2004

HC-CS

169/169

0–15

Tawam Hospital, Al Ain

Hospital (healthy subjects)

ALL (N = 103); HD (N = 32); NHL (N = 34)

0–6 vs. > 6

Telephone interviews with mothers

Matched: age and sex.Adjusted: none.

6

Moderate

MacArthur, 2008, Canada [54]

1990–1994

PC-CS

399/399

0–14

Pediatric oncology treatment centers and cancer registries

Population

Leukemia (N = 399)

Never/0–3/4–6/7–12/> 12

Interview of parents or guardians

Matched: age, gender, and area.Adjusted: maternal age at birth, maternal education, annual household income, ethnicity, and number of residences since birth.

6

Moderate

Flores-Lujano, 2008, Mexico [55]

1998–2006

HC-CS

57/218

0–19

The institutions that treat children with cancer in Mexico

Children with Down syndrome

Leukemia (N = 57)

Never/≤ 6/≥ 7; Ever vs. never

Interview of parents

Matched: none.Adjusted: sex, weight at birth < 2500 g, age of child, firstborn child, low standard of living and cardiovascular diseases.

6

Moderate

Rudant, 2010, France [56]

2003–2004

PC-CS

720/1494

1–14

ESCALE, 2003–2004

Population

ALL (N = 634); AML (N = 86)

Never/≤ 2/3–5/6–11/≥ 12; Ever vs. never

Telephone interview of mothers

Matched: age and gender.Adjusted: age, gender, parental professional category, degree of urbanization, and maternal age at child’s birth.

8

Moderate

Rudant, 2011, France [57]

2003–2004

PC-CS

291/2149

2–14

ESCALE, 2003–2004

Population

HD (N = 127); NHL (N = 164)

Never/< 6/≥ 6

Telephone interview of mothers

Matched: age and gender.Adjusted: age, gender, parental professional category, degree of urbanization, maternal age at child birth and housing, for contact with animals.

8

Moderate

Waly, 2011, Sultanate of Oman [58]

2008–2010

HC-CS

70/70

NA2

The Sultan Qaboos University Hospital

Relatives of the cases

ALL (N = 70)

< 6/6–12/12–24/ > 24

Interview of mothers

Matched: none.Adjusted: none.

6

Serious

Urayama, 2012, USA [59]

1995–2008

PC-CS

507/762

1–14

The Northern California Childhood Leukemia Study

Population

ALL (N = 507)

Ever vs. never

Questionnaire to parents or guardians

Matched: date of birth, sex, Hispanic status, and maternal race.Adjusted: age, sex, maternal age, maternal education, annual household income and race/ethnicity.

8

Moderate

Lupo, 2014, USA [60]

1982–1988

PC-CS

319/317

0–20

Intergroup Rhabdomyosarcoma Study Group (IRSG)

Population

Rhabdomyosarcoma (N = 319)

Never/< 6/6–12/≥ 12; Ever vs. never

Telephone interview to mothers

Matched: race, sex, and age.Adjusted: age, race, sex, household income, maternal, and paternal education.

7

Moderate

Mattioli, 2014, Italy [61]

1998–2003

PC-CS

82/1040

0–10

Childhood acute leukemia in 14 Italian Regions

Population

AnLL (N = 82)

Never/1–3/4–6/> 6

Interview of parents

Matched: date of birth, sex and residence area.Adjusted: none.

6

Serious

Schraw, 2014, USA [62]

1997–2011

PC-CS

142/284

0–14

The Texas Children’s Cancer Center

Healthy subjects

ALL (N = 142)

Ever vs. never

Questionnaire to mothers

Matched: age, sex, race, and ethnicity.Adjusted: none.

7

Moderate

Ajrouche, 2015, France [63]

2010–2011

PC-CS

617/1225

1–14

ESTELLE, 2010–2011

Population

ALL (N = 617)

Never/< 6/≥ 6; Ever vs. never

Telephone interview of mothers

Matched: age and gender.Adjusted: age, gender, parental professional category, maternal age, and degree of urbanization.

8

Moderate

Greenop, 2015, Australia [64]

2003–2006;2005–2010

PC-CS

592/1389

0–14

Aus-ALL and Aus-CBT

Population

ALL (N = 314); brain tumors (N = 278)

Never/< 3/3- < 6/≥ 6; Ever vs. never

Questionnaire to mothers

Matched: age, sex, and state of residence.Adjusted: Matched variables, maternal education, maternal age at birth, birth order, proportion of optimum birth weight.

7

Moderate

Heck, 2015, USA and Canada [65]

2006–2011

HC-CS

243/134

0–15

Wills Eye Hospital in Philadelphia, or the Children’s Oncology Group

Friends or unrelated children of case family

Retinoblastoma (N = 243)

< 1/1–6/7–11/≥ 12; Ever vs. never

Telephone interview of parents

Matched: age.Adjusted: child’s age at interview, mother’s race/ethnicity, mother’s educational attainment, and household income.

7

Moderate

Amitay, 2016, Israeli [66]

2005–2013

PC-CS

178/357

1–18

The hematologic departments of five large Israeli hospitals

Population

Leukemia (N = 117); lymphoma (N = 61)

≤ 6 vs. > 6

Interview of mothers

Matched: age, gender, and spoken language.Adjusted: none.

7

Moderate

Rios, 2016, France [67]

2003–2004;2010–2011

PC-CS

269/1589

0.5–6

ESCALE, 2003–2004; ESTELLE, 2010–2011

Population

Neuroblastoma (N = 269)

Never/< 3/3–5/≥ 6; Ever vs. never

Telephone interview of mothers

Matched: age and gender.Adjusted: age and sex, birth order, maternal age, urban status of the area of residence and study.

8

Moderate

Bailey, 2017, France [68]

2003–2004;2010–2011

PC-CS

469/2719

1–14

ESCALE, 2003–2004; ESTELLE, 2010–2011

Population

Brain tumors (N = 469)

Never/< 3/3- < 6/≥ 6; Ever vs. never

Telephone interview of mothers

Matched: age and gender.Adjusted: age and gender.

8

Moderate

Schraw, 2017, USA [69]

1997–2012

PC-CS

171/342

0–14

Texas Children’s Cancer Center in Houston

Population

ALL (N = 171)

Ever vs. never

Questionnaire to parents

Matched: sex, ethnicity, and age.Adjusted: none.

7

Moderate

Gao, 2018, China [70]

2008–2017

HC-CS

958/785

0–14

The Children’s Hospital of Zhejiang University

Hospital patients

Leukemia (N = 958)

Never/1–3/4–6/7–9/10–12/≥ 13

Medical records

Matched: none.Adjusted: family history of cancer, the family history of neoplasm of the lymphatic/hematopoietic systems, history of bedroom decoration, smoking during pregnancy, the history of using birth control pills before pregnancy, abortion history, Down’s syndrome and parents use of hair dye.

8

Moderate

Jiménez-Hernández, 2018, Mexico [18]

2010–2015

HC-CS

1455/1455

0–17.6

Private and public hospitals in Mexico City

Hospital patients

Leukemia (N = 1455)

Never/0–3.9/4–6.9/7–12.9/> 13

Interview of mothers

Matched: none.Adjusted: none.

5

Serious

Lingappa, 2018, India [71]

2015

HC-CS

120/120

1–15

Kidwai Institute of Oncology

the elder sibling of the cases

Leukemia (N = 120)

Never/< 4/4–6/6–9/ 9–12/13–18/ 19–24/> 24;Ever vs. never

Interview of mothers

Matched: parental education, socioeconomic status, and the region of residence.Adjusted: none.

5

Moderate

Rafieemehr, 2019, Iran [72]

2015–2018

HC-CS

125/130

1–12

Be’sat Hospital of Hamadan University of Medical Sciences

Hospital (healthy subjects)

ALL (N = 125)

Ever vs. never; 1–3/4–6/7–9/ 10–12/≥ 24

Interview of parents

Matched: age, sex, gender, and residence location.Adjusted: none.

6

Serious

Bauer, 2020, France [73]

2015–2018

PC-CS

112/996

0.5–11

ESTELLE, 2010–2011

Population

Wilms tumor (N = 112)

Never/ < 3/3–5/≥ 6; Ever vs. never

Telephone interview of mothers

Matched: age and gender. Adjusted: age, gender, birth order, and maternal age.

7

Moderate

  1. Abbreviations: PC-CS population-based case-control study, HC-CS hospital-based case-control study, CNS central nervous system, ALL acute lymphoblastic leukemia, AML acute myeloid leukemia, AnLL acute nonlymphoblastic leukemia, HD Hodgkin’s disease, NHL non-Hodgkin lymphoma, NA not applicable, UKCCS United Kingdom Childhood Cancer Study, Aus-ALL The Australian Study of the Causes of Acute Lymphoblastic Leukemia, Aus-CBT Australian Study of Childhood Brain Tumors, STS Soft-tissue sarcoma, ESCALE and ESTELLE The ESCALE and ESTELLE studies were two nationwide population-based studies in France, designed to investigate the role of environmental, infectious, and genetic factors of childhood cancers
  2. 1No. of cases/controls in breastfeeding analysis; 2Mean ± SD of age in cases and controls were 12.1 ± 2.72 and 13.5 ± 2.85, respectively, while age range had not been reported