Subclavian vein thrombosis following IVF and ovarian hyperstimulation: a case report

Anjali K. Rao, Usha Chitkara and Amin A. Milki1

Department of Obstetrics and Gynecology, Divisions of Reproductive Endocrinology/Infertility and Maternal Fetal Medicine, Stanford University Medical Center, Stanford, CA 94305, USA

1 To whom correspondence should be addressed at: amilki{at}stanford.edu


    Abstract
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 Abstract
 Introduction
 Case report
 Discussion
 References
 
Thromboembolic phenomena are a serious consequence of assisted reproductive technology. We present a case of upper extremity deep vein thrombosis (DVT) at 7 weeks gestation following ovarian hyperstimulation syndrome (OHSS) and IVF. Three weeks after recovering from OHSS, the patient presented with left neck pain and swelling. Ultrasound revealed a thrombus in the left jugular vein and left subclavian vein. Low molecular weight heparin (LMWH) was initiated with symptom resolution within 1 week. The patient remained on LWMH throughout her pregnancy and delivered at term. A literature review showed 97 published cases of thromboembolism following ovulation induction. A majority of these cases was associated with OHSS and pregnancy and the site of involvement was predominantly in the upper extremity and neck. Infertility physicians and obstetricians should be aware of this complication and keep in mind that it may occur weeks after resolution of OHSS symptoms.

Key words: IVF/ovarian hyperstimulation/subclavian vein thrombosis


    Introduction
 Top
 Abstract
 Introduction
 Case report
 Discussion
 References
 
Thromboembolic phenomena are an uncommon yet grave consequence of assisted reproductive technology. Deep vein thrombosis (DVT) is more common following ovarian hyperstimulation syndrome (OHSS). It has been surmised that the underlying hypercoagulable state characteristic of OHSS due to high serum levels of estrogen and haemoconcentration contributes to the development of DVT (Pride et al., 1990Go).

In this report, we present a case of upper extremity DVT following OHSS and IVF. We also review published case reports of thrombosis following ovulation induction to update the medical literature about this rare yet serious complication that may be encountered both by physicians providing infertility treatment and obstetricians providing prenatal care.


    Case report
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 Abstract
 Introduction
 Case report
 Discussion
 References
 
A 32 year old female with primary infertility was referred to our programme for IVF and ICSI. Her weight was 47 kg and her height was 161 cm. The patient had a history of oligomenorrhoea and had failed to ovulate on up to 200 mg of clomiphene citrate. She did not conceive after two ovulation induction cycles with gonadotrophins combined with intrauterine insemination (IUI). Her partner had oligoasthenozoospermia with a concentration of 13.6x106 sperm/ml and 14% motility. Hysterosalpingogram showed an unremarkable uterine cavity and patent tubes. Her hormonal work-up was normal. A fasting insulin and an insulin level 2 h after the oral administration of 75 g of glucose were also normal.

On baseline ultrasound, the patient’s right ovary contained seven antral follicles and the left ovary contained 10 antral follicles. The patient’s stimulation protocol for IVF consisted of 21 days of oral contraceptive pills (OCP) with 0.5 mg of leuprolide acetate (TAP Pharmaceuticals, Lake Forest, IL, USA) overlapping with the last 5 days of OCP and continuing for 6 additional days to achieve down-regulation. The dose was then reduced to 0.25 mg and stimulation was started using 75 IU of recombinant FSH (Gonal F; Serono, Randolph, MA, USA) and 75 IU of HMG (Pergonal; Serono) which was subsequently reduced to 37.5 IU. After 12 days of stimulation, she received 10 000 IU of hCG. At that point, there were 13 follicles between 14 and 20 mm in diameter, and 12 additional follicles ≤12 mm. She had transvaginal oocyte retrieval of 19 oocytes of which 18 were mature and underwent ICSI resulting in 15 embryos. Luteal support in the form of 200 mg progesterone vaginal capsules was administered three times daily starting 2 days after oocyte retrieval. The embryos were cultured to day 5 and six viable blastocysts were available for transfer. The option of freezing all embryos to decrease the risk of OHSS was discussed with the patient. However, since she had gained only 0.5 kg over the previous 5 days, maintained good urine output and had no significant nausea, she elected to proceed with the transfer. A single blastocyst was replaced in an effort to reduce the higher risk of OHSS seen in the setting of multiple birth.

Two days later, the patient presented to clinic with abdominal pain, mild shortness of breath and increasing weight gain. She was still able to tolerate food and had an adequate urine output. Blood analysis showed a normal haematocrit of 38.3%, platelets 379 000, sodium 135 (normal 135–145 mEq/l), potassium 3.7 (normal 3.5–5.5 mEq/l), creatinine 0.6 (normal <1.2 mg/dl) and BUN 11 (normal <25 mg/dl). Although her ovaries were only moderately enlarged at 7.2x6.5 and 6.6x6.1 cm and she did not appear to have a marked amount of ascites, a vaginal paracentesis was performed for symptomatic relief yielding 1.4 l. Intravenous hydration was also administered.

She did well initially, but 4 days later, her symptoms worsened and she was admitted to the ambulatory treatment unit for observation and i.v. hydration. Repeat blood analysis showed a haematocrit of 46.5% with sodium of 131 and potassium of 4.2 mEq/l. A repeat paracentesis was performed to drain 2.1 l. The {beta}-HCG at this time was 55 mIU/ml. She was discharged home but the following day she was readmitted to the ambulatory treatment unit for 24 h observation. Her ovaries at that time measured 8x6 cm and 7x7 cm. Her haematocrit was 42.3%, sodium 132 and potassium 3.7 mEq/l. She had a final paracentesis the next day with drainage of 2.3 l. She continued to improve afterwards with a follow-up assessment 3 days later showing ovaries measuring 6.8x4.8 and 8.7x6.6 cm and a haematocrit of 38.0%, sodium 134 and potassium 3.4 mEq/l. The patient was asymptomatic at the time of her first obstetrical ultrasound at 6 weeks and 1 day of gestation when a single viable intrauterine pregnancy was documented.

However, at 7 weeks and 6 days of gestation, the patient presented to urgent care with the complaint of left side neck pain and swelling. She underwent ultrasound of the left upper extremity and neck that revealed a thrombus in the left jugular vein and left subclavian vein. The patient was admitted to the hospital and started on low molecular weight heparin (LMWH). The progesterone supplementation was discontinued at this time.

Joint management was coordinated with the internal medicine, reproductive endocrinology, maternal fetal medicine, haematology and interventional radiology departments. On hospital day 3, the patient developed worsening neck pain and swelling and a repeat ultrasound revealed extension of the thrombus into the left axillary vein. The interventional radiology team initially suggested performing thrombolysis, given that the risk of developing pulmonary embolism following upper extremity DVT is 4–12% (Horattas et al., 1988Go; Burihan et al., 1993Go). Since iodine is not actively concentrated in the fetal thyroid gland until 70 days post-conception, it would have been possible to perform thrombolysis with little risk of harming the fetal thyroid (Mountford, 1997Go). However, in order to avoid an invasive procedure, the maternal fetal medicine and interventional radiology teams decided to pursue a conservative course of action with further anticoagulation therapy. The patient’s dose of LMWH was increased from 50 mg Subcutaneously twice a day (SQ BID) to 60 mg SQ BID because of a subtherapeutic anti-XA level.

The patient’s pain and swelling resolved and she was discharged home on the 7th day of anticoagulation and remained on therapeutic doses of LMWH therapy until 36 weeks gestation when she was switched to heparin. Her pregnancy course was otherwise uncomplicated. A thrombophilia work-up including antiphospholipid antibody, lupus anticoagulant, proteins C and S, antithrombin III, prothrombin G20210A, factor V Leiden and methylene tetrahydrofolate reductase (MTHFR) was performed. The work-up was negative except for a low protein S activity (49%, normal 61–140%). Since pregnancy can artificially lower levels of protein S, we attempted to repeat the test postpartum. However, the patient had left the country and we were unable to repeat the test.

The patient delivered a female infant with Apgars 8 and 8 weighing 2360 g via a vacuum-assisted vaginal delivery at 37 weeks gestation. She resumed LMWH therapy postpartum and then transitioned to coumadin therapy which she continued for another 6 weeks. The patient was counselled to avoid oral contraceptive pills and was also advised that she would need prophylactic anticoagulation during any future pregnancies.


    Discussion
 Top
 Abstract
 Introduction
 Case report
 Discussion
 References
 
Thromboembolic disease associated with ovarian stimulation is an uncommon yet potentially fatal complication of assisted reproductive technology. Knowledge about its pathogenesis and prevention is limited. Stewart et al. (1997a)Go performed a review of cases of thromboembolic disease associated with ovulation induction and reported 54 cases between 1964 and 1997. The authors found that 66% of these cases were associated with OHSS and 84% were associated with pregnancy. In addition, 75% of cases were venous in origin while 25% were arterial thromboses (mostly intracerebral). Sixty per cent of venous sites were located in the upper limbs, neck and head.

We performed a review of all cases since Stewart et al.’s (1997a) paper and found an additional 42 cases of thromboembolism associated with ovulation induction (see Table I) some of which were included in a review by Ou et al. (2003)Go. Of the 97 cases to date, including the present report, 33% were arterial in origin while 67% were venous. Of the venous sites, 71% of reported cases involved the upper limb, neck and head veins. Seventy-seven per cent of cases were associated with pregnancy while 74% were associated with OHSS, mirroring the results obtained by Stewart et al. (1997a)Go.


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Table I. Summary of reported cases of thromboembolic disease following ovulation induction since 1997

 

While OHSS may be an important factor in the pathogenesis of thrombosis, it does not precede all cases. Severe OHSS is reported to account for 0.56–6.5% of all cases of OHSS (Pride et al., 1990Go) and it is estimated that one in 128 women with severe OHSS develops thromboembolic disease (Delvigne et al., 1993Go). Ovarian hyperstimulation is responsible for the presence of haemoconcentration, elevated estrogen levels along with reduced venous return caused by enlarged ovaries that may in part explain the development of DVT. In our review of the literature, 74% of cases of thromboembolism following ovulation induction were associated with OHSS. However, it is interesting to note that the thrombosis often presents weeks after resolution of the clinical syndrome, as was the case with our patient.

Kodama et al. (1996)Go showed that in pregnant patients with OHSS, thrombosis markers remained elevated for >3 weeks after the onset of OHSS with some persisting for >4 weeks. The authors concluded that disturbances of the coagulation system may persist even after the clinical symptoms of OHSS have resolved. Therefore, it is likely that thrombophilic tendencies associated with OHSS contributed to the DVT in our patient despite the fact that it occurred >2 weeks after the symptoms had resolved.

The incidence of venous thromboembolism in pregnancy has been estimated to be 1–2 per 1000 (Toglia and Weg, 1996Go). A meta-analysis by Ray and Chan (1999)Go showed that 21.9% of DVT during pregnancy occurred within the first trimester. This suggests an incidence of 1 in 2500 to 1 in 5000, 20–40-fold lower than what has been reported with OHSS. In addition, venous thromboembolism in pregnancy is most commonly located in the lower extremity with 70% occurring in the ileo-femoral region (Kyrle and Eichinger, 2005Go). In contrast, our review showed that the majority of thrombosis following ovarian stimulation occurred in the upper extremity. Therefore, it is likely that our patient’s complication was related to OHSS rather than pregnancy alone.

Not all cases of DVT following ovarian stimulation are associated with OHSS and not all patients with OHSS develop thromboembolism. Therefore, investigators have proposed that other predisposing factors must exist which act to precipitate thrombus formation. All patients who develop a thrombus deserve a work-up for the presence of thrombophilias. Several case reports have documented thromboembolism in patients with thrombophilias (Horstkamp et al., 1996Go; McGowan et al., 2003Go). Our patient had a possible protein S deficiency but no family or personal history of thromboembolism.

Should patients be screened for thrombophilias prior to IVF? Fabregues et al. (2004)Go suggested that thrombophilia screening in the general IVF population is not cost-effective and also reported that the prevalence of thrombophilia is not increased in women with severe OHSS. However, since the coexistence of thrombophilia and OHSS could have catastrophic sequelae, consideration should be given to screening patients with severe OHSS. Given the increased likelihood of thromboembolism, should patients with severe OHSS receive prophylactic anticoagulation regardless of thrombophilia testing? Stewart et al. (1997b)Go reported that they prescribe twice daily doses of heparin for hospitalized patients with OHSS. To our knowledge, there have been no randomized controlled studies to address these issues.

All of our IVF patients start baby aspirin at the onset of ovarian stimulation. Although it is possible that anticoagulation with low molecular weight heparin may be beneficial in cases of severe OHSS, it is not a uniformly established practice to give it to all women with OHSS. In a recent review on ovarian hyperstimulation by Navot (2001)Go, the concluding statement reads, ‘Most authors reserve treatment by heparin for special circumstances in which thromboembolic events have already occurred, or there is abnormal clotting, often owing to congenital coagulopathy. Although low dose preventive treatment with heparin is of some theoretical value, rapid alleviation of hemoconcentration is far more important.’ In our case, we promptly treated this patient by hydration and paracentesis in an effort to rapidly alleviate her haemoconcentration. Thrombosis unfortunately may occur despite appropriate management and even when prophylactic anticoagulation is administered (Hignett et al., 1995Go).

Our patient’s case is also notable for the location of the thrombosis in the subclavian vein. While lower extremity DVT may be considered a natural consequence of OHSS given the diminished venous return secondary to enlarged ovaries, we found that 71% of documented cases of venous thromboembolism secondary to ovulation induction are actually located in the upper extremity. It is unclear why there appears to be a predilection for thrombi in the upper extremities since none of the published case reports involves indwelling venous catheterization (the most common risk factor for upper extremity venous thrombosis). There is a possibility that lower extremity DVT has been underreported in the literature (Stewart et al., 1997bGo).

This case demonstrates a serious and potentially fatal complication of assisted reproductive treatment. Early diagnosis and treatment is crucial for both maternal and fetal well-being. Obstetricians should be aware that patients may present with symptoms of upper extremity DVT weeks after OHSS symptoms have resolved. Pregnant patients complaining of neck pain and swelling should undergo a thorough and complete evaluation for upper extremity DVT. In addition, consideration must be given to screening patients at risk for OHSS for thrombophilias as well as administering prophylactic heparin for patients who develop OHSS. Further clinical studies are required to elucidate the role of anticoagulation in patients with OHSS following ovulation induction.


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 Abstract
 Introduction
 Case report
 Discussion
 References
 
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Submitted on March 21, 2005; resubmitted on May 12, 2005; accepted on June 29, 2005.





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