Ovarian Vein Thrombosis

Review

HJOG 2022, 21 (4), 173-186 | doi: 10.33574/hjog.0516

Theoni Kanellopoulou

Department of Clinical Haematology, Blood Bank and Haemostasis, Onassis Cardiac Surgery Centre, Athens, Greece

Correspondence: Theoni Kanellopoulou, Onassis Cardiac Surgery Centre, Athens, Greece, e-mail: theokanel@gmail.com

Abstract

Ovarian vein thrombosis (OVT) is a rare type of venous thromboembolism most common diagnosed in the postpartum period and peaking around 2-6 days after delivery. Clinical symptoms are not specific including fever and abdominal pain and the right ovarian vein is more frequently involved (70-80% of cases). The diagnosis of OVT is a clinical challenge because there are multiple other conditions that can present similarly, including ovarian torsion, tubo-ovarian abscess, pelvic inflammatory disease, puerperal endometritis, appendicitis, inflammatory bowel disease and pyelonephritis. Ultrasound Doppler is the first-line imaging; however, most cases are confirmed with computed tomography or magnetic resonance imaging. Mortality related to ovarian vein thrombosis is low due to the combination treatment of broad-spectrum antibiotics and anticoagulation. Extension of thrombus to inferior vena cava or renal veins and rarely pulmonary embolism could also occur. OVT is actually a type of deep vein thrombosis that could be life-threatening however mortality is low due to the combination treatment of broad-spectrum antibiotics and anticoagulation. Anticoagulant treatment duration of 3 to 6 months has been recommended like typical cases of venous thromboembolism.

Keywords: Anticoagulation, ovarian vein, postpartum, thrombosis

Introduction

Ovarian vein thrombosis (OVT) is a rare condition most often seen in the immediate postpartum period that has been reported in approximately 0.01–0.18% of vaginal and in 2% of caesarian births. Although most cases occur in puerperal patients, OVT could also occur in other conditions like pelvic inflammatory diseases, malignancy, sepsis, pelvic surgeries and hypercoagulable states including autoimmune diseases or inherited thrombophilia factors. However, in 4 to 16% of cases, it can be classified as idiopathic.1-3

OVT remains poorly understood with no consensus regarding its importance and the best treatment approach. In this review article an attempt is made to highlight the risk factors that predispose to OVT, the common symptoms, the diagnostic approach, the complications and the recommended treatment.

Review of the Literature

A Pubmed search of English literature was performed in order to review reported cases of non-malignant OVT during the period 1980-2021.

Demographic Data – Risk Factors (Table 1)

Review of the literature revealed 208 patients with median age 31 years (range, 15-73 years). Cases with insufficient data were not analyzed.

Most cases (74.6%) were diagnosed postpartum;3-118 52.5% after vaginal delivery4,5,7,9,13-15,18,19,21-24, 27,29-34,36,38,41-48,50,51,55,60,62-64,66,71,74,76,77,79,80,84,86,88,92,93,96-101,105,108,111,113-115,118 and the rest after caesarian section.3,6,8,10-12,16,19,20,26,28,35,37,39,40,42,49,52,53,57-59,61,65,67,70,73,78,88-91,95-97,102,106,107,109,116,117 The analysis of puerperal patients shown 17 cases with multiple pregnancies (mostly twin)18,19,40,42,52,53,88,91,92,94,96,97,99,107,109,112 and in 28 cases a pregnancy complication was reported like urgent or preterm delivery, HELLP (Hemolysis, Elevated Liver Enzymes and low Platelets) syndrome, or other less frequent complications.8,17,30,39,49,54,56,57, 61,67,73,75,82,87,88,90,93,97,99,102,106,115,116

In non-puerperal related cases a possible endometrial reason was reported most common fibroids (11 cases)4,23 or intrauterine device (IUD) (4 cases).112 Twenty-one patients underwent pelvic surgery or other gynecological procedures, mostly hysterectomy (11 cases).10,16,21,25,26,59,60,120,122,124,125

Thrombophilia screening was performed only in a minority of cases. The most common inherited risk factor was heterozygocity of FV-Leiden. Other procoagulant risk factors included the presence of antiphospholipid antibodies or other risk factors including past medical history of thromboembolic disease or use of oral contraceptive pills (OCP).11,28,31,36,39,47,62,68,70,73,88

During COVID-19 pandemic, 7 cases have already been reported within a recent infection and more cases are expected to be published within 2022.7,13,128

Yet, in 17 cases a causal related-factor could not be prescribed and the case was reported as idiopathic.14,64,132

Symptoms

Symptoms are nonspecific. They include mainly lower abdominal tenderness with or without flank pain and fever that could be associated with tachycardia, chills, nausea and vomiting.

Diagnosis (Table 2)

In 84% of patients the diagnosis was made with non-invasive imaging techniques, mainly by computer tomography (CT) with contrast augmentation. In 15% of patients the diagnosis was made intraoperatively.4,30,38,42,43,46,47,54,59,71,76,83,86,87,92-94,99,101,103,111,112,114-116,118,136,140 88% of patients for whom the diagnosis was made during operation were postpartum and there was a highly suspicion of acute abdomen due to appendicitis before the diagnosis of OVT.

The localization was the right ovarian vein in 54% of reported cases,3,5-8,10,11,15,16,18,20,23-28,30-32,35,37,38,40-56,60-66,69,71-74,76-78,82,86,89,90-94,96-98,102,107,108,111,115,119,123,125,126,128-131,134-136,138,140,141,146,149 the left in 37%4,14,19,21,29,34,39,57,67,70,73,80,83,93,120,121,122,124,127,133,139,143,145 and both veins in 9%. 17,19,22,36,52,59,79,86,87,93,95,132,137,142

Extension of thrombus in inferior vena cava (IVC) was observed in 81 cases,5,6,9,11,12,16,18,20,22-28,31,35,37-42,45,46,48,50,53,55,56,61-67,71,73-75,77-79,85-90,93,96-99,102,105-109,115,118-120,126,129,132,140,146,149,154,157,161,162,164 in renal veins in 27 cases,21,22,28,29,39-41,59,66,70,77,93,96-98,103,106,109,124,127,133,149,157,158,164 iliac veins 11 cases.40,42,62,65,71,79,88,93,98,105 In 25 patients pulmonary embolism (PE) was also diagnosed.11,20,26, 40,42,48,61,62,65,71,73,79,89,98,119,120,126,132,139,140,149,157,161,162

Treatment

Anticoagulation treatment was given in the majority of cases (97%). Unfractionated heparin (UFH) or low molecular weight heparin (LMWH) was initiated in 70% of the cases and subsequently bridging to vitamin K antagonists (VKAs) in 40%.4,7,9,10,12,14,17,19,21, 23-28,30,34,36,39,42-46,48,51,55,59,60,64,65,67,73,74,79,82,89,91,96,98,99,102,105,106,109,115,118,120,121,122,129,138,144-147,152,154,159,161 In 14 patients novel direct oral anticoagulants (DOACs) were used.11,16,20,119,125,128,132,134,136,140-143,150 Thrombolysis with alteplase (tissue-type plasminogen activator-tPA) was given in 8 patients.66,71,77,78,90,105,133,149 One patient was treated with antiplatelet treatment with aspirin.101 IVC filter was implanted in 6 patients40,42,58,75,85,133,164 and surgical treatment with ligation was performed in 23 patients.22,38,53,61,63,76,80,83,84,88,95-97,100,113,114,116, 117,123,160,163

Septic thrombophlebitis was demonstrated in few cases with positive cultures (Table 3). However, antibiotics were administered in 123 patients (59%).4-7,9-12,15,17-19,22-34,37,38,41,43-48,51-53,56-60,62,63,65-67,71,72,74-80,82,84-86,88-99,101,102,105-109,111,114-118,120-124,126-128,135,144,154,156,160 In 4 patients a ureteral intervention was performed (either aspiration, stent insertion or nephrostomy).36,42,50,131 Three patients were also treated with immunosuppressive drugs.150,159,161

Follow-Up

The duration of anticoagulation treatment varied from less than one month to more than a year and in most of the cases there were no data about actual duration. Improvement was observed in 115 patients4,5,7,9,12,14-23,25-32,34,36,37,39-44,46-51,54,55,60,62-67,69-80,82-84,86,87,90,91,96-99,101,106-109,111,15,116,118-123,127,129,130,132-134,136,138,140,143,145-147,149,150,152,159-162 and adverse events in 6 patients53,84,93,95,126,139 including death in 3 patients.84,126,139

Discussion

Austin described the first known case of OVT in the postpartum setting in 1956.165 With the improvement in antiseptic techniques and the use of antibiotics, mortality has improved, but complications of OVT continue to be reported and include thrombus extension, PE, and ureteral obstruction.166

The pathogenesis of postpartum OVT is not clearly understood. The changes in fibrinolysis and coagulation during pregnancy are possibly the most important factors resulting in hypercoagulability in combination with the increase in the diameter and the capacity of the ovarian veins during pregnancy. It has also been demonstrated that the velocity of the blood flow in the ovarian veins decreases considerably immediately following delivery.1,166 History of thromboembolic disease, inherited thrombophilia or other concomitant diseases associated with hypercoagulability have not been directly correlated. Ιn the majority of reported cases of OVT, screening for thrombophilia risk factors was not performed. Salomon et al. retrospectively analyzed 22 patients with postpartum OVT and reported inherited prothrombotic risk factors in 50% of them; Five had heterozygocity of FV-Leiden and the rest either protein S deficiency or MTHFR C677T homozygocity. However, it should be noted that 73% had a caesarian section delivery.167 In present review of the literature, thrombophilia screening was performed in a minority of reported cases and the most common reported inherited prothrombotic risk factor was heterozygocity of FV-Leiden.

Diagnosis requires a very high index of suspicion owing to its rarity and non-specific presentation. In the past, before the introduction into clinical practice of modern imaging techniques, diagnosis in most cases was based only on laparotomy. Nowadays, the diagnosis of OVT has become easier with non-invasive imaging techniques. Ultrasound is the initial imaging study of choice as it is inexpensive, free of radiation and doesn’t require intravenous contrast. However, detection rates for OVT are poor, because it may not show the entire length of the vein in most cases secondary to obesity and/or overlying bowel gas.168 In those cases the diagnosis could be made by CT with contrast augmentation or magnetic resonance imaging (MRI). On the other hand, symptomatic presentations are less common than those who are asymptomatic that makes the suspicion of OVT even more difficult. The rise in the use of imaging may identify OVT that may not have been otherwise clinically evident. The incidence of OVT is higher in the right ovarian vein, with 70–90% of cases occurring on the right side, whereas 11–14% is bilateral. This is apparently from the longer length and the lack of competent valves on the right side.151 Equivalent percentages are also observed in this review article and in almost 90% of cases the OVT occurred in the right ovarian vein. However, in the analysis by Assal et al. there was a similar incidence of right and left OVT (44.6 versus 41.4%, respectively) with a high percentage of bilateral thrombi (14.0%). Though, when the peripartum group was examined separately, a significantly higher incidence of right OVT (60%) and bilateral OVT (25%) was noted (P. 0.03).166

OVT is usually managed conservatively and most patients respond to antibiotics, anticoagulation, hydration and bed rest. Appropriate medical treatment should be started soon after diagnosis is confirmed to prevent serious complications. Heparin and warfarin have been traditionally used even in the postpartum period because are considered safe during lactation. To date, there are no data to support the use of DOACs in OVT. Single case reports and small series of patients have demonstrated good efficacy and safety in patients with portal vein thrombosis and cerebral venous thrombosis. These results are promising and may possibly extend the use of DOACs in other rare types of thrombosis as OVT. In literature there are few reports of patients with OVT treated with DOACs that showed similar efficacy with traditional treatment. However, in postpartum cases DOACs are contraindicated during lactation as they are excreted into breast milk. Thrombolytic drugs (alteplase, urokinase) have been used in few cases but are associated with a high risk of bleeding therefore they should be reserved for patients with massive thrombosis. Retrievable IVC filters can be used in cases of active bleeding including emergent surgical cases where anticoagulation is contraindicated or who have had a PE while on therapeutic anticoagulation. Surgical treatment with ovarian vein excision or ligation is rarely performed nowadays and is indicated only after the failure of conservative therapy or when the risk of PE is high. Initiation and appropriate duration of anticoagulation are also a matter of debate. Some argue that incidentally found OVT related to surgery may not need anticoagulation unless complications are noted116 while a majority of experts believe rare thrombosis should be treated like lower extremity deep vein thrombosis (DVT).169 There are no definitive guidelines for duration of anticoagulation. Some case reports suggest repeating imaging after 40 or 60 days and stopping anticoagulation if the resolution of thrombus or calcification is noted on follow-up imaging.

Even if prompt administration of anticoagulation is administered, thrombus expansion into the IVC and PE may develop. In fact, the risk of PE is up to 13% in cases with mortality of approximately 4%.170 In the cohort of Assal et al. 9.9% of patients experienced recurrent VTE events, mostly DVT (82%) with average time to recurrence 409 days. All patients with recurrence were not during postpartum period and there recurrence was more common in patients with left OVT and bilateral OVT as compared with right OVT (P 0.01). The VTE recurrence rate in patients with a history of VTE was almost twice that of the overall group (18.2%), but was not statistically significant. Conversely, no statistically significant association between recurrence rate and a predisposing factor has been found. Moreover, even if there was a reduction in venous thromboembolism recurrence in the group that received anticoagulation, the results were not significant.171

OVT associated with septic pelvic thrombophlebitis could evolve into septic shock or emboli, which have a high mortality rate. Thus, physicians should consider OVT in any woman in the peripartum period, after pelvic operations or in the setting of gynecological malignancy, with unexplained fever and lower abdominal pain not responding to antibiotics and analgesics and suggestive of acute appendicitis, endometritis, hydronephrosis, or ovarian torsion. A high index of suspicion and the ability to rule out other processes that may produce similar symptoms is important, because untreated OVT could even prove fatal. Prompt diagnosis and management especially in cases that mimic acute abdomen especially in the current endemic context of COVID-19 where thromboembolic complications are common. With the ongoing pandemic, the number of such cases is only expected to rise, and OVT should be a part of the differential.

References
  1. Riva N, Calleja-Agius J. Ovarian Vein Thrombosis: A Narrative Review. Hamostaseologie. 2021; 41:257-266.
  2. Sharma P, Abdi S. Ovarian vein thrombosis. Clin Radiol. 2012;67:893-8.
  3. Dunphy L, Tang AW. Ovarian vein thrombosis in the postnatal period. BMJ Case Rep. 2021;14:e243872.
  4. Tesfaye S, Tariku M, Hirigo AT. Postpartum left ovarian vein thrombosis. SAGE Open Med Case Rep. 2020 Sep 30;8:2050313X20962637.
  5. Ben Oun M, Skraková M, Paulovičová M, Adamec A, Vargová M, Korbeľ M. Postpartum ovarian vein thrombosis: case report and review of literature. Ceska Gynekol. 2020 Winter;85:254-258..
  6. Chiang TL, Chang CY, Ong JR. Postpartum ovarian vein thrombophlebitis presenting as vaginal bleeding: A case report. Medicine (Baltimore). 2021;100:e24632.
  7. Fatimazahra M, Harras ME, Bensahi I, Kassimi M, Oualim S, Elouarradi A, Abdeladim S, Sabry M. Ovarian vein thrombosis after coronavirus disease (COVID-19) mimicking acute abdomen: two case reports. J Thromb Thrombolysis. 2021;52:493-496.
  8. Teytelbaum DE, Meade JD, Swanson J. Ovarian vein thrombosis: a potential clinical consequence of ruptured ectopic pregnancy. BMJ Case Rep. 2021;14:e240940.
  9. Zabihi Mahmoudabadi H, Najjari K, Oklah E, Kor F. Ovarian vein and IVC thrombosis due to normal vaginal delivery; a case report and literature review. Int J Surg Case Rep. 2021;83:105975.
  10. Shi Q, Gandi DS, Hua Y, Zhu Y, Yao J, Yang X, Xu Y, Zhang Y. Postpartum septic pelvic thrombophlebitis and ovarian vein thrombosis after caesarean section: a rare case report . BMC Pregnancy Childbirth. 2021;21:561.
  11. Finianos ES, Yacoub SF, Chammas MF. Ovarian Vein Thrombosis Complicated by Pulmonary Embolism after Cesarean Delivery in the Presence of a Large Fibroid: Case Report and Literature Review of Contributing Factors. Case Rep Obstet Gynecol. 2021;2021:6389713.
  12. Yapar Eyi, E.G., Halıcı Öztürk, F. and Alkan, M. (2020), Cover Information. J Clin Ultrasound, 48: i-i.
  13. Veyseh M, Pophali P, Jayarangaiah A, Kumar A. Left gonadal vein thrombosis in a patient with COVID-19-associated coagulopathy. BMJ Case Rep. 2020;13:e236786.
  14. Alalqam MM, Al Abbas R, Abualsaud AS, AlQattan AS, Almabyouq F. The challenges of diagnosing idiopathic ovarian vein thrombosis: Case report. Int J Surg Case Rep. 2019;60:63-65.
  15. Abrantes J, Teixeira E, Gomes F, Fernandes C. Postpartum ovarian vein thrombosis and venous anatomical variation. BMJ Case Rep. 2019;12:e228399.
  16. Naoum J, Mohsen A, Daher J, Eid T. Novel management of ovarian vein thrombosis: A case report. Saudi Pharm J. 2018 Jul;26(5):608-610.
  17. Ghimire A, Singh M, Bista KD, Ojha N, Bajracharya S, Katuwal N. An Unusual Case of Acute Abdomen: Ovarian Vein Thrombosis. J Nepal Health Res Counc. 2018;16:102-104.
  18. Khalid S, Khalid A, Daw H. A Case of Postpartum Ovarian Vein Thrombosis. Cureus. 2018;10:e2134.
  19. Østergaard S, Hvas AM, Medrud L, Fuglsang J. Ovarian vein thrombosis after delivery. Hamostaseologie. 2018 Feb;38(1):9-10.
  20. Oda Y, Fujita M, Motohisa C, Nakata S, Shimada M, Komatsu R. Pulmonary embolism caused by ovarian vein thrombosis during cesarean section: a case report. JA Clin Rep. 2018;4(1):3.
  21. Barros NA, Torrão MM, Ferreira M, Pinheiro A. Left ovarian and renal vein thrombosis after emergency postpartum hysterectomy. BMJ Case Rep. 2016;2016:bcr2016216292.
  22. Egawa M, Miyasaka N, Kubo T, Naitou M, Ito T, Kubota T. A case of puerperal group a streptococcal sepsis complicated by ovarian vein thrombosis. J Obstet Gynaecol. 2016;36:857-858.
  23. Sorbi F, Mannini L, Aldinucci M, Ghizzoni V, Fambrini M. Ovarian Vein Thrombosis Presenting as Acute Abdomen in Puerperium. J Clin Diagn Res. 2016;10:QD03-4.
  24. Djakovic I, Mustapic M, Marleku F, Grgic O, Djakovic Z, Kosec V. Ovarian vein thrombosis–a case report. Acta Clin Belg. 2015;70:445-6.
  25. Gupta A, Gupta N, Blankstein J, Trester R. Ovarian Vein Thrombosis as a Complication of Laparoscopic Surgery. Case Rep Obstet Gynecol. 2015; 2015:682941.
  26. Jenayah AA, Saoudi S, Boudaya F, Bouriel I, Sfar E, Chelli D. Ovarian vein thrombosis. Pan Afr Med J. 2015;21:251.
  27. Parino E, Mulinaris E, Saccomano E, Gallo JC, Kohan G. Postpartum Ovarian Vein Thrombophlebitis with Staphylococcal Bacteremia. Case Rep Infect Dis. 2015;2015:589436.
  28. Togan T, Turan H, Cifci E, Çiftci C. Ovarian and Renal Vein Thrombosis: A Rare Cause of Fever Outer the Postpartum Period. Case Rep Obstet Gynecol. 2015;2015:817862.
  29. Liu S, Wen J. Ovarian Vein Thrombosis with Involvement of the Renal Vein After Cesarean Section. A Case Report. J Reprod Med. 2015;60:269-72.
  30. Mone F, McKeown G, Adams B. Ovarian vein thrombosis in pregnancy and the puerperium – A case series. J Obstet Gynaecol. 2015;35:853-4.
  31. Farran HE, Haddad AG, Radwan AH, Nassar AH, Hourani R, Taher AT. Post-partum ovarian vein thrombosis: combined effect of infection and factor v leiden mutation. Turk J Haematol. 2015;32:80-1.
  32. De Cuyper K, Eyselbergs M, Bernard P, Clabout L, Vanhoenacker FM. Added value of diffusion weighted MR imaging in the diagnosis of postpartum ovarian vein thrombosis. JBR-BTR. 2014;97:242-4.
  33. Karrasch M, Rödel J, Mühler N, Edel B, Sachse S, Schmidt KH, Schneider U, Schlembach D, Mentzel HJ, Pfister W, Schleußner E. Ovarian vein thrombosis (OVT) following invasive group A Streptococcus (iGAS) puerperal sepsis associated with expression of streptococcal pyrogenic exotoxin genes speC, speG and speJ. Eur J Obstet Gynecol Reprod Biol. 2015;184:127-30.
  34. Bhandari HM, Jeevan D, Slinn J, Goswami K. Postpartum ovarian vein thrombosis in a 29-year-old woman with ulcerative colitis. BMJ Case Rep. 2014;2014:bcr2014206452.
  35. Herek D, Kocyigit A, Yagci AB. Total right ovarian vein thrombosis after cesarean section. J Emerg Med. 2015;48:e25-7.
  36. Vendittelli F, Savary D, Storme B, Rieu V, Chabrot P, Charpy C, Lémery D, Jacquetin B. Ovarian thrombosis and uterine synechiae after arterial embolization for a late postpartum haemorrhage. Case Rep Womens Health. 2014;5:1-4.
  37. Arslan H, Ada S, Celik S, Toptaş T. Postpartum ovarian vein and inferior vena cava thrombosis. Case Rep Med. 2014;2014:609187.
  38. Adesiyun AG, Samaila MO, Ojabo A. Postpartum ovarian vein thrombosis: incidental diagnosis at surgery. Case Rep Obstet Gynecol. 2014; 2014: 898342.
  39. Guler S, Kokoglu OF, Ucmak H, Ozkan F. Postpartum ovarian vein thrombosis and renal vein thrombosis in a woman with protein S and C deficiency. BMJ Case Rep. 2013;2013:bcr2013009164.
  40. Fiengo L, Bucci F, Patrizi G, Giannotti D, Redler A. Postpartum deep vein thrombosis and pulmonary embolism in twin pregnancy: undertaking of clinical symptoms leading to massive complications. Thromb J. 2013;11:4.
  41. Bilgin M, Sevket O, Yildiz S, Sharifov R, Kocakoc E. Imaging of postpartum ovarian vein thrombosis. Case Rep Obstet Gynecol. 2012;2012:134603.
  42. Angelini M, Barillari G, Londero AP, Bertozzi S, Bernardi S, Petri R, Driul L, Marchesoni D. Puerperal ovarian vein thrombosis: two case reports. J Thromb Thrombolysis. 2013;35:286-9.
  43. Hoffmann J, Amaya B, Grothoff M, Schrock C, Lampe D. Ovarian vein thrombosis as a rare cause of postpartal abdominal pain: a case report. Arch Gynecol Obstet. 2012;286:1331-2.
  44. Arkadopoulos N, Dellaportas D, Yiallourou A, Koureas A, Voros D. Ovarian vein thrombosis mimicking acute abdomen: a case report and literature review. World J Emerg Surg. 2011;6:45.
  45. Dhinakar M, Dhinakar L, Kamona A, Saifudeen A. Puerperal ovarian vein thrombosis presenting as Rt loin pain and hydronephrosis: report of 2 cases. Oman Med J. 2010;25:299-302.
  46. Basili G, Romano N, Bimbi M, Lorenzetti L, Pietrasanta D, Goletti O. Postpartum ovarian vein thrombosis. JSLS. 2011;15:268-71.
  47. Wiggermann P, Stroszczynski C. Images in clinical medicine. Ovarian-vein thrombosis. N Engl J Med. 2011;364:1544.
  48. Khlifi A, Kebaili S, Hammami M, Berregaya L, Hidar S, Affes N, Khairi H. Postpartum ovarian vein thrombophlebitis: Report of a case and review of the literature. N Am J Med Sci. 2010;2:389-91.
  49. Kafali H, Onaran YA, Keskin E, Sari U, Kirbas I. Ovarian vein thrombosis and mirror syndrome in association with sacrococcygeal teratoma. Clinics (Sao Paulo). 2010;65:452-5.
  50. Holmström SW, Barrow BP. Postpartum ovarian vein thrombosis causing severe hydronephrosis. Obstet Gynecol. 2010;115(2 Pt 2):452-454.
  51. Kolluru A, Lattupalli R, Kanwar M, Behera D, Kamalakannan D, Beeai MK. Postpartum ovarian vein thrombosis presenting as ureteral obstruction. BMJ Case Rep. 2010;2010:bcr0320102863.
  52. Akinbiyi AA, Nguyen R, Katz M. Postpartum ovarian vein thrombosis: two cases and review of literature. Case Rep Med. 2009;2009:101367.
  53. Kuehnl A, Assadian A, Reeps C, Schneider KT, Stangl M, Berger H, Eckstein HH. Floating caval thrombus arising from the ovarian vein. Ann Vasc Surg. 2009;23:688.e7-9.
  54. Tzortzatos G, Sioutas A, Beckman MO. Ovarian vein thrombosis in the first trimester of pregnancy. Thromb Haemost. 2009;102:601-2.
  55. Johnson A, Wietfeldt ED, Dhevan V, Hassan I. Right lower quadrant pain and postpartum ovarian vein thrombosis. Uncommon but not forgotten. Arch Gynecol Obstet. 2010;281:261-3.
  56. Suleyman T, Gultekin H, Abdulkadir G, Tevfik P, Abdulkerim UM, Ali A, Ismail K. Acute right lower quadrant abdominal pain as the presenting symptom of ovarian vein thrombosis in pregnancy. J Obstet Gynaecol Res. 2008;34:680-2.
  57. Royo P, Alonso-Burgos A, García-Manero M, Lecumberri R, Alcázar JL. Postpartum ovarian vein thrombosis after cesarean delivery: a case report. J Med Case Rep. 2008 ;2:105.
  58. Sinha S, Roman AS, Cayne NS, Saltzberg S, Rebarber A. Use of a retrievable suprarenal inferior vena cava filter as a primary intervention for postpartum ovarian vein thrombosis: a case report. J Reprod Med. 2008;53:135-7.
  59. Klima DA, Snyder TE. Postpartum ovarian vein thrombosis. Obstet Gynecol. 2008;111:431-5.
  60. Hakim FA, Khan NN, Qushmaq KA, Al-Shami SY. An unusual presentation of postpartum ovarian vein thrombosis. Saudi Med J. 2007;28:273-5.
  61. Carr S, Tefera G. Surgical treatment of ovarian vein thrombosis. Vasc Endovascular Surg. 2006; 40:505-8.
  62. Hammami S, Golli M, Addad F, Hafsa C, Hamzaoui A, Mahjoub S, Gannouni A. An unusual case of Behçet’s disease presenting with postpartum ovarian iliac vein thrombosis and pulmonary embolism. Thromb J. 2006;4:20..
  63. Takach TJ, Cervera RD, Gregoric ID. Ovarian vein and caval thrombosis. Tex Heart Inst J. 2005; 32:579-82.
  64. Yildirim E, Kanbay M, Ozbek O, Coskun M, Boyacioglu S. Isolated idiopathic ovarian vein thrombosis: a rare case. Int Urogynecol J Pelvic Floor Dysfunct. 2005;16:308-10.
  65. Sinha D, Yasmin H, Samra JS. Postpartum inferior vena cava and ovarian vein thrombosis–a case report and literature review. J Obstet Gynaecol. 2005;25:312-3.
  66. Ortín X, Ugarriza A, Espax RM, Boixadera J, Llorente A, Escoda L, Cabezudo E. Postpartum ovarian vein thrombosis. Thromb Haemost. 2005;93:1004-5.
  67. El Sakka M, Sharara H. Postpartum ovarian vein thrombosis with massive inferior vena cava thrombus formation. J Obstet Gynaecol. 1999;19:76-7.
  68. Morales-Roselló J, Villa P, Amrani M. Postpartum ovarian vein thrombosis with positive lupus anticoagulant. Int J Gynaecol Obstet. 200;87:163-4.
  69. Scialpi M, Di Maggio A, Trisciuzzi G, Resta MC, Lupattelli L, Rotondo A. Postpartum ovarian vein thrombosis with simultaneous pyelocaliectasis: diagnosis and follow-up by MR imaging. Case report and literature review. Emerg Radiol. 2003;10:60-3.
  70. Roqué H, Stephenson C, Lee MJ, Funai EF, Popiolek D, Kim E, Hart D. Pregnancy-related thrombosis in a woman with congenital afibrinogenemia: a report of two successful pregnancies. Am J Hematol. 2004;76:267-70.
  71. Prieto-Nieto MI, Perez-Robledo JP, Rodriguez-Montes JA, Garci-Sancho-Martin L. Acute appendicitis-like symptoms as initial presentation of ovarian vein thrombosis. Ann Vasc Surg. 2004;18:481-3.
  72. Beigi RH, Wiensenfeld HC. Enoxaparin for postpartum ovarian vein thrombosis. A case report. J Reprod Med. 2004;49:55-7.
  73. André M, Delèvaux I, Amoura Z, Corbi P, Courthaliac C, Aumaître O, Piette JC. Ovarian vein thrombosis in the antiphospholipid syndrome. Arthritis Rheum. 2004;50:183-6.
  74. Al-toma A, Heggelman BG, Kramer MH. Postpartum ovarian vein thrombosis: report of a case and review of literature. Neth J Med. 2003;61:334-6.
  75. Rochelson B, Scher L, Warshawsky R, Simon D. Use of a temporary vena cava filter in a woman with septic abortion and inferior vena cava thrombosis. A case report. J Reprod Med. 2003;48:557-9.
  76. Dessole S, Capobianco G, Arru A, Demurtas P, Ambrosini G. Postpartum ovarian vein thrombosis: an unpredictable event: two case reports and review of the literature. Arch Gynecol Obstet. 2003;267:242-6.
  77. Rajab KE, Malik N, Skirman JH. Septic postpartum ovarian vein thrombosis. Saudi Med J. 2002; 23:1136-8.
  78. Lee EH, Im CY, Kim JW. Ultrasound diagnosis of postpartum ovarian vein thrombosis: case report. Ultrasound Obstet Gynecol. 2001;18:384-6.
  79. Jassal DS, Fjeldsted FH, Smith ER, Sharma S. A diagnostic dilemma of fever and back pain postpartum. Chest. 2001;120:1023-4.
  80. Gourlay M, Gutierrez C, Chong A, Robertson R. Group A streptococcal sepsis and ovarian vein thrombosis after an uncomplicated vaginal delivery. J Am Board Fam Pract. 2001;14:375-80.
  81. Warde L, McDermott EW, Hill AD, Gibney RG, Murphy JJ. Post-partum ovarian vein thrombosis. J R Coll Surg Edinb. 2001;46:246-8.
  82. Sreenarasimhaiah S, McAlister R. Ovarian vein thrombosis after elective abortion. Obstet Gynecol. 2000;96:828-30.
  83. Hill DA. Late-onset puerperal ovarian vein thrombophlebitis treated laparoscopically. J Am Assoc Gynecol Laparosc. 2000;7:261-3.
  84. Hippach M, Meyberg R, Villena-Heinsen C, Mink D, Ertan AK, Schmidt W, Friedrich M. Postpartum ovarian vein thrombosis. Clin Exp Obstet Gynecol. 2000;27:24-6.
  85. Clarke CS, Harlin SA. Puerperal ovarian vein thrombosis with extension into the inferior vena cava. Am Surg. 1999;65:147-50.
  86. Quane LK, Kidney DD, Cohen AJ. Unusual causes of ovarian vein thrombosis as revealed by CT and sonography. AJR Am J Roentgenol. 1998;171:487-90.
  87. Bertsch NM, Mastrobattista JM, Kawashima A, Kramer LA. Antepartum bilateral ovarian vein thrombosis: magnetic resonance imaging diagnosis. Am J Perinatol. 1997;14:597-9.
  88. Giraud JR, Poulain P, Renaud-Giono A, Darnault JP, Proudhon JF, Grall JY, Mocquet PY. Diagnosis of post-partum ovarian vein thrombophlebitis by color Doppler ultrasonography: about 10 cases. Acta Obstet Gynecol Scand. 1997;76:773-8.
  89. Sherer DM, Fern S, Mester J, Barnhard Y, Divon MY. Postpartum ultrasonographic diagnosis of inferior vena cava thrombus associated with ovarian vein thrombosis. Am J Obstet Gynecol. 1997;177:474-5.
  90. Wernekinck C, Dahmane N, Persson A, Thomassen P. Ovarian vein thrombosis with symptoms prior to term–a case report. Eur J Obstet Gynecol Reprod Biol. 1997;74:99-102.
  91. Skinner J, Greene RA, Stuart B. Puerperal ovarian vein thrombosis in a triplet pregnancy complicated by a single intrauterine death. J Obstet Gynaecol. 1997;17:585.
  92. Adkins J, Wilson S. Unusual course of the gonadal vein: a case report of postpartum ovarian vein thrombosis mimicking acute appendicitis clinically and sonographically. J Ultrasound Med. 1996; 15:409-12.
  93. Witlin AG, Sibai BM. Postpartum ovarian vein thrombosis after vaginal delivery: a report of 11 cases. Obstet Gynecol. 1995;85:775-80.
  94. Van Hoe L, Baert AL, Marchal G, Spitz B, Penninckx F. Thrombosed ovarian vein collateral mimicking acute appendicitis on CT. J Comput Assist Tomogr. 1994;18:643-6.
  95. Govaerts I, Braude P, De Paepe J, Kirkpatrick C. Postpartum ovarian veins thrombophlebitis. Eur J Obstet Gynecol Reprod Biol. 1994;57:56-8.
  96. Chawla K, Mond DJ, Lanzkowsky L. Postpartum ovarian vein thrombosis. Am J Emerg Med. 1994; 12:82-5.
  97. Hassen-Khodja R, Gillet JY, Batt M, Bongain A, Persch M, Libo L, Declemy S, Checler E, LeBas P. Thrombophlebitis of the ovarian vein with free-floating thrombus in the inferior vena cava. Ann Vasc Surg. 1993;7:582-6.
  98. Magee KP, Blanco JD, Graham JM. Massive septic pelvic thrombophlebitis. Obstet Gynecol. 1993; 82:662-4.
  99. Simons GR, Piwnica-Worms DR, Goldhaber SZ. Ovarian vein thrombosis. Am Heart J. 1993; 126: 641-7.
  100. Toland KC, Pelander WM, Mohr SJ. Postpartum ovarian vein thrombosis presenting as ureteral obstruction: a case report and review of the literature. J Urol. 1993;149:1538-40.
  101. Keogh J, MacDonald D, Kelehan P. Septic pelvic thrombophlebitis: an unusual treatable postpartum complication. Aust N Z J Obstet Gynaecol. 1993;33:204-7.
  102. Grant TH, Schoettle BW, Buchsbaum MS. Postpartum ovarian vein thrombosis: diagnosis by clot protrusion into the inferior vena cava at sonography. AJR Am J Roentgenol. 1993;160:551-2.
  103. Reddy SC, Reddy SC. Ovarian vein thrombophlebitis diagnosed by computerized tomography. South Med J. 1989;82:1425-8.
  104. Warde L, McDermott EW, Hill AD, Gibney RG, Murphy JJ. Post-partum ovarian vein thrombosis. J R Coll Surg Edinb. 2001;46:246-8.
  105. Khurana BK, Rao J, Friedman SA, Cho KC. Computed tomographic features of puerperal ovarian vein thrombosis. Am J Obstet Gynecol. 1988;159:905-8.
  106. Rozier JC Jr, Brown EH Jr, Berne FA. Diagnosis of puerperal ovarian vein thrombophlebitis by computed tomography. Am J Obstet Gynecol. 1988; 159:737-40.
  107. Baran GW, Frisch KM. Duplex Doppler evaluation of puerperal ovarian vein thrombosis. AJR Am J Roentgenol. 1987;149:321-2.
  108. Martin B, Mulopulos GP, Bryan PJ. MRI of puerperal ovarian-vein thrombosis (case report). AJR Am J Roentgenol. 1986;147:291-2.
  109. Bahnson RR, Wendel EF, Vogelzang RL. Renal vein thrombosis following puerperal ovarian vein thrombophlebitis. Am J Obstet Gynecol. 1985; 152:290-1.
  110. Berlin M, Fleishman P. Puerperal ovarian vein thrombosis. Int Surg. 1985;70:179-80.
  111. Tang LC, Woo JS, Choo YC. Puerperal ovarian vein thrombophlebitis. Postgrad Med J. 1985; 61:179-80.
  112. Adachi A, Segen J, Li JK. Ovarian vein thrombosis mimicking ectopic pregnancy. N Y State J Med. 1984;84:567-8.
  113. Warhit JM, Fagelman D, Goldman MA, Weiss LM, Sachs L. Ovarian vein thrombophlebitis: diagnosis by ultrasound and CT. J Clin Ultrasound. 1984;12:301-3.
  114. Wilson PC, Lerner RM. Diagnosis of ovarian vein thrombophlebitis by ultrasonography. J Ultrasound Med. 1983;2:187-90.
  115. Fong DY, Salmon PA. Diagnosis and treatment of postpartum ovarian vein thrombosis. Can Med Assoc J. 1982;126:661-2.
  116. Trang N, Kalluri M, Bajaj T, Petersen G. Idiopathic Left Ovarian Vein Thrombosis. J Investig Med High Impact Case Rep. 2020;8:2324709620947257.
  117. Shaffer PB, Johnson JC, Bryan D, Fabri PJ. Case report. Diagnosis of ovarian vein thrombophlebitis by computed tomography. J Comput Assist Tomogr. 1981;5:436-9.
  118. Rao AK, Zucker M, Sacks D. Right ovarian vein thrombosis with extension to the inferior vena cava. Br J Radiol. 1980;53:160-1.
  119. Nakamura S, Tokunaga T, Yamaguchi A, Kono T, Kasano K, Yoshiwara H, Hattori E, Niwa A, Hirao K. Paradoxical embolism caused by ovarian vein thrombosis extending to inferior vena cava in a female with uterine myoma. J Cardiol Cases. 2018;18:207-209.
  120. Takeda A, Yamase Y, Koike W, Hayashi S, Imoto S, Nakamura H. Pulmonary thromboembolism as a result of ovarian vein thrombosis after laparoscopic-assisted vaginal hysterectomy for uterine myoma. J Obstet Gynaecol Res. 2016;42:743-747.
  121. Haynes MC, Lu BY, Winkel AF. Ovarian vein thrombophlebitis related to large uterine myoma. Obstet Gynecol. 2014;123:450-453.
  122. Tanaka Y, Kato H, Hosoi A, Isobe M, Koyama S, Shiki Y. Ovarian vein thrombosis following total laparoscopic hysterectomy. Asian J Endosc Surg. 2012;5:179-82.
  123. Wu CJ, Huang KH, Liu JY. Ovarian vein thrombosis associated with compression by a uterine myoma. Eur J Obstet Gynecol Reprod Biol. 2011;159:485-7.
  124. Gayer G. Ovarian vein thrombosis–computerized tomography diagnosis. Isr Med Assoc J. 2001; 3:627-8.
  125. Kumar A, Gupta S. Ovarian Vein Thrombosis Can Be a Complication of Hysteroscopy. Cureus. 2021;13:e16196.
  126. Roepke RML, de Campos FPF, Lovisolo SM, Santos EHS. Septic pelvic thrombophlebitis of unknown origin: an ever threatening entity. Autops Case Rep. 2014;4:39-46.
  127. Rousset J, Garetier M, Chinellato S, Barberot C, Feuvrier Y, Nicolas X, le Bivic T. Ovarian venous thrombosis during septicemia due to Fusobacterium necrophorum. Diagn Interv Imaging. 2012; 93:894-6.
  128. Vurture G, Palmieri A, Jacobson N. Ovarian Vein Thrombosis after Pelvic Surgery in Patient with Recent Coronavirus Disease. J Minim Invasive Gynecol. 2021;28:1951-1952.
  129. Minagawa M, Etoh M, Masuda M, Kurihara K, Fukuyama M, Yamamoto A, Katoh S, Fujita H. Transient elevations of liver enzymes and ovarian vein thrombosis arising after total laparoscopic hysterectomy. Gynecol Minim Invasive Ther. 2017;6:205-206.
  130. Al-Αchmar SN, Stavrou S, Protopapas A, Drakakis P, Siemou P, Chatzipapas I. Ovarian vein thrombosis after total laparoscopic hysterectomy with unilateral adnexectomy: A case report. Int J Surg Case Rep. 2017;41:1-4.
  131. Ho L, Hall G, Thomas R, Beiko D. Ovarian vein thrombosis: A complication of percutaneous nephrolithotomy. Can Urol Assoc J. 2016; 10:E309-E311.
  132. Garcia R, Gasparis AP, Loh SA, Labropoulos N. A rare case of idiopathic bilateral ovarian vein thrombosis. J Vasc Surg Venous Lymphat Disord. 2017;5:567-570.
  133. Cook RM, Rondina MT, Horton DJ. Rivaroxaban for the Long-term Treatment of Spontaneous Ovarian Vein Thrombosis Caused by Factor V Leiden Homozygosity. Ann Pharmacother. 2014; 48:1055-1060.
  134. DeBoer RE, Oladunjoye OO, Herb R. Right Ovarian Vein Thrombosis in the Setting of COVID-19 Infection. Cureus. 2021;13:e12796.
  135. Badrawi N, Abdulghaffar S. Ovarian vein thrombosis as a first manifestation of COVID-19 infection. Radiol Case Rep. 2021;16:3491-3493.
  136. Glanzer R, Rogers N, Patrick RJ, Hassebroek-Johnson J. Diagnostic laparoscopy and oophorectomy for ovarian vein thrombosis in a patient with COVID-19: a surgical case report and literature review. J Surg Case Rep. 2021;2021:rjab389.
  137. Christy J, Jarugula D, Kesari K, Kunadi A. Idiopathic bilateral ovarian vein thrombosis. BMJ Case Rep. 2021;14:e238243.
  138. Al-Shokri SD, Sardar S, Shajeedha Ameerudeen F, Abdul Moqeeth M. Non-pregnancy-related ovarian vein thrombosis: A rare cause of chronic abdominal pain. Qatar Med J. 2021;2021:13.
  139. Ogiwara M, Ozaki M, Nishino Y, Miyahara T. Fatal pulmonary thromboembolism caused by idiopathic ovarian vein thrombosis. Respirol Case Rep. 2021;9:e00795.
  140. Li W, Cao S, Zhu R, Chen X. Idiopathic ovarian vein thrombosis causing pulmonary embolism: case report and literature review. J Int Med Res. 2021;49:3000605211010649.
  141. Tahir N, Sherchan R, Farooqi A, Shrestha J, Jeelani HM. Idiopathic Ovarian Vein Thrombosis: A Rare Cause of Abdominal Pain. Cureus. 2021; 13:e16756.
  142. Basit A, Kaur P, Villanueva DM, Tahir M, Sonnenschine M. Idiopathic Bilateral Ovarian Vein Thrombosis in a Non-Pregnant Healthy Patient: A Case Report and Review of the Literature. Cureus. 2020;12:e10111.
  143. Trang N, Kalluri M, Bajaj T, Petersen G. Idiopathic Left Ovarian Vein Thrombosis. J Investig Med High Impact Case Rep. 2020;8:2324709620947257.
  144. Khishfe BF, Sankovsky A, Nasr I. Idiopathic ovarian vein thrombosis: a rare cause of abdominal pain. Am J Emerg Med. 2016;34:935.e1-2.
  145. Doherty K, New M. Idiopathic ovarian vein thrombosis in a nonperipartum patient. Obstet Gynecol. 2015;125:1468-1470.
  146. Harris K, Mehta S, Iskhakov E, Chalhoub M, Maniatis T, Forte F, Alkaied H. Ovarian vein thrombosis in the nonpregnant woman: an overlooked diagnosis. Ther Adv Hematol. 2012;3:325-8.
  147. Stafford M, Fleming T, Khalil A. Idiopathic ovarian vein thrombosis: a rare cause of pelvic pain – case report and review of literature. Aust N Z J Obstet Gynaecol. 2010;50:299-301.
  148. Graupera B, Pascual MA, Garcia P, Di Paola R, Ubeda B, Tresserra F. Atypical ultrasonographic presentation of ovarian vein thrombosis. Eur J Gynaecol Oncol. 2011;32:439-40.
  149. Razvi K, Al-Katib M, McCall J, Barton DP. Suprarenal vena caval thrombosis and pulmonary embolism associated with a benign ovarian cyst. J Obstet Gynaecol. 2002;22:697-8.
  150. Kim IY, Kim SH, Hwang IT, Ha JG, Cha JH. A rare case of ovarian vein thrombosis in a gestational trophoblastic neoplasia patient. Obstet Gynecol Sci. 2019;62:190-193.
  151. Kodali N, Veytsman I, Martyr S, Lu K. Diagnosis and management of ovarian vein thrombosis in a healthy individual: a case report and a literature review. J Thromb Haemost. 2017;15:242-245.
  152. Toman E, Beaven A, Balogun M, Porter K. Ovarian vein thrombosis in a polytrauma patient. BMJ Case Rep. 2015;2015:bcr2015213071.
  153. Murphy CS, Parsa T. Idiopathic ovarian vein thrombosis: a rare cause of abdominal pain. Am J Emerg Med. 2006;24:636-7.
  154. Teh HS, Chiang SH, Tan AG, Sng LH, Oh HM. A case of right loin pain: septic ovarian vein thrombosis due to Campylobacter fetus bacteraemia. Ann Acad Med Singap. 2004;33:385-8.
  155. Marcovici I, Goldberg E. Ovarian vein thrombosis associated with Crohn’s disease: a case report. Am J Obstet Gynecol. 2000;182:743-4.
  156. Maldjian PD, Zurlow J. Ovarian vein thrombosis associated with a tubo-ovarian abscess. Arch Gynecol Obstet. 1997;261:55-8.
  157. Qureshi M, Alabi F, Christian F, Romero C. The forgotten urinalysis: an integral part of unmasking thrombophilia. J Community Hosp Intern Med Perspect. 2019;9:40-44.
  158. Chawla A, Mishra D, Sharma P. Renal artery aneurysm with an ovarian vein thrombosis. BMJ Case Rep. 2013;2013:bcr2013201490.
  159. Tan JW, Howe HS, Chng HH. Ovarian vein thrombosis in Behçet disease. J Clin Rheumatol. 2012; 18:89-91.
  160. Heavrin BS, Wrenn K. Ovarian vein thrombosis: a rare cause of abdominal pain outside the peripartum period. J Emerg Med. 2008;34:67-9.
  161. Wang IK, Lee CH, Yang BY, Chang HY, Lin CL, Chuang FR. Low-molecular-weight heparin successfully treating a nephrotic patient complicated by renal and ovarian vein thrombosis and pulmonary embolism. Int J Clin Pract Suppl. 2005;(147):72-5.
  162. Benfayed WH, Torreggiani WC, Hamilton S. Detection of pulmonary emboli resulting from ovarian vein thrombosis. AJR Am J Roentgenol. 2003; 181:1430-1.
  163. Lenihan JP Jr, Kovanda C. Bilateral ovarian vein thromboses in a postmenopausal woman with uterine prolapse. J Minim Invasive Gynecol. 2010; 17:280-1.
  164. Abujudeh H, Lim H. Emergency suprarenal inferior vena cava filter placement in ovarian vein thrombosis. Emerg Radiol. 2004;10:270-2.
  165. Austin OG. Massive thrombophlebitis of the ovarian veins; a case report. Am J Obstet Gynecol. 1956;72:428-9.
  166. Assal A, Kaner JD, Danda N, Cohen HW, Billett HH. Risk factors and prognosis of ovarian vein thrombosis. Blood Coagul Fibrinolysis. 2017; 28:468-474.
  167. Salomon O, Apter S, Shaham D, Hiller N, Bar-Ziv J, Itzchak Y, Gitel S, Rosenberg N, Strauss S, Kaufman N, Seligsohn U. Risk factors associated with postpartum ovarian vein thrombosis. Thromb Haemost. 1999;82:1015-9.
  168. Virmani V, Kaza R, Sadaf A, Fasih N, Fraser-Hill M. Ultrasound, computed tomography, and magnetic resonance imaging of ovarian vein thrombosis in obstetrical and non obstetrical patients. Can Assoc Radiol J. 2012;63:109-18.
  169. Martinelli I, Franchini M, Mannucci PM. How I treat rare venous thromboses. Blood. 2008; 112:4818-23.
  170. Dunnihoo DR, Gallaspy JW, Wise RB, Otterson WN. Postpartum ovarian vein thrombophlebitis: a review. Obstet Gynecol Surv. 1991;46:415-27.
  171. Assal A, Kaner JD, Danda N, Cohen HW, Billett HH. Risk factors and prognosis of ovarian vein thrombosis. Blood Coagul Fibrinolysis. 2017;28:468-474.