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Obstetrics & Gynecology 2001;98:471-475
© 2001 by The American College of Obstetricians and Gynecologists
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ORIGINAL RESEARCH

Venous Thromboembolism in Pregnant Chinese Women

L. Y. Chan, MB, BS, MRCOG, W. H. Tam, MBChB, MRCOG and T. K. Lau, MD

From the Department of Obstetrics and Gynaecology, the Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, Hong Kong.

Address reprint requests to: L. Y. Chan, MB, BS, MRCOG, Department of Obstetrics and Gynecology, Prince of Wales Hospital, The Chinese University of Hong Kong, Shatin, Hong Kong, China; E-mail: lyschan{at}netvigator.com.


   ABSTRACT
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ABSTRACT
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
OBJECTIVE: To evaluate the incidence, disease pattern, and risk factors for thromboembolism in pregnant Chinese women.

METHODS: We conducted a study from January 1998 to December 2000. Women with thromboembolic diseases were identified and their case records retrieved and reviewed. Demographic characteristics were compared between women with and without thromboembolism.

RESULTS: Thirty-two women were diagnosed as having thromboembolic disease during the study period. The total number of deliveries over the study period was 16,993, giving an incidence of 1.88 per 1000 deliveries. There were two cases of pulmonary embolism and one resulted in a maternal death. The others had deep vein thrombosis of which over 80% were limited to calf veins only. The ultrasound examinations requested for suspected deep venous thrombosis before and after the event of maternal death were 1.62 and 10.7 per 1000 deliveries (P < .001); and the corresponding cases of deep venous thrombosis diagnosed were 0.29 and 2.94 per 1000 deliveries, respectively (P < .001). The majority (75%) of cases were diagnosed in the postpartum period, mainly after cesarean delivery. Women with venous thromboembolism were older, had higher body mass index, and a higher incidence of preeclampsia.

CONCLUSION: Thromboembolic disease is not uncommon among pregnant Chinese women. The incidence was similar to that of the white population, although the sites of vascular occlusion were different. The long-standing belief that thromboembolism is rare among Chinese is at least partly because of underdiagnosis.

Thromboembolism is a major health problem among the white population. It is the leading cause of maternal deaths in Western countries.1 The prevention of deep vein thrombosis is of paramount importance because it is the most common source of pulmonary embolism. Deep venous thrombosis is also associated with long-term morbidity, and the risk of developing chronic deep venous insufficiency in later life has been estimated to be as high as 65%.2

Thromboembolism has long been regarded as a rare complication among Chinese patients.3–6 It was stated in a popular surgical textbook that "other epidemiological associations include the fact that it (deep venous thrombosis) is virtually unknown in equatorial regions, eg, Singapore."7 Because of the perceived rare occurrence of thromboembolism in Chinese patients, preoperative measures against deep venous thrombosis are usually considered to be unnecessary. It was suggested that the rare occurrence of deep venous thrombosis among the Chinese was related to a more efficient fibrinolytic activity,8,9 which in turn is caused by a low dietary fat intake.10 Lawrence et al have demonstrated that the incidence of deep venous thrombosis is higher in the six cold months of the year.11 Thus, the tropical climate of Southeast Asia may be partly responsible for a low incidence of venous thromboembolism in Asians.12 However, recent data suggest the incidence of deep venous thrombosis in Chinese patients is rising. In autopsy studies, the incidence of significant thromboembolism increased from 0.58% between 1975 and 1979 to 2.08% between 1985 and 198913 and to 4.7% between 1990 to 1994.14 The latest figure is within the lower range of the incidence of thromboembolism in the white population.15 This rising incidence of thromboembolism had also been observed in clinical studies. Woo et al reported that the incidence of thromboembolism among Hong Kong Chinese had increased from 34.3 per million population in 1977 to 79.3 per million in 1985.16 Possible explanations for this rising trend include the growing elderly population, the more aggressive approach by surgeons, and the westernization of the diet of Hong Kong Chinese.13,16

Pregnancy has been found to be a significant risk factor in the development of deep venous thrombosis. The reported incidence of venous thromboembolism associated with pregnancy in white populations varies from 0.7 to 1.3 per 1000 deliveries.17–20 It is generally believed that the incidence of venous thromboembolism in pregnant Chinese women is extremely low. In a review article, it was stated that "In Africa and the Far East the condition (thromboembolism complicating pregnancy) is almost unknown."21 However, there is no objective information in the literature to confirm or refute this widespread belief. The aim of the current study is to investigate the incidence, pattern, and risk factors for thromboembolism in pregnant Chinese women.


   MATERIALS AND METHODS
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ABSTRACT
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
This was a retrospective study conducted over a 3-year period from January 1, 1998 to December 31, 2000 in an obstetric unit of a tertiary university teaching hospital in Hong Kong. The unit has an average of 6000 deliveries annually, and over 95% of the obstetric population was ethnic Chinese.

All cases of deep venous thrombosis or pulmonary embolism diagnosed during pregnancy or within 42 days postpartum were identified. Only ethnic Chinese subjects were included. Only deep venous thrombosis diagnosed by objective methods (by Duplex ultrasound examination, venogram, or autopsy) were included. Similarly, only objectively confirmed pulmonary embolism (by ventilation perfusion scan, angiogram, or autospy) were included. Superficial venous thrombosis of lower limbs was excluded. All case notes were retrieved and reviewed, and the incidence of thromboembolism was calculated. Because of the perceived rare occurrence of thromboembolism in our population, it was not a routine practice to prescribe any form of thromboprophylaxis. All women were encouraged to mobilize 8 hours after vaginal delivery and 36–48 hours after cesarean delivery.

In the second part of the study, a case-control analysis was carried out to identify the risk factor for venous thromboembolism in pregnant Chinese women. The study group included all women with venous thromboembolism who delivered after 24 weeks’ gestation or with birth weight of 500 g or greater; cases associated with abortions or ectopic pregnancies were excluded. The control group consisted of all Chinese women without venous thromboembolism delivered after 24 weeks’ gestation or with birth weight 500 g or greater during the same period. Demographic characteristics and obstetric information was retrieved from computerized obstetric database, and comparisons were made between those women with and without thromboembolism. Unpaired t test, Mann-Whitney U test, {chi}2, and Fisher exact tests were used where appropriate. P values less than .05 were considered significant. All analyses were performed using the Statistical Package for Social Sciences for Windows version 10.0 (SPSS Inc., Chicago, IL).


   RESULTS
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ABSTRACT
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
During the study period, there were 32 cases of thromboembolism: 30 cases of deep venous thrombosis alone and two cases of deep venous thrombosis with pulmonary embolism. None of these women had a past history of venous thromboembolism or sustained any major trauma during pregnancy. The total number of deliveries during the study period was 16,993, giving an incidence of 1.88 per 1000 deliveries (95% confidence interval [CI] 1.18, 2.58 per 1000 deliveries). Figure 1Go shows the number of cases and the number of pregnant/postpartum women who had ultrasound scan performed for suspected deep venous thrombosis. The number of women subjected to ultrasound examination for suspected deep venous thrombosis and the number of diagnosed venous thromboembolism in 1999/ 2000 were more than four times higher than the corresponding figures in 1998.



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  		Figure 1. Incidence of ultrasound examination for suspected deep venous thrombosis from January 1998 to December 2000. DVT = deep venous thrombosis; numbers on bars = number of women.

Chan. Thrombosis in Chinese Parturients. Obstet Gynecol 2001.

 
There was a case of maternal death caused by massive pulmonary embolism in March 1999. The number of ultrasound examinations requested for suspected deep venous thrombosis before and after the event were 1.62 and 10.7 per 1000 deliveries (P < .001); and the corresponding number of deep venous thrombosis diagnosed was 0.29 and 2.94 per 1000 deliveries, respectively (P < .001).

Twenty-four cases were diagnosed in the postpartum period (75.0%) and eight in the antepartum period (25.0%) (three each in the first and second trimester and two in the third trimester). The median interval between delivery and diagnosis of deep venous thrombosis in the 24 postpartum cases was 3 days (range, 1 to 9 days). Four women had prolonged hospitalization (10 days or longer) before diagnosis of deep venous thrombosis. The reasons for hospital admission were placenta previa and/or polyhydramnios. Twenty-seven women had delivery after 24 weeks’ gestation, two had medical termination of pregnancy for fetal anomaly, one had dilation and curettage after incomplete abortion, and two had laparoscopic surgery for suspected ectopic pregnancy. If only women with delivery after 24 weeks’ gestation were included, the incidence of thromboembolism would have been 1.59 per 1000 deliveries.

In the majority of cases, deep venous thrombosis was limited to calf veins (27 cases, 84.4%). The left and right leg veins were involved in 15 cases (46.9%) and 13 cases (40.6%), respectively. Four patients had bilateral deep venous thrombosis. There were two cases of pulmonary embolism. One resulted in a maternal death, and the other patient was treated by pulmonary embolectomy. Eleven women had thrombophilia screening, which included tests for antiphospholipid syndrome, antithrombin III, and protein C and S deficiency. Only one woman was found to have protein S deficiency; all other screening results were negative.

The demographic characteristics and other risk factors were compared between the women with thromboembolism who delivered after 24 weeks’ gestation and the rest of the pregnant women delivered in our institution during the study period. In the 16,966 women without thromboembolism, 657 had missing data on body weight, height, or duration of labor, and hence were excluded from the control group. Women with thromboembolism were significantly older, had higher body mass index, and had a higher incidence of preeclampsia than the control group (Table 1Go). Cesarean delivery was a strong risk factor for the development of thromboembolism. One woman had sudden collapse and died because of pulmonary embolism 2 days after emergency cesarean delivery, giving a 3.7% incidence of maternal mortality in the study group. There was also one case of maternal death in the control group (P = .003).


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  		Table 1. Demographic Characteristics, Risk Factors of Thromboembolism, and Pregnancy Outcome
 

   DISCUSSION
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ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
Our study showed that the incidence of thromboembolism complicating pregnancy in the Chinese population (1.88 per 1000 deliveries) is similar, if not higher than, the reported incidence in the white population (0.7–1.3 per 1000 deliveries).17–20 This observation contrasts sharply with the earlier experience in the same unit from 1988 to 1992 that there was only one case of deep venous thrombosis diagnosed. There are several possible reasons to explain this increase in incidence over the last decade. The sudden increase in the incidence of deep venous thrombosis after the single case of maternal death was good evidence that increased awareness by clinicians and the more liberal use of diagnostic Doppler studies contributed at least partly to the observed change in disease pattern. However, based on other studies in the nonpregnant Chinese population,13,14,16 we believe that there was also a true increase in thromboembolism during the last decades, which might be associated with the more westernized diet and affluent lifestyle among Hong Kong Chinese.14 Although the study was conducted in a tertiary referral hospital, most of the women delivered in our unit are low-risk parturients. We then consider that our finding would be applicable to other pregnant Chinese women around the world.

Because venous thromboembolism has been considered rare in our population, it was not a routine practice to provide specific thromboprophylaxis in women undergoing cesarean delivery. This may partly explain the high incidence of deep venous thrombosis in our study when compared with studies of white populations in which prophylaxis against deep venous thrombosis were given after cesarean delivery in high-risk women.

In the majority (75%) of our cases, deep venous thrombosis was diagnosed in the postpartum period. In a recent meta-analysis, only 34.5% of objectively confirmed deep venous thromboses in the white population were diagnosed in the postpartum period.22 In agreement with other studies, cesarean delivery, particularly emergency operations, represents a significant risk factor for deep venous thrombosis. However, the effect of cesarean delivery seems to be stronger in our population. Cesarean delivery was associated with a more than ten-fold increased risk of venous thrombosis in our study, compared with a two- to five-fold increased risk in other populations.17,20,23 The proportion of postpartum thromboses associated with cesarean delivery was much higher (83%) when compared with another study (41%).17

The pattern of thromboembolism was different in our population. More than 80% of our patients had isolated calf vein thrombosis. On the contrary, previous studies among white populations showed that the majority of symptomatic deep venous thrombosis complicating pregnancy were located in the major veins above the knee.19,24–26 Polak and Wilkinson reported that more than 70% of deep vein thromboses complicating pregnancy were iliofemoral thromboses.24

One may question whether the high incidence we found resulted from the inclusion of cases with isolated calf vein thrombosis. However, studies from white populations also included objectively diagnosed isolated calf vein thrombosis,19,20 and the incidence of venous thromboembolism is similar between the populations. It appeared that the difference in proportion of calf vein thrombosis represents a genuine difference between the two ethnic groups. This preferential pattern of calf vein thrombosis had also been observed in other nonpregnant Chinese patients.3,27–29 Isolated calf vein thrombosis is more difficult to diagnose or to suspect clinically because it is often asymptomatic30,31; even if symptomatic, symptoms (such as calf pain) are often nonspecific,32 and they are less likely to cause pulmonary emboli and therefore escape detection easily.33 The higher proportion of calf vein thrombosis among our population might contribute, at least partly, to the lower reported incidence of deep venous thrombosis in Chinese previously.


   Footnotes
 
PII S0029-7844(01)01476-4

Received March 1, 2001. Received in revised form May 10, 2001. Accepted May 24, 2001.


   REFERENCES
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ABSTRACT
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
1. Why mothers die: Report on confidential enquires into maternal deaths in the United Kingdom 1994–1996. London: Her Majesty’s Stationery Office, 1998.

2. Lindhagen A, Bergqvist A, Bergqvist K, Hallbook T. Late venous function in the leg after deep venous thrombosis occurring in relation to pregnancy. Br J Obstet Gynaecol 1986;93:348–52.[Medline]

3. Nandi P, Wong KP, Wei WI, Ngan H, Ong GB. Incidence of postoperative deep vein thrombosis in Hong Kong Chinese. Br J Surg 1980;67:251–3.[Medline]

4. Tso SC, Wong V, Chan V, Chan TK, Ma HK, Todd D. Deep vein thrombosis and changes in coagulation and fibrinolysis after gynaecological operations in Chinese: The effect of oral contraceptives and malignant disease. Br J Haematol 1980;46:603–12.[Medline]

5. Hwang WS. The rarity of pulmonary thromboembolism in Asians. Singapore Med J 1968;9:269–79.

6. Peng YY, Jeng JS, Shen MC, Tsay W, Wang BS, Lin WH, et al. Aetiologies and prognosis of Chinese patients with deep vein thrombosis of the lower extremities. Q J Med 1998;91:681–6.

7. Mann CV, Russel RC, eds. Bailey and Love’s short practice of surgery. 21st ed. London: HK Lewis & Co., 1991: 241.

8. Ho CH, Jap TS. Fibrinolytic activity in Chinese patients with diabetes or hyperlipidemia in comparison with healthy controls. Thromb Haemost 1991;65:3–6.[Medline]

9. Ho CH, Jap TS. Relationship of plasminogen activator inhibitor-1 with plasma insulin, glucose, triglyceride and cholesterol in Chinese patients with diabetes. Thromb Res 1993;69:271–7.[Medline]

10. Gans H, Mori K, Quinlan R, Richter D, Tan BH. The intestine as a source of plasminogen activator activity. Ann Surg 1971;174:826–9.[Medline]

11. Lawrence JC, Xabregas A, Gray L, Ham JM. Seasonal variation in the incidence of deep vein thrombosis. Br J Surg 1977;64:777–80.[Medline]

12. Nandi PL, Li WS, Leung R, Chan J, Chan HT. Deep vein thrombosis and pulmonary embolism in the Chinese population. Hong Kong Med J 1998;4:305–10.[Medline]

13. Chau KY, Yuen ST, Ng TH, Ng WF. An autopsy study of pulmonary thromboembolism in Hong Kong Chinese. Pathology 1991;23:181–4.[Medline]

14. Chau KY, Yuen ST, Wong MP. Clinicopathological pattern of pulmonary thromboembolism in Chinese autopsy patients: Comparison with Caucasian series. Pathology 1997;29:263–6.[Medline]

15. Dismuke SE, Wagner EH. Pulmonary embolism as a cause of death. The changing mortality in hospitalized patients. JAMA 1986;255:2039–42.[Abstract]

16. Woo KS, Tse LKK, Tse CY, Metreweli C, Vallance-Owen J. The prevalence and pattern of pulmonary thromboembolism in the Chinese in Hong Kong. Int J Cardiol 1988;20:373–80.[Medline]

17. Lindqvist P, Kahlback B, Marsal K. Thrombotic risk during pregnancy: A population study. Obstet Gynecol 1999;94:595–9.[Abstract/Free Full Text]

18. McColl MD, Ramsay JE, Tait RC, Walker ID, McCall F, Conkie JA, et al. Risk factors for pregnancy associated venous thromboembolism. Thromb Haemost 1997;78: 1183–8.[Medline]

19. James KV, Lohr JM, Deshmukh RM, Cranley JJ. Venous thrombotic complications of pregnancy. Cardiovasc Surg 1996;4:777–82.[Medline]

20. Kierkegaard A. Incidence and diagnosis of deep vein thrombosis associated with pregnancy. Acta Obstet Gynecol Scand 1983;62:239–43.[Medline]

21. de Swiet M. Thromboembolism. Clin Haematol 1985;14: 643–60.[Medline]

22. Ray JG, Chan WS. Deep vein thrombosis during pregnancy and the puerperium: A meta-analysis of the period of risk and the leg of presentation. Obstet Gynecol Surv 1999;54:265–71.[Medline]

23. Macklon NS, Greer IA. Venous thrombolic diseases in obstetrics and gynaecology: The Scottish experience. Scot Med J 1995;41:83–6.

24. Polak JF, Wilkinson DL. Ultrasonographic diagnosis of symptomatic deep venous thrombosis in pregnancy. Am J Obstet Gynecol 1991;165:625–9.[Medline]

25. Bergqvist A, Bergqvist D, Hallbook T. Deep vein thrombosis during pregnancy. A prospective study. Acta Obstet Gynecol Scand 1983;62:443–8.[Medline]

26. Bergqvist D, Hender U. Pregnancy and venous thromboembolism. Acta Obstet Gynecol Scand 1983;62:449–53.[Medline]

27. Tso SC. Deep venous thrombosis after strokes in Chinese. Aust N Z J Med 1980;10:513–4.[Medline]

28. Mok CK, Hoaglund FT, Rogoff SM, Chow SP, Yao AC. The pattern of deepvein thrombosis and clinical course of a group of Hong Kong Chinese patients following hip surgery for fracture of proximal femur. Clin Orthop 1980; 147:115–20.

29. Kew J, Lee YL, Davey IC, Ho SY, Fung KC, Metreweli C. Deep vein thrombosis in elderly Hong Kong Chinese with hip fractures detected with compression ultrasound and Doppler imaging: Incidence and effect of low molecular weight heparin. Arch Orthop Trauma Surg 1999;119: 156–8.

30. Ciccone WJ, Fox PS, Neumyer M, Rubens D, Parrish WM, Pellegrini VD. Ultrasound surveillance for asymptomatic deep venous thrombosis after total joint replacement. J Bone Joint Surg Am 1998;80:1167–74.[Abstract/Free Full Text]

31. Oishi CS, Grady-Benson JC, Otis SM, Colwell CW, Walker RH. The clinical course of distal deep vein thrombosis after total hip and total knee arthroplasty, as determined with Duplex ultrasonography. J Bone Joint Surg Am 1994;76:1658–63.[Abstract/Free Full Text]

32. Krunes U, Teubner K, Knipp H, Holzapfel R. Thrombosis of the muscular calf veins — reference to a syndrome which receives little attention. Vasa 1998;27:172–5.[Medline]

33. Kohn H, Konig B, Mostbeck A. Incidence and clinical feature of pulmonary embolism in patients with deep vein thrombosis: A prospective study. Eur J Nucl Med 1987; 13(Suppl):513–5.




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