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Practice Patterns Surrounding Pregnancy After Heart Transplantation

Editor


WHAT IS NEW?

  • Many heart transplant recipients are of, or survive to, childbearing age.

  • A survey of heart transplant providers was performed to assess attitudes and practices surrounding posttransplant pregnancy.

  • Many providers feel that pregnancy is contraindicated in all heart transplant recipients.

  • The majority of centers do not have policies in place for recipients who become pregnant.

WHAT ARE THE CLINICAL IMPLICATIONS?

  • More education is needed regarding the feasibility of pregnancy after heart transplantation.

  • Heart transplant centers may benefit from institutional policies to manage posttransplant pregnancy.

  • This survey highlights the opportunity for research and standardization of policies regarding the choice of contraception, the safety of breastfeeding, and optimal immunosuppressive regimens and cardiac surveillance during pregnancy.

Introduction

As survival after heart transplantation (HT) continues to improve, many transplant recipients are of, or survive to, childbearing age.1 According to the 2019 International Society for Heart and Lung Transplantation (ISHLT) Registry Report, adult 1-year posttransplant survival is ≈90% with a conditional half-life of over 13 years.2 Pregnancy after HT has been performed safely in select patients, though many patients may not understand that pregnancy is feasible, what their individual risk might be based on their transplant course, or the impact of potential predisposing genetic risks.3,4

The ISHLT guidelines5 recommend a multidisciplinary approach to reproductive health after HT. Multiple factors should be considered, including preconception counseling, genetic counseling if the patient is unclear on the underlying etiology of heart failure, safety of immunosuppression, comorbid conditions, and the hemodynamic effects of pregnancy on the allograft.6 A consensus statement from the American Society of Transplantation expands on reproductive issues after transplantation including discussion of obstetric management and future research goals.7 One major difference between pregnancy in an abdominal versus thoracic organ transplant recipient is that the normal hemodynamic effects of pregnancy may directly impact or be influenced by graft function. Yet, there are limited data regarding providers’ attitudes, practices, and center policies surrounding pregnancy in HT recipients. The aim of the current study was to explore these concepts using a national population of transplant providers.

Methods

We conducted an independent, confidential, voluntary, electronic, web-based survey of HT providers between June and August 2019. The Cedars-Sinai Institutional Review Board reviewed and approved the survey before its distribution. Providers were sent an email message inviting them to participate in the survey and 2 subsequent reminder messages over the next 2 months. The data that support the findings of this study are available from the corresponding author upon request.

Study data were collected and managed using Research Electronic Data Capture (REDCap). Participants accessed the survey using a web link provided in the email invitation. The survey software uses web cookies to prohibit respondents from filling out multiple surveys from the same device. No login information was required to access the survey. Participants were able to forward the survey invitation to colleagues.

The survey contained 21 multiple choice and free text questions (Data Supplement). None of the questions were mandatory. All responses were anonymous, but the survey did query general provider demographic information including age, sex, role, and place of practice. Individual responses were downloaded from the survey and analyzed using Microsoft Excel. Descriptive analyses were conducted and are presented as means and SDs for continuous variables and numbers and percentages for categorical variables. Logistic regression was used to assess the impact of factors including respondent age, sex, specialty, transplant center volume, and experience with posttransplant pregnancies on the presence of a center policy or personal recommendation to avoid posttransplant pregnancy. A P-value of <0.05 was considered statistically significant. Statistical analyses were performed using STATA 16.0 software (College Station, TX).

Results

Respondents

The survey was sent to 1643 contacts in the United States; responses were received from 122 individuals (response rate, 7.4%). The majority of respondents were cardiologists (n=85, 70%), followed by nurse or transplant coordinators (n=22, 18%), surgeons (n=7, 6%), and advanced practice providers (nurse practitioners and physician’s assistants; n=6, 5%; Table 1; Figure 1). Two respondents were transplant nephrologists. Roughly half of respondents were women (n=58; 48%). All except 2 respondents practiced in the United States; 1 reported practicing in Asia and 1 in Canada. The largest percentage of respondents (n=48, 39%) practiced at an institution performing 20 to 39 HTs per year, while 13 (11%) practiced at an institution that performed 80 or more heart transplants annually. The majority (n=73; 60%) reported that their programs had at least one HT recipient who had become pregnant.

Table 1. Characteristics of Survey Respondents
No. (%)Total=122 Respondents
Age, y (median) 48
Sex
 Male 63 (52)
 Female 58 (48)
 Unknown 1
Provider role
 Cardiologist 85 (70)
 Surgeon 7 (6)
 Nurse or transplant coordinator 22 (18)
 Other 8 (6)
Location of practice
 United States 120 (98)
 Canada 1 (1)
 Asia 1 (1)
Number of transplants annually
 <20 27 (22)
 20–39 48 (39)
 40–59 20 (16)
 60–79 11 (9)
 >80 13 (11)
 Not provided 3 (3)
Figure 1.

Figure 1. Distribution of specialties of survey respondents. The majority of respondents were cardiologists by training with other groups including nurses, transplant coordinators, surgeons, advanced practice providers, and transplant nephrologists.

Attitudes and Policies for Posttransplant Pregnancy

Of 122 respondents, 121 individuals responded to the question, “Which of the following best describes your center’s policy (or your personal recommendations in the absence of a policy) on planned pregnancy following HT?” Roughly one-third (n=37; 31%) of respondents believed that pregnancy should be avoided in all female HT recipients while 67% of recipients (n=81) felt that pregnancy was feasible in select cases (Figure 2). Three respondents felt pregnancy was feasible for all female HT recipients. The responses by profession were not significantly different and are shown in Figure I in the Data Supplement.

Figure 2.

Figure 2. Responses regarding safety of pregnancy after heart transplant. The majority (67%) of respondents felt pregnancy was feasible for select heart transplant recipients (yellow sector).

Less than half of the respondents (n=52, 43%) reported that their centers had established policies regarding pregnancy following transplant. Notably, even at high-volume centers (>80 transplants annually), only 62% of respondents reported having an institutional policy surrounding pregnancy after transplant.

Certain conditions were considered contraindications to pregnancy in a HT recipient (Figure 3). The most commonly reported contraindications included nonadherence (n=109, 89%), reduced left ventricular ejection fraction (n=104, 85%), coronary allograft vasculopathy (n=86, 70%), history of rejection (n=76, 62%), presence of donor-specific antibodies (n=69, 57%), and prior peripartum cardiomyopathy pretransplant (n=57, 47%).

Figure 3.

Figure 3. Commonly reported contraindications to pregnancy. The bar graph below depicts percentages of respondents who reported that the condition would be a contraindication to pregnancy after heart transplantation. LV indicates left ventricular.

Regarding timing of pregnancy, the majority of respondents (n=98, 80%) would recommend that a female HT recipient who desires pregnancy should wait 1 year post-transplantation before planning conception. The remaining respondents (n=20, 16%) recommended waiting at least 1 to 5 years, 1 respondent answered 6 months, and 3 did not offer a time frame.

Contraception

Recommended forms of contraception included: intrauterine devices (n=82, 67%), barrier contraception (n=61, 50%), combined estrogen-progestin (n=49, 40%), depo-medroxyprogesterone acetate (n=47, 39%), and progestin-only oral contraception (n=35, 29%). Other forms recommended included tubal ligation (Figure 4). Three respondents explicitly recommended 2 simultaneous forms of contraception for transplant recipients. Thirty-four of 118 respondents (28.8%) would screen patients for hypercoagulable states before initiation of hormonal contraception. The majority of contraception was prescribed by a gynecologist (n=104, 85%), followed by a primary care physician (n=15, 12%). Three transplant providers reported that they prescribed contraception for their transplant patients.

Figure 4.

Figure 4. Recommended forms of contraception after heart transplantation (HT). Bar graph depicting the percentages of respondents who recommended various forms of contraception after HT. IUD indicates intrauterine device; and OCP, oral contraceptive pill.

Counseling

Of the 84 (69%) respondents who supported pregnancy in heart transplant recipients, 50% (n=42) would recommend preconception genetic counseling for all patients. An additional 36% (n=30) would consider genetic counseling if the patient had a genetic cause for their heart failure or cardiomyopathy.

With regard to breastfeeding, 68% (55 of 81 respondents) felt the decision should be deferred to the gynecologist or maternal fetal medicine specialist. However, 21% (n=17) felt it was not safe and should not be allowed.

With regard to assisted reproductive technologies, 69% (56 of 81 respondents) would endorse the use of assisted reproductive technologies if recommended by a fertility specialist.

Immunosuppression and Surveillance During Pregnancy

Seventy-nine respondents provided immunosuppression regimens. The most commonly recommended agents during pregnancy were calcineurin inhibitors with azathioprine (n=37; 47%), calcineurin inhibitor monotherapy (n=34, 43%), and calcineurin inhibitor with proliferation signal inhibitor (n=6, 8%; Figure 5). The addition of corticosteroids was recommended by 44 (56%) respondents. Two respondents (1 surgeon and 1 cardiologist) recommended calcineurin inhibitor with mycophenolate.

Figure 5.

Figure 5. Immunosuppression regimens recommended during pregnancy. Bar graph is shown depicting percentages of respondents who recommended each regimen. AZA indicates azathioprine; CNI, calcineurin inhibitor; MMF, mycophenolate mofetil; and PSI, proliferation signal inhibitor.

Responses were mixed regarding the frequency of echocardiography during pregnancy. Of 116 respondents, the majority (49, 42%) would recommend an echocardiogram every 3 months during pregnancy while 22% (n=25) recommended an echocardiogram at 2-month intervals and 28% (n=33) recommended monthly echocardiograms.

Experience With Pregnancy After Transplant

Seventy-three (60%) respondents had prior experience with pregnant heart transplant recipients. Of these, 64 (65%) respondents reported experience with between 1 and 5 pregnancies. Nine (12%) had experience with more than 5 pregnancies, ranging up to 30 pregnancies. Of the respondents who reported at least one posttransplant pregnancy at their institution, 24 (33%) also felt pregnancy should be avoided in all heart transplant recipients. Furthermore, of the 9 respondents who noted their centers had cared for >5 pregnant transplant recipients, 5 (56%) had an established policy to manage posttransplant pregnancy.

Factors Associated With Posttransplant Pregnancy Attitudes

We sought to determine what factors were associated with a respondent’s belief that pregnancy should be uniformly avoided after HT (Table 2). Female sex (OR, 1.46 [95% CI, 0.60–3.57]), respondent age >60 years (OR, 0.50 [95% CI, 0.17–1.50]), physician (OR, 0.45 [95% CI, 0.19–1.10]), higher-volume transplant center (<40 transplants/year; OR, 0.875 [95% CI, 0.38–2.04]), and prior experience with pregnancy (>1 posttransplant pregnancy at their centers; OR, 1.49 [95% CI, 0.63–3.53]) were not associated with opinions regarding the safety of posttransplant pregnancy. The only factor predictive of an established policy to manage pregnancy was prior experience with pregnancy (OR, 2.28 [95% CI, 1.01–5.11]).

Table 2. Univariate Predictors of Pregnancy Avoidance and Center Policy
Odds Ratio (95% CI) P Value
Pregnancy avoidance
 Respondent sex
  Female 1.46 (0.60–3.57) 0.41
  Male Reference
 Age, y
  Age ≥60 0.51 (0.17–1.50) 0.22
  Age <60 Reference
 Specialty
  Physician 0.45 (0.19–1.10) 0.08
  Nonphysician Reference
 Transplant volume
  ≥40/y 0.88 (0.38–2.04) 0.76
  <40/y Reference
 Prior experience with pregnancy after HT
  Yes 1.49 (0.63–3.53) 0.37
  No Reference
Center policy
 Respondent sex
  Female 1.09 (0.47–2.53) 0.84
  Male Reference
 Age
  Age ≥60 0.68 (0.27–1.69) 0.40
  Age <60 Reference
 Specialty
  Physician 0.83 (0.36–1.95) 0.67
  Nonphysician Reference
 Transplant volume
  ≥40/y 1.46 (0.66–3.20) 0.35
  <40/y Reference
 Prior experience with pregnancy after HT
  Yes 2.28 (1.01–5.11) 0.046
  No Reference

Discussion

To our knowledge, this is the first study to investigate transplant providers’ attitudes regarding pregnancy after HT. Despite ISHLT guidelines and improving posttransplant survival, a significant proportion indicate that pregnancy is contraindicated in all HT recipients and the majority do not have a center-specific policy to manage pregnancies. This is particularly important as heart transplant recipients are increasingly young and female.8,9 These findings indicate that education on the feasibility of pregnancy post-HT is indicated as many female transplant recipients are of, or are surviving to, childbearing age.

Current Transplant Society Recommendations

The ISHLT recommends that pregnancy management plans be individualized according to the status of the mother and allograft.5 Pregnancy should not be attempted before one year after HT.5 According to the American Society of Transplantation Consensus Summary, transplant recipients considering pregnancy should have had no rejection in the past year, adequate and stable graft function, and stably dosed immunosuppression.7 ISHLT recommends baseline assessment of graft function before conception with an ECG, echocardiogram, and coronary angiogram if not performed within the previous 6 months; right heart catheterization and biopsy may also be considered.5 Special consideration should be given to patients with rejection within the first posttransplant year, history of peripartum cardiomyopathy, advanced maternal age, comorbid factors, and nonadherence to medical care.7,10 Patients should be closely monitored for development of preeclampsia, gestational diabetes mellitus, and rejection.5 The ISHLT guidelines also recommend that preconception counseling be offered to both the patient and her partner.

Additional considerations include the lifespan of the patient, the possible need for re-transplantation, and the impact of hospitalizations or death on the life of children born under these circumstances. While the risks of donor-specific antibodies in pregnancy post–heart transplantation are unknown, the practice of some centers is to perform HLA testing for potential fathers before conception and offer counsel regarding the increased risk of allograft rejection in case of mismatch.9,11

Outcomes in Pregnancy Post–Heart Transplantation

Although pregnancy is becoming more commonplace, existing data are derived primarily from case reports, small series, and data from voluntary registries such as the National Transplantation Pregnancy Registry and the UK Transplant Pregnancy Registry.7 Across all solid organ transplants, pregnant woman seem to be at increased risk for preterm birth and hypertensive disorders of pregnancy.12 The largest study performed of pregnancy after organ transplant evaluated 1290 pregnancies in 885 female liver transplant recipients.13 Preterm birth occurred in 32% and preeclampsia was reported in 16%. Of the 1290 pregnancies, 1014 live births were recorded.13

Studies in HT recipients specifically have been limited by smaller sample sizes.4,7,14 In a report from the National Transplantation Pregnancy Registry of 60 pregnancies in 36 HT recipients, 43% developed hypertension of pregnancy, 11% developed preeclampsia, and 19% developed rejection.15 There were livebirths in 70% of pregnancies with 18% spontaneous abortions. Another single-center report of 22 pregnancies in 17 women demonstrated a live birth rate of 91%. Hypertension occurred in 13.6% and preeclampsia in 13.6% of the population.4 The most recent report of 18 pregnancies in 8 patients importantly noted that 56% of pregnancies post–heart transplant were unplanned and there were complications including 15% with preeclampsia, 38.5% with hypertension, and 15.4% with diabetes mellitus9 though long-term survival and graft function were not affected.

A recent systematic review and meta-analysis of 385 pregnancies in 272 cardiothoracic transplant recipients, included 220 pregnancies were in 140 heart transplant patients. Mean transplant-to-pregnancy interval was 81.4 months for heart transplant recipients with average maternal age of 28 years.16 Among heart transplant recipients, there were no maternal deaths during pregnancy and 2/203 deaths within 1 year of delivery.16 Graft rejection during pregnancy was the highest for heart-lung transplant recipients (11%) and the lowest for heart transplant recipients (9.4%).17

Despite some centers’ reluctance surrounding pregnancy after transplant, they must be prepared in case of unintended pregnancies. Approximately half of all pregnancies are unintended, and this has also been shown in the transplant population despite recommendations for preconception counseling.9,18

Multiple characteristics including respondent sex, age, specialty, volume of transplant center, and prior experience with pregnancy were not predictors of beliefs surrounding pregnancy after HT. One might anticipate that centers with prior pregnancy experience might have supported pregnancy after transplant, though it is possible that experience with posttransplant pregnancy complications prevented respondents from encouraging future pregnancies in transplant recipients.

Knowledge Gaps

There are knowledge gaps regarding the choice of contraception post-transplantation. The ISHLT guidelines recommend against the use of combined hormonal contraception in patients with liver disease, known coronary allograft vasculopathy, hypertension, and estrogen-sensitive malignancies.5 Furthermore, HT recipients have an increased risk of venous thromboembolism particularly early after transplantation.19 While all forms of contraception are allowable in the absence of important comorbidities,20 immunosuppression can result in an increased rate of hypertension, hyperlipidemia, and diabetes mellitus, which may impact the choice of contraception. In patients with complicated transplants (ie, history of graft failure or rejection), IUD may be preferred given that combined estrogen and progesterone therapies can increase overall cardiovascular risk.20 In our study, IUD was the most commonly prescribed form of contraception, but combined hormonal contraception was still recommended in 40% of cases; it would be essential to ensure that patients met no contraindications before initiation.

Potential contraindications to pregnancy are also an area for education. Fifteen percent of respondents did not select LV dysfunction as a contraindication despite the American Society of Transplantation Guidelines indicating that transplant recipients planning pregnancy should have stable and adequate graft function.

There are also significant knowledge gaps regarding the ideal immunosuppressive regimens and surveillance during pregnancy. Tacrolimus and cyclosporine are considered safe in pregnancy though the pharmacokinetics change, affecting the interpretation of whole blood levels.21 ISHLT guidelines recommend continuing calcineurin inhibitors and corticosteroids but avoiding mycophenolate mofetil (MMF) given higher incidence of structural malformations.5,22 In fact, MMF is included in a Risk Evaluation and Mitigation Strategies programs through the US Food and Drug Administration to reduce the risk of teratogenicity associated with mycophenolate use during pregnancy.23 These programs were initiated to ensure that healthcare providers and patients are educated about the risks associated with pregnancy. Nonetheless, 2 respondents to our survey recommended MMF highlighting the need for broader education about this topic. This knowledge gap could be remedied by multicenter collaborations and guidelines aimed at uniform pregnancy management.

A significant proportion of respondents felt that breastfeeding was absolutely contraindicated post-transplantation. However, an analysis of the National Transplant Registry indicates that in 2012, breastfeeding occurred in 36% of births after solid-organ transplants,24 up from 18% in 2007.24 Furthermore, the LactMed database indicates that commonly used posttransplant medications (prednisone, tacrolimus, mycophenolate mofetil, aspirin, statin) are deemed safe in breastfeeding.25 This is another area of opportunity to educate transplant providers on the safety and benefits of breastfeeding in transplant recipients.

These knowledge gaps demonstrate the need for increased education. This could lead to center-specific policies, supported by guidelines, outlining indications and contraindications to posttransplant pregnancy as well as recommended preconception planning, immunosuppressive regimens in pregnancy, plan for graft surveillance, and peripartum management. Such policies would benefit patients and providers by offering clear expectations and protocols.

Limitations

The survey was subject to voluntary response and leading question biases as has been reported with similar questionnaire studies. However, we provided free-text options wherever indicated to reduce this bias.

In addition, our response rate was low and, therefore, the responses may not be representative of transplant providers nationally. A higher response rate would have allowed greater generalizability and applicability of our responses but the survey was anonymous both to encourage respondents to participate and as stipulated by our Institutional Review Board. We presume that those who were motivated to respond were also those most interested and well versed in posttransplant pregnancy. We realize that the response population may be different than the general advanced heart failure physician population, especially as 48% of the respondents were women; however, this also included advanced practice providers as well as transplant coordinators. Still, a significant proportion of this motivated group of respondents exhibited knowledge gaps in the absence of center-specific policies, preconception planning, and peripartum immunosuppression and graft surveillance. Thus, the survey results, despite the low response rate, still illustrate the importance of increased education across disciplines and center-specific policies.

Furthermore, although respondents were asked to report the number of transplants performed annually, they were not asked to identify their center affiliation. Therefore, it is possible that some individuals were from the same center, which could skew responses regarding institutional policies, though the direction of this impact cannot be presumed.

In determining predictors of responses, it is possible that the sample size was too small to detect the effects given the wide CIs of the odds ratios. Nonetheless, even if not widely generalizable, the responses of motivated providers offer valuable insight into posttransplant pregnancy attitudes and practices and highlight the need for further study of attitudes and practices regarding posttransplant pregnancy.

Conclusions

Transplant providers’ attitudes regarding posttransplant pregnancy vary widely. Despite ISHLT guidelines, a significant proportion indicates pregnancy is contraindicated in all recipients, and the majority of programs have no center-specific policy to manage such pregnancies. Knowledge gaps exist, particularly in the feasibility of pregnancy, the choice of contraception, the safety of breastfeeding, and optimal immunosuppressive regimens and cardiac surveillance during pregnancy. This survey highlights the opportunity for education, research, and standardization of policies regarding posttransplant pregnancy to offer the best care to heart transplant recipients of childbearing age.

Nonstandard Abbreviations and Acronyms

HT

heart transplantation
ISHLT

International Society for Heart and Lung Transplantation

Footnotes

For Sources of Funding and Disclosures, see page 8.

The Data Supplement is available at https://www.ahajournals.org/doi/suppl/10.1161/CIRCHEARTFAILURE.119.006811.

Correspondence to: Michelle M. Kittleson, MD, PhD, Division of Cardiology, Smidt Heart Institute, Cedars-Sinai Medical Center, 8536 Wilshire Blvd, Suite 301, Los Angeles, California 90211. Email

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