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Keywords:

  • cancer;
  • oncology;
  • pregnancy;
  • distress;
  • long-term;
  • Cancer and Pregnancy Registry

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Background: Cancer occurs during one in 1000–5000 of the approximately 6 million yearly US pregnancies identified by the American Pregnancy Association. Although a newly diagnosed cancer is associated with substantial distress, little is known about cancer's emotional impact on women when diagnosed during pregnancy, and no studies have been conducted on the subject.

Objective: The Cancer and Pregnancy Registry was developed by Elyce H. Cardonick MD, specialist in Maternal and Fetal Medicine and Associate Professor of Obstetrics and Gynecology at Robert Wood Johnson Medical School, to examine the consequences of maternal cancer diagnosis and treatment during pregnancy on maternal, fetal, and neonatal outcomes, including the impact of in utero exposure to chemotherapy.

Methods: Participants were asked to complete questionnaires, including measures of psychological distress, permitting the examination of variables associated with long-term psychological distress in women following a cancer diagnosis in pregnancy.

Results: Seventy-four women completed the Brief Symptom Inventory-18 and Impact of Event Scale on average 3.8 years (SD 2.5) following their cancer diagnosis. Potential variables related to distress included information on: sociodemographics, disease, pregnancy, birth, cancer treatment, and health status. Multiple regression analyses revealed that women were at higher risk of long-term distress if they had not received fertility assistance, had been advised to terminate the pregnancy, had had a preterm baby, had had a cesarean delivery, had not produced sufficient milk to breastfeed, had been experiencing a recurrence, and/or had undergone surgery post-pregnancy.

Conclusion: Results are discussed in light of our current knowledge of the normal developmental phase of pregnancy and motherhood. Copyright © 2011 John Wiley & Sons, Ltd.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Cancer reportedly occurs in one in 1000–5000 of the approximately 6 million yearly US pregnancies identified by the American Pregnancy Association [1]. Most prevalent cancers diagnosed during pregnancy include breast cancer, cervical cancer, lymphoma, and melanoma [2]. While a cancer diagnosis is already fraught with distress [3, 4] and can exacerbate pregnancy-related challenges (e.g. fear of childbirth, anticipatory anxiety, nausea, fatigue) [5], little is known about the emotional toll of a cancer diagnosed during pregnancy, and no studies have been conducted on the subject [6–9]. The existing literature consists mostly of case studies or descriptions of the experience [1, 7–9]. The dearth of research on the topic may be explained by the infrequency of the event, which renders study recruitment challenging and necessitates the creation of nationwide registries to collect sufficient data for analysis.

The Cancer and Pregnancy Registry [10] was created in 1997 by Elyce H. Cardonick MD, specialist in Maternal & Fetal Medicine and Associate Professor of Obstetrics and Gynecology at Robert Wood Johnson Medical School, and includes a total of 231 women diagnosed with cancer during pregnancy. Patients enrolled voluntarily from various institutions internationally between August 1, 1995, and September 1, 2008, comprising a sufficient pool of participants to study. The majority of patients called the registry themselves after learning from the Internet or their physicians. Other patients had their physicians make the initial contact and then agreed to contact the registry to complete enrolment forms. The primary purpose of the registry was to examine the consequences of a maternal cancer diagnosis and treatment during pregnancy on maternal, fetal, and neonatal outcomes, including the impact of in utero exposure to chemotherapy [2, 11]. Following Institutional Review Board approval, the women in the registry completed a battery of questionnaires including psychological measures. The purpose of the current study is to explore variables associated with long-term psychological distress in women following a cancer diagnosed during pregnancy. Early identification of women at risk of experiencing enduring distress can orient preventive psychosocial efforts to enhance quality of life in this vulnerable population.

Methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Design

Women were eligible to enroll in the registry if their cancer was diagnosed between their last menstrual period and delivery, miscarriage, or termination. There were no other participant inclusion/exclusion criteria in this study. Women joined the database by voluntarily contacting the registry. Data for the registry were collected via medical chart review, physician input, and self-administered questionnaires. It includes details of pregnancy outcomes, treatment received during pregnancy, follow-up after delivery over several years, and several self-administered psychological measures, including the Impact of Event Scale (IES) and the Brief Symptom Inventory-18 (BSI-18) questionnaires.

Measures

The IES [12, 13] is a self-administered, 22-item questionnaire measuring subjective distress following a stressful event. It comprises three subscales: intrusion, avoidance, and hyperarousal. The scale has adequate internal consistency (Cronbach's α = 0.82–0.86), test–retest reliability (0.79–0.87), and convergent validity. An overall score of 19 or above indicates clinically significant stress responses.

The BSI-18 [14–16] is a self-administered, 18-item, brief screening inventory measuring levels of distress in three subscales: anxiety, depression, and somatization. This abbreviated measure of the BSI has psychometric properties similar to those of the original instrument. A score of 63 or above on this scale is considered clinically significant.

The following variables were also collected through self-administered questionnaires and chart reviews and were considered to be potentially related to distress based on their clinical relevance. Data collected through self-administered questionnaires included: sociodemographic data: age upon cancer diagnosis; if the woman had other children before cancer was diagnosed. Data collected through chart reviews comprised the following five categories. Cancer-related information: Time elapsed from cancer diagnosis to survey completion; cancer site; cancer was a first occurrence or a recurrence (i.e. patient was diagnosed with cancer prior to pregnancy and then experienced a recurrence—local or systemic—during pregnancy); cancer stage (I–IV); family history of cancer; BRCA testing; experienced recurrence following birth. Pregnancy information: Received fertility assistance to conceive; cancer was diagnosed (or recurred) before or during pregnancy; gestational age upon diagnosis; doctor advised termination of the pregnancy. Birth information: Stem cell saved; birth complications and defects; mode of delivery (vaginal, cesarean, other); had twins; 1 and 5 min Apgar scores; baby weighed <10%; baby delivered preterm (<37 gestational weeks); extended hospital stay; did not have enough milk production to breastfeed. Cancer treatment information: Received treatment (surgery, chemotherapy, and/or radiation) during/post-pregnancy. Health status: Health of mother and child at time of questionnaire completion (including medical conditions and cancer recurrence).

Data analysis

Data were analyzed using the Statistical Program for the Social Sciences (SPSS), version 18.0. Kolmogorov–Smirnov goodness of fit tests were run for the IES and BSI-18 to assess the normality of the distributions. Independent samples t-tests and ANOVAs (for categorical independent variables) and two-tailed Pearson correlations (for continuous independent variables) were computed to determine associations between level of distress (as measured by the BSI-18 and IES) and the above-mentioned variables. Multiple linear regressions were performed, including all patients who completed the IES and BSI-18 and significant variables and trends from the exploratory analyses. Dummy variables were created for the only categorical variable with more than two levels: experienced a recurrence since pregnancy (no recurrence, recurrence more than 1 year ago, recurrence currently (within 1 month of questionnaire completion)).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

Sample

Seventy-four women completed the IES and BSI-18 on average 3.8 years (SD = 2.5) following their cancer diagnosis. Table 1 summarizes sociodemographic, disease, pregnancy, birth, and cancer treatment characteristics of these women.

Table 1. Distress levels, sociodemographic and medical characteristics of women diagnosed with cancer during pregnancy
CharacteristicsMean (SD)n (%)
  • a

    One woman was pregnant 4 weeks before being diagnosed with cancer. She was included in the study as the discovery of her pregnancy coincided with her being diagnosed with cancer.

  • b

    Major birth defects (3 of 70 or 4.3%) were a rare event, albeit higher than the expected rate of 3% identified in the general population [17]. Birth defects included syndactyly, pulmonary artery fistula, and spina bifida.

  • c

    For the purpose of analyzing the relationship between levels of distress and mode of delivery, delivery using forceps was considered a vaginal delivery as it was a rare event with a n of 1.

  • d

    Although half the women had their babies preterm (37 of 72 or 51.4%), with a mean gestational age of 36.4 weeks (SD 3.1), this reflects a tendency to induce delivery at approximately 36–37 weeks if additional cancer therapy is indicated postpartum.

  • e

    Medical conditions included: asthma and mild gastric reflux in the first child; warts on foot, possible dyslexia (suspected by mother), otitis media and reactive airway disease in the second; and mild expressive speech delay in the third. All initial birth complications resolved, as they represented neonatal issues.

Impact of Event Scale (IES)20.4 (16.6) 
 Clinically significant distress (IES>19) 34/66 (51.5)
Brief Symptom Inventory-18 (BSI-18)52.3 (11.4) 
 Clinically significant distress (BSI-18>63) 14/67 (20.9)
Time elapsed from cancer diagnosis to survey completion (years)3.8 (2.5) 
 1 8/67 (11.9)
 2 15/67 (22.4)
 3 20/67 (29.9)
 4 5/67 (7.5)
 5+ 19/67 (28.4)
Age upon cancer diagnosis34.2 (4.5) 
Cancer site
 Breast 48/74 (64.9)
 Hodgkin's lymphoma 8/74 (10.8)
 Ovarian 4/74 (5.4)
 Melanoma 4/74 (5.4)
 Other 10/74 (13.5)
Cancer stage upon diagnosis
 I 18/71 (25.4)
 II 37/71 (52.1)
 III 10/71 (14.1)
 IV 6/71 (8.5)
Cancer trajectory
 First occurrence 69/73 (94.5)
 Recurrence 4/73 (5.5)
Cancer was first diagnosed during pregnancya 73/74 (98.6)
Gestational age when cancer was diagnosed (weeks)14.7 (8.4) 
Anti-cancer treatment during pregnancy
 Surgery 53/72 (73.6)
 Chemotherapy 59/73 (80.8)
 Radiotherapy 1/72 (1.4)
Surgery after pregnancy 26/72 (36.1)
 With cancer recurrence 5/26 (19.2)
Had other children before pregnancy 48/73 (65.8)
Received fertility assistance 10/73 (13.7)
Doctor advised to terminate pregnancy 19/73 (26.0)
Had birth complications 14/72 (19.4)
Baby had birth defectb 3/70 (4.3)
Fetal or infant death 0
Mode of deliveryc
 Vaginal 44/71 (62.0)
 Cesarean 26/71 (36.6)
 Forceps 1/71 (1.4)
Had twins 3/72 (4.2)
Apgar score (min)
 17.9 (1.6) 
 58.9 (0.8) 
 108.0 (1.0) 
Weight (g) 2757.94 (652.9)
Weight <10% 2/72 (2.8)
Termd 35/72 (48.6)
Gestational age at delivery (weeks)36.4 (3.1) 
Tried breastfeeding 31/72 (43.1)
Had enough milk production to breastfeed 21/72 (29.2)
Experienced recurrence since birth 12/74 (16.2)
 Time elapsed from birth to recurrence (months)18.5 (13.7) 
Experienced recurrence upon questionnaire completion 4/74 (5.4)
Child presenting with medical condition upon questionnaire completione 3/74 (4.1)

Variables related to level of distress

Scores on the IES and BSI-18 were distributed normally. On average, women experienced high levels of distress on the IES (x = 20.4, SD = 16.6) and on the BSI-18 (mean = 52.3, SD = 11.4), with 51.5 and 20.9% experiencing clinically significant levels of distress, respectively. On the IES, distress was mostly expressed through intrusive thoughts (mean = 11.0, SD = 8.8) rather than avoidance (mean = 8.6, SD = 8.6) or hyperarousal (mean = 0.80, SD = 2.73), [t(64) = 2.85, p = 0.006 and t(64) = −9.34, p = 0.001]. On the BSI-18, it was mostly due to anxiety (mean = 52.7, SD = 11.8) and somatization (mean = 53.0, SD = 12.7), [t(66) = 0.27, p = 0.79], rather than depression (mean = 49.0, SD = 11.9), [t(66) = 3.4, p = 0.001 and t(66) = 3.7, p = 0.001, respectively].

Multiple linear regression analyses revealed that women were at higher risk of long-term distress on the IES if they: had not received fertility assistance [adjusted β = 0.26, p = 0.02], had been advised to terminate the pregnancy [adjusted β = 0.27, p = 0.02], had had a preterm baby [adjusted β = 0.34, p = 0.005], or had undergone surgery post-pregnancy [adjusted β = 0.28, p = 0.01]. Together, these variables explained 24% of the variance in scores on the IES [R2 adjusted = 0.24]. Women scored higher on the BSI-18 if they: had had a cesarean delivery (trend) [adjusted β = 0.23, p = 0.06], had not had a baby weighing <10% (trend) [adjusted β = 0.23, p = 0.05], had not produced sufficient milk to breastfeed [adjusted β = 0.29, p = 0.02], or were currently experiencing a recurrence [adjusted β = 0.26, p = 0.03]. Together, these variables explained 18% of the variance in scores on the BSI-18 [R2 adjusted = 0.18]. Table 2 details the levels of distress associated with the above-mentioned variables and those of the exploratory analyses.

Table 2. Variables related to scores on the Impact of Event Scale (IES) and the Brief Symptom Inventory-18 (BSI-18) in women diagnosed with cancer during pregnancy
 Mean (SD) 
VariablesYesNot
  • Bold scores indicate significantly higher levels of distress.

  • *

    p<0.05; 1 = trend.

Impact of Event Scale (IES)
 Received fertility assistance9.9 (11.2)22.3 (16.7)2.25*
 Advised to terminate the pregnancy26.1 (18.1)18.5 (15.8)−1.611
 Underwent surgery during pregnancy18.5 (16.6)25.9 (15.6)1.611
 Baby born preterm24.8 (16.6)15.8 (15.5)−2.25*
 Had enough milk production to breastfeed15.3 (16.3)22.5 (16.4)1.611
 Underwent surgery post-pregnancy25.7 (17.7)16.9 (15.0)−2.18*
 Experienced a cancer recurrence27.2 (16.9)18.7 (16.2)−1.691
Brief Symptom Inventory-18 (BSI-18)
 Had a cesarean delivery56.1 (12.3)50.4 (10.5)−1.951
 Baby born preterm55.0 (12.6)50.2 (9.5)−1.731
 Baby weighed <10%37.5 (6.4)53.1 (11.2)1.961
 Produced sufficient milk to breastfeed48.5 (10.4)54.2 (11.4)1.851
 Experienced a cancer recurrence (currently)62.0 (9.8)51.7 (11.3)−1.691

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References

As defined by the National Comprehensive Cancer Network (NCCN): ‘Distress is a multifactorial unpleasant emotional experience of a psychological (cognitive, behavioral, emotional), social, and/or spiritual nature that may interfere with the ability to cope effectively with cancer, its physical symptoms and its treatment. Distress extends along a continuum, ranging from common normal feelings of vulnerability, sadness, and fears to problems that can become disabling, such as depression, anxiety, panic, social isolation, and existential and spiritual crisis’ [17].

When patients are diagnosed with cancer during pregnancy, feelings of hopelessness and fear of death can be intertwined with the joy and normal stresses of becoming a mother. Recognizing early signs of distress in such women is essential, allowing referral to needed psychosocial services. This is especially important in light of the association between maternal exposure to stressful situations during pregnancy and adverse outcomes such as preterm birth, low birth weight, and neurodevelopmental impairments and disabilities [18]. Distress during pregnancy is also known to affect mother–infant attachment, with its important impact on child development and maternal identity [19].

On average, women who participated in the Cancer and Pregnancy Registry demonstrated clinically significant levels of distress on the IES and BSI-18 questionnaires, suggesting the long-standing impact of cancer diagnosed during pregnancy. The number of patients identified as clinically distressed (up to 51.5%) is higher than the 33% found in breast cancer patients (the main cancer site of women in the registry) upon diagnosis and higher than the 15% found 1 year post-diagnosis in Burgess et al.'s 2005 study [20]. Pregnant women may be particularly disposed to react with high levels of distress when diagnosed with cancer, as the disease is especially distressing for young adults [21, 22], and pregnancy can already be a challenging experience [23].

Our study suggests that women were at higher risk of experiencing long-term distress if (i) they had not received fertility assistance to conceive in the pregnancy in which they were diagnosed with cancer, (ii) they had been advised to terminate their pregnancy, (iii) they had undergone a cesarean delivery, (iv) they had had a preterm baby, (v) they had not produced enough milk to breastfeed, (vi) they were currently experiencing a recurrence, and/or (vii) they had undergone surgery post-pregnancy.

The association of an increased level of distress with breastfeeding difficulties and preterm birth underlines the issue of directionality. On one hand, decreased milk production resulting from exposure to chemotherapy [11] could increase the levels of distress in women wishing to breastfeed, given that breastfeeding is promoted as the safest and healthiest choice for mother and baby, and that breastfeeding difficulties can lead to feelings of guilt and failure at not being able to adequately provide for, or emotionally bond with, baby [24–26]. In addition, having a preterm baby has been associated with elevated stress and increased risk for depression [27]. On the other hand, baseline levels of distress could have resulted in the preterm birth [17], deceased milk production [28], or decreased motivation to breastfeed [29, 30].

Despite that termination of pregnancy has not been shown to improve prognosis or survival of pregnant women with breast cancer [31] and that chemotherapy can be relatively safe, especially during the second and third trimester [32], some women had still been advised to terminate their pregnancy when diagnosed with cancer. Deciding to continue a pregnancy against medical advice can be a particularly stressful choice [33, 34], highlighting the importance of shared decision-making, patient-centered communication, and continued physician support [35].

An increased level of distress has already been found in women having undergone a cesarean section at the term of a normal, non-cancer-related pregnancy [36]. A cesarean delivery requires a longer recovery period than a vaginal delivery, and women foresee a more difficult time caring for their home and child/ren post-cesarean [37]. Undergoing surgery post-pregnancy may increase levels of distress for similar reasons. Furthermore, when the surgery is motivated by a cancer recurrence, the fear of uncontrollable disease and mortality may reappear, increasing psychological distress [38]. As such, 45% of women experiencing a recurrence of breast cancer manifested depression and/or anxiety within 3 months post-diagnosis in Burgess et al.'s 2005 study [20].

The analyses showed an increased level of distress in women who did not use fertility assistance. While fertility treatments are generally associated with an increase in psychological and marital distress, this distress usually resolves with time after the birth of a healthy child [39]. Women who have had fertility treatments may fare better than others following a cancer diagnosis, as their fertility experience may have accentuated the central meaning attached to childrearing in their lives [40]. Moreover, attending fertility clinics may have provided extra opportunities for receiving counseling and support [41].

This study constitutes a significant contribution to the literature by identifying variables associated with a high level of long-term distress following a cancer diagnosed in pregnancy. However, several limitations are noteworthy. First, this study includes a small sample size due to the infrequent occurrence of cancer during pregnancy. However, the Cancer and Pregnancy Registry is the first initiative allowing recruitment of a sufficient number of women for an initial study of factors associated with elevated distress. Second, we lack information on initial distress levels upon diagnosis. Third, time elapsed between diagnosis and questionnaire completion differed among women in the registry, with its associated recall bias due to the occurrence of events in past years. However, we did not find an association between time and distress levels in our sample. Finally, there could have been a selection bias related to participants self-referring into the registry. It is possible that women with the highest levels of distress were increasingly motivated to share their stories through participating in this study, whereas others might have preferred to avoid any reminder of their cancer. It is also possible that the participants were those with a better prognosis from the start, as they had survived long enough to participate in the study. These limitations restrict the generalizability of our findings, which may not be representative of all women diagnosed with cancer during pregnancy.

In summary, some women may be at particular risk of experiencing high levels of long-term distress when diagnosed with cancer during pregnancy. While awaiting future prospective studies, physicians can pay particular attention to these possible markers of distress as indicative of a need for referral to psychological supports. The finding that patients who survived for four years experienced anxiety and distress is important and deserves further attention and clinical interventions.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Methods
  5. Results
  6. Discussion
  7. References
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