Original Article

Bone Marrow Transplantation (2006) 37, 1023–1029. doi:10.1038/sj.bmt.1705364; published online 10 April 2006

Post-Transplant Events

Prevalence of conception and pregnancy outcomes after hematopoietic cell transplantation: report from the bone marrow transplant survivor study

A Carter1, L L Robison2, L Francisco1, D Smith1, M Grant1, K S Baker3, J G Gurney4, P B McGlave3, D J Weisdorf3, S J Forman5 and S Bhatia1,5

  1. 1Population Sciences, City of Hope Cancer Center, Duarte, CA, USA
  2. 2Epidemiology and Cancer Control, St Jude Children's Research Hospital, Memphis, TN, USA
  3. 3Blood and Marrow Transplant Program, University of Minnesota, Minneapolis, MN, USA
  4. 4General Pediatrics, University of Michigan, Ann Arbor, MI, USA
  5. 5Hematology and Hematopoietic Cell Transplantation, City of Hope Cancer Center, Duarte, CA, USA

Correspondence: Dr S Bhatia, City of Hope Cancer Center, 1500 East Duarte Road, Duarte, CA 91010-3000, USA. E-mail: sbhatia@coh.org

Received 24 February 2006; Revised 8 March 2006; Accepted 9 March 2006; Published online 10 April 2006.

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Abstract

We conducted a retrospective study to describe the magnitude of compromise in reproductive function and investigate pregnancy outcomes in 619 women and partners of men treated with autologous (n=241) or allogeneic (n=378) hematopoietic cell transplantation (HCT) between 21 and 45 years of age, and surviving 2 or more years. Median age at HCT was 33.3 years and median time since HCT 7.7 years. Mailed questionnaires captured pregnancies and their outcomes (live birth, stillbirth, miscarriage). Thirty-four patients reported 54 pregnancies after HCT (26 males, 40 pregnancies; eight females, 14 pregnancies), of which 46 resulted in live births. Factors associated with reporting no conception included older age at HCT (greater than or equal to30 years: odds ratio (OR)=4.8), female sex (OR=3.0), and total body irradiation (OR=3.3). Prevalence of conception and pregnancy outcomes in HCT survivors were compared to those of 301 nearest-age siblings. Although the risk for not reporting a conception was significantly increased among HCT survivors (OR=36), survivors were not significantly more likely than siblings to report miscarriage or stillbirth (OR=0.7). Although prevalence of conception is diminished after HCT, if pregnancy does occur, outcome is likely to be favorable. Patients should be counseled prior to transplant regarding strategies to preserve fertility.

Keywords:

late effects, conception, pregnancy outcomes, hematopoietic cell transplantation

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Introduction

Hematopoietic cell transplantation (HCT) is being increasingly used for the treatment of malignant and non-malignant disorders, with over 45 000 transplants performed worldwide annually.1 The widespread use of HCT can be attributed to its improved treatment efficacy, wider variety of stem cell sources, and improved transplantation strategies and supportive care, and has resulted in a growing number of long-term survivors.1, 2 Most pre-transplant conditioning regimens for HCT include alkylating agents and/or irradiation, both of which may cause germ cell injury, gonadal dysfunction and infertility.3, 4 The risk of gonadal damage is higher with increasing doses of alkylating agents, total body irradiation (TBI), and older age in women at the time of transplant.5

Although successful pregnancies after HCT have been reported previously,6, 7, 8, 9, 10, 11 the evidence suggests that female survivors may be at an increased risk of spontaneous abortions and miscarriages, pre-term delivery and low birth weight babies.12, 13 To further investigate pregnancy outcomes and describe the magnitude of compromise in reproductive function, as indicated by prevalence of self-reported pregnancy occurrence and pregnancy outcomes, we utilized the cohort of survivors participating in the Bone Marrow Transplant Survivor Study (BMTSS) and compared their experience with a sibling comparison group.

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Materials and methods

The BMTSS, a collaborative effort between the City of Hope Cancer Center and the University of Minnesota, examines the long-term outcomes of individuals who have survived 2 or more years after undergoing HCT, as well as similar outcomes in a cohort of siblings with a similar age and gender distribution. The aim of the current study was to determine the prevalence of post-HCT conception, and outcome of pregnancy in 619 adult women and partners of men previously treated with autologous or allogeneic HCT. The present report from BMTSS is restricted to individuals who met the following eligibility criteria: (i) HCT between 1974 and 1998 at the City of Hope or University of Minnesota; (ii) age at transplant 21–45 years; and, (iii) survival of at least 2 years from HCT, irrespective of disease status. The Human Subjects Committees at the participating institutions approved the BMTSS protocol. Informed consent was provided according to the Declaration of Helsinki. Data collection included completion of a 255-item mailed questionnaire designed to capture a wide range of demographic characteristics and health information. Specific to this report, participants provided a complete pregnancy history by supplying details about all pregnancies and outcomes both before and subsequent to HCT. Data collected included age at beginning of each pregnancy, weeks the pregnancy lasted, date of delivery and outcome of each pregnancy (i.e. whether the pregnancy resulted in a livebirth, stillbirth, spontaneous miscarriage or medical abortion). Only post-HCT pregnancies were used for the purpose of the current analysis. The two primary outcomes of interest were inability to conceive after transplant, and pregnancy outcomes (i.e. livebirths, stillbirths and spontaneous miscarriages). Pregnancies in gestation were not included in outcome analyses. We compared the information obtained from the HCT survivors to that obtained from 301 closest-age siblings who completed an identical BMTSS questionnaire. Analyses were restricted to pregnancies occurring between the ages of 21 and 45 for both survivors and the sibling comparison group.

Statistical analysis

Standard parametric and non-parametric tests were used to report descriptive analyses. To test for associations between ordinal and categorical end points, we applied chi2 tests for independence. The primary outcomes of interest were inability to conceive (yes vs no) and pregnancy outcomes (live births, miscarriages and spontaneous abortions). Data were analyzed with SAS version 9.1 (SAS Institute, Cary, NC, USA).14

Conception

Comparison with siblings
 

Potential risk factors for not reporting a conception were analyzed using unconditional logistic regression and included age at study participation, sex, race, annual household income (<$20 000 vs $20 000–$60 000 vs >$60 000), availability of health insurance, and highest level of education (high school or less vs high school degree with or without some college or training after high school, vs college graduate). Odds ratio15 was used to estimate magnitude of association between the risk of not reporting a conception and the potential risk factors.

Within survivor comparison
 

Potential risk factors for not reporting a conception were analyzed within the survivor cohort, using unconditional logistic regression and included age at HCT (younger than 30 years vs 30 years or older), sex, race, annual household income (as above), availability of health insurance, highest level of education (as above), primary diagnosis (chronic myelogenous leukemia (CML), acute myeloid leukemia (AML), Hodgkin disease (HD), non-Hodgkin lymphoma (NHL), acute lymphoblastic leukemia (ALL), aplastic anemia (AA) and other miscellaneous diagnoses (other)), type of transplant (autologous vs allogeneic), disease status at transplant (standard vs high risk of relapse at HCT), preparative regimens, presence of chronic graft-vs-host disease (cGVHD), immunosuppressive agents used for GVH prophylaxis (yes vs no) and report of pre-transplant pregnancy ending in live birth (yes vs no). Patients considered being at standard risk for relapse included those in first or second complete remission after acute leukemia or lymphoma, those with severe aplastic anemia, and first chronic phase of CML. All other patients were placed into the high-risk category.

Pregnancy outcomes

Risk factors were analyzed for the occurrence of a live birth or the occurrence of an adverse pregnancy outcome (stillbirth or miscarriage).

Comparison with siblings
 

Potential risk factors for adverse pregnancy outcomes (miscarriage or stillbirth) included age at study participation (younger than 45 years vs 45 years or older), sex, race, annual household income, availability of health insurance and highest level of education. chi2 tests were performed to determine whether the rate of pre-term delivery (less than or equal to37 weeks gestation) differed with respect to the sibling controls.16

In order to account for multiple pregnancies in or by one survivor or one sibling (within person correlation), we used generalized estimating equations with a binominal distribution and a logit link to estimate the relative odds of pregnancy outcomes among survivors compared to siblings. Our models also included a variance component for within family correlation.14, 17, 18, 19

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Results

Of the 978 patients eligible for participation in this study, 897 were successfully contacted with 619 (69%) agreeing to participate (Table 1). The median age at study participation was 42.6 years (range 23.3–60.4 years), median age at transplant 33.3 years (range 21.0–45.0) and median length of follow-up 7.7 years (2.0–24.4 years). Twenty-nine percent of participants had received HCT for CML, 22.9% for AML, and 29.9% for HD or NHL.


Comparison of study participants with the potentially eligible non-participants showed that participants were more likely to be female (47 vs 39%, P=0.02), and have received a conditioning regimen containing TBI (81 vs 73%, P=0.003). Participants did not differ statistically from non-participants in other conditioning agents received, race/ethnicity, primary diagnosis and length of follow-up, age at survey, age at transplant, risk of relapse at HCT, type of HCT, presence of cGVHD or the receipt of immunosuppressive agents.

Conception

A total of 34 (5.5%) survivors reported 54 post-HCT conceptions; these included 26 (8%) male survivors and eight (3%) female survivors (Table 2). Among the autologous transplant recipients, eight males (7%) reported nine post-transplant conceptions, had a median age at HCT of 29.7 years, a median age at first post-transplant delivery of 34.2 years and 25% had received a conditioning regimen including TBI. Four female autologous transplant survivors (3%) reported nine post-transplant conceptions, had a median age at HCT of 27.4 years, a median age at first post-transplant delivery of 31.3 years and 50% had received TBI. Among the allogeneic transplant recipients, 18 males (9%) reported 31 post-transplant conceptions in their partners, had a median age at transplant of 27.2 years, a median age at first delivery of 30.7 years and 72.2% had received TBI. Four female allogeneic transplant survivors (2%) reported five pregnancies post-HCT, had a median age at transplant of 22.0 years, a median age at first delivery of 25.7 years, and 75% received TBI. In the sibling comparison group, 66% of male siblings and 72% of female siblings reported conceptions for a total of 211 siblings (70%) reporting 539 pregnancies.


HCT survivors were at a 36-fold increased risk of not reporting a conception compared to siblings (OR=35.9, 95% CI: 23.2–55.8, P<0.0001). Furthermore, study participants with an annual income of <$20 000 were at an increased risk of not reporting a conception compared to those with a higher income (OR=2.9, 95% CI: 1.1–7.8, P=0.03), as were participants who were younger at the time of survey completion compared to older participants (OR=1.03, 95% CI: 1.01–1.05, P=0.002). Risk did not vary statistically by race/ethnicity, education, sex or health insurance status (Table 3).


Restricting the analysis to HCT survivors demonstrated that age at transplantation greater than or equal to30 years (OR=4.8, 95% CI: 2.1–10.7, P<0.001), female sex (OR=3.0, 95% CI: 1.3–6.9, P<0.001) and receipt of TBI-containing conditioning (OR=3.3, 95% CI: 1.5–7.3, P=0.003), were associated with an increased risk of not reporting a post-HCT conception. The analysis was adjusted for ethnicity, income, health insurance status, report of pre-transplant live birth, immunosuppressive agents received, chemotherapeutic exposures, type of transplant, presence of cGVHD, primary diagnosis, disease status at HCT and level of education (Table 3).

Pregnancy outcomes

Provided in Table 4 are the outcomes of pregnancies reported by survivors and siblings. Eighty-five percent of conceptions reported by the HCT survivors resulted in live birth, which was significantly higher than the 75% of live birth outcomes reported by siblings (P=0.05). Thus, outcomes of the 54 reported post-HCT conceptions included 46 live births (85.2%), five miscarriages (9.2%), one stillbirth (1.9%) and two pregnancies in gestation (3.7%) at the time of survey. In contrast, outcomes of the 539 pregnancies reported by the siblings included 401 live births (74.4%), 89 miscarriages (16.5%), 37 medical abortions (6.9%), six stillbirths (1.1%) and six pregnancies in gestation (1.1%). This pattern was observed both in male survivors (proportion of pregnancies resulting in livebirths: 84.6 vs 78.5%, P=0.5), as well as female survivors (100 vs 73.5%, P=0.07) when compared with same sex siblings. Survivors were not more likely than siblings to report pre-term deliveries (defined as less than or equal to37 weeks gestation; 33.3 vs 40.8%, P=0.5).


Multivariate analysis of pregnancy outcomes among study participants reporting the occurrence of pregnancy, indicated that HCT survivors were statistically as likely as siblings to report a livebirth (OR=2.2, 95% CI: 0.8–6.2, P=0.1), and that the survivors were not at an increased risk for miscarriage or stillbirth (RR=0.7, 95% CI: 0.2–2.1, P=0.5). This analysis was adjusted for age at survey completion, race/ethnicity, income, sex, health insurance and education (Table 5).


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Discussion

The results of this study demonstrate that the prevalence of conception following HCT was significantly diminished compared to siblings with a comparable age and gender distribution. Risks for not reporting conception were significantly higher among survivors undergoing HCT at an older age, females, those exposed to TBI and those with a low-household income. We have, however, identified 54 self-reported post-transplant conceptions in a patient population that has a high prevalence of infertility. Although we have confirmed that the overall prevalence of pregnancy following HCT is low, as in all previous studies, the true magnitude of infertility following HCT will always be difficult to determine, in part because of lack of complete data on pre- and post-transplant fertility status, and lack of sufficiently detailed information regarding desire to become pregnant after undergoing HCT.20

Post-pubertal recipients of high-dose cyclophosphamide have a high probability of recovery of gonadal function, and exposure to TBI may also result in occasional recovery of normal gonadal function.21, 22, 23, 24 Nevertheless, infertility following HCT is widespread, although it has been established that select patients may retain or recover fertility. Moreover, female survivors have been reported to be at an increased risk of spontaneous abortions and miscarriages, pre-term delivery and low birth weight babies.6, 12, 13, 24 However, previous research has generally not included comprehensive systematic assessments of the prevalence of conception after both autologous and allogeneic HCT, nor have the previous studies described the outcome of these pregnancies using a concurrent comparison group. Our goal was to determine the prevalence of conception and outcome of pregnancy in adult women and partners of men treated with autologous or allogeneic HCT by directly surveying the survivors rather than relying upon data abstracted from medical records or obtained from central registries. Moreover, our goal was to report on the outcomes after HCT, thus broadening the base of information available to help educate pre-transplant patients.

Several case series have described pregnancy outcomes among female HCT survivors.7, 12, 23, 24, 25, 26, 27, 28, 29, 30 Data from Sanders et al.12 suggest that pregnancies among female HCT recipients who had received TBI were significantly more likely to end in miscarriage, reporting a miscarriage rate of 38% after TBI as a 10.0 Gy single exposure or 12–14.0 Gy fractionated exposure. Furthermore, they reported a miscarriage rate of 7% among female survivors who had received cyclophosphamide alone, and no miscarriages among the five females who had received TBI at a much lower dose of 5–8.0 Gy. Pregnancy outcomes analyses in the current study indicated that 85% of the pregnancies resulted in live birth, compared with 75% of those reported by the nearest-age siblings and 62% of those reported by the Centers for Disease Control/National Center for Health Statistics on trends in the United States in Pregnancy Rates by Outcome.31 Our study demonstrates that, after adjusting for key variables, the survivors were as likely as sibling controls to report a pregnancy ending in live birth, and survivors were not more likely to report a pregnancy ending in miscarriage or stillbirth. Overall, 11% of the pregnancies resulted in miscarriages or stillbirths, compared with 17.6% of those reported by the nearest age siblings and 15.7% of those reported by the CDC/NCHS.31 Furthermore, while 14% of the pregnancies partnered by male HCT survivors resulted in miscarriages, none of the pregnancies reported by female survivors resulted in miscarriage. It is unlikely that a reporting bias would be more prevalent among either the patient or sibling participant groups, thus indicating that HCT was not associated with an increased prevalence of miscarriage in the current study. A recent large cohort study from the EBMT Late Effects Working Party did not find an increase in the rate of miscarriage, among transplant survivors when compared with general population rates.13 There is a possibility that the reported incidence of miscarriage underestimates the actual rate, since successful pregnancies are more likely to be reported, and recall of events representing a spontaneous abortion have been found to be inaccurate;32 approximately one in five pregnancies as detected by human chorionic gonadotropin assay are clinically unrecognized.33

Pre-term labor and delivery may result from pre-eclampsia, multiple gestation, intrauterine infection and distortion of the uterine cavity due to a variety of reasons. Irradiation has been shown to reduce the elasticity of the uterine musculature, probably secondary to intrauterine vascular damage.34 In contrast to previous studies that suggested female survivors of HCT are at an increased risk of delivering low birth weight and pre-term infants,12, 13 we did not find a higher reported prevalence of pre-term delivery after HCT when compared with the sibling comparison group.

The current study did not obtain information regarding assisted reproductive techniques that might have been utilized by the survivors. Thus, it is unclear what role the use of assisted reproductive techniques, such as sperm or oocyte cryopreservation, in vitro fertilization or pharmacological interventions, played in the current findings of rate of post-transplant pregnancy.35 The observation of the present study that low income is a risk factor for not reporting a post-transplant pregnancy may suggest that lower income survivors may have limited access to medical care, including assisted reproductive technologies.

Pre-transplantation counseling typically includes discussions regarding the likelihood of post-transplant infertility, and the chance of uncomplicated pregnancy, should conception be achieved. This study provides encouraging data for HCT survivors, indicating that although the prevalence of conception is significantly diminished after HCT, if pregnancy occurs, the outcome is likely to be favorable. Therefore, thought should be given prior to transplant to possible strategies to preserve fertility, such as cryopreservation of sperms, oocytes, ovaries, testes and embryos. Reduced intensity conditioning, or non-myeloablative HCT might avoid the necessity for TBI without compromising disease-free survival, but has been largely understudied.

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Acknowledgements

This work was supported in part by R01 CA078938 from the National Cancer Institute, and The Lymphoma-Leukemia Society of America Clinical Scholar Award 2191-02. This study was presented at the American Society of Hematology, San Diego, CA, 2004.