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Received: 27 May 2017    Revised: 4 September 2017    Accepted: 31 October 2017    First published online: 24 November 2017

DOI: 10.1002/ijgo.12375

REVIEW ARTICLE
Obstetrics

Meta-­analysis of associations between maternal breast

cancer and the risk of adverse delivery outcomes

Chenyu Sun1,‡ | Xiuxiu Ding2,‡ | Yile Wu3 | Liqi Yang3,*

1
The First Affiliated Hospital of Anhui Medical
University, Hefei, Anhui, China Abstract
2
Lianhua Community Health Service Background: Research into the effects of breast cancer on delivery outcomes has
Centre, The Second Affiliated Hospital of
­generated inconsistent findings.
Anhui Medical University, Hefei, Anhui, China
3 Objectives: To pool data from existing observational studies of the effect of breast
The Second Affiliated Hospital of Anhui
Medical University, Hefei, Anhui, China cancer on preterm delivery and low delivery weight.
Search strategy: A systematic literature search of PubMed, Embase, and Web of
*Correspondence
Liqi Yang, The Second Affiliated Hospital of Science databases using keywords including, “breast cancer” and “birth outcome” up
Anhui Medical University, Hefei, Anhui, China.
to March 7, 2017, was performed.
Email: yanglqaydefy@163.com.
Selection criteria: Observational studies of the effect of breast cancer on delivery
‡
These authors contributed equally to
outcomes were included.
this work.
Data collection and analysis: Articles were reviewed independently by two authors
and data were extracted. Risk ratios and 95% confidence intervals were calculated.
Main results: Preterm delivery data were included from seven studies including
6 687 579 patients and low delivery weight data were retrieved from five studies
including 6 687 103 patients. Maternal breast cancer was associated with an increased
risk of preterm delivery (pooled risk ratio 1.82, 95% confidence interval 1.44–2.30)
and low delivery weight (pooled risk ratio 1.41, 95% confidence interval 1.15–1.74).
No publication bias was detected in the meta-­analysis.
Conclusions: The present meta-­analysis demonstrated that maternal breast cancer
was associated with increased risk of preterm delivery and low delivery weight.

KEYWORDS
Breast cancer; Low birth weight; Meta-analysis; Preterm

1 | INTRODUCTION
Breast cancer is the most common cancer among women worldwide,
with 1.7 million new diagnoses made in 2012.1 This number accounted
for approximately 12% of all new cancers among the general popula-
1
tion and 25% of all new cancers among women. Breast cancer was
the most common pregnancy-­related cancer, with a incidence of
122.9 per 100 000 pregnancies.2 Approximately 25% of breast can-
cers are diagnosed in premenopausal women.3 With an increasing
population of women choosing to delay childbearing, and improved
breast cancer survival rates owing to recent developments in chemo-
4,5
therapy and hormonal therapy, it can be expected that more women
of childbearing age will be diagnosed with breast cancer and face deci-
sions that could influence their future reproductive health.6 Owing
to growing numbers of breast cancer survivors, concerns have been
raised about the adverse effects of breast cancer and cancer therapy
on neonatal outcomes.7
Breast cancer diagnosis and treatment can have long-­lasting
adverse effects on reproductive health outcomes in survivors.6
Research has shown that premenopausal women could experience
temporary chemotherapy-­related amenorrhea, premature ovarian
failure, and other adverse reproductive events during chemother-
apy.8,9 The findings from a large population-­based cohort study10
indicated that the fertility rate among women diagnosed with breast

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© 2017 International Federation of Int J Gynecol Obstet 2018; 140: 146–152
Gynecology and Obstetrics
Sun ET AL.
cancer was three-­fold lower compared with women without breast
cancer. Few studies have addressed the effects of breast cancer
on delivery outcomes, and results have been inconsistent.6,11–17
A previous population-­based cohort study14 revealed that deliv-
eries by women exposed to breast cancer were associated with an
increased risk of adverse delivery outcomes including delivery com-
plications, cesarean delivery, very preterm delivery, and low delivery
weight. Additionally, a recent large population-­based study6 has also
reported increased adjusted prevalence ratios for preterm delivery,
low delivery weight, and small for gestational age neonates among
women with a history of breast cancer compared with the general
population. Inconsistently, a retrospective population-­based cohort
study with a large sample size12 demonstrated that women with
breast cancer were not at statistically elevated risk of preterm deliv-
ery and low delivery weight in comparison with women without can-
cer. A study conducted by Jacob et al.11 reported reduced early and
late pregnancy loss among women with a history of breast cancer
compared with a control group; breast cancer history was associated
with advantageous effects on a subsequent pregnancy. However, the
sample size in this study was limited and could have resulted in lower
statistical power.11
Improved understanding of associations between breast cancer and
risks of preterm delivery and low delivery weight could have important
implications for reproductive healthcare. It is important to estimate
the magnitude of any increased risk of adverse delivery outcomes
such as preterm delivery and low delivery weight. Consequently, the
present meta-­analysis was conducted to pool existing observational
studies of the effects of breast cancer diagnosed before, during, or
shortly after pregnancy.
2 | MATERIALS AND METHODS
2.1 | Search strategy
The present meta-­analysis was conducted according to PRISMA
guidelines.18 A systematic literature search of PubMed, Embase,
and Web of Science up to March 7, 2017, was performed. The
following search terms were used to identify studies for inclu-
sion: (“breast cancer” OR “breast neoplasms”) AND (“preterm” OR
“low birth weight” OR “birth outcome” OR “pregnancy outcome”
OR “infant outcome”). The reference lists of retrieved studies,
review articles, and conference abstracts were reviewed to identify
­additional studies.
2.2 | Selection of studies
Studies were included if they met the following inclusion criteria: (1)
original articles; (2) studies with human patients; (3) providing a sum-
mary estimate (e.g. risk ratio [RR], odds ratio) with corresponding 95%
confidence intervals (CIs) or incidence rates of preterm delivery and/
or low delivery weight in women with breast cancer and a control
group of people without cancer; (4) women with breast cancer who
were diagnosed at any time before pregnancy, during pregnancy, or
|
      147
within 1 year following delivery. When overlapping data were avail-
able from multiple publications, the most complete article with the
largest study population was included. Abstracts, case reports, and
reviews were all excluded. For the purpose of the present study,
preterm delivery and low delivery weight were defined as delivery
before 37 complete weeks of pregnancy and delivery weight below
2500 g, respectively.
2.3 | Data extraction
Studies were reviewed independently by two authors (CS and XD) and
the data were extracted using a uniform standardized data collection
form. Discrepancies in the data collection process were resolved by
discussion within the research team. The first author’s name, publica-
tion year, country, study design, number of patients in both breast
cancer and control groups, association estimates, and adjusted con-
founding factors were recorded for each article. The estimate that
reflected the greatest adjustment for potential confounders was
extracted from each study. As preterm delivery and low delivery
weight are relatively rare outcomes, distinctions between estimates
(RR, hazard ratio, or odds ratio) were ignored and were all interpreted
as RRs in the present meta-­analysis.
2.4 | Assessment of study quality
The quality of the studies included was assessed using the
Newcastle–Ottawa Scale,19 a comprehensive and validated tool
for assessing the quality of non-­randomized studies. A maximum of
nine stars were awarded to each study, with stars assigned based
on three broad subscales: the selection process of study groups
(0–4 stars), the comparability of the groups (0–2 stars), and the
elucidation of the exposures and outcomes for participants (0–3
stars). A study awarded at least seven stars was considered a high-­
quality study.
2.5 | Statistical analysis
Pooled RRs and 95% CIs were used to measure the effects of
maternal breast cancer on preterm delivery and/or low delivery
weight. The analyses were then stratified by country, publication
year, and confounding factor adjustments. Statistical heterogene-
ity between studies for each pooled result was assessed using χ2
and I2 statistics.20 Random-­effects models were used to calculate
pooled RRs21 owing to moderate/high heterogeneity being detected
in most of the pooled analyses.22 Potential publication bias was
detected through visual inspection of funnel plot symmetry and
the Begg test and Egger test were applied as further quantitative
analyses.23 Sensitivity analyses were also conducted by removing
each study individually and recalculating the pooled result to assess
whether the overall finding could be markedly affected by a single
study. Statistical analyses were performed with Stata version 9.0
(StataCorp, College station, TX, USA) and two-­sided P<0.05 was
considered statistically significant.
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148       Sun ET AL.

3 |  RESULTS Records identified

from electronic
Additional records
identified from other
databases (n=1452) sources (n=6)
3.1 | Study characteristics
Duplicate records
A total of 1458 articles were identified initially. After removing (n=520)
duplicate records, 938 article titles and abstracts were screened.
Title and abstract
Subsequently, 59 articles were selected for full-­article review. After screening (n=938)
full-­text examination, 52 articles were excluded and seven articles Records excluded
were included in present meta-­analysis6,11,12,14–17 (Fig. 1). The stud- (n=879)

ies included were published between 1992 and 2017 (Table 1); two
were conducted in the USA,6,16 four in Europe,11,12,14,15 and one in
Australia.17 The population sizes of the studies ranged from 146 to
3 168 911.
3.2 | Meta-­analysis of the primary outcomes
3.2.1 | Breast cancer and risk of preterm delivery
In the pooled analysis of data from 6 687 579 pregnant patients,
maternal breast cancer was associated with an increased risk of pre-
term delivery (pooled RR 1.82, 95% CI 1.44–2.30); significant study
heterogeneity was identified (I2 71.8%, P=0.002) (Table 2 and Fig. 2).
The increased risk of preterm delivery associated with breast
cancer was still significant when analyses were restricted to studies
conducted in the USA, Europe, and Australia (Table 2), with an ele-
vated association observed in the single Australian study (RR 3.28,
Full-text article
screening (n=59)
Excluded (n=52)
• Review article (n=2)
• Case report (n=1)
• No target outcome (n=47)
• Overlapping study (n=2)
Included in meta-
analysis (n=7)
F I G U R E   1   Flow of articles included in the meta-­analysis.
95% CI 1.27–8.52).17 The analysis was stratified by publication year;
the risk associated with breast cancer appeared larger among studies
published before 2010 (RR 2.18, 95% CI 1.83–2.60) compared with
studies published after 2010 (RR 1.42, 95% CI 1.04–1.94). When the
studies were grouped by whether they included analyses adjusted for
potential confounders, a lower risk was observed among studies that
did include adjustments (RR 1.62, 95% CI 1.17–2.24) compared with
those that did not (RR 2.16, 95% CI 1.69–2.76) (Table 2).

T A B L E   1   Characteristics of studies included in the meta-­analysis.

RR (95% CI) of outcome among

patients with a history of breast
cancera
No. of patients in Adjusted for
cancer and control Time of Low delivery Quality confounding
Study Country groups diagnosis Study design Preterm delivery weight score variables

Black (2017)6 USA 512 and 1 911 757 Prior to delivery Retrospective 1.67 (1.42–1.97) 1.50 (1.23–1.84) 8 Adjustedb
cohort
Jacob (2017)11 German 165 and 165 Prior to Case–control 2.01 (0.18–22.41) 7 Unadjusted
pregnancy
Mogos Sweden 1032 and 1 570 753 Prior to 30 days Retrospective 1.18 (0.96–1.44) 1.09 (0.85–1.40) 8 Adjustedc
(2013)12 postpartum cohort
Dalberg Swedish 331 and 2 870 518 Prior to Retrospective 2.23 (1.57–3.14) 1.73 (1.10–2.47) 7 Unadjusted
(2006)14 pregnancy cohort
Langagergaard Danish 695 and 33 443 Before and Cohort 1.96 (1.35–2.85) 1.30 (0.49–3.48) 7 Unadjusted
(2006)15 during
pregnancy
Smith (2001)16 USA 423 and 3 168 488 Prior to 12 mo Retrospective 2.20 (1.70–2.80) 2.00 (1.00–4.10) 7 Adjustedd
postpartum cohort
Zemlickis Australia 73 and 73 Prior to 3 mo Retrospective 3.28 (1.27–8.52) 6 Unadjusted
(1992)17 after the last cohort
day of first
treatment
a
Distinctions between risk ratio, hazard ratio, and odds ratio were ignored and were included in the meta-­analysis as risk ratios.
b
Adjusted for maternal age at delivery, education, marital status, parity, race/ethnicity, and smoking.
c
Adjusted for age, race, marital status, education, parity, adequacy of prenatal care, tobacco use, alcohol use, drug abuse, and pregnancy-­related clinical/
medical conditions.
d
Adjusted for age.
Sun ET AL. |
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T A B L E   2   Summary of pooled risk for preterm delivery associated with a history of breast cancer compared with no history of breast cancer.

Association Heterogeneity
No. of
Analysis studies Pooled riska z P value χ2 P value I2, %

All studies 7 1.82 (1.44–2.30) 5.01 <0.001 21.3 0.002 71.8

Location
USA 2 1.88 (1.44–2.46) 4.63 <0.001 3.3 0.070 69.5
Europe 4 1.70 (1.13–2.56) 2.53 0.012 12.4 0.006 75.8
Australia 1 3.28 (1.27–8.52) 2.45 0.014
Publication year
Before 2010 4 2.18 (1.83–2.60) 8.74 <0.001 1.04 0.791 0.0
After 2010 3 1.42 (1.04–1.94) 2.20 0.028 6.89 0.032 71.0
Data adjusted for confounding factors
Yes 3 1.62 (1.17–2.24) 2.93 0.003 15.2 0.001 86.8
No 4 2.16 (1.69–2.76) 6.19 <0.001 1.0 0.793 0.0
a
Values are given as pooled risk ratios (95% confidence interval).

3.2.2 | Breast cancer and risk of low delivery weight
There were five studies including 6 687 103 pregnant women
included in the meta-­analysis of associations between breast cancer
and the risk of low delivery weight. Breast cancer was associated
with an increased risk of low delivery weight (pooled RR 1.41, 95% CI
1.15–1.74) and the study heterogeneity was not significant (I2 37.1%,
P=0.174) (Table 3).
In subgroup analyses stratified by location, breast cancer was
associated with increased risk of low delivery weight in studies
conducted in the USA (RR 1.53, 95% CI 1.26–1.86) but not in studies
conducted in Europe (RR 1.31, 95% CI 0.93–1.85). No association
between breast cancer and risk of low delivery weight was observed
in studies published after 2010 (RR 1.29, 95% CI 0.94–1.76); how-
ever, among studies published before 2010, breast cancer was
associated with an increased risk (RR 1.73, 95% CI 1.24–2.41). An
increased risk of low delivery weight was associated with breast can-
cer among studies that did (RR 1.37, 95% CI 1.03–1.82) and did not
(RR 1.66, 95% CI 1.14–2.41) include adjustments for confounding
factors (Table 3).

Study %

ID RR (95% CI) Weight

Black (2017) 1.67 (1.42, 1.97) 22.26

Jacob (2017) 2.01 (0.18, 22.41) 0.91

Mogos (2013) 1.18 (0.96, 1.44) 21.04

Langagergaard (2006) 1.96 (1.35, 2.85) 15.28

Dalberg (2006) 2.23 (1.57, 3.14) 16.16

Smith (2001) 2.20 (1.70, 2.80) 19.47

Zemlickis (1992) 3.28 (1.27, 8.52) 4.88

Overall (I-squared=71.8%, p=0.002) 1.82 (1.44, 2.30) 100.00

NOTE: Weights are from random effects analysis

.0446 1 22.4

F I G U R E   2   Forest plot of random effect meta-­analysis of the association between maternal breast cancer and risk of preterm delivery.
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150       Sun ET AL.

T A B L E   3   Summary of pooled risk for low delivery weight associated with a history of breast cancer compared with no history of
­breast cancer.

Association Heterogeneity

Analysis No. of studies Pooled riska z P value χ2 P value I2, %

All studies 5 1.41 (1.15–1.74) 3.24 0.001 6.36 0.174 37.1

Location
USA 2 1.53 (1.26–1.86) 4.63 <0.001 0.6 0.442 0.0
Europe 3 1.31 (0.93–1.85) 1.56 0.118 3.6 0.162 45.0
Publication year
Before 2010 3 1.73 (1.24–2.41) 3.25 0.001 0.5 0.783 0.0
After 2010 2 1.29 (0.94–1.76) 1.60 0.110 3.8 0.051 73.7
Data adjusted for confounding factors
Yes 3 1.37 (1.03–1.82) 2.13 0.033 5.1 0.079 60.5
No 2 1.66 (1.14–2.41) 2.66 0.008 0.3 0.597 0.0
a
Values are given as pooled risk ratios (95% confidence interval).

rate of neonatal mortality has been observed in patients with can-

3.3 | Sensitivity analyses
After excluding each study individually, the sensitivity analysis con-
firmed the significant associations between history of breast cancer
and increased risk of preterm delivery and low delivery weight, sug-
gesting high stability in the meta-­analysis results.
3.4 | Bias diagnostics
No evidence of funnel plot asymmetry was observed (Fig. S1), and
no publication bias was detected by quantitative analyses for pre-
term delivery (Begg test z=0.00, P>0.99; Egger test t=1.06, P=0.338)
or low delivery weight (Begg test z=0.24, P=0.806; Egger test
­t=0.53, P=0.634).
4 |  DISCUSSION
The present meta-­analysis evaluated the potential association
between maternal breast cancer and preterm delivery among
6 687 579 patients from seven studies, and between breast cancer
and low delivery weight among 6 687 103 patients from five stud-
ies. The meta-­analysis demonstrated that maternal breast cancer was
associated with an increased risk of preterm delivery (RR 1.82, 95%
CI 1.44–2.30) and low delivery weight (RR 1.41, 95% CI 1.15–1.74).
There are several mechanisms through which maternal breast
cancer could increase the risk of preterm delivery and low delivery
weight. A potential explanation is that metabolic alterations, hor-
mone distribution, febrile illness, and malnutrition related to the
breast cancer disease process could have a damaging impact on the
fetus.7 Other reproductive cancers, such as cervical cancer, ovarian
cancer, and corpus uteri cancer, have also been suggested as poten-
tially associated with subsequent adverse delivery outcomes.24 Long-­
term effects of cancer treatment are another possible explanation for
these findings. A high rate of iatrogenic preterm delivery with a high
cer during pregnancy that underwent treatment.25 Pregnancies
among cancer survivors following chemotherapy and radiotherapy
could have a direct effect on the reproductive tract or could cause
mutations in germ cells.26 During the first trimester of pregnancy,
fetal malformations can be as high as 15%–25% in fetuses with
chemotherapy exposure compared with 2%–3% among fetuses
without.27 The mechanism of teratogenesis could be that most che-
motherapeutic agents target and destroy cells that divide rapidly.28
A previous study29 demonstrated that both preterm delivery and
low delivery weight were more common among women treated with
chemotherapy; this could be explained, in part, by cardiovascular or
pulmonary impairments due to chemotherapy that impact the reg-
ulation of blood volume, adversely affecting pregnancy outcomes.
Psychological stress related to cancer diagnosis could also have
adverse effects on delivery outcomes.29 Some studies have reported
associations between stress during pregnancy and preterm deliv-
ery,30 low delivery weight,31 and congenital anomalies.32
Several subgroup analyses were conducted and statistically sig-
nificant associations were observed across most subgroups. In the
subgroup analysis stratified by location, the association between
breast cancer and preterm delivery risk were significant in studies
conducted in the USA, Europe, and Australia. However, a signifi-
cant association between breast cancer and the risk of low delivery
weight was only observed in studies conducted in the USA, and was
not observed in studies conducted in Europe. The different results
from the two geographic regions could be explained by ethnic dif-
ferences, living environment, or medical conditions. These similar
results suggest that the adjustments to the RRs had little effect on
the associations in this meta-­analysis.
When stratifying by publication year, the association between
breast cancer history and the risks of preterm delivery and low deliv-
ery weight appeared to be slightly stronger in studies published
before 2010 compared with those published after 2010. Notably,
no statistically significant association between breast cancer and the
Sun ET AL.
risk of low delivery weight was observed among studies published
after 2010, whereas a strong association was recorded in studies
published before 2010. The lack of statistical significance could be
due to the small sample size and insufficient statistical power to
detect any difference.
Finally, studies with adjusted estimates should reflect associations
of breast cancer with preterm delivery and low delivery weight more
accurately than those with unadjusted estimates. However, in a sub-
group analysis stratified by adjusting for potential confounders, statis-
tically significant associations between breast cancer and the risks of
preterm delivery and low delivery weight were detected both in stud-
ies adjusted for confounding factors and those not.
The present meta-­analysis had several notable strengths. To
the best of our knowledge, this was the first meta-­analysis exam-
ining associations between maternal breast cancer and the risks of
preterm delivery and low delivery weight. Moreover, results from the
sensitivity analysis demonstrated that no single study exerted a sig-
nificant influence on the pooled results. Additionally, the large over-
all sample size, established through pooling evidence from multiple
studies, enhanced statistical power, generating more precise and reli-
able estimations compared with individual studies. However, several
limitations should be noted. First, preterm delivery and low delivery
weight are outcomes that likely result from various factors,33 but not
all the included studies evaluated potential multiple confounders.
Second, owing to the observational nature of the data, it is possible
that the significant associations observed could be due to unmea-
sured or residual confounding factors. Despite visual inspection of
a funnel plot and the Begg test and Egger test for publication bias
indicating that the results were not affected substantially by bias,
it was still likely that studies with negative results were under pub-
lished and that no eligible study came from low-­ or middle-­income
countries. Third, information on breast cancer stage, the time of
diagnosis, and treatment (i.e., surgery, chemotherapy, or endocrine
therapy) were not available and, consequently, the analysis could not
be stratified by these variables.
In conclusion, the results of the present meta-­analysis of obser-
vational studies provided further evidence that maternal breast
cancer is associated with a significantly increased risk of adverse
delivery outcomes, including preterm delivery and low delivery
weight. Patients surviving breast cancer could be at an increased
risk of preterm delivery and low delivery weight, suggesting that
additional surveillance of pregnancies should be performed in this
population. There is a need to conduct large cohort studies to ana-
lyze the effects of cancer or cancer treatment on delivery outcomes
by stratifying data based on the time of breast cancer diagnosis,
stages, and treatment.
AUT HOR CONTRI BUTI O N S
CS and XD performed the data extraction and contributed to writing
the manuscript. YW performed the literature search and contributed
to writing the manuscript. LY contributed to designing the study, data
analysis, and contributed to writing the manuscript.
|
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CO NFL I C TS O F I NT ER ES T
The authors have no conflicts of interest.
REFERENCES
1. World Cancer Research Fund International. Breast cancer statistics
[Internet]. 2015. http://www.wcrf.org. Accessed April 27, 2017.
2. Parazzini F, Franchi M, Tavani A, et al. Frequency of pregnancy related
cancer: A population based linkage study in Lombardy, Italy. Int J
Gynecol Cancer. 2017;27:613–619.
3. Schover LR. Premature ovarian failure and its consequences:
Vasomotor symptoms, sexuality, and fertility. J Clin Oncol. 2008;26:
753–758.
4. Mathews TJ, Hamilton BE. First births to older women continues to
rise. NCHS Data Brief, No 152. Hyattsville: National Center for Health
Statistics; 2014.
5. Early Breast Cancer Trialists’ Collaborative Group (EBCTCG). Effects
of chemotherapy and hormonal therapy for early breast cancer on
recurrence and 15-­year survival: An overview of the randomised tri-
als. Lancet. 2005;365:1687–1717.
6. Black KZ, Nichols HB, Eng E, et  al. Prevalence of preterm, low
birthweight, and small for gestational age delivery after breast can-
cer diagnosis: A population-­based study. Breast Cancer Res. 2017;
19:11.
7. Langagergaard V. Birth outcome in women with breast cancer, cuta-
neous malignant melanoma, or Hodgkin’s disease: A review. Clin
Epidemiol. 2011;3:7.
8. Bouchlariotou S, Tsikouras P, Benjamin R, et al. Fertility sparing in can-
cer patients. J Soc Minim Invasive Ther. 2012;21:282–292.
9. Hickey M, Peate M, Saunders CM, et  al. Breast cancer in young
women and its impact on reproductive function. Hum Reprod Update.
2009;15:323–339.
10. Kroman N, Jensen M-B, Wohlfahrt J, et  al. Pregnancy after treat-
ment of breast cancer – a population-­based study on behalf of
Danish Breast Cancer Cooperative Group. Acta Oncol Stockh Swed.
2008;47:545–549.
11. Jacob L, Kalder M, Arabin B, Kostev K. Impact of prior breast can-
cer on mode of delivery and pregnancy-­associated disorders: A ret-
rospective analysis of subsequent pregnancy outcomes. J Cancer Res
Clin Oncol. 2017;143:1069–1074.
12. Mogos MF, Salihu HM, Aliyu MH, et al. Association between repro-
ductive cancer and fetal outcomes: A population-­based study. Int J
Gynecol Cancer. 2013;23:218–226.
13. Partridge AH, Gelber S, Peppercorn J, et al. Fertility and menopausal
outcomes in young breast cancer survivors. Clin Breast Cancer.
2008;8:65–69.
14. Dalberg K, Eriksson J, Holmberg L. Birth outcome in women with pre-
viously treated breast cancer—a population-­based cohort study from
Sweden. PLoS Med. 2006;3:e336.
15. Langagergaard V, Gislum M, Skriver MV, et  al. Birth outcome in
women with breast cancer. Br J Cancer. 2006;94:142–146.
16. Smith LH, Dalrymple JL, Leiserowitz GS, et al. Obstetrical deliveries
associated with maternal malignancy in California, 1992 through
1997. Am J Obstet Gynecol. 2001;184:1504–1513.
17. Zemlickis D, Lishner M, Degendorfer P, et  al. Maternal and fetal
outcome after breast cancer in pregnancy. Am J Obstet Gynecol.
1992;166:781–787.
18. Moher D, Liberati A, Tetzlaff J, et  al. Preferred reporting items for
systematic reviews and meta-­analyses: The PRISMA statement. Ann
Intern Med. 2009;151:264–269.
19. Wells GA, Shea B, O’Connell D, et  al. The Newcastle–Ottawa
Scale (NOS) for assessing the quality of non-randomised studies
in  meta-analyses. 2000. http://www.ohri.ca/programs/clinical_epi
demiology/oxford.htm. Accessed April 29, 2017.
 |
152       Sun ET AL.
20. Higgins JP, Thompson SG, Deeks JJ, et al. Measuring inconsistency in
meta-­analyses. BMJ. 2003;327:557–560.
21. DerSimonian R, Laird N. Meta-­analysis in clinical trials. Control Clin
Trials. 1986;7:177–188.
22. Poole C, Greenland S. Random-­effects meta-­analyses are not always
conservative. Am J Epidemiol. 1999;150:469–475.
23. Egger M, Davey SG, Schneider M, et al. Bias in meta-­analysis detected
by a simple, graphical test. BMJ. 1997;315:629–634.
24. Mogos MF, Rahman S, Salihu HM, et al. Association between repro-
ductive cancer and fetal outcomes: A systematic review. Int J Gynecol
Cancer. 2013;23:1171–1177.
25. Lataifeh IM, Barahmeh S, Otay L, et al. Management of cancer during
pregnancy: Obstetric and neonatal outcomes. Int J Gynecol Cancer.
2011;21:1159–1164.
26. Ring AE, Smith IE, Jones A, et  al. Chemotherapy for breast cancer
during pregnancy: An 18-­year experience from fve London teaching
hospitals. J Clin Oncol. 2005;23:4192–4197.
27. Amant F, Deckers S, Van Calsteren K, et  al. Breast cancer in preg-
nancy: Recommendations of an international consensus meeting. Eur
J Cancer. 2010;46:3158–3168.
28. Shlensky V, Hallmeyer S, Juarez L, et al. Management of breast cancer
during pregnancy: Are we compliant with current guidelines? AJP Rep.
2017;7:e39–e43.
29. Anderson C, Engel SM, Mersereau JE, et  al. Birth outcomes
among adolescent and young adult cancer survivors. JAMA Oncol.
2017;3:1078–1084.
30. Su Q, Zhang H, Zhang Y, et al. Maternal stress in gestation: Birth out-
comes and stress-­related hormone response of the neonates. Pediatr
Neonatol. 2015;56:376–381.
31. Loomans EM, Van Dijk AE, Vrijkotte TGM, et  al. Psychosocial stress
during pregnancy is related to adverse birth outcomes: Results from a
large multi-­ethnic community-­based birth cohort. Eur J Public Health.
2013;23:485–491.
32. Hansen D, Lou HC, Olsen J. Serious life events and congenital mal-
formations: A national study with complete follow-­up. Lancet.
2000;356:875–880.
33. Weck RL, Paulose T, Flaws JA. Impact of environmental fac-
tors and poverty on pregnancy outcomes. Clin Obstet Gynecol.
2008;51:349–359.
S U P P O RT I NG I NFO R M AT I O N
Additional Supporting Information may be found online in the
­supporting information tab for this article.
Figure S1. Funnel plot of the random effect meta-­analysis of the
­association between maternal breast cancer and the risks of preterm
delivery (A) and low delivery weight (B).