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doi:10.1111/jog.12443

J. Obstet. Gynaecol. Res. Vol. 40, No. 9: 2031–2036, September 2014

Analysis of pregnancies in women with Takayasu arteritis: Complication of Takayasu arteritis involving obstetric or cardiovascular events Hiroaki Tanaka, Kayo Tanaka, Chizuko Kamiya, Naoko Iwanaga and Jun Yoshimatsu Department of Perinatology, National Cerebral and Cardiovascular Center, Osaka, Japan

Abstract Aims: The incidence of Takayasu arteritis during child-bearing years is relatively high. The management of pregnancies in patients with this disease is of great importance in clinical obstetrics. Here we analyzed pregnancies of women with Takayasu arteritis with and without complications. Material and Methods: We retrospectively identified 27 pregnancies in 20 women with Takayasu arteritis seen between 1983 and 2005 at the National Cardiovascular Center, in Osaka, Japan. The incidences of obstetric events, steroid dose increase in pregnancy, and cardiovascular events were compared between group I (no complications), group II (one complication), and group III (two or more complications). Results: None of the pregnancies showed Takayasu arteritis activity. The obstetric events were pre-eclampsia in four pregnancies (15%), fetal growth restriction in one (4%), and abruption in one (4%). Three pregnancies involved a steroids dose increase. There were no cardiovascular events. Eighty percent of the pregnancies that included an obstetric event also involved the mother’s chronic hypertension. Conclusions: Pregnant women without active Takayasu arteritis have a low risk of developing a cardiovascular event. For women with chronic hypertension, it might be important to note the development of preeclampsia, fetal growth restriction and abruption. Key words: fetal growth restriction, hypertension, pre-eclampsia, pregnancy, Takayasu arteritis.

Introduction Takayasu arteritis is a rare idiopathic chronic inflammatory disease. The cause is not known.1 The incidence of Takayasu arteritis is 2–3 per million persons per year with a female : male ratio of 9:1. It is estimated that in Japan there are approximately 5000 individuals with Takayasu arteritis.2 The disease preferentially involves arteries, including the aorta, major branches, vertebral, subclavian, carotid, brachiocephalic, iliac, and renal. Because the incidence of Takayasu arteritis during child-bearing years is relatively high, the management

of pregnancy with this disease is of great importance in clinical obstetrics. Some pregnancies accompanied by Takayasu arteritis are not problematic. Takayasu arteritis is not influenced by pregnancy. Nevertheless, during the course of a pregnancy of a woman with Takayasu arteritis, maternal complications, such as sustained hypertension, superimposed pre-eclampsia, congestive heart failure and progression of renal involvement, should be anticipated.3 The increased severity of Takayasu arteritis may be associated with an increased likelihood of low-birthweight babies.4 Although Takayasu arteritis is a potentially severe

Received: November 1 2013. Accepted: March 3 2014. Reprint request to: Dr Hiroaki Tanaka, Department of Perinatology, National Cardiovascular Center, 5-7-1 Fujishirodai, Suita, Osaka 565-8565, Japan. Email: [email protected]

© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

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condition during pregnancy, successful pregnancy outcomes are possible if extreme caution is taken.5 Blood pressure control is important in obtaining successful outcomes.6 A case of pregnancy involving Takayasu arteritis was recently reported.5 However, risk factors associated with obstetrical complications and cardiovascular events in such cases are not clear. The relation of vascular involvement is also unclear. Our goal was to clarify risk factors involving obstetrical complications and cardiovascular events. We analyzed Takayasu arteritis cases with and without complications.

Methods We retrospectively identified 27 pregnancies in 20 women with Takayasu arteritis seen between 1983 and 2005 at the Department of Perinatology, National Cardiovascular Center, Osaka, Japan. Historical data on previous pregnancies and the course of the present pregnancy were abstracted from maternal medical records. Takayasu arteritis was defined as non-specific inflammatory disease of uncertain cause causing stricture, blockage or enhanced changes to the aorta, the major branch, the pulmonary artery, or coronary artery. The definitive diagnosis was made based on diagnostic imaging (i.e., digital subtraction angiography [DSA], computed tomography [CT], magnetic resonance angiography [MRI]). Takayasu arteritis was diagnosed according to criteria cited by Ishikawa and Matsuura:7 one obligatory criterion (age < 40 years); two major criteria (left and right mid-subclavian artery lesion); and nine minor criteria (high erythrocyte sedimentation rate, carotid artery tenderness, hypertension, aortic artery regurgitation or annuloaortic ectasia, pulmonary artery lesion, left mid-common carotid artery lesion, distal brachiocephalic trunk lesion, descending thoracic aorta lesion and abdominal aorta lesion). In addition to the obligatory criterion, the presence of two major criteria, or one major and two minor criteria or four or more minor criteria suggests the presence of Takayasu arteritis. The maternal characteristics examined were age, parity, age at diagnosis of Takayasu arteritis, complications of Takayasu arteritis (retinopathy, chronic hypertension, aortic regurgitation and aortic or arterial aneurysm and pulmonary arterial involvement), steroids use, antiplatelet treatment, and antihypertensive drug use. Maternal outcomes that are assumed to be an obstetric event included abruption, pre-eclampsia,

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fetal growth restriction (FGR), steroids dose increase in pregnancy, and cardiovascular events. Neonatal outcomes were assessed by gestational week, birthweight, Apgar score at 5 min, and pH of the umbilical artery (UA). We categorized the patients into three groups according to the Ishikawa criteria.8 Group I had no complications. Group II had one of the following complications: retinopathy, chronic hypertension, aortic regurgitation and aortic or arterial aneurysm. Group III had two or more of those complications.9 We compared the groups’ obstetric events, steroids dose increase in pregnancy, and cardiovascular events. The univariate analysis by χ2-test was used for the statistical analysis. P-values < 0.05 were considered significant.

Results Our analysis examined a total of 27 pregnancies in 20 women. All patients continued the pregnancy and delivered. All pregnancies showed no manifestations of Takayasu arteritis. The maternal background data for the pregnancies and patients are shown in Table 1. The median age was 30 years (range 22–35 years). The mother was nulliparous in 19 pregnancies (70%) and multiparous in eight (30%). The median age at the diagnosis of Takayasu arteritis was 21 years (16–33 years). The maternal complications for Takayasu arteritis were chronic hypertension in five pregnancies (18%) and aortic regurgitation in five (18%), renal obstruction in none (0%), aortic and arterial aneurysm in three (11%), and pulmonary arterial involvement in none (0%). Steroid use was present in 15 pregnancies (55%), but there were no cases in which Takayasu arteritis showed activity. Antiplatelet treatment was used in four pregnancies (15%). Three pregnancies (11%) involved antihypertensive drug use, and an antihypertensive drug was administered for anti-arrhythmia in case 27. Obstetric events included pre-eclampsia in four pregnancies (15%), FGR in one (4%), and abruption in one (4%). Three pregnancies involved a steroids dose increase. There were no cardiovascular events. The mode of delivery was cesarean section in nine pregnancies (33%). The indications for cesarean section among these patients were pre-eclampsia (four pregnancies), fetal disorder (one), abruption (one), and previous cesarean section (three). The gestational ages at delivery included preterm birth in three pregnancies (11%). Low birthweight infants occurred in three pregnancies

© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

18 27 21 21 21 27 29 29 27 28 17 17 20 33 21 24 24 24 24 19 22 22 16 21 21 21 17

22 34 24 30 32 30 33 35 30 28 24 28 23 33 30 31 33 29 31 29 32 33 29 29 30 33 32

0 0 0 1 0 0 0 1 0 0 0 1 0 1 0 0 1 0 1 0 0 1 0 0 1 0 0

No No No No No No No No No No No No No No No No No No No No No No No No No No No

Yes Yes Yes Yes Yes No No No No No No No No No No No No No No No No No No No No No No

No No Yes Yes No No No No No No No No No No No No No No No No No No Yes No No Yes Yes

No No No No No No Yes No No No No No No No No No No No No No No No No No No No No

No No No No No No No No No Yes No No Yes No No No No No No Yes No No No No No No No

No No No No No No No No No No No No No No No No No No No No No No No No No No No

No No No No Yes Yes Yes Yes No No No No No No Yes Yes Yes Yes No Yes Yes Yes No Yes Yes Yes Yes

No No No No No Yes No No No No No No No No No No No No No No No No No Yes Yes No Yes

No Yes No No Yes No No No No No No No No No No No No No No No No No No No No No Yes

Case Age at Age at Parity Complications of Takayasu arteritis Steroids Antiplatelet Antihypertensive diagnosis delivery Retinopathy Chronic Aortic Renal Aortic and Pulmonary use treatment drug use hypertension regurgitation obstruction arterial arterial aneurysm

Table 1 Maternal background

Pregnancy and Takayasu arteritis

© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

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(11%). Apgar score (5-min) and pH of the UA were excellent, except in case 1 (involving abruption), in which both the Apgar score and the pH of the UA were low (Table 2). Table 3 shows the correlations among obstetric events, steroid dose increase in pregnancy, cardiovascular events and complication of Takayasu arteritis. Group I included 16 pregnancies (59%). Group II included nine pregnancies (33%), with chronic hypertension in three pregnancies (11%), aortic regurgitation in three (11%), and aortic and arterial aneurysm in three (11%). Group III included chronic hypertension and aortic regurgitation in two pregnancies (7%). Obstetric events occurred in five pregnancies, and 80% of the pregnancies that included an obstetric event also involved the mother’s chronic hypertension. There were significantly more obstetric events among the chronic hypertension patients of group II compared to group I (P = 0.04). Three pregnancies involved a steroids dose increase, with no significant difference between group I and groups II or III regarding this parameter. Cardiovascular events did not occur in any of the 27 pregnancies. The arterial involvement is summarized in Table 4. Various arteries were involved, but no cardiovascular events occurred, as mentioned above. Moreover, four of the five cases with renal arterial involvement (80%) also showed chronic hypertension. Cases involving the exacerbation of heart function and aortic regurgitation with Takayasu arteritis that were investigated at 1 month postpartum, were not included in this study.

Discussion We conclude that in some pregnancies, Takayasu arteritis does not affect the outcome. Moreover, Takayasu arteritis is not influenced by pregnancy. The rates of pre-eclampsia and FGR are increased among women with Takayasu arteritis.4,9,10 Blood pressure control during pregnancy is important to achieving successful outcomes.6 In the present study, our goal was to clarify risk factors involving obstetrical complications and cardiovascular events. Obstetric events developed in six of the 27 present pregnancies with Takayasu arteritis (22%), as preeclampsia (n = 4), FGR (n = 1) and abruption (n = 1). This result corresponds to those of previous reports.4,9,10 The neonatal outcome was excellent when there was no obstetric event. When we began our investigation of the complications of Takayasu arteritis, we suspected

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that chronic hypertension was related to obstetric events. Although blood pressure control during pregnancy is important,5 we suspected that it was a risk factor not only for blood pressure control but also for the existence of chronic hypertension, and important obstetrics events. We found that 80% of the pregnancies involving chronic hypertension had a stricture of the renal artery. In a word, there were many cases of renal hypertension. A prior study reported that renal artery stenosis is related to FGR, and that renal artery stenosis is descended in association with chronic hypertension.3 This is related not only to FGR but also pre-eclampsia and abruption. The rate of increases in steroid dose during pregnancy in the present study was 11%, but Takayasu arteritis does not progress with increased steroids alone. Our result agrees with that of a past report showing that Takayasu arteritis is not influenced by pregnancy.5 However, it must be borne in mind that all 27 of the present study’s pregnancies were not active Takayasu arteritis cases. The post-partum heart function and aortic regurgitation values were unchanged. Takayasu arteritis presents as a stricture and blood vessels enhanced due to inflammation. At the same time, the compliance of the blood vessel is decreased by the inflammatory change. The post load increases to the change in circulating blood volume by the pregnancy compared with a normal pregnancy and increases the strain on the heart. However, it is important to be able to achieve no exacerbation of the heart function and aortic regurgitation during the postpartum period. In the present patient population, a cardiovascular event did not occur. We expected to observe deterioration of the aortic regurgitation and/or the exacerbation of chronic hypertension because the circulating blood volume doubles during pregnancy. The results did not meet this expectation. We cannot be certain of the rationale underlying the decision, because this study was performed as a retrospective analysis. However, pregnancy with Takayasu arteritis without activity is predicted to have a low possibility of cardiovascular events, and no deterioration of arteritis. Considering obstetrics events, the presence of chronic hypertension might be an important factor in the complications of Takayasu arteritis. The obstetrician of a woman with Takayasu aortitis should confirm that there is no Takayasu aortitis activity and carefully monitor the pregnancy. Women without Takayasu arteritis activity who are pregnant have a low risk of the

© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

Abruption FGR Pre-eclampsia Pre-eclampsia Pre-eclampsia Pre-eclampsia No No No No No No No No No No No No No No No No No No No No No

Obstetric event

No No Yes No No No No No No No No No No No No No No No Yes No No No No No No No Yes

No No No No No No No No No No No No No No No No No No No No No No No No No No No

Maternal outcome Steroid dose Cardiovascular increase in event pregnancy CS CS CS CS CS CS VD VD VD CS VD VD VD VD VD CS CS VD VD VD VD VD VD VD VD VD VD

Delivery mode

CS, cesarean section; FGR, fetal growth restriction; UA, umbilical artery; VD, vaginal delivery.

1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27

Case

Table 2 Maternal and neonatal outcomes

36+2 33+2 39+2 38+1 28+2 39+4 38+6 38+1 40+3 39+3 39+4 38+6 40+1 37+0 39+2 40+1 38+4 39+6 39+2 39+4 38+1 38+0 39+0 38+5 38+6 38+6 39+0

Gestational age at delivery (weeks) 2140 1554 3522 3044 975g 3490 2788 3196 3558 2654 2860 2744 3614 3006 3074 2988 2842 3062 2856 2632 3053 2636 2758 2474 2600 2790 2640

2 8 9 9 9 9 9 9 9 8 10 9 10 9 9 6 9 9 9 9 9 10 9 9 9 8 8

Neonatal outcome Birthweight Apgar (g) score (5-min)

7.16 7.25 7.21 7.31 7.31 7.24 7.21 7.34 7.25 7.32 7.32 7.29 7.27 7.34 7.32 7.14 7.27 7.23 7.36 7.34 7.38 7.15 7.33 7.25 7.27 7.26 7.32

pH of UA

Pregnancy and Takayasu arteritis

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Table 3 Correlations among obstetric events, steroid dose increase in pregnancy, cardiovascular events and complications Group I None

Obstetric event Steroids dose increase in pregnancy Cardiovascular event

Chronic hypertension

Group II Aortic regurgitation

n = 16

n=3

n=3

Aortic or arterial aneurysm n=3

1 (6%) 1 (6%) 0 (0%)

2 (66%)* 0 (0%) 0 (0%)

0 (0%) 1 (33%) 0 (0%)

0 (0%) 0 (0%) 0 (0%)

Group III Chronic hypertension and aortic regurgitation n=2 2 (100%) 1 (50%) 0 (0%)

*P = 0.04.

Table 4 Arterial involvement among patients with Takayasu arteritis n = 20 Ascending aorta Arch of aorta Common carotid artery Brachiocephalic artery Internal carotid artery External carotid artery Subclavian artery Vertebral artery Abdominal aorta Renal artery

3 (11%) 3 (11%) 11 (53%) 2 (11%) 1 (4%) 1 (4%) 13 (70%) 9 (44%) 4 (18%) 5 (26%)

development of a cardiovascular event. For pregnant women with chronic hypertension, it might be important to check for the development of pre-eclampsia, FGR, and abruption.

Disclosure The sponsor of the study had no role in the study design, conduct of the study, data collection, data interpretation or preparation of the report.

References

2. Arend WP, Michel BA, Bloch DA, Hunder GG, Calabrese LH. The American College of Rheumatology 1990 criteria for the classification of Takayasu arteritis. Arthritis Rheum 1990; 33: 1129–1134. 3. Papantoniou N, Katsoulis I, Papageorgiou I, Antsaklis A. Takayasu arteritis in pregnancy: Safe management options in antenatal care. Fetal Diagn Ther 2007; 22: 449–451. 4. Gasch O, Vidaller A, Pujol R. Takayasu arteritis and pregnancy from the point of view of the internist. J Rheumatol 2009; 36: 1554–1555. 5. Hidaka N, Yamanaka Y, Fujita Y, Fukushima K, Wake N. Clinical manifestations of pregnancy in patients with Takayasu arteritis: Experience from a single tertiary center. Arch Gynecol Obstet 2012; 285: 377–385. 6. Mandal D, Mandal S, Dattaray C et al. Takayasu arteritis in pregnancy: An analysis from eastern India. Arch Gynecol Obstet 2012; 285: 567–571. 7. Ishikawa K, Matsuura S. Occlusive thromboaortopathy (Takayasu’s disease) and pregnancy. Clinical course and management of 33 pregnancies and deliveries. Am J Cardiol 1982; 50: 1293–1300. 8. Abdul-Karim R, Assalin S. Pressor response to angiotonin in pregnant and nonpregnant women. Am J Obstet Gynecol 1961; 82: 246–251. 9. Matsumura R, Moriwaki R, Numano F. Pregnancy in Takayasu arteritis from the view of internal medicine. Heart Vessels Suppl 1992; 7: 120–124. 10. Wong VC, Wang RY, Tse TF. Pregnancy and Takayasu’s arteritis. Am J Med 1983; 75: 597–601.

1. Ishikawa K. Diagnosis approach, proposed criteria for the clinical diagnosis of Takayasu arteriopathy. J Am Coll Cardiol 1988; 12: 964–972.

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© 2014 The Authors Journal of Obstetrics and Gynaecology Research © 2014 Japan Society of Obstetrics and Gynecology

Analysis of pregnancies in women with Takayasu arteritis: complication of Takayasu arteritis involving obstetric or cardiovascular events.

The incidence of Takayasu arteritis during child-bearing years is relatively high. The management of pregnancies in patients with this disease is of g...
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