Abstract
Background:
Individuals with cancer during pregnancy are a medically complex patient population that is anticipated to grow. A better understanding of this population and patterns of risk at time of delivery offers an opportunity for providers to mitigate maternal morbidity.
Objective:
To estimate the prevalence in the United States of concurrent cancer diagnoses at time of delivery by cancer type and associated maternal morbidity and mortality.
Methods:
Using the National Inpatient Sample, we identified delivery-associated hospitalizations between 2007–2018. Concurrent cancer diagnoses were classified using Clinical Classification Software developed by the Healthcare Cost and Utilization Project. Main outcomes included severe maternal morbidity as defined by The Centers for Disease Control and Prevention indicators and mortality during delivery hospitalization. We calculated adjusted rates for cancer diagnosis at time of delivery and adjusted odds ratios (aOR) of severe maternal morbidity and maternal death during hospitalization using survey weighted multivariable logistic regression models.
Results:
In this sample of 9,418,761 delivery-associated hospitalizations, 63 per 100,000 deliveries had a concurrent cancer diagnosis (95% confidence intervals [CI] 60–66; national weighted estimate 46,654,042). The most common cancer types were breast (8.4 per 100,000 deliveries), leukemia (8.4 per 100,000 deliveries), Hodgkin’s lymphoma (7.4 per 100,000 deliveries), non-Hodgkin’s lymphoma (5.4 per 100,000 deliveries), and thyroid cancer (4.0 per 100,000 deliveries). Patients with cancer were at significantly higher risk for any severe maternal morbidity (aOR 5.25, 95% CI 4.73, 5.83) and maternal death (aOR 67.5, 95% CI 45.1, 101.4). Risk of hysterectomy (aOR 16.92, 95% CI 13.96, 20.52), acute respiratory distress (aOR 12.76, 95% CI 9.92, 16.42), sepsis (aOR 11.91, 95% CI 8.68, 16.32), and embolism (aOR 11.12, 95% CI 6.94, 17.82) were particularly heightened among patients with cancer. Patients with leukemia, specifically, had the highest risk of adverse maternal outcomes (adjusted rate 113 per 1,000 deliveries, 95% 91–135 per 1,000) when evaluating risk by cancer type.
Conclusions:
Patients with cancer are at a significantly increased risk of maternal morbidity and all-cause mortality during delivery-associated hospitalization. Risk was distributed unevenly within this population, with certain cancer types carrying unique risks for specific morbidity events.
Keywords: Cancer, pregnancy, maternal morbidity, maternal mortality, leukemia, epidemiology
Tweetable abstract:
Concurrent cancer diagnosis at time of delivery is linked to markedly increased risk of severe maternal morbidity and mortality, with different cancer types related to distinct adverse events.
INTRODUCTION
Patients with cancer in pregnancy are a medically complex group that is anticipated to grow as individuals with cancer live longer and as child-bearing is deferred to later in life.1–3 Much of current guidance regarding how to best care for these patients during pregnancy focuses on prenatal care considerations and care coordination between obstetrician and oncologists throughout gestation.4 However, information about the risks these patients face at time of delivery is scarce.
As maternal morbidity and mortality continues to be a critical public health concern, it is imperative to better understand populations that are at unique risk.5, 6 Severe maternal morbidity encompasses a variety of complications or procedures around time of delivery that can result in long-term health implications. Studies leveraging data from cancer-based registries have demonstrated an increased risk of adverse pregnancy outcomes, such as preterm birth and postpartum hemorrhage, among cancer survivors.7, 8 However, little is known about specific risks to patients who carry a cancer diagnosis at time of delivery. It is reasonable to believe that conditions often coexisting with cancer due to the nature of the malignancy or the sequalae of treatment, such as hypercoagulability, poor tissue healing, or immunocompromise, predispose patients for adverse outcomes. A more specific elucidation of risks could help provide a guide when counseling these patients in pregnancy and caring for them at time of delivery.
The National Inpatient Sample provides a rich resource for understanding risk among patient populations with conditions of rare incidence, such as pregnant patients with cancer. The objective of this study is to leverage this resource to provide a more precise estimate of cancer prevalence at time of delivery and to understand the most common cancers represented in this population. Further, we aim to quantify the association between concurrent cancer diagnosis at time of delivery and risk of severe maternal morbidity and mortality, with a secondary objective of detecting risks that were unique to specific cancer types.
METHODS
We identified delivery-associated hospitalizations within the National (Nationwide) Inpatient Sample (NIS) to perform a population-based retrospective cohort study.9 The NIS is a product of the Healthcare Cost and Utilization Project and is the largest publicly available, all-payer inpatient database in the United States. It is a stratified sample of 20% of all inpatient hospitalizations in the country. The database was designed such that estimates calculated using survey-weighted methods produce nationally representative estimates. Delivery associated hospitalizations were identified using ICD procedure codes indicating vaginal or C-section delivery. Our sample includes hospitalizations for deliveries between January 2007 and December 2018. Because the NIS is a Limited Data Set as defined by the Health Insurance Portability and Accountability Act, this study was considered exempt from review by the Duke Health Institutional Review Board (Pro00106911).
International Classification of Disease (ICD) diagnosis codes during delivery hospitalizations were used to identify cancer diagnoses, maternal morbidity events, and death. Cancer diagnoses were classified using Clinical Classification Software (CCS) developed by the Healthcare Cost and Utilization Project. The categories used to define cancers became more granular with adoption of ICD-10th edition in October 2015. Therefore, we retained use of ICD-9 era clinical classifications to categorize cancer diagnoses for consistency and performed a comparison of ICD-9 and ICD-10 era codes to confirm consistent categorization across ICD eras (Appendix A). We excluded diagnoses that described a history of cancer to focus our analysis on current cancer diagnoses at time of delivery hospitalization. We also limited the definition of cervical cancer from that used in CCS to cases of confirmed malignant neoplasm of the cervix by excluding diagnoses of carcinoma in situ or abnormal pap smears. Measures of maternal morbidity were based on the Centers for Disease Control and Prevention (CDC) criteria.10, 11 We defined maternal mortality as documentation of maternal death during delivery hospitalization.
All analyses were performed using statistical methods that accommodate the stratified and weighted natures of the NIS data. We calculated weighted estimates of cancer cases per 100,000 deliveries for any cancer diagnosis at time of delivery and by cancer type. We examined the association between patient characteristics and maternal cancer using both unadjusted and adjusted weighted logistic regression models. Next, we quantified the association between cancer diagnosis at time of delivery hospitalization and maternal morbidity and mortality. We quantified risk estimates for the presence of any cancer diagnosis and for the five most prevalent cancer types. Severe maternal morbidity during delivery hospitalization was evaluated as the presence of any CDC-defined indicators: acute myocardial infarction, aneurysm, acute renal failure, acute respiratory distress syndrome, amniotic fluid embolism, cardiac arrest/ventricular fibrillation, conversion of cardiac rhythm, disseminated intravascular coagulation, eclampsia, heart failure, puerperal cerebrovascular disorders, pulmonary edema/acute heart failure, severe anesthesia complications, sepsis, shock, sickle cell disease with crisis, air and thrombotic embolism, blood products transfusion, hysterectomy, temporary tracheostomy, ventilation. Given blood products transfusion alone has been thought to not represent the same level of maternal morbidity as other CDC indicators, the analysis was repeated when excluding the transfusion of blood products from the definition of severe maternal morbidity.12 The association between maternal cancer and individual CDC indicators of maternal morbidity were estimated for events that occurred in at least 1 in 1,000 delivery-associated hospitalizations among patients with cancer. Post-estimation commands were used to calculate weighted estimates of event rate per 1,000 deliveries for individuals with and without cancer.
Adjusted models included potential confounders selected a priori using directed acyclic graphs. Directed acyclic graphs are used to depict the suspected relationships between an exposure, outcome, and potentially related variables to inform which set of covariates to include in an adjusted model to minimize risk of bias in calculated estimates (Appendix B). We tested for effect modification of the association between cancer diagnosis at time of hospitalization and severe maternal morbidity and mortality by mode of delivery using the likelihood ratio test for the inclusion of interaction terms. A two-sided alpha level of 0.05 was prespecified to determine statistical significance. All analyses were completed in Stata statistical software (Version 17.0, Stata-corp, College Station, TX).
RESULTS
We identified 9,418,761 delivery-associated hospitalizations in the National Inpatient Sample between 2007 and 2018 (weighted national estimate of 46,654,042 deliveries). A cancer diagnosis was present in a weighted estimate of 63 per 100,000 deliveries (95% confidence interval [CI] 60–66 per 100,000). Risk of cancer increased steadily with maternal age (adjusted odds ratio [aOR] 1.05 per year, 95% CI 1.04–1.06) and was more common among patients of White and Black race compared to those of Asian and Hispanic race (Table 1). The most common cancer types were breast (8.4 per 100,000 deliveries), leukemia (8.4 per 100,000 deliveries), Hodgkin’s lymphoma (7.4 per 100,000 deliveries), Non-Hodgkin’s lymphoma (5.4 per 100,000 deliveries), and thyroid cancer (4.0 per 100,000 deliveries, Figure 1), with hematologic cancers being the most common cancer type among younger patients and breast cancer becoming increasingly more prevalent with increasing maternal age (Figure 2).
Table 1.
Maternal demographics and concurrent cancer diagnosis at delivery, nationally weighted estimates (weighted N=46,623,832)
| With Cancer n (%) N=5,927 Weighted N=29,511 | Without Cancer n (%) N=9,418,761 Weighted N=46,654,042 | Adjusted Rate per 100,000 (95% CI)a | aOR (95% CI) | |
|---|---|---|---|---|
| Maternal age, years | ||||
| <20 | 1,279 (4.3) | 3,603,623 (7.8) | 35 (30, 41) | Referentb |
| 20–24 | 5,327 (18.2) | 10,491,423 (22.5) | 51 (45, 56) | 1.43 (1.25, 1.65) |
| 25–29 | 7,508 (25.5) | 13,284,887 (28.5) | 56 (53, 60) | 1.59 (1.37, 1.86) |
| 30–34 | 8,444 (28.5) | 11,979,886 (25.7) | 70 (67, 75) | 2.01 (1.72, 2.35) |
| 35–39 | 5,183 (17.6) | 5,885,582 (12.6) | 89 (84, 95) | 2.53 (2.15, 2.96) |
| 40–44 | 1,615 (5.4) | 1,275,610 (2.7) | 128 (114, 143) | 3.64 (3.02, 4.39) |
| >45 | 115 (0.4) | 103,518 (0.2) | 113 (67, 160) | 3.20 (2.06. 4.96) |
| Maternal race | ||||
| White | 15,329 (52.0) | 21,872,532 (46.9) | 69 (65, 72) | Referentc |
| Black | 4,147 (14.1) | 6,016,204 (12.9) | 73 (65, 82) | 1.07 (0.96, 1.19) |
| Hispanic | 4,879 (16.5) | 9,053,808 (19.4) | 56 (51, 61) | 0.81 (0.74, 0.89) |
| Asian | 1,046 (3.5) | 2,332,680 (5.0) | 39 (34, 45) | 0.57 (0.49, 0.67) |
| Native American | 166 (0.6) | 336,072 (0.7) | 53 (35, 70) | 0.77 (0.55, 1.07) |
| Other | 970 (3.3) | 2,002,679 (4.3) | 48 (40, 54) | 0.69 (0.60, 0.81) |
| Not specified | 2,973 (10.1) | 5,010,556 (10.7) | 60 (54, 67) | 0.88 (0.78, 0.99) |
| Payor | ||||
| Private | 15,271 (51.8) | 23,476,078 (50.4) | 59 (56, 62) | Referentd |
| Medicaid | 12,001 (40.7) | 20,054,629 (43.1) | 68 (63,72) | 1.14 (1.07, 1.22) |
| Medicare | 679 (2.3) | 326,921 (0.7) | 191 (157, 226) | 3.24 (2.69, 3.90) |
| Self-pay | 640 (2.2) | 1,328,701 (2.9) | 51 (41,61) | 0.87 (0.72, 1.04) |
| No charge | 55 (0.2) | 65,420 (0.1) | 90 (41,138) | 1.52 (0.89, 2.61) |
| Other | 836 (2.8) | 1,299,940 (2.8) | 65 (54, 76) | 1.10 (0.93, 1.30) |
Abbreviations: aOR, adjusted odds ratio; CI, confidence interval
Adjusted cancer rate per 100,000 deliveries, rate adjusted for same covariates included in logistic regression model to yield adjusted odds ratio
Model adjusted for self-reported maternal race
Model adjusted for maternal age (continuous)
Model adjusted for maternal age (continuous) and self-reported race
Figure 1.
Prevalence of cancer at time of delivery by cancer type (weighted N=46,623,832).
Figure 2.
Cancer cases per 100,000 deliveries stratified by most common cancer type across maternal age (A) and self-reported race (B; weighted N=46,623,832).
Patients with a cancer diagnosis experience severe maternal morbidity in 78 per 1,000 deliveries compared to a weighted rate of 16 per 1,000 deliveries for patients without cancer (aOR 5.25; 95% confidence intervals [CI] 4.73, 5.83; Table 2). Maternal death during delivery hospitalization occurred in 3.68 per 1,000 deliveries among patients with cancer compared to 0.06 per 1,000 deliveries among those without (aOR 67.6; 95% CI 45.1, 101.4). Mode of delivery was an effect modifier for both maternal morbidity and mortality (p<0.01). Patients with cancer who had a C-section delivery were at higher risk of maternal morbidity than those who delivered vaginally (adjusted OR 1.62, 95% CI 1.30, 2.04) and were at an increased risk of death (adjusted OR 7.70, 95% CI 6.17, 9.62).
Table 2.
Maternal morbidity and mortality by cancer type (weighted N=46,623,832)
| Outcome | Crude OR | Adjusted ORa | Adjusted Rate per 1,000a |
|---|---|---|---|
| Any severe maternal morbidity (weighted n=743,164) | |||
| No Cancer | Referent | Referent | 16 |
| Any Cancerb | 5.36 (4.84, 5.94) | 5.25 (4.73, 5.83) | 78 |
| Breast | 2.86 (1.04, 4.01) | 2.70 (1.92, 3.79) | 42 |
| Leukemia | 7.97 (6.39, 9.94) | 7.96 (6.36, 9.95) | 113 |
| Hodgkin’s lymphoma | 2.61 (1.80, 3.79) | 2.69 (1.85, 3.92) | 42 |
| Non-Hodgkin’s lymphoma | 4.91 (3.50, 6.89) | 4.62 (3.29, 6.49) | 69 |
| Thyroid | 1.87 (1.03, 3.42) | 1.89 (1.04, 3.46) | 30 |
| Any severe maternal morbidity-No transfusion (weighted n=303,054) | |||
| No Cancer | Referent | Referent | 6.5 |
| Any Cancerb | 8.09 (7.17, 9.15) | 7.50 (6.63, 8.48) | 46 |
| Breast | 4.02 (2.59, 6.26) | 3.28 (2.10, 5.10) | 21 |
| Leukemia | 9.16 (6.71, 12.50) | 8.77 (6.41, 12.01) | 54 |
| Hodgkin’s lymphoma | 3.45 (2.08, 5.74) | 3.33 (2.00, 5.54) | 21 |
| Non-Hodgkin’s lymphoma | 7.60 (5.07, 11.39) | 6.58 (4.38, 9.90) | 41 |
| Thyroid | 2.06 (0.85, 4.98) | 1.92 (0.79, 4.66) | 12 |
| Maternal Death (weighted n=2,675) | |||
| No Cancer | Referent | Referent | 0.06 |
| Any Cancerb | 76.2 (51.0, 114.1) | 67.6 (45.1, 101.4) | 3.6 |
| Breast | 46.7 (11.6, 187.6) | 32.4 (8.01, 131.25) | 1.7 |
| Leukemia | 69.6 (22.3, 216.5) | 66.1 (21.2, 206.2) | 3.6 |
| Hodgkin’s lymphoma | - | - | - |
| Non-Hodgkin’s lymphoma | 72.2 (17.9, 291.0) | 56.3 (13.9, 227.8) | 3.0 |
| Thyroid | - | - | - |
Abbreviations: CI, confidence intervals; OR, odds ratio
Estimates are adjusted for maternal age, self-reported race, and obesity
Estimates for risk associated for any cancer derived from separate model stratifying most common cancer types
Patients with cancer were at a higher risk for all CDC indicators of maternal morbidity and had at least five times greater odds of the following: hysterectomy (aOR 16.9, 95% CI 14.0, 20.5), acute respiratory distress (aOR 12.8, 95% CI 9.9, 16.4), air or thrombotic embolism (aOR 11.1, 95% CI 6.9, 17.8), sepsis (aOR 11.9, 95% CI 8.6, 16.3), ventilation (aOR 11.2, 95% CI 6.0, 20.9); cardiac arrest (aOR 10.9, 95% CI 7.0, 16.8), shock (aOR 8.1, 95% CI 5.5, 12.1), and acute renal failure (aOR 6.9, 95% CI 4.9, 9.6; Figure 3). Certain cancer types carried unique risk for specific maternal morbidity indicators (Figure 4). For example, individuals with cervical cancer were much more likely to have a hysterectomy at time of delivery compared to patients with other cancer types. The adjusted rate among patients with cervical cancer was 275 per 1,000 deliveries (95% CI 225, 325), compared to patients with a different cancer type (4 per 1,000 [95% CI 3, 6]) or patients without cancer (0.9 per 1,000 deliveries [95% CI 0.9, 1.0]). Patients with leukemia had a disproportionate risk of sepsis (adjusted rate among patients with leukemia 21 per 1,000 deliveries [95% CI 11, 32], compared to patients with a different cancer type [4 per 1,000 deliveries, 95% CI 3, 6] or no cancer [0.5 per 1,000 deliveries 95% CI 0.5, 0.6]).
Figure 3.
Risk of severe maternal morbidity among patients with cancer at time of delivery compared to patients without cancer as defined by CDC indicators (weighted N=46,623,832; only includes indicators that occurred in greater than 1 in 1,000 delivery-associated hospitalizations among patients with cancer). Abbreviations: ARDS, acute respiratory distress syndrome; DIC, disseminated intravascular coagulation.
Figure 4.
Cases of severe maternal morbidity during delivery hospitalization by most common cancer types (excluding blood transfusion).
COMMENT
Principal Findings
Patients with cancer are at a strikingly increased risk of maternal morbidity and mortality during delivery hospitalization. In this national sample, hematologic cancers were the most common cancer type among younger patients, with breast cancer becoming increasingly prevalent with maternal age. While any cancer diagnosis was associated with an elevated risk of maternal morbidity and mortality, cancer types were uniquely associated with different maternal morbidity events.
Results in the Context of What is Known
This analysis aligns with other estimates of the prevalence of cancer in pregnancy.1, 3 In contrast to this analysis, other studies have found cervical cancer among the top five most common cancer types. This difference is likely due to exclusion of abnormal pap smears and cases of in situ carcinoma in our estimates.13, 14
A prior analysis identified elevated risk of severe maternal morbidity and mortality among patients with cancer.2 Our analysis furthers that work by providing prevalence estimates for the most common cancer types and elucidating the breakdown of cancer types by key maternal demographics. We also uncovered distinct relationships between specific cancer types and individual morbidity events, which provides more specific information for counseling patients about risk and understanding risks at time of delivery.
Clinical Implications
Maternal morbidity is a critical public health concern and identifying vulnerable populations can help with risk stratification when providing care.15, 16 Much of clinical guidance concerning pregnancy among patients with cancer focuses on navigating cancer treatments and their side effects during gestation. However, delivery is the time when this medically complex patient population is most vulnerable, and this analysis offers insight into the nature of morbidity incurred. Understanding patterns of risk provides an opportunity for early recognition and mitigation of adverse health events. For example, we found that women with cancer were at a much higher risk of disseminated intravascular coagulation compared to their counterparts. A heightened understanding of this risk could prompt earlier recognition and response by clinicians in the setting of excessive bleeding during a C-section or a postpartum hemorrhage following a vaginal delivery. Women with cancer were also at a notably increased risk of acute respiratory distress syndrome compared to the general population. An appreciation of this specific risk may motivate closer attention to abnormal vital signs or physical exam findings in a way that could mitigate respiratory decompensation.
Research Implications
This analysis has uncovered distinct risk associations between specific cancer types and maternal morbidity events that could be helpful in guiding further studies to better understand mechanisms of risk. While it can be useful to treat maternal morbidity as a composite outcome for identifying at-risk populations, once vulnerable groups are identified, a deeper look into which types of events are driving maternal morbidity is necessary for providing direction for intervention.
For instance, in this analysis, patients with leukemia were found to bear a larger burden of risk compared with patients with other cancer types. Risk was driven specifically by the occurrence of sepsis, acute respiratory distress syndrome, and disseminated intravascular coagulation. This observation and others like it invite scrutiny to the underlying causes of these patterns. For example, are rates of sepsis higher in patients with leukemia because they are more likely to be immunosuppressed by their treatment regiments or the nature of their cancer? Or are these more patients more likely to have ports and are therefore vulnerable to the additional risk of catheter-related bloodstream infections? Research aimed to address these sorts of questions will allow us to better understand the etiology of risk and how to combat it.
Strengths and Limitations
Given that deliveries in the United States occur in a hospital,17 The National Inpatient Sample is poised to estimate prevalence of disease in pregnancy. It is especially well-suited for understanding and quantifying the occurrence of relatively rare conditions, such as cancer, in pregnancy because of its scale. Still, data that are derived from diagnoses codes are vulnerable to misclassification error. This error would most likely lead to an underestimation of cancer cases among pregnant individuals. Similarly, instances of maternal morbidity may be missed if not coded. However, this potential source of error is not expected to differ among patients with and without cancer, so should not unduly bias estimates.
Additionally, the National Inpatient Sample is limited by only providing information about events during delivery hospitalization. We lack data about timing of cancer diagnosis, cancer stage, and treatments prior to delivery, which undoubtedly influence risks. Cancers that predated pregnancy and cancers that were diagnosed during gestation are present in this analysis without the ability to distinguish temporality of diagnosis. Also, this analysis does not provide information about maternal morbidity and mortality events that occur beyond the delivery hospitalization.
Conclusions
Patients with cancer are at an increased risk of morbidity and mortality at delivery. Within this population, risk is distributed unevenly, with certain cancer types shouldering the greatest burden.
Supplementary Material
AJOG at a Glance:
A. Why was this study conducted?
Patients with cancer during pregnancy are a medically complex group and little is known about their risks at delivery.
Understanding patterns of risk provides an opportunity for early recognition and mitigation of maternal morbidity events.
B. What are the key findings?
Individuals with cancer bear a disproportionate amount of risk of severe maternal morbidity and mortality at delivery and this risk is unevenly distributed across cancer types.
C. What does this study add to what is already known?
This analysis provides an updated estimate of prevalence of cancer among pregnant patients as well as detailed breakdown of most common cancer types and associated demographics.
We present a depiction of severe maternal morbidity risk by cancer type, uncovering distinct risk profiles for different cancer diagnoses.
Funding:
This research was supported by The National Center for Advancing Translational Sciences and the Eunice Kennedy Shriver National Institute of Child Health and Human Development of the National Institutes of Health under award numbers UL1TR002553 and K12HD103083. The funding bodies had no role in the design or conduct of this experiment Paper presentation information: This work was presented at SMFM 43rd Annual Pregnancy Meeting, February 6-11, 2023, San Francisco, CA
Footnotes
Conflict of interest: The authors report no conflict of interest.
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