Clinical Characteristics and Outcomes of Pregnancy-Associated Venous Thromboembolism　― Report From the Japanese Nationwide Hospital Administrative Database ―

Abstract

Background: Pregnant women are at high risk of venous thromboembolism (VTE), which is one of the important causes of maternal death.

Methods and Results: Using a Japanese nationwide hospital administrative database, we identified 410 pregnant women who were admitted to hospital with VTE between April 2008 and September 2023. We evaluated clinical characteristics and outcomes. Of the 410 women, 110 (26.8%) developed pulmonary embolism (PE). The median week of pregnancy at the time of VTE onset was 31 weeks. The incidence of VTE exhibited a bimodal distribution: 126 (30.7%) women developed VTE in the first trimester (before 14 weeks gestation) and 236 (57.6%) developed VTE in the third trimester (after 28 weeks gestation). PE was more common in the later stages of pregnancy. Regarding anticoagulation therapy, 374 (91.2%) women received unfractionated heparin and 18 (4.4%) received low-molecular-weight heparin. During the 6-month follow-up period, 17 (4.1%) women experienced VTE recurrence and 3 (0.7%) developed bleeding events, including intracranial hemorrhage and gastrointestinal bleeding. During hospitalization, 4 (1.0%) women died, 3 of whom had a history of surgical procedures, including cesarean section and hysterectomy.

Conclusions: This large nationwide database revealed important clinical features and outcomes of pregnancy-associated VTE, highlighting its bimodal incidence and the need for early vigilance, benefiting cardiologists and obstetricians.

Venous thromboembolism (VTE), which includes pulmonary embolism (PE) and deep vein thrombosis (DVT), is a major health problem worldwide. Risk factors for the development of VTE are collectively known as Virchow’s triad (blood flow stasis, endothelial injury and hypercoagulability), and may be common in pregnant women.¹ Studies have reported that the incidence of VTE in pregnant women is relatively high compared with that in non-pregnant women.^1–3 Previous studies have reported that the incidence of VTE is approximately 1–12 cases per 10,000 pregnancies, which is 6- to 7-fold higher than in age-matched controls.^2–4 Pregnancy-associated VTE is considered an important complications during pregnancy.^5–7 Notably, PE is estimated to account for approximately 10% of maternal deaths in the US⁸ and has been reported to be a common cause of maternal death in Japan.^9,10

Although anticoagulation therapy is the mainstay of the treatment and secondary prevention of VTE,^11,12 the management of VTE in pregnant women presents several unique challenges due to the potential effects of anticoagulants on the fetus, and this may complicate daily clinical practice. Consequently, the epidemiologic profile of pregnancy-associated VTE may differ from that of non-pregnancy-associated VTE. Gaining an understanding of the epidemiologic data of women with pregnancy-associated VTE may be clinically relevant to identify current issues and unmet needs related to the condition. However, there are limited data on pregnancy-associated VTE in Japan. Therefore, the aim of this study was to investigate the clinical characteristics, management strategies, and outcomes of pregnancyassociated VTE using a nationwide hospital administrative database in Japan.

Methods

Data Source

The data used in this study were obtained from a nationwide hospital administrative database provided by Medical Data Vision Co., Ltd. (MDV; Tokyo, Japan). The structure of the MDV database has been described in detail elsewhere.^13–16 As of 2024, the database contains anonymized data from 48.27 million inpatients and outpatients across 519 acute care hospitals, which account for approximately 29.1% of all acute care hospitals in Japan.¹⁷ Hospitals in the MDV database have adopted the Diagnosis Procedure Combination (DPC) system, which is a patient classification system developed in Japan for inpatients in the acute phase of a disease. The MDV database includes longitudinal claims and DPC information on demographics, diagnoses, procedures, and prescriptions.

The present study was conducted in accordance with the principles of the Declaration of Helsinki. The research protocol was approved by the Ethics Committee of Kyoto University Graduate School and Faculty of Medicine (Approval no. R4306). In accordance with the current Japanese ethical guidelines, the requirement for individual written informed consent was waived because the data were anonymous.

Patient Selection

We identified 15,470 pregnant women in the MDV database who had been admitted to hospital with a DPC claim for VTE between April 1, 2008 and September 30, 2023. Index PE and DVT were defined by the combination of a corresponding disease code, at least 1 diagnostic imaging procedure performed during hospitalization, and the administration of anticoagulants on the same day as the diagnostic imaging. Imaging modalities included computed tomography for PE and DVT, ventilation-perfusion lung scanning for PE, and ultrasound examination of leg veins for DVT. The date of anticoagulant therapy was defined as the cohort entry date.

Of the 15,470 pregnant women identified in the database, 15,062 were excluded from this study: 9,475 who did not receive any anticoagulants for VTE at cohort entry; 5,516 who did not undergo diagnostic imaging at cohort entry; 63 who had received anticoagulants within 90 days before cohort entry; 1 who had another indication for anticoagulant therapy (atrial fibrillation or atrial flutter); 2 who had endocarditis or heart valve disease; 2 who developed VTE at 0 weeks of pregnancy; and 3 who were transferred to another hospital or clinic at cohort entry. Thus, 410 pregnant women who developed VTE were included in the present study (Figure 1). Detailed inclusion and exclusion criteria for VTE are presented in Supplementary Table 1.

Figure 1.

Study flowchart. MDV, Medical Data Vision; VTE, venous thromboembolism.

Baseline Characteristics

We collected information on baseline characteristics, including demographics, comorbidities, VTE presentation, treatment strategies, and concomitant medications. Detailed definitions of patient characteristics are provided in Supplementary Table 2.

Outcomes and Follow-up

Clinical outcomes in this study were 6-month VTE recurrence, 6-month bleeding events, and in-hospital all-cause death. VTE recurrence included both PE and DVT recurrence. Based on previous studies,^13,18 VTE recurrence was determined by a combination of the following 2 components: (1) an inpatient diagnosis of VTE recorded in the DPC claims as a “main condition,” “trigger-for-hospitalization condition,” “most resource-consuming condition,” or “condition occurring after admission;” and (2) diagnostic imaging performed during hospitalization. VTE recurrence during hospitalization for the index VTE was excluded to ensure that there was only 1 VTE episode per hospitalization. In line with a previous study,¹⁹ outpatient VTE diagnoses were not included because they may not have indicated recurrence, but rather a follow-up visit. Bleeding events included intracranial hemorrhage and gastrointestinal bleeding. Detailed outcome definitions are provided in Supplementary Table 3.

Follow-up started on the cohort entry date. For VTE recurrence and bleeding events, follow-up continued until the first occurrence of these study outcomes, death, or the end of the 6-month follow-up period, whichever came first. For in-hospital all-cause death, follow-up continued until death or discharge, whichever occurred first.

Statistical Analysis

Categorical variables are presented as numbers and percentages, and continuous variables are presented as the mean±SD or the median with interquartile range depending on data distribution. Considering the nature of this study, results are presented in a descriptive manner. All statistical analyses were conducted using JMP version 14.0.0 (SAS Institute, Cary, NC, USA).

Results

Patient Characteristics

In the present study population, the mean age was 33 years and the mean body mass index was 23.8 kg/m² (Table 1). Of the 410 women included in this study, 110 (26.7%) developed PE with or without DVT, and 300 (73.2%) developed DVT only. The median time of VTE onset during pregnancy was 31 weeks. The incidence of VTE exhibited a bimodal distribution, with 126 (30.7%) women developing VTE in the first trimester (before 14 weeks) and 236 (57.6%) developing VTE in the third trimester (after 28 weeks; Figure 2). Regarding the onset of PE specifically, the distribution of onset showed that PE was more common in the late stages of pregnancy, particularly in the third trimester (after 28 weeks; Figure 2). Regarding anticoagulation therapy, 374 (91.2%) patients received unfractionated heparin, whereas 18 (4.4%) patients were treated with low-molecular-weight heparin (LMWH; 2 with dalteparin and 16 with enoxaparin). In terms of acute treatment, 2 (0.5%) patients received thrombolysis, 17 (4.1%) underwent inferior vena cava filter placement, 8 (2.0%) required invasive mechanical ventilation, and 5 (1.2%) needed extracorporeal membrane oxygenation. Cesarean section was performed in 91 (22%) women within 6 months after the onset of VTE, consisting of 23 women with PE and 68 with DVT.

Table 1.

Patient Characteristics at Baseline (n=410)

Demographics
Age (years)	33.0±5.4
Body weight (kg)	60.1±11.7
BMI (kg/m2)	23.8±4.6
Time of VTE onset (weeks gestation)	31 [11–37]
Comorbidities
Hypertension	10 (2.4)
Dyslipidemia	7 (1.7)
Diabetes	19 (4.6)
Renal dysfunction	1 (0.2)
Liver dysfunction	3 (0.7)
Active cancer	0 (0)
Heart failure	7 (1.7)
History of stroke	3 (0.7)
Varicose veins	3 (0.7)
Peptic ulcer disease	13 (3.2)
Previous bleeding	17 (4.1)
Antiphospholipid syndrome	6 (1.5)
Autoimmune disordersA	8 (2.0)
Congenital coagulation disordersB	17 (4.1)
Presentation
PE with or without DVT	110 (26.8)
DVT only	300 (73.7)
Treatment
Anticoagulation therapy
Parenteral anticoagulants
UFH	374 (91.2)
Low-molecular-weight heparin	18 (4.4)
Dalteparin	2 (0.5)
Enoxaparin	16 (3.9)
Oral anticoagulants
Warfarin	19 (4.6)
DOAC	21 (5.1)
Edoxaban	9 (2.2)
Rivaroxaban	5 (1.2)
Apixaban	7 (1.7)
Thrombolysis	2 (0.5)
Inferior vena cava filter	17 (4.1)
Mechanical ventilation	8 (2.0)
ECMO	5 (1.2)
Concomitant medications
NSAIDs	49 (12.0)
Histamine H2 receptor antagonist	42 (10.2)
Proton pump inhibitor	25 (6.1)

Categorical variables are presented as n (%), and continuous variables are presented as either the mean±SD or the median [interquartile range] depending on their distribution. ^AAutoimmune disorders include systemic lupus erythematosus, rheumatoid arthritis, myasthenia gravis, Hashimoto’s disease, and Graves’ disease. ^BCongenital coagulation disorders include protein C deficiency, protein S deficiency, and antithrombin deficiency. BMI, body mass index; DOAC, direct oral anticoagulants; DVT, deep vein thrombosis; ECMO, extracorporeal membrane oxygenation; NSAIDs, non-steroidal anti-inflammatory drugs; PE, pulmonary embolism; UFH, unfractionated heparin; VTE, venous thromboembolism.

Figure 2.

Distribution of the time of deep vein thrombosis (DVT) and pulmonary embolism (PE) onset during pregnancy. VTE, venous thromboembolism.

Clinical Outcomes

During the 6-month follow-up period, 17 (4.1%) patients developed VTE recurrence (Table 2). Full details for these patients are presented in Supplementary Table 4. Of the 17 patients with VTE recurrence, 4 experienced PE and 13 had DVT alone. Regarding the timing of recurrence, 4 (23.5%) patients had VTE recurrence in the second trimester, whereas 13 (76.5%) experienced recurrence in the third trimester or within 30 days postpartum. All patients with VTE recurrence were treated with unfractionated heparin at the time of recurrence, and 1 patient underwent inferior vena cava filter placement at the onset of index VTE.

Table 2.

Clinical Outcomes During the Follow-up Period

	No. patients (%)	Time from VTE onset to event (days)
6-month VTE recurrence	17 (4.1)	70 [42–108]
6-month bleeding events	3 (0.7)	0 [0–1]
In-hospital all-cause death	4 (1.0)	7 [4–29]

The time from VTE onset to an events is presented as the median [interquartile range]. VTE, venous thromboembolism.

During the 6-month follow-up period, 3 (0.7%) patients developed bleeding events (Table 2): 1 patient experienced an intracranial hemorrhage and 2 patients experienced gastrointestinal bleeding. Prior to these bleeding events, 2 patients had been treated with unfractionated heparin, whereas 1 patient was receiving apixaban. All bleeding events occurred within 1 day after the onset of the index VTE.

Of the 410 patients included in this study, 4 (1.0%) died during hospitalization (Table 2). Full details for these deaths are presented in Table 3. Of the 4 patients who died, 3 underwent surgical procedures, including cesarean section and hysterectomy, and all received unfractionated heparin as the initial anticoagulation therapy.

Table 3.

Detailed Characteristics of Patients Who Died

Patient no.	Age (years)	Time from VTE onset to death (days)	Time of VTE onset (weeks gestation)	Body weight (kg)	BMI (kg/m2)	Type of VTE at onset	Initial anticoagulation therapy	Mechanical support	Comorbidities and history of surgical procedures
1	29	9	42	108.4	41.8	PE	UFH	ECMO	–
2	30	36	4	64.2	26.7	PE	UFH	–	Hysterectomy
3	42	4	6	87.4	31.0	DVT	UFH	–	Planned cesarean section, peptic ulcer diseases
4	38	4	38	55.0	20.2	PE	UFH	ECMO	Emergency cesarean section, hysterectomy

Abbreviations as in Table 1.

Discussion

The major findings of this study are: (1) the identification of several clinical features of pregnancy-associated VTE, including the timing of VTE onset during pregnancy; and (2) the elucidation of clinical outcomes, including in-hospital mortality.

A previous study from the Registro Informatizado de la Enfermedad TromboEmbolica (RIETE) Registry reported that pregnant women with VTE less frequently had provoking risk factors for VTE, such as recent immobilization, active cancer, and recent long-distance travel, compared with non-pregnant women aged under 50 years,²⁰ suggesting that pregnancy itself could be a strong risk factor for the development of VTE. A previous national survey questionnaire on thrombosis in pregnant women in Japan reported that the incidence of VTE in pregnant women was approximately 0.082%.¹⁰ Another survey in Japan also reported that VTE was common during not only during the late phase of pregnancy but also in the early phase, and that PE was more common during the postpartum period, particularly following cesarean delivery.⁴ Consistent with these previous reports, the present study found that the incidence of VTE appeared to have a bimodal peak (during the early and late phases of pregnancy) and that PE was most common in the late phase of pregnancy. The underlying reasons for this distribution may include dehydration caused by hyperemesis gravidarum, periods of prolonged bed rest, pregnancy-induced hypertension, placental abnormalities, and compression of the inferior vena cava by the uterus. In general, the risk of VTE peaks around 2 weeks after delivery, and a minimum of 6 weeks of postpartum anticoagulation is recommended, with an ideal duration of up to 3 months.²¹ Patients may either continue the same anticoagulant regimen or switch to warfarin or other anticoagulants. In cases of abortion, direct oral anticoagulants (DOACs) could be an alternative option.

Heparin, including LMWH and unfractionated heparin, has been established as a safe and effective anticoagulant for VTE during pregnancy.²² In contrast, warfarin has been contraindicated during pregnancy,²³ and DOACs have not been recommended during pregnancy due to limited data on safety for the fetus. In fact, in the present study, a vast majority of patients received unfractionated heparin. It should be noted that the use of LMWH for VTE is not covered by Japanese national insurance, and it was difficult to measure anti-Factor Xa activity, which is an indicator of the efficacy of LMWH. Therefore, unfractionated heparin was mostly used as the anticoagulation therapy, although LMWH is recommended over unfractionated heparin in guidelines from Western countries.^23,24 The unavailability of LMWH for VTE during pregnancy has been a considerable issue in Japan, and needs to be addressed urgently. An inferior vena cava filter could be an alternative option for anticoagulation therapy when anticoagulation therapy is contraindicated; however, its use should be approached cautiously due to potential complications including migration during pregnancy.²⁵ The present study showed that only a minority of patients (4.2%) received an inferior vena cava filter, which should be further investigated in future studies.

The present study revealed that a small but significant number of patients developed VTE recurrence during pregnancy or the postpartum period despite anticoagulation therapy, which is fully consistent with a previous report from France.²⁶ Considering the potential strong thrombogenesis in pregnant women, these patients should be followed up with care, even if anticoagulation therapy is administered. Conversely, the present study also showed that only a minority of patients experienced bleeding events, and that the bleeding events occurred just after the initiation of anticoagulation therapy. Because pregnant women could be an essentially healthy, young population with few comorbidities, prolonged anticoagulation therapy may not significantly increase the bleeding risk after successful initiation of anticoagulation therapy. A previous national survey questionnaire in Japan reported that the mortality rate in pregnant women was significantly higher among those with than without thrombosis (1.6% vs. 0.0054%).¹⁰ Consistent with this previous report, the present study also found that a non-negligible number of patients died during hospitalization. Among the women who died, there was considerable variety in patient characteristics, including age, obesity, the timing of VTE onset during pregnancy, and history of surgical procedures; this suggests that all types of patients could develop fatal PE. Thus, clinicians should be cautious regarding the development of VTE in all pregnant women, which may enable early diagnosis and appropriate treatment.

Study Limitations

The present study has several limitations. First, the MDV database collected data only from acute care hospitals, and data were unavailable for patients who had been treated in other clinics and hospitals. Thus, the present results may only be partially applicable to patients treated in clinics and long-term care hospitals. In addition, this may have led to outcome misclassification and underestimation of cumulative incidence. However, the majority of patients with pregnancy-associated VTE are seen in acute care hospitals, and the treatment for VTE is likely to continue in the same hospital. Second, because the data used in this study were derived from claims and DPC information, several key variables, including detailed clinical data, such as vital signs, PE severity, and laboratory test results, could not be sufficiently extracted, making it difficult to fully assess the overall status of the patient population. Third, there was a possibility of PE underdiagnosis, because not all patients were evaluated by computed tomography and ventilation-perfusion lung scanning. Finally, we excluded VTE recurrence during hospitalization for the index VTE to ensure valid recurrence assessments, which could underestimate VTE recurrence during the acute phase.

Conclusions

The large nationwide database revealed important clinical features and outcomes of pregnancy-associated VTE, highlighting its bimodal onset and the need for early vigilance, benefiting cardiologists and obstetricians.

Acknowledgment

The authors are grateful to Medical Data Vision Co., Ltd. for the generous provision of the medical data.

Sources of Funding

This study was supported, in part, by research funding for investigator-initiated studies from the Japanese Society on Thrombosis and Hemostasis. The research funder had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; or preparation, review, or approval of the manuscript.

Disclosures

Y.Y. has received lecture fees from Bayer Healthcare, Bristol-Myers Squibb, Pfizer, and Daiichi Sankyo, and grant support from Bayer Healthcare and Daiichi Sankyo. T.F. was employed by the Department of Digital Health and Epidemiology with support from Eisai Co., Ltd., Kyowa Kirin Co., Ltd., and Real World Data Co., Ltd., and has received research funds from AstraZeneca K.K. and the Pfizer Health Research Foundation, consulting fees from JMDC Inc. and Real World Data Co., Ltd., and honoraria from EPS Corporation and Research Institute of Healthcare Data Science (RIHDS); his spouse is employed by MSD K.K. K.O. is a member of Circulation Journal’s Editorial Team. No other disclosures are reported.

IRB Information

This study was approved by the Ethics Committee of Kyoto University Graduate School and Faculty of Medicine, Japan (Approval no. R4306).

Data Availability

The deidentified participant data will be shared on a request basis. Please contact the corresponding author directly to request data sharing. All datasets used will be available, including the study protocol. Data will be shared as soon as the ethics committee at Kyoto University approves the request, and will be available thereafter.

Supplementary Files

Please find supplementary file(s);

https://doi.org/10.1253/circj.CJ-25-0124

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