Pregnancy rate, maternal and neonatal outcomes among breast cancer survivors: A systematic review

Marzieh Azizi; Elham Ebrahimi; Zahra Behboodi Moghadam; Zohreh Shahhosseini; Maryam Modarres

doi:10.1002/nop2.1941

. 2023 Aug 1;10(10):6690–6707. doi: 10.1002/nop2.1941

Pregnancy rate, maternal and neonatal outcomes among breast cancer survivors: A systematic review

Marzieh Azizi ¹, Elham Ebrahimi ¹, Zahra Behboodi Moghadam ¹, Zohreh Shahhosseini ², Maryam Modarres ^3,^✉

PMCID: PMC10495738 PMID: 37528519

Abstract

Aim

This study investigated the pregnancy rate, maternal and neonatal outcomes, and breast cancer (BC) recurrence status after pregnancy among BC survivors.

Design

A systematic review.

Methods

Electronic databases such as PubMed, Web of Science [WOS], Scopus, ScienceDirect, Google Scholar, and Scientific Information Database were systematically searched. The quality of included studies was evaluated using the Newcastle–Ottawa Scale (NOS). Observational studies reported the pregnancy rate, maternal and neonatal outcomes among reproductive‐aged BC survivors, and the recurrence status of BC after pregnancy were eligible to include in this study.

Results

Of the 29 included studies, 13 studies were prospective cohorts or prospective multicenter or population‐based cohorts, 14 studies were retrospective cohort or retrospective population‐based cohort studies, and two studies were cross‐sectional retrospective surveys or population‐based descriptive studies. This systematic review showed that the pregnancy rate was estimated at 3.1%–48.5% among BC survivors who attempted to conceive. The most prevalent maternal outcomes of pregnancy were miscarriage (1.8%–33.3%) and induced abortion (5.0%–44%) as well as preterm birth (PTB) or very PTB (1.2%–21.1%), and twin birth (1.1%–38.8%) were the most prevalent neonatal outcomes occurring among BC survivors, respectively. In addition, most of the included studies indicated that pregnancy had no adverse effect on the status of BC recurrence among survivors. Surviving women can be encouraged and receive a carefully multidisciplinary approach regarding healthy pregnancy.

No Patient or Public Contribution.

Keywords: breast cancer, pregnancy outcome, prevalence, survivors

1. INTRODUCTION

Breast cancer (BC) is the most prevalent cancer among women worldwide (Assi et al., 2020; McCray et al., 2016). Annually, more than 11,000 women aged <40 years are diagnosed with BC in the United States (Poorvu et al., 2021). Among the Iranian population, the prevalence of BC is reported to be 20 per 10,000 women (Montazeri et al., 2003). Compared with different countries, 10% of women in developed countries and 25% of women in developing countries were affected by BC before age 40 (Assi et al., 2013; Azim Jr et al., 2011).

In recent decades, the increasing trend of postponing pregnancy to the end years of the reproductive period and the growing number of young women diagnosed with BC led to some reproductive‐aged women with BC intending to experience pregnancy after completing BC treatment (Pagani et al., 2015; Ruggeri et al., 2019).

Literature review showed that women with a diagnosis of BC are often advised to delay their attempt to conceive at least 2 years after treatment as, in the first few years after diagnosis, the risk of recurrence is the highest (Ives et al., 2007; Poorvu et al., 2021).

Breast cancer diagnosis and its treatment, such as adjuvant chemotherapy and hormone therapy, may have long‐term effects on women's reproductive health (Black et al., 2017), including the impairment of their ovarian function (Assi et al., 2020; McCray et al., 2016). Also, due to the higher risk of congenital malformations and spontaneous abortion during chemotherapy and radiotherapy, pregnancy is strictly discouraged during the treatment process (Kopeika et al., 2019). Various techniques were developed to preserve the fertility of patients with BC, used before the initiation of cancer therapy, including embryo or oocyte cryopreservation (Assi et al., 2020; Mahajan, 2015).

Despite the high rates of survivors of BC who tend to achieve pregnancy after completing cancer treatment, they had a lower pregnancy than the general population (Stensheim et al., 2011). The lower pregnancy rate among patients with BC may be attributed to several factors, such as constant or transient amenorrhoea associated with the complete discharge of germ cells, menstrual irregularity, and transient fertility due to the consumption of gonadotoxic chemotherapeutic agents (Kopeika et al., 2019). According to a Danish population‐based cohort study, the pregnancy rate among BC survivors was threefold lower than among women without a history of BC (Kroman et al., 2008). The studies showed that the total pregnancy rate among BC cancer survivors differed from 3.6% to 16% (Blakely et al., 2004; Kroman et al., 2008; Lambertini, Kroman, et al., 2020; Velentgas et al., 1999).

1.1. Background

Studies conducted among BC survivors regarding the pregnancy complications, such as maternal and neonatal outcomes, showed contradicting results. Although some studies did not report higher maternal (Black et al., 2017; Mueller et al., 2003) and neonatal (Assi et al., 2020; Leproux et al., 2021) complications among BC survivors, in some population‐based cohort studies, an increased risk of adverse delivery complications such as caesarean section, low birth weight (LBW), very preterm birth (PTB), and neonate small for gestational age (SGA) was reported compared with the healthy women (Black et al., 2017; Mogos et al., 2013). Reproductive‐aged BC survivors are considered a high‐risk population, and their pregnancy health should be noticed by healthcare providers, especially midwives, and gynaecologists (Bien et al., 2014). One of the aspects of midwifery practice is antenatal care, including providing high‐quality and sustainable healthcare services to high‐risk pregnant women, and healthcare providers should have comprehensive information regarding the pregnancy outcomes in particular diseases such as cancer (Beldon & Crozier, 2005). Overall, studies regarding the pregnancy outcomes of BC survivors are limited with contradictory results (Kroman et al., 2008; Labrosse et al., 2021; Lee et al., 2020); thus, the results of this systematic review can serve as a guide for midwives to understand the pregnancy outcomes to effectively manage these cases during pregnancy. Literature review showed that although some review studies assessed BC during pregnancy (Monteiro et al., 2013) or outcomes of pregnancy during or after the BC diagnosis (Gerstl et al., 2018; Raphael et al., 2015), no systematic review has yet investigated both the pregnancy rate and outcomes of pregnancy among BC survivors.

The research questions guiding this review were as follows: What is the prevalence of pregnancy among BC survivors? What are the neonatal and maternal outcomes of pregnancy in BC survivors? And is pregnancy an effect on the recurrence of cancer among BC survivors? So, the present study aimed to systematically investigate the pregnancy rate and maternal and neonatal outcomes among BC survivors. In addition, BC recurrence status after the pregnancy was assessed in this systematic review.

2. METHODS

2.1. Design

This systematic review followed the Preferred Reporting Items for Systematic Reviews and Meta‐Analyses (PRISMA) guidelines (Page et al., 2021; For more information, see: http://www.prisma‐statement.org/).

Before data extraction, the study was registered in the International Prospective Register of Systematic Reviews (PROSPERO; Registration no. CRD42022309051; available from https://www.crd.york.ac.uk/prospero/).

2.2. Literature search and search strategy

Electronic scientific databases were systematically searched, including PubMed, Web of Science (WOS), Scopus, ScienceDirect, Google Scholar, and the Iranian database, including the Scientific Information Database. The latest search was performed from “December 2021 to March 2022”. To ensure that all possible studies regarding the pregnancy rate and outcomes following BC survival were retrieved, no publication year restriction was considered for selecting articles.

The search was typically performed using Persian and English keywords. To search in PubMed databases, at first, the search terms were extracted using Medical Subject headings included ((pregnancy [MeSH Terms]) OR (pregnancies [MeSH Terms])) OR (spontaneous pregnancy [MeSH Terms])) OR (unplanned pregnancy [MeSH Terms])) OR (unwanted pregnancy [MeSH Terms])) OR (conception [MeSH Terms])) OR (conceiving[MeSH Terms]))) AND (prevalence[Title])) OR (rate[Title])) OR (incidence[Title])) AND (pregnancy outcomes [MeSH Terms])) OR (pregnancy complications[MeSH Terms])) OR (adverse birth outcomes[MeSH Terms])) AND (breast cancer [MeSH Terms])) OR (breast neoplasms[MeSH Terms])) OR (inflammatory breast carcinoma [MeSH Terms])) OR (malignant neoplasm of breast [MeSH Terms])) AND (survivors[MeSH Terms])) OR (adult survivors [MeSH Terms]). The related text words were used to search in other databases by following each database's guidelines for advanced search. The search strategy in databases is shown in Table 1. Also, the reference lists of included studies were searched manually to ensure that all additional published articles were retrieved. To collect the references and exclude the duplicate records, the reference manager software EndNote X7 was applied.

TABLE 1.

Search strategy in databases.

Last search date	The latest search was performed from “December 2021 to march 2022”
Database	Search strategy	Number of articles retrieved	Search filters
PubMed	(pregnancy[TIAB]) OR (spontaneous pregnancy [TIAB] OR (unplanned pregnancy [TIAB]) OR (unwanted pregnancy [TIAB]) OR (conception [TIAB]) OR (conceiving [TIAB]) OR (fertilityTIAB]) OR (pregnancy rate[TIAB]) OR (live‐birth[TIAB])) OR (pregnancy outcome[TIAB])) OR (pregnancy complication[TIAB]) OR (adverse birth outcome[TIAB]) AND (breast cancer[TIAB]) OR (cancer of breast[TIAB]) OR (breast neoplasm[TIAB]) OR (breast tumour[TIAB]) OR (breast carcinoma[TIAB]) OR (mammary cancer[TIAB]) OR (breast malignant tumour[TIAB]) OR (cancer survivors[TIAB]) OR (cancer survivorship[TIAB]) OR (long‐term cancer survivors[TIAB]) OR (adult survivors [TIAB])	316	Species: Human Article Language: English, Persian Article type: Observational studies
Scopus	TITLE‐ABS‐KEY (pregnan* OR pregnant womn OR spontaneous pregnancy OR pregnancy rate OR live‐birth OR pregnancy outcome* OR pregnancy complication* OR adverse birth outcome* OR fertility) AND (breast cancer OR breast neoplasm* OR breast tumour OR breast carcinoma* OR cancer surviv* OR cancer survivorship)	253	Subject areas: Medicine Document types: Article Source type: Journal
WOS	TS = (pregnan* OR pregnant womn OR spontaneous pregnancy OR pregnancy rate OR live‐birth OR pregnancy outcome* OR pregnancy complication* OR adverse birth outcome* OR fertility) AND (breast cancer OR breast neoplasm* OR breast tumour OR breast carcinoma* OR mammary cancer OR breast malignant tumour OR cancer surviv* OR cancer survivorship)	219	Document types: Article
ScienceDirect	pregnancy OR pregnancy rate OR pregnancy outcomes OR pregnancy complications AND breast cancer survivors	112	Article type: Research article Publication title: Midwifery Subject areas: Nursing and health profession Access type: Open access & Open archive
Google Scholar	“pregnancy rate” OR “pregnancy outcomes” OR “pregnancy complications” AND “breast cancer survivors” NOT “breast cancer patients”	906	Year of publication: Any time Sort by relevance Keywords anywhere in the article
SID	pregnancy rate OR pregnancy outcomes OR pregnancy complications AND breast cancer	11	No search filters were applied

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2.3. Inclusion and exclusion criteria

The inclusion criteria were as follows:

Observational studies such as cross‐sectional, retrospective case–control, and retrospective or prospective cohort or longitudinal studies published in valid scientific journals.
Observational studies reported the pregnancy rate or incidence of pregnancy among reproductive‐aged BC survivors.
Observational studies with available information regarding the maternal and neonatal outcomes among reproductive‐aged BC survivors.
Observational studies assessed the recurrence status of BC after pregnancy among reproductive‐aged BC survivors.

Articles were excluded if there were:

case reports, case series, letters, reviews, and randomized controlled trials (RCTs) studies regarding pregnancy after BC;
conference papers;
studies reporting the pregnancy during the diagnosis or treatment of BC;
studies reporting on pregnancy‐associated BC;
studies reporting the pregnancy rate in each cancer survivor except BC.

2.3.1. Study selection

At first, all references were downloaded into EndNote X7, and two main authors (MA & MM) independently screened the titles of retrieved articles. Then, the abstracts were reviewed by two independent reviewers according to the eligibility criteria. Notably, discrepancies were resolved through consensus during the search and screening stages. Screening criteria were piloted and modified as required.

To select the eligible articles, the PICO was designed as follows:

Participants (P): Reproductive‐aged BC survivors who complete cancer treatment such as chemotherapy, radiotherapy, surgery, etc.

Intervention (I): Not applicable.

Comparison (C): Reproductive‐aged BC survivors without attempting to become pregnant.

Outcome (O): pregnancy rate, maternal and neonatal outcomes, and the effect of pregnancy on the recurrence of cancer among reproductive‐aged BC survivors.

2.4. Outcome measure

In this study, the primary outcome was a systematic assessment of the pregnancy rate in BC survivors based on the published relevant articles. BC survivors were defined as those who were ≥2 years from the initial diagnosis of BC and had completed treatment. Pregnancy in BC survivors was defined as the experience of pregnancy after completing the BC treatment after the physician's permission for conceiving.

The secondary outcome was reporting BC survivors' maternal and neonatal pregnancy outcomes. Neonatal outcomes refer to LBW, PTB, SGA, and severe neonatal conditions such as congenital malformations in pregnancy. Also, the maternal outcomes were defined as pregnancy complications (e.g., physical symptoms) and mortality among BC survivors compared to healthy pregnant women with no history of BC. In addition, the tertiary outcome measured was to investigate the possibility of BC recurrence after pregnancy after BC treatment.

2.5. Data extraction and analysis

A data extraction sheet using Microsoft Excel software was developed to extract relevant information needed for further analysis. The extracted data included the first author, publication year, country, study design, participants in each group, mean ± standard deviation (SD) of participants' age (years), mean ± SD or median (range) time between BC treatment to pregnancy (months or years), a primary and secondary outcome, pregnancy rate (%), number (%) of live birth in BC survivors, fetal or neonatal outcomes in BC survivors, maternal outcomes in BC survivors and BC recurrence after pregnancy (Table 2).

TABLE 2.

Characteristics of the included studies.

First author, publication year, country	Study design	Number of participants in each group	Mean ± SD or n (%) of participants' age (years) in each group	Mean ± SD or median (range) time between treatment to pregnancy (years)	Primary and secondary outcome	Pregnancy rate (%)	Number (%) of live birth in BC survivors	Fetal or neonatal outcomes in BC survivors	Maternal outcomes in BC survivors	BC recurrence after pregnancy
Kaidar‐Person, O. (2022), Israel	Population‐based cohort	2,103,216 Attempt to conceive = 617 Control = 2,102,599	Attempt to conceive = 34.0 ± 0.0 Control = 28.0 ± 0.0	Not reported	Obstetrical outcomes among BC survivors	Not reported	Not reported	PTB = 62 (10.0) FD = 164 (26.6) Haemorrhage = 23 (3.7) IUGR = 25 (4.0)	Eclampsia = 62 (10.0) Maternal infection = 63 (10.2)	Not reported
Mangiardi‐Veltin, M. (2022), France	Prospective, multicenter cohort	517 Attempt to conceive = 127 Control = 450	18–43 38.0 ± 0.0 <30 = 7.4 30–35 = 25.5 35–40 = 41.6 ≥40 = 25.5	35.8 ± 32.4	Fertility preservation procedures in BC survivors	133 (25.7) Spontaneous = 113 (87.6) Medical interventional = 16 (12.4)	68 (51.1)	PTB = 2 (1.6) CMV seroconversion = 1 (0.8) Twin birth = 2 (1.6)	Pre‐eclampsia = 2 (1.6) Post‐partum peritonitis = 1 (0.8) GDM = 3 (2.4) Ectopic pregnancy = 6 (4.5) Elective abortion = 6 (4.5) Medical abortion = 1 (0.8) Miscarriage = 31 (23.3)	Not reported
Abel, M.K. (2021), USA	Prospective cohort	157 Attempt to conceive = 46 Not attempt = 111	18–45 Attempt to conceive = 33.0 ± 4.4 Not attempt = 35.0 ± 5.0	Mean = 3.2 ± 2.1	Pregnancy attempts and outcomes in BC survivors	30 (22.5)	20 (66.6)	IUGR = 1 (2.0) Termination due to fetal abnormality = 1 (2.0)	GDM = 1 (2.0) Gestational HTN = 1 (2.0) Miscarriage = 8 (26.6)	BC recurrence has occurred in only one of the 46 patients who attempted conception
Leproux, C. (2021), France	Retrospective cohort	61 Attempt to conceive = 31 Control = 30	18–40 32.6 ± 4.35	36.4 months (4.1–51.3)	The rate of live births. overall survival, disease‐free survival, spontaneous or APR	18 (29.5)	10 (55.6)	None	Medical termination = 2 (11.0) Miscarriage = 3 (16.0)	No recurrence or death in women with pregnancy was reported
Labrosse, J. (2021), France	Retrospective cohort	133	18–43 36.8 (range 26.4–48.1 years)	4.3 months	Pregnancy after BC and the subsequent obstetrical and neonatal outcomes	197 One pregnancy = 89 two pregnancies = 29 three pregnancies = 12 four pregnancies = 1 five pregnancies = 2	131 (64.0)	PTB = 2 (7.7) IUGR = 2 (7.7) Hemorragia = 1 (3.8) Hydramnios = 1 (3.8) Macrosomia = 1 (3.8) Multiple birth = 6 (4.6)	GDM = 10 (38.5) Preeclampsia = 5 (19.2) HTN = 2 (7.7) Induced abortion = 11 (9.0) EP = 3 (2.0) Metastatic Recurrence = 1 (3.8) Placenta previa = 1 (3.8) Miscarriage = 42 (21.0)	Only one patient showed metastatic recurrence after BC
Assi, H. (2020), Lebanon	Retrospective cohort	39 Attempt to conceive = 4 Control = 35	31–40 years Attempt to conceive = 28.33 ± 3.0 Control = 36.6 ± 5.2	3.83 ± 0.0	Completion of pregnancy and child delivery and fertility discussion	6 (15.3)	2 (33.3)	None	Miscarriage = 2 (33.3) Ongoing pregnancies = 2 (33.3)	None of them experienced BC recurrence
Lambertini, M. (2020), Italy	Multicenter, hospital‐based, retrospective cohort	704 Subsequent pregnancy = 176 Control = 528	<45 subsequent pregnancy ≤30 = 102 (52.3) 31–35 = 67 (34.4) 36–40 = 26 (13.3) Control ≤30 = 170 (16.1) 31–35 = 365 (34.5) 36–40 = 522 (49.4)	4.3 years (3.0–6.1)	Pregnancy rate and disease‐free survival between patients with and without a pregnancy after BC	146 (20.7) Spontaneous pregnancy = 124 (85.0) Use ART = 22 (15.0)	137 (94.0) One live birth = 118 (86.1) Twin birth = 19 (13.9)	Congenital abnormalities = 2 (2.0)	Delivery complications = 11 (10.9) Induced abortion = 14 (8.0) Miscarriage = 18 (10.2)	Pregnancy in women with a history of BC is safe and does not increase the risk of recurrence
Lee, M.H. (2020), Korea	Prospective cohort	31,761 Subsequent pregnancy = 992 Control = 30,769	≤45 Subsequent pregnancy = 31.8 ± 4.5 Control = 39.6 ± 4.5	1176.4 ± 868.6 days	The risks of recurrence and mortality from BC depending on pregnancy	992 (3.1)	622 (67.5)	None	Miscarriage = 195 (19.6) Termination = 120 (12.0) Miscarriage + termination = 55 (5.5)	Women who became pregnant did not have a different risk of recurrence
Poorvu, Ph. (2020), USA	Multicenter prospective cohort	1026 Attempt to pregnancy = 130 Not attempt Control = 896	17–40 ≤30 = 94 (9.1) 31–35 = 245 (23.9) 36–40 = 687 (67.0)	5.0 years (0.5–5.9)	Evaluating postdiagnosis pregnancies	152 (10.0) One pregnancy = 70 Two pregnancies = 34 Three pregnancies = 3 Five pregnancies = 1	91 (59.8)	Stillbirth = 1 (0.6) Twin birth = 6 (3.0)	Termination = 11 (7.2) Miscarriages = 49 (32.2)	Not reported
Kopeika, J. (2019), UK	Retrospective cohort	163 Attempt to conceive = 27 Control = 111 Did not answer = 25	25–42	6.00 years (range 1–21)	Intentions to conceive and pregnancy outcome in BC survivors	26 (16.0)	16 (61.5)	None	Miscarriage = 6 (23.0)	Not reported
Dieci, M. (2019), Italy	Retrospective cohort	590 Attempt to conceive = 26 Control = 564	≤40 First cohort ≤35: 19 (38.0) >35: 31 (62.0)	64 months (19–108)	BC outcome and pregnancy the outcome of consecutive patients who became pregnant after BC	26 (4.4)	8 (30.7)	None	Miscarriage = 8 (30.7)	Pregnancy does not increase the risk of BC relapse
Black, K. (2017), USA	Population‐based retrospective cohort	2,325,229	18–50 Attempt to conceive = 31.8 ± 4.7 Control = 27.1 ± 5.7	3.3 ± 2.8 years	Association between BC history and birth outcomes	Not reported	Attempt to conceive = 512 (2.2) Control = 1,911,757 (82.2)	PTB = 108 (21.1) LBW = 76 (14.8) SGA = 68 (13.3)	None	Not reported
Jacob, L. (2017), Germany	Retrospective cohort	330 Attempt to conceive = 165 Control = 165	18–45 years Attempt to conceive = 34.6 ± 5.2 Control = 34.6 ± 5.2	Not reported	The impact of prior BC on the delivery of a live‐born child in a subsequent pregnancy, pregnancy complications	Not reported	136 (82.3)	PTB = 2 (1.2)	Early and late pregnancy loss = 29 (17.7) Miscarriage = 3 (1.8) Medical abortion = 10 (6.1)	Not reported
Oktay, K. (2015), USA	Prospective cohort	131 Attempt to conceive = 33 Control = 98	≤45 Attempt to conceive = 36.2 ± 4.2 Control = 35.4 ± 4.1	Not reported	The pregnancy and FP outcomes when embryos generated with the same protocol	20 (15.2)	18 (90.0)	Twin birth = 7 (38.8)	Miscarriage = 3 (15.0)	No significant increase in short‐term recurrence risk
Dillon, K. E. (2013), USA	Prospective Cohort	182 Attempt to conceive = 84 Control = 98	15–39 Attempt to conceive = 30.1 (26.8–31.7) Control = 28.9 (26.7–29.9)	3.7 months (0–12)	Pregnancy rates in young female cancer survivors and similar‐aged controls	27 (39.0)	19 (70.0)	None	Induced abortion = 3 (11.0) Ectopic pregnancy = 1 (3.0) Miscarriage = 4 (15.0)	Not reported
Córdoba, O. (2012), Spain	Retrospective cohort	115 Attempt to conceive = 18 Control = 97	Attempt to conceive = 31.5 (26–35) Control = 33 (20–35)	44.5 months (10–84)	Prognosis of BC among patients who became pregnant after treatment and those who did not	18 (15.6)	10 (55.5)	None	Termination of the pregnancy = 8 (44.4)	Pregnancy after BC not only did not adversely affect the prognosis of the neoplasm but also may have a protective effect
Kranick, J. (2010), USA	Retrospective cohort	451 Subsequent pregnancies = 107 Control = 344	≤45 Subsequent pregnancies = 32.0 ± 4.0 Control = 34.1 ± 3.9	≤1 year = 46 (43.0) >2 years = 24 (22.4) 2–4 years =21 (19.6) ≥4 years = 16 (15.0)	Compare prognosis among BC patients with and without a subsequent pregnancy	107 (23.7)	57 (53.2)	None	Induced abortion = 38 (35.5) Miscarriage = 11 (10.3) Ectopic pregnancy = 1 (0.9)	Having a subsequent pregnancy did not influence the risk of recurrence or death from BC
Rippy, E. (2009), UK	Retrospective Cohort	262 Attempt to conceive = 24 Control = 237	≤45	60 months	The effect of BC, its treatment, and counselling on future pregnancy and fertility	18 (6.8)	17 (94.4)	Twin birth = 4 (16.0)	Induced abortion = 1 (5.0)	None of the patients have so far had a recurrence or died.
Partridge, A. H. (2008), USA	Cross‐sectional retrospective	440 Attempt to conceive = 307 Control = 133	32.6 ± 0.0 ≤30 = 118 (27.0) 31–35 = 184 (42.0) 36–40 = 138 (31.0)	Not reported	Fertility outcomes in young BC survivors	87 (19.7)	52 (59.7) ≥1 Live Birth = 40 (9.0) >1 Live Birth = 12 (3.0)	None	Spontaneous abortion = 10 (2.0) Therapeutic Abortion = 12 (3.0)	No evidence of recurrent disease was observed
Kroman, N. (2008), Denmark	Population‐based cohort	10,236 Subsequent pregnancy = 371 Control = 9865	Subsequent pregnancy <35 = 225 (58.0) 35–39 = 113 (32.0) 40–45 = 33 (10.0) Non‐pregnancy <35 = 1065 (11.0) 35–39 = 2487 (25.0) 40–45 = 6313 (64.0)	39 months (10–228)	The effect of pregnancy on the prognosis of BC	465 (4.5) More than one pregnancy = 74	236 (50.7)	None	Miscarriage = 36 (8.0) Induced abortions = 193 (41.5)	Pregnancy after treatment of BC has no negative influence on the prognosis
Ives, A. (2006), Australia	Population‐based descriptive	2539 Subsequent pregnancies = 123 Control = 2416	<45 years Subsequent pregnancies 25–34 = 54.6 35–44 = 43.9 ≥45:1.5 Control 25–34 = 84.2 35–44 = 15.7 ≥45 = 0.1	0–2 years: 62 (50.4) >2 years: 61 (49.6)	The rate of pregnancy and the first subsequent pregnancy	123 (4.8)	66 (53.6)	None	Termination 42 (34.0) Miscarriage = 15 (12.0)	No disease recurrence was seen among women
Dalberg, K. (2006), Sweden	Population‐based Prospective cohort	2,870,849 Subsequent pregnancies = 331 Control = 2,870,518	Subsequent pregnancies ≤19 years = 1 (1.0) 20–29 years = 51 (15.0) 30–34 years = 104 (31.0) ≥35 years = 175 (53.0) Control: ≤19 years = 107,766 (4.0) 20–29 years = 1,731,074 (60.0) 30–34 years = 718,985 (25.0) ≥35 years = 311,700 (11.0)	37 months (7–163)	Birth outcome in women with previously treated BC	Not reported	327 (0.1)	Very PTB = 36 (11.0) Birth Trauma = 6 (2.0) Congenital abnormalities = 24 (7.0) Stillbirth = 2 (1.0)	Instrumental delivery = 33 (10.0) Pregnancy bleeding = 4 (1.0) delivery complications = 171 (52.0)	There is no evidence that pregnancy can trigger a relapse
Blakely, L. (2003), USA	Prospective cohort	370 Subsequent pregnancies = 47 control = 323	<35 years Subsequent pregnancies ≤30 = 27 (57.0) >30 = 20 (43.0) Control ≤30 = 103 (32.0) >30 = 220 (68.0)	123 months	The effect of pregnancy on the subsequent risk of recurrence after treatment for BC	47 (12.7)	32 (68.0)	PTB = 1 (2.0)	Miscarriage = 10 (21.0) Miscarriage = 4 (8.5)	Pregnancy was not associated with an increased risk of disease recurrence
Mueller, B. A. (2003), USA	Retrospective population‐based cohort	3213 Subsequent pregnancies = 438 control = 2775	<45 Subsequent pregnancies = 31.1 ± 4.7 Control = 32.3 ± 4.0	≤10 ≤ months	Childbearing and Survival after BC in young women	Not reported	438 (13.6)	None	None	Subsequent childbearing is unlikely to increase their risk of mortality.
Gelber, Sh. (2001), USA	Retrospective cohort	282 Subsequent pregnancies = 94 Control = 188	Subsequent pregnancies = 31.2 ± 0.00 Control = 36.6 ± 0.00	33.0 ± 21.1	The effect of subsequent pregnancy on the prognosis of patients	137 (48.5) one pregnancy = 67 (49.0) Twin pregnancies = 17 (25.0) Three pregnancies = 7 (15.0) Four pregnancies = 2 (6.0) Seven pregnancies = 1 (5.0)	89 (64.9)	Stillbirth = 1 (1.0)	Therapeutic abortions = 33 (24.0) Miscarriage = 12 (9.0)	Subsequent pregnancy does not adversely affect the prognosis or recurrence of BC
Velentgas, P. (1999), USA	A population‐based prospective cohort	318 Subsequent pregnancies = 53 Control = 265	<45 Subsequent pregnancies <26 = 3 (35.7) 26–30 = 18 (34.0) 31–35 = 23 (43.4) 36–40 = 9 (17.0) Control <26 = 4 (31.5) 26–30 = 12 (34.5) 31–35 = 82 (30.9) 36–40 = 167 (63.0)	97 months (22–179)	The effect of pregnancy on the outcome and mortality of BC survivors	87 (28.0)	59 (68.8)	Multiple birth = 1 (1.1)	EP = 2 (2.3) Induced abortion = 15 (17.2) Miscarriage = 15 (17.2)	Pregnancy after a diagnosis of BC has no adverse effect on recurrence and survival
Kroman, N. (1997), Denmark	Population‐based retrospective cohort	5725 Subsequent pregnancies = 173 control = 5552	<45 Subsequent pregnancies <35 = 103 (59.5) 35–39 = 49 (28.0) 40–45 = 21 (29.0) Control <35 = 603 (11.0) 35–39 = 1436 (26.0) 40–45 = 3513 (63.0)	32 months (11–147)	The RR of death among women who became pregnant after BC treatment compared with the control group	211 (3.7)	97 (46.0)	None	Miscarriage = 22 (10.0) Induced abortion = 92 (44.0)	No evidence that a pregnancy after BC treatment increased the risk of a recurrence outcome
Sankila, R. (1994), Finland	Retrospective population‐based cohort	562 Subsequent pregnancies = 91 Control = 471	<40 Subsequent pregnancies = 31.8 (20–39) Control = 31.5 (22–39)	≥10 months	Survival of BC patients after subsequent term pregnancy	91 (3.6)	NS	None	None	The survival rate was significantly higher among BC survivors who gave birth compared to a control group
Sutton, R. (1990), USA	Prospective cohort	227 Subsequent pregnancies = 25 Control = 202	31 years (17–35)	12 months (0–87)	The frequency of pregnancy and its effect on the clinical course of the BC	33 (14.5)	19 (57.5)	None	Pregnancy termination = 10 (30.3) Miscarriage = 2 (6.0)	Subsequent pregnancy did not affect on recurrence or overall survival of the patients

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Abbreviations: APR, assisted pregnancy rate; BC, breast cancer; EP, ectopic pregnancy; FD, fetal distress; GDM, gestational diabetes mellitus; HTN, hypertension; IUGR, intrauterine growth restriction; LBW, low birth weight; PTB, preterm birth; RR, risk ratio; SD, standard deviation; SGA, small for gestational age.

The authors independently extracted data into a data extraction sheet and validated the main results. If there was any discrepancy in the data extraction process, a consensus was reached through discussion after repeating the same process.

The analysis of the findings was presented as a narrative according to the Cochrane Collaboration (Deeks et al., 2019). A summary with a discussion regarding the study characteristics and findings was performed. Descriptive statistics represent the characteristics of the included studies' results.

2.6. Methodological quality assessment

The Newcastle–Ottawa Scale (NOS) for cohort (Table 3) and cross‐sectional studies (Table 4) were used to evaluate the methodological quality of the included studies (Margulis et al., 2014; Stang, 2010). In the NOS scale for cohort studies, three quality parameters, including selection, comparability, and outcome, were assessed by designing nine specific items, and the scoring of this tool for cohort studies is as follows: Studies with 3 or 4 stars in the selection domain, 1 or 2 stars in the comparability and 2 or 3 stars in outcome domain have good quality. Also, if studies acquire two stars in the selection domain, one or two stars in the comparability domain, and two or three stars in the outcome domain, have considered acceptable quality and poor quality is recognized for studies with 0 or 1 stars in the selection domain, 0 stars in the comparability domain and 0 or one stars in the outcome domain = (Luchini et al., 2017; Wells et al., 2016).

TABLE 3.

Methodological quality assessment through NEWCASTLE – OTTAWA scale (for cohort studies).

Row	First author/year	Selection				Comparability	Outcome			Scoring
Row	First author/year	Representativeness of the sample	Selection of the non‐exposed cohort	Ascertainment of exposure	Demonstration that outcome of interest was not present at the start of the study	The subjects in different outcome groups are comparable based on the study design or analysis. Confounding factors are controlled	Assessment of the outcome	Was follow‐up long enough for outcomes to occur	Adequacy of follow‐up of cohorts	Scoring
1	Kaidar‐Person, O. (2022)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	b	d	Good
2	Mangiardi‐Veltin, M. (2022)	b (^*)	a (^*)	c	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
3	Abel, M.K. (2021)	b (^*)	a (^*)	b (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
4	Labrosse, J. (2021)	b (^*)	b	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	Good
5	Leproux, C. (2021)	b (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
6	Assi, H. (2020)	b (^*)	a (^*)	a (^*)	a (^*)	a (^*)	c	a (^*)	b (^*)	Good
7	Lambertini, M. (2020)	a (^*)	a (^*)	c	a (^*)	a (^*)	c	a (^*)	a (^*)	Good
8	Lee, M.H. (2020)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
9	Poorvu, Ph. (2020)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
10	Kopeika, J. (2019)	b (^*)	a (^*)	c	a (^*)	c	c	a (^*)	a (^*)	Fair
11	Dieci, M. (2019)	b (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
12	Black, K. (2017)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
13	Jacob, L. (2017)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
14	Oktay, K. (2015)	b (^*)	c	c	a (^*)	c	c	a (^*)	a (^*)	Fair
15	Dillon, K. E. (2013)	b (^*)	a (^*)	b (^*)	a (^*)	a (^*)	c	a (^*)	a (^*)	Good
16	Córdoba, O. (2012)	b (^*)	a (^*)	a (^*)	a (^*)	c	b (^*)	a (^*)	a (^*)	Good
17	Kranick, J. (2010)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
18	Rippy, E. (2009)	b (^*)	a (^*)	a (^*)	a (^*)	c	c	a (^*)	a (^*)	Fair
19	Kroman, N. (2008)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
20	Dalberg, K. (2006)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
21	Blakely, L. (2003)	b (^*)	a (^*)	c	a (^*)	a (^*)	c	a (^*)	a (^*)	Good
22	Mueller, B. A. (2003)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
23	Gelber, Sh (2001)	b (^*)	a (^*)	a (^*)	a (^*)	a (^*)	c	a (^*)	a (^*)	Good
24	Velentgas, P. (1999)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
25	Kroman, N. (1997)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
26	Sankila, R. (1994)	a (^*)	a (^*)	a (^*)	a (^*)	a (^*)	b (^*)	a (^*)	a (^*)	Good
27	Sutton, R. (1990)	a (^*)	a (^*)	a (^*)	a (^*)	c	b (^*)	b	d	Fair

Open in a new tab

One score.

TABLE 4.

Methodological quality assessment through NEWCASTLE – OTTAWA scale (for cross‐sectional studies).

Row	First author/year	Selection				Comparability	Outcome		Score
Row	First author/year	Representativeness of the sample	Sample size	Non‐respondent	Ascertainment of the exposure	The subjects in different outcome groups are comparable based on the study design or analysis. Confounding factors are controlled	Assessment of the outcome	Statistical test	0–10 stars
1	Partridge, A. H. (2008)	b (^*)	b	a (^*)	c	a (^*)	b (^**)	a (^*)	6
2	Ives, A. (2006)	a (^*)	b	c	b (^*)	a (^*)	b (^**)	a (^*)	6

Open in a new tab

One score.

^**

Two score.

The NOS for cross‐sectional studies also investigated three parameters, selection, comparability, and outcome, through eight particular questions. Each question in this scale is scored from one point, except for the comparability domain, in which each item is scored up to two points. Therefore, the maximum score for studies is computed at 9, and studies with estimated scores of fewer than 5 points have been identified as having a high risk of bias or low methodological quality (Luchini et al., 2017; Wells et al., 2016).

3. RESULTS

3.1. Results of search and selection strategy

The systematic search in the databases yielded a total of 1817 results. After removing duplicate records (n = 300), 1517 articles remained for further assessment. In the record screening, 724 articles were excluded due to the non‐relevance title and abstract. Among remained articles, 74 studies were not retrieved due to not having access to full texts. In this stage, from 719 articles that were assessed for eligibility, studies that reported the pregnancy rate during the diagnosis or treatment of BC (n = 143), studies evaluated the pregnancy‐associated BC (n = 103), studies represented the pregnancy rate in each cancer survivor except BC (n = 165), and case reports (n = 6), case series (n = 9), RCTs (n = 55), letter (n = 5), and each type of review studies including narrative review, systematic review and meta‐analysis regarding pregnancy during or after BC (n = 210), were excluded. Also, among 311 additional records identified through other sources, such as reference lists of searched studies, 159 duplicate records were removed. From 117 remaining records for eligibility assessment, 110 papers were excluded. Finally, 29 articles were used in this systematic review (Figure 1).

The PRISMA diagram for the search of records and study selection.

3.2. The characteristics of the included studies

Of the 29 included studies, 12 studies were conducted in the United States (USA; Abel et al., 2021; Black et al., 2017; Blakely et al., 2004; Dillon et al., 2013; Gelber et al., 2001; Kranick et al., 2010; Mueller et al., 2003; Oktay et al., 2015; Partridge et al., 2008; Poorvu et al., 2021; Sutton et al., 1990; Velentgas et al., 1999), three studies was performed in France (Labrosse et al., 2021; Leproux et al., 2021; Mangiardi‐Veltin et al., 2022), two studies were conducted in Italy (Dieci et al., 2019; Lambertini, Ameye, et al., 2020), two studies in Denmark (Kroman et al., 1997, 2008), two studies in the United Kingdom (UK; Kopeika et al., 2019; Rippy et al., 2009), one study was in Germany (Jacob et al., 2017), one study in Korea (Lee et al., 2020), one study in Spain (Córdoba et al., 2012), one study in Sweden (Dalberg et al., 2006), one study in Australia (Ives et al., 2007), one study in Finland (Sankila et al., 1994), one study in Israel (Kaidar‐Person et al., 2022) and one study was carried out in Lebanon (Assi et al., 2020). The included studies were published between “1990 and 2022” regarding the publication year. Of the 29 included studies, 13 studies were prospective cohorts or prospective multicenter or population‐based cohort (Abel et al., 2021; Blakely et al., 2004; Dalberg et al., 2006; Dillon et al., 2013; Kaidar‐Person et al., 2022; Kroman et al., 2008; Lambertini, Ameye, et al., 2020; Lee et al., 2020; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Poorvu et al., 2021; Sutton et al., 1990; Velentgas et al., 1999), 14 studies were retrospective cohort or retrospective population‐based cohort studies (Assi et al., 2020; Black et al., 2017; Córdoba et al., 2012; Dieci et al., 2019; Gelber et al., 2001; Jacob et al., 2017; Kopeika et al., 2019; Kranick et al., 2010; Kroman et al., 1997; Labrosse et al., 2021; Leproux et al., 2021; Mueller et al., 2003; Rippy et al., 2009; Sankila et al., 1994), and two studies were cross‐sectional retrospective survey or population‐based descriptive studies (Ives et al., 2007; Partridge et al., 2008). The sample size from 29 assessed studies was from 39 to 2,325,229 women. According to the results of 24 of 29 included studies, the shortened mean ± SD time between treatments and pregnancy occurrence among BC survivors was 3.7 months. The primary and secondary outcomes measured in most of the included studies were the pregnancy rate or live birth after BC (Dillon et al., 2013; Ives et al., 2007; Labrosse et al., 2021; Lambertini, Ameye, et al., 2020; Leproux et al., 2021; Sutton et al., 1990) or pregnancy attempt or post BC diagnosis pregnancies (Abel et al., 2021; Kopeika et al., 2019; Poorvu et al., 2021), fertility preservation procedures or fertility discussion regarding the effect of BC on future pregnancy among BC survivors (Assi et al., 2020; Mangiardi‐Veltin et al., 2022; Rippy et al., 2009), the pregnancy or birth outcomes or complications among survived women with BC (Dalberg et al., 2006; Dieci et al., 2019; Jacob et al., 2017; Kaidar‐Person et al., 2022; Labrosse et al., 2021; Oktay et al., 2015; Partridge et al., 2008), the association between BC and birth outcomes (Black et al., 2017), the risks of recurrence and mortality due to pregnancy (Blakely et al., 2004; Kroman et al., 1997; Lee et al., 2020; Velentgas et al., 1999) or BC outcomes or prognosis due to pregnancy among survivors (Córdoba et al., 2012; Gelber et al., 2001; Kranick et al., 2010; Kroman et al., 2008; Sutton et al., 1990) and overall survival rate among BC survivors (Lambertini, Ameye, et al., 2020; Leproux et al., 2021; Mueller et al., 2003; Sankila et al., 1994; Table 2).

3.3. The pregnancy rate among BC survivors

The pregnancy rate among BC survivors was reported in 24 included studies. According to this systematic review, the pregnancy rate was estimated at 3.1%–48.5% among BC survivors who attempted to conceive after completing the treatments. Since the included studies had different sample sizes, the pregnancy rate was reported in a wide range. The lowest pregnancy rate was reported in the Lee study, which was carried out to investigate the pregnancy rate among Korean women after treatment with BC (Lee et al., 2020). The results of this study indicated that 992 (3.1%) women became pregnant after completing BC treatment. Among them, 662 (67.5%) women successfully delivered (Lee et al., 2020). Also, the highest pregnancy rate was estimated in a study by Gelber et al. (2001) that reported 137 pregnancies (48.5%) for 94 patients in the study group and among which 67 patients had one; 17 patients had two; seven had three, two had four, and one patient had experienced seven pregnancies after the treatment of BC. Also, 89 (64.9%) pregnancies resulted in live births in this study (88 singletons and one set of triplets births). According to the included studies, the pregnancy rate is reported in Table 2.

3.4. The pregnancy outcomes among BC survivors

3.4.1. Maternal outcomes in pregnancies of BC survivors

A total of 27 studies out of 29 included studies reported maternal outcomes of pregnancy among BC survivors (Abel et al., 2021; Assi et al., 2020; Blakely et al., 2004; Córdoba et al., 2012; Dalberg et al., 2006; Dieci et al., 2019; Dillon et al., 2013; Gelber et al., 2001; Ives et al., 2007; Jacob et al., 2017; Kaidar‐Person et al., 2022; Kopeika et al., 2019; Kranick et al., 2010; Kroman et al., 1997, 2008; Labrosse et al., 2021; Lambertini, Ameye, et al., 2020; Lee et al., 2020; Leproux et al., 2021; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Partridge et al., 2008; Poorvu et al., 2021; Rippy et al., 2009; Sutton et al., 1990; Velentgas et al., 1999). These outcomes included ectopic pregnancy (Dillon et al., 2013; Kranick et al., 2010; Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022; Velentgas et al., 1999), induced abortion (Dillon et al., 2013; Kranick et al., 2010; Kroman et al., 1997, 2008; Lambertini, Kroman, et al., 2020; Rippy et al., 2009; Velentgas et al., 1999), gestational diabetes mellitus (GDM; Abel et al., 2021; Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022), pre‐eclampsia (Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022) and eclampsia (Kaidar‐Person et al., 2022), and metastatic recurrence of BC (Labrosse et al., 2021). Miscarriage and induced abortion were the most prevalent maternal outcome of pregnancy among BC survivors, according to the results of this study.

Miscarriage

According to the results of 22 studies, miscarriage as a pregnancy complication was reported in 1.8%–33.3% of BC survivors (Abel et al., 2021; Assi et al., 2020; Blakely et al., 2004; Dieci et al., 2019; Dillon et al., 2013; Gelber et al., 2001; Ives et al., 2007; Jacob et al., 2017; Kopeika et al., 2019; Kranick et al., 2010; Kroman et al., 1997, 2008; Labrosse et al., 2021; Lambertini, Ameye, et al., 2020; Lee et al., 2020; Leproux et al., 2021; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Partridge et al., 2008; Poorvu et al., 2021; Sutton et al., 1990; Velentgas et al., 1999). The lowest rate of miscarriage was estimated in the Jacob et al. study, which was performed to investigate the effect of previous BC on delivery mode and pregnancy outcomes. The results of this study showed spontaneous abortion was 1.8% and 3.1% among pregnant women with a history of BC and women with no history of cancer in the control group, respectively (OR = 0.59 (0.14–2.52), p = 0.478; Jacob et al., 2017). In contrast, the results of a survey by Assi et al. (2020) in the middle east indicated that out of six pregnancies, 2 (33.33%) were miscarriages.

Induced abortion

Seven studies reported induced abortion as a pregnancy complication among BC survivors (Dillon et al., 2013; Kranick et al., 2010; Kroman et al., 1997, 2008; Lambertini, Kroman, et al., 2020; Rippy et al., 2009; Velentgas et al., 1999). This maternal outcome ranged from 5.0% to 44.0% among pregnant women. The lowest rate of induced abortion was estimated in the Rippy et al. (2009) study, which was performed to investigate the effect of BC, its treatment, and counselling on future pregnancy and fertility. The results of this study showed one patient had an induced abortion due to concerns regarding fetal damage despite receiving specific counselling about fertility before BC treatment. Kroman et al. (1997) study showed that 211 pregnancies occurred among 173 women who attempted to conceive after treatment of BC. In this study, miscarriages and induced abortions after BC treatment did not influence the disease prognosis.

3.4.2. Fetal or neonatal outcomes in pregnancies of BC survivors

A total of 13 studies out of 29 included studies investigated the fetal or neonatal effects of pregnancy among BC survivors (Abel et al., 2021; Black et al., 2017; Blakely et al., 2004; Dalberg et al., 2006; Gelber et al., 2001; Jacob et al., 2017; Kaidar‐Person et al., 2022; Labrosse et al., 2021; Lambertini, Ameye, et al., 2020; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Poorvu et al., 2021; Velentgas et al., 1999). These outcomes included PTB or very PTB (Black et al., 2017; Blakely et al., 2004; Dalberg et al., 2006; Jacob et al., 2017; Kaidar‐Person et al., 2022; Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022), LBW (Black et al., 2017), SGA (Black et al., 2017), Cytomegalovirus seroconversion (Mangiardi‐Veltin et al., 2022), twin or multiple births (Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Poorvu et al., 2021; Velentgas et al., 1999), intrauterine growth restriction (IUGR; Abel et al., 2021; Kaidar‐Person et al., 2022; Labrosse et al., 2021), hemorragia (Kaidar‐Person et al., 2022; Labrosse et al., 2021), hydramnios (Labrosse et al., 2021), fetal distress (Kaidar‐Person et al., 2022), macrosomia (Labrosse et al., 2021), malformation or congenital abnormalities (Dalberg et al., 2006; Lambertini, Ameye, et al., 2020), birth trauma (Dalberg et al., 2006), stillbirth (Dalberg et al., 2006; Gelber et al., 2001; Poorvu et al., 2021). According to the results of included studies, PTB or very PTB and twin birth were the most common neonatal outcomes occurring among BC, respectively.

PTB or very PTB

A total of seven studies reported PTB or very PTB was a neonatal outcome among BC survivors (Black et al., 2017; Blakely et al., 2004; Dalberg et al., 2006; Jacob et al., 2017; Kaidar‐Person et al., 2022; Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022). Based on the study's results, the prevalence of PTB or very PTB ranged from 1.2% to 21.1%. The lowest rate of PTB reported in the Jacob et al. (2017) study examined the effect of BC history on the delivery mode and following pregnancy outcomes. The results of this study demonstrated that 1.2% of pregnant women with BC and 0.6% of pregnant women in the control group experienced PTB (OR = 2.01 (0.18–22.41), p = 0.570); thus, the results showed that in comparison with the control group, the incidence of PTB in women with BC not significantly increased (p = 0.570). The Black et al. (2017) study, which assessed the prevalence of PTB, LBW, and SGA delivery after BC diagnosis, indicated that in women with a history of BC, the prevalence ratio for PTB was significantly higher in BC survivors compared to the general population (PR = 1.50 (95% CI, 1.23–1.84), p < 0.05).

Twin birth

Six studies reported the occurrence of twin or multiple births among BC survivors (Kroman et al., 2008; Labrosse et al., 2021; Mangiardi‐Veltin et al., 2022; Oktay et al., 2015; Poorvu et al., 2021; Rippy et al., 2009; Velentgas et al., 1999). The incidence of twin birth ranged from 1.1% to 38.8% based on the included studies. The study by Velentgas et al. (1999), which assessed the pregnancy outcomes and its effect on the mortality rate of BC women, indicated that only one (1.1%) of 53 pregnant women experienced multiple births, which were similar to healthy pregnant women (p > 0.05). Oktay et al. (2015) investigated the success of fertility preservation (FP) after ovarian stimulation in women with BC. In this study, embryo freezing with the simultaneous consumption of Letrozole was used for FP in women with BC. The results of this study indicated that 7 (38.8%) of the 18 pregnancies were twins and presented that performing the embryo cryopreservation after ovarian trigger through using Letrozole helped preserve the fertility potential of women with BC and led to a comparable pregnancy rate to women with no history of BC and under the in vitro fertilization (p = 0.20).

3.4.3. The effect of pregnancy on the recurrence of BC among survivors

Overall, 22 of 29 included studies assessing BC recurrence status after pregnancy in BC survivors (Assi et al., 2020; Blakely et al., 2004; Córdoba et al., 2012; Dalberg et al., 2006; Dieci et al., 2019; Gelber et al., 2001; Ives et al., 2007; Kranick et al., 2010; Kroman et al., 1997, 2008; Lambertini, Ameye, et al., 2020; Lee et al., 2020; Leproux et al., 2021; Mueller et al., 2003; Oktay et al., 2015; Partridge et al., 2008; Rippy et al., 2009; Sankila et al., 1994; Sutton et al., 1990; Velentgas et al., 1999). In two studies, cases of BC recurrence were observed. The first was Abel et al. (2021) study that showed that only one of the 46 patients who attempted conception experienced BC recurrence during pregnancy. However, this woman was delivered without pregnancy complications 3 years after completing treatment. Also, in the study by Labrosse et al. (2021), only one patient showed metastatic recurrence after BC.

Other studies showed pregnancy after the treatment of BC had not increased the risk of disease recurrence among BC survivors. In Sankila et al. (1994) study, the risk of death among the control group without pregnancy was 4.8 times more than those with a history of delivery after the diagnosis of BC (95% CI 2.2 to 10.3, p < 0.001).

3.5. Quality assessment

The quality of 27 studies was assessed using the NOS for cohort studies. Among them, 23 studies had good, and four had fair methodological quality (Kopeika et al., 2019; Oktay et al., 2015; Rippy et al., 2009; Sutton et al., 1990). Two cross‐sectional studies in this review were methodologically assessed through NOS cross‐sectional studies. Both of these studies had good quality (low risk of bias; Ives et al., 2007; Partridge et al., 2008). The details of the studies' scoring are presented in Tables 3 and 4.

4. DISCUSSION

This manuscript presents a systematic review investigating the pregnancy rate, maternal and neonatal outcomes, and BC recurrence status among BC survivors after pregnancy. A total of 29 studies were included in the review, comprising various study designs such as prospective cohorts, retrospective cohorts, and cross‐sectional surveys.

The results of the current study indicated that the pregnancy rate was estimated at 3.1%–48.5% among BC survivors. A recent systematic review reported the pregnancy rate following BC was 3%–14% (Gerstl et al., 2018). The differences between studies can be attributed to the different inclusion criteria. The results of a meta‐analysis investigated the pregnancy rate according to observational studies presented that the pregnancy rate after the treatment of BC was approximately 40% lower than the general population's (Azim Jr et al., 2011). The results of previous population‐based studies have also indicated that cancer treatment significantly decreased the pregnancy rate in BC survivors compared to healthy women (Anderson et al., 2018; Poorvu et al., 2021).

In recent decades, many women have postponed childbearing for different reasons; therefore, more BC patients will intend to experience pregnancy after treatment (Higgins & Haffty, 1994). Psychological stress regarding the possibility of infertility following cancer treatment, the probability of the negative effect of cancer treatment on fetus health, and the risk of cancer recurrence were the main concerns of reproductive‐aged BC survivors women with no pregnancy and may lead to further delay in pregnancy or terminating pregnancies (Dalberg et al., 2006; Haggar et al., 2014; Langagergaard et al., 2006). Moreover, factors such as decreased rate of disease recurrence and death after BC caused physicians progressively pay more concentrate to fertility issues and provide more specialized counselling to patients in this regard (Litton, 2012). In addition, available clinical guidelines regarding managing reproductive‐aged BC survivors recommend that these women be educated regarding the possible transient or permanent effects of BC treatment on the fertility potential of BC survivors, which helps them make appropriate decision‐making (Gerstl et al., 2018). Unfortunately, no critical documents have yet been published to assist physicians in providing multidimensional counselling to patients regarding the appropriate time of pregnancy after BC treatment (Raphael et al., 2015). In this regard, high‐quality published evidence recommended that pregnancy should be delayed approximately 2 years after the end of BC treatment. Although this delay may be logical for a resumption of ovarian function and increase the possibility of recognizing the disease recurrence, it may reduce the possible occurrence of conceiving among survivors (Lutchman Singh et al., 2005; Raphael et al., 2015).

In this systematic review, the pregnancy outcomes in studies carried out on BC survivors were also assessed. However, the current evidence‐based documents regarding the effect of BC on pregnancy outcomes are limited, and overall available evidence about the pregnancy outcome after BC treatment has contradictory results. Although cancer or its treatment may have an adverse effect on fetus growth and development and also maternal status (Langagergaard et al., 2006), among the included studies, a few studies reported fetal and maternal outcomes in BC survivors were significantly higher than BC survivors without a history of pregnancy after treatment. A multicenter population‐based study showed that of pregnancies that occurred 2 years after BC, 47% were terminated, and the abortion rate was inversely associated with the duration of BC diagnosis to pregnancy occurrence (Güth et al., 2016). A Swedish study that reported medical birth registry data showed that delivery complications, caesarean section, and very PTB increased in BC survivors' pregnancies (Dalberg et al., 2006).

In contrast, various studies showed no higher pregnancy complications in BC survivors than in BC survivors without a history of pregnancy after treatment (Black et al., 2017; Dieci et al., 2019; Kopeika et al., 2019). According to a systematic review and meta‐analysis that evaluated the pregnancy after a diagnosis of BC, BC survivors had significantly fewer subsequent pregnancies than the general population. Regarding the neonatal outcomes, the risk of LBW, PTB, and SGA was considerably higher than in BC survivors, specially among those with previous chemotherapy exposure compared to the general population. Regarding maternal outcomes, the risk of caesarean section increased in BC survivors compared to the general population (Lambertini et al., 2021).

The results of this systematic review also indicate that pregnancy has no adverse effect on BC recurrence status in BC survivors. In recent decades, the survival rate 5 years after the initial diagnosis of BC has substantially increased and is estimated at approximately 90% (Jacob et al., 2017). This increasing survival rate caused more women insistently follow medical counselling regarding the possible effect of pregnancy on fetal or neonatal outcomes after BC treatment (Hickey et al., 2009). Regarding the relationship between pregnancy after BC treatment and survival rate and BC, recurrence studies have indicated that BC survivors who conceived had higher survival and lowered BC recurrence compared with those who did not conceive (Blakely et al., 2004; Ives et al., 2007; Kroman et al., 2008; Mueller et al., 2003).

4.1. Strengths and limitations

4.1.1. Strengths

The study employs a systematic approach and includes a comprehensive search of multiple databases, enhancing the robustness of the review. Including quality assessment using the Newcastle‐Ottawa Scale adds credibility to the findings. The review encompasses many study designs, providing a comprehensive overview of the available evidence.

4.1.2. Limitations

The review is limited to observational studies, which inherently have certain limitations in establishing causality and controlling for confounding factors. The heterogeneity observed among the included studies in design, sample size, and population characteristics may introduce variability in the results. The review does not analyse the potential factors influencing pregnancy outcomes and breast cancer recurrence.

5. CONCLUSION

This systematic review revealed that the estimated pregnancy rate among BC survivors who attempted to conceive ranged from 3.1% to 48.5%. Notably, most of the included studies indicated that pregnancy did not adversely affect the recurrence status of BC among survivors. This systematic review provides valuable insights into pregnancy outcomes and BC recurrence status among BC survivors. The findings suggest that BC survivors who desire to conceive can be encouraged and supported in their decision while receiving a carefully managed multidisciplinary approach to ensure a healthy pregnancy.

AUTHOR CONTRIBUTIONS

MA, MM & EE did the literature search and independent review for eligibility, collected the data, independently reviewing for eligibility and drafted the manuscript. ZBM & ZSH contributed in the conception of the work, study design and writing of the protocol; identifying the studies and editing the manuscript. All authors read and approved the final manuscript.

FUNDING INFORMATION

Tehran University of Medical Sciences financially supports this systematic review.

CONFLICT OF INTEREST STATEMENT

The authors declared that they have no conflicts of interest.

RESEARCH ETHICS COMMITTEE APPROVAL

PROSPERO; Registration no. CRD42022309051; available from https://www.crd.york.ac.uk/prospero/. In addition, the ethical code for this study was IR.TUMS.FNM.REC.1400.016.

ACKNOWLEDGEMENTS

The authors sincerely appreciate Tehran University of Medical Sciences that assisted with conducting the research and providing financial support.

Azizi, M. , Ebrahimi, E. , Moghadam, Z. B. , Shahhosseini, Z. , & Modarres, M. (2023). Pregnancy rate, maternal and neonatal outcomes among breast cancer survivors: A systematic review. Nursing Open, 10, 6690–6707. 10.1002/nop2.1941

DATA AVAILABILITY STATEMENT

The data supporting this study's findings are available from the corresponding author upon request.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The data supporting this study's findings are available from the corresponding author upon request.

[nop21941-bib-0001] Abel, M. K. , Wald, K. , Sinha, N. , Letourneau, J. M. , Simbulan, R. , Mok‐Lin, E. , Cedars, M. I. , & Rosen, M. P. (2021). Conception after chemotherapy: Post‐chemotherapy method of conception and pregnancy outcomes in breast cancer patients. Journal of Assisted Reproduction and Genetics, 38(7), 1755–1765. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0002] Anderson, R. A. , Brewster, D. H. , Wood, R. , Nowell, S. , Fischbacher, C. , Kelsey, T. W. , & Wallace, W. H. B. (2018). The impact of cancer on subsequent chance of pregnancy: A population‐based analysis. Human Reproduction, 33(7), 1281–1290. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0003] Assi, H. A. , Khoury, K. E. , Dbouk, H. , Khalil, L. E. , Mouhieddine, T. H. , & El Saghir, N. S. (2013). Epidemiology and prognosis of breast cancer in young women. Journal of Thoracic Disease, 5(Suppl 1), S2. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0004] Assi, H. I. , Kakati, R. T. , Attieh, R. M. , Khoury, J. , Sukhon, F. , Berro, J. , Sbaity, E. , Salem, Z. , Tfayli, A. , Alameh, I. A. , & Saghir, N. E. (2020). Fertility in breast cancer survivors in the Middle East: A retrospective study. The Breast, 52, 58–63. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0005] Azim, H. A., Jr. , Santoro, L. , Pavlidis, N. , Gelber, S. , Kroman, N. , Azim, H. , & Peccatori, F. A. (2011). Safety of pregnancy following breast cancer diagnosis: A meta‐analysis of 14 studies. European Journal of Cancer, 47(1), 74–83. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0006] Beldon, A. , & Crozier, S. (2005). Health promotion in pregnancy: The role of the midwife. The Journal of the Royal Society for the Promotion of Health, 125(5), 216–220. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0007] Bien, A. M. , Korzynska‐Pietas, M. , & Iwanowicz‐Palus, G. J. (2014). Assessment of midwifery student preparation for performing the role of breast cancer educator. Asian Pacific Journal of Cancer Prevention, 15(14), 5633–5638. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0008] Black, K. Z. , Nichols, H. B. , Eng, E. , & Rowley, D. L. (2017). Prevalence of preterm, low birthweight, and small for gestational age delivery after breast cancer diagnosis: A population‐based study. Breast Cancer Research, 19(1), 1–8. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0009] Blakely, L. J. , Buzdar, A. U. , Lozada, J. A. , Shullaih, S. A. , Hoy, E. , Smith, T. L. , & Hortobagyi, G. N. (2004). Effects of pregnancy after treatment for breast carcinoma on survival and risk of recurrence. Cancer, 100(3), 465–469. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0010] Córdoba, O. , Bellet, M. , Vidal, X. , Cortés, J. , Llurba, E. , Rubio, I. T. , & Xercavins, J. (2012). Pregnancy after treatment of breast cancer in young women does not adversely affect the prognosis. The Breast, 21(3), 272–275. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0011] Dalberg, K. , Eriksson, J. , & Holmberg, L. (2006). Birth outcome in women with previously treated breast cancer—A population‐based cohort study from Sweden. PLoS Medicine, 3(9), e336. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0012] Deeks, J. J. , Higgins, J. P. , Altman, D. G. , & Cochrane Statistical Methods Group . (2019). Analysing data and undertaking meta‐analyses. Cochrane Handbook for Systematic Reviews of Interventions, 241–284. [Google Scholar]

[nop21941-bib-0013] Dieci, M. V. , Ghiotto, C. , Barbieri, C. , Griguolo, G. , Saccardi, C. , Gangemi, M. , Pluchinotta, A. , Di Liso, E. , Giorgi, C. A. , Giarratano, T. , Tasca, G. , Vernaci, G. , Faggioni, G. , Conte, P. , & Guarneri, V. (2019). Patterns of fertility preservation and pregnancy outcome after breast cancer at a large comprehensive cancer center. Journal of Women's Health, 28(4), 544–550. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0014] Dillon, K. E. , Sammel, M. D. , Ginsberg, J. P. , Lechtenberg, L. , Prewitt, M. , & Gracia, C. R. (2013). Pregnancy after cancer: Results from a prospective cohort study of cancer survivors. Pediatric Blood & Cancer, 60(12), 2001–2006. [DOI] [PMC free article] [PubMed] [Google Scholar]

[nop21941-bib-0015] Gelber, S. , Coates, A. S. , Goldhirsch, A. , Castiglione‐Gertsch, M. , Marini, G. , Lindtner, J. , Edelmann, D. Z. , Gudgeon, A. , Harvey, V. , Gelber, R. D. , & International Breast Cancer Study Group . (2001). Effect of pregnancy on overall survival after the diagnosis of early‐stage breast cancer. Obstetrical & Gynecological Survey, 56(9), 531–532. [DOI] [PubMed] [Google Scholar]

[nop21941-bib-0016] Gerstl, B. , Sullivan, E. , Ives, A. , Saunders, C. , Wand, H. , & Anazodo, A. (2018). Pregnancy outcomes after a breast cancer diagnosis: A systematic review and meta‐analysis. Clinical Breast Cancer, 18(1), e79–e88. [DOI] [PubMed] [Google Scholar]

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PERMALINK

Pregnancy rate, maternal and neonatal outcomes among breast cancer survivors: A systematic review

Marzieh Azizi

Elham Ebrahimi

Zahra Behboodi Moghadam

Zohreh Shahhosseini

Maryam Modarres

Abstract

Aim

Design

Methods

Results

1. INTRODUCTION

1.1. Background

2. METHODS

2.1. Design

2.2. Literature search and search strategy

TABLE 1.

2.3. Inclusion and exclusion criteria

2.3.1. Study selection

2.4. Outcome measure

2.5. Data extraction and analysis

TABLE 2.

2.6. Methodological quality assessment

TABLE 3.

TABLE 4.

3. RESULTS

3.1. Results of search and selection strategy

FIGURE 1.

3.2. The characteristics of the included studies

3.3. The pregnancy rate among BC survivors

3.4. The pregnancy outcomes among BC survivors

3.4.1. Maternal outcomes in pregnancies of BC survivors

Miscarriage

Induced abortion

3.4.2. Fetal or neonatal outcomes in pregnancies of BC survivors

PTB or very PTB

Twin birth

3.4.3. The effect of pregnancy on the recurrence of BC among survivors

3.5. Quality assessment

4. DISCUSSION

4.1. Strengths and limitations

4.1.1. Strengths

4.1.2. Limitations

5. CONCLUSION

AUTHOR CONTRIBUTIONS

FUNDING INFORMATION

CONFLICT OF INTEREST STATEMENT

RESEARCH ETHICS COMMITTEE APPROVAL

ACKNOWLEDGEMENTS

DATA AVAILABILITY STATEMENT

REFERENCES

Associated Data

Data Availability Statement

ACTIONS

PERMALINK

RESOURCES

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