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Pathogenesis, clinical manifestations, and diagnosis of ovarian hyperstimulation syndrome

Pathogenesis, clinical manifestations, and diagnosis of ovarian hyperstimulation syndrome
Literature review current through: Jan 2024.
This topic last updated: Sep 29, 2023.

INTRODUCTION — Ovarian hyperstimulation syndrome (OHSS) is the most serious complication of controlled ovarian hyperstimulation (COH) for assisted reproduction technologies (ART). It occurs when the ovaries are hyperstimulated and enlarged due to fertility treatments (or rarely, mutations in the follicle-stimulating hormone [FSH] receptor), resulting in the shift of serum from the intravascular space to the third space, mainly to the abdominal cavity. In its severe form, OHSS is a life-threatening condition because it can cause venous or arterial thromboembolic events, including stroke and loss of perfusion of an extremity.

The pathogenesis, clinical manifestations, and diagnosis of OHSS are reviewed here. The prevention and management of OHSS are discussed separately. (See "Prevention of ovarian hyperstimulation syndrome" and "Management of ovarian hyperstimulation syndrome".)

EPIDEMIOLOGY — The frequency of OHSS depends upon the clinical setting (eg, ovulation induction/ovarian stimulation followed by timed intercourse or intrauterine insemination versus in vitro fertilization [IVF]) and the classification criteria used for OHSS (table 1) (see 'Classification' below). Although the most severe form of OHSS is rare, it represents an iatrogenic complication with a potentially fatal outcome in young women undergoing fertility treatment.

When ovulation is induced with clomiphene citrate or aromatase inhibitors, either for timed intercourse or intrauterine insemination, ovarian enlargement consistent with mild OHSS may occur, but moderate to severe OHSS is rarely seen [1].

The incidence of moderate and severe OHSS while undergoing IVF has decreased in the last decade due to modern approaches in prevention strategies: use of gonadotropin-releasing hormone (GnRH) agonist triggering, dopamine agonists, and others.

Data from a Japanese registry analyzing 1,435,108 ART cycles found 11,378 cases of moderate/severe OHSS (0.79 percent) [2].

In a retrospective analysis of 4894 consecutive ART cycles conducted in Portugal, 51 cases (1 percent) of OHSS were reported (all OHSS patients received human chorionic gonadotropin [hCG] for final oocyte maturation). In another 71 cases considered high risk for OHSS (1.5 percent), patients received GnRH agonists for final oocyte maturation and did not develop OHSS [3].  

No cases of moderate/severe OHSS were seen in a study of of high responders (25 to 35 follicles ≥12 mm) who received a GnRH agonist as the ovulatory trigger [4]. However, 17 percent of the subjects reported symptoms of mild OHSS.

PATHOGENESIS

Overview — In the spontaneous ovulatory cycle, hypothalamic-pituitary-ovarian feedback mechanisms limit follicle recruitment to a small number of early antral follicles, followed by selection of a single dominant follicle that ovulates in response to the midcycle luteinizing hormone (LH) surge (see "Normal menstrual cycle"). In the setting of ovarian stimulation for in vitro fertilization (IVF), high-dose gonadotropin administration overrides the normal feedback mechanisms seen in the normal menstrual cycle, resulting in multiple folliculogenesis. For many years, human chorionic gonadotropin (hCG) was administered for final oocyte maturation. In high responders (eg, recruitment of >20 follicles), hCG leads to the potential risk of OHSS. When hCG is not administered, moderate and severe forms of OHSS are rarely seen. (See "Prevention of ovarian hyperstimulation syndrome".)

OHSS can be viewed as an exaggeration of a physiologic process. The successive stages of OHSS are (algorithm 1):

Recruitment of a large number of small antral follicles into a functional cohort

Sustained development of numerous large antral follicles until ovulation (or luteinization)

Excessive production of vascular endothelial growth factor (VEGF) by the developing corpora lutea, after hCG administration

Exaggerated perifollicular neovascularization with some of the new blood vessels exhibiting increased permeability

Escape of follicular fluid and perifollicular blood containing large amounts of VEGF into the peritoneal cavity

Functional impairment of blood vessels (not only within the ovary)

Massive fluid shift from the intravascular to the third compartment, also known as "third spacing," resulting in intravascular hypovolemia concomitant with the development of edema, ascites, hydrothorax, diminished renal blood flow, and/or pericardial effusion

Impairment of cardiac, renal, pulmonary, and liver function

OHSS typically occurs in the setting of (table 2):

Ovarian stimulation with gonadotropins with an exuberant ovarian response, evidenced by multiple follicular development, high serum estradiol concentrations, and ovarian enlargement by the end of stimulation [5]

Use of exogenous hCG to trigger the final steps of oocyte maturation [6]

Production and release of vasoactive substances by granulosa/luteal cells

Binding of the vasoactive substances to their receptors and activation of downstream signalling, leading to increased vascular permeability [7]

Pregnancy following ovarian stimulation, where rising hCG secretion from the placenta can stimulate increased VEGF secretion from the ovary

Ovulatory hCG injection — Exogenous human chorionic gonadotropin (hCG) administration plays a key role in the pathogenesis of OHSS. Regardless of the degree of ovarian response to gonadotropin stimulation, OHSS rarely occurs unless an ovulatory dose of hCG is administered [8,9]. Exogenous hCG induces massive luteinization of granulosa cells, which leads to the production of vasoactive substances such as VEGF that increase vascular permeability. (See 'VEGF/vascular permeability' below.)

Such massive luteinization is usually not observed when the final steps of oocyte maturation are achieved with drugs other than hCG (eg, gonadotropin-releasing hormone [GnRH] agonists) [10]. The effect of hCG is related to its high biological activity, which is six to seven times that of endogenous LH (because of hCG's longer half-life) [11]. (See "Prevention of ovarian hyperstimulation syndrome", section on 'Keys to prevention'.)

VEGF/vascular permeability — A number of substances have been proposed as the cause of increased vascular permeability post-hCG administration, but vascular endothelial growth factor (VEGF) appears to play the main role [10,12-18]. VEGF is a member of the family of heparin-binding proteins that act directly on endothelial cells to induce proliferation and angiogenesis. VEGF mRNA and protein are expressed by granulosa and theca cells late in follicular development and after ovulation. Studies on ascitic fluid from patients with severe OHSS have demonstrated that VEGF is the major capillary permeability agent [19].

VEGF serum concentrations are positively correlated with the risk of developing OHSS and with the severity of its form [20-22]. The presence of VEGF receptor 2 (VEGFR-2) in granulosa-lutein cells after hCG administration has been confirmed in humans [16].

Increased capillary permeability and fluid shift to the third space are usually confined to the ovaries and abdomen [23]. Additionally, patients who get pregnant after oocyte donation do not have OHSS, despite high free VEGF levels [24].

Very little is known about the steps through which the VEGF-VEGFR-2 complex increases vascular permeability, but potential downstream elements involved in endothelial cell-to-cell junctions may play a role [25-27].

Rare causes — Rarely, OHSS may be seen in the absence of exogenous gonadotropin administration. In these cases, OHSS may be the consequence of the high production of endogenous gonadotropins (hCG) or gonadotropin-like molecules (thyroid-stimulating hormone [TSH]), or enhanced sensitivity to endogenous gonadotropins (mutations in the follicle-stimulating hormone [FSH] receptor).

RISK FACTORS — There are a number of risk factors for OHSS, including (table 2) [28]:

Previous episode of OHSS [29,30].

Polycystic ovary syndrome (PCOS) [5,29,31-33]. In a meta-analysis of 10 studies, women with PCOS were at higher risk for OHSS than women with other infertility diagnoses (odds ratio [OR] 6.8, 95% CI 4.9-9.6) [34].

Potential biomarkers of risk – Basal serum anti-müllerian hormone (AMH) concentration >3.3 ng/mL and an antral follicle count (AFC) >8. These were predictors of OHSS risk in a retrospective study of 41 women who developed OHSS compared with an age-matched control group who did not develop OHSS [35].

Secondary risk factors related to ovarian response [31]:

Number of follicles (risk rises with increasing number of follicles >20 over 10 mm in diameter).

High (or rapidly rising) serum estradiol concentration. In one report, the incidence of OHSS in women with preovulatory serum estradiol concentrations >3500 pg/mL (12,850 pmol/L) or >6000 pg/mL (22,028 pmol/L) was 1.5 and 38 percent, respectively [33]. The role of serum estradiol monitoring for preventing OHSS is discussed separately. (See "Prevention of ovarian hyperstimulation syndrome".)

Number of oocytes retrieved in in vitro fertilization (IVF) cycle (risk increases with increasing number of oocytes) [33].

Administration of human chorionic gonadotropin (hCG) rather than progesterone for luteal phase support [36].

Pregnancy, which increases not only the risk of late OHSS, but also the duration and severity of OHSS (due to the persistent stimulation by endogenous hCG) [37].

Although younger age and low body weight have been reported as possibly associated with OHSS, neither is a good predictor of risk [29,30,32,37-39].

CLINICAL MANIFESTATIONS — Clinical manifestations of OHSS are the consequence of the processes that define the syndrome: enlarged ovaries (which may cause abdominal discomfort) and increased vascular permeability, resulting in fluid accumulation in the abdomen [40].

Onset — "Early" OHSS is usually mild to moderate and begins four to seven days after the ovulatory dose of human chorionic gonadotropin (hCG). "Late" OHSS typically begins at least nine days after the ovulatory dose of hCG in the setting of a conception cycle. Late OHSS may be more severe because the rising hCG of pregnancy exacerbates the course of OHSS. Early symptoms include abdominal distension and possibly pain due to ovarian enlargement and accumulation of abdominal fluid.

Classification — OHSS may be classified into four stages based upon the severity of symptoms, signs, and laboratory findings (table 1).

Mild OHSS – Mild OHSS is characterized by bilateral ovarian enlargement with multiple follicular and corpus luteum cysts, abdominal distention and discomfort, mild nausea, and, less frequently, vomiting and diarrhea. There are no biochemical abnormalities (table 1).

Mild OHSS is frequently seen after ovarian stimulation with gonadotropins for in vitro fertilization (IVF) in women with a strong ovarian response. Typically, no special care is necessary, but surveillance of the patient is indicated.

Moderate OHSS – The clinical features of moderate OHSS include those of mild OHSS plus ultrasonographic evidence of ascites. Ovaries are frequently enlarged up to 12 cm in their longest dimension. Abdominal discomfort and gastrointestinal symptoms (eg, nausea, vomiting, and diarrhea) are more frequent and intense than in mild OHSS. A sudden increase in weight of more than 3 kg (6.6 lbs) may be an early sign of moderate OHSS (table 1).

Laboratory features include a hematocrit above 41 percent and white blood cell concentration (WBC) above 15,000/microL, with hypoproteinemia.

Severe OHSS – In addition to the findings of moderate OHSS, severe OHSS is defined by the presence of clinical evidence of ascites with severe abdominal pain and, in some patients, pleural effusion. Women with severe OHSS can gain as much as 15 to 20 kg (33 to 44 lbs) over 5 to 10 days and display progressive leukocytosis. Ascites and pleural effusion may compromise pulmonary function, resulting in hypoxia (table 1) [41].

Hypovolemia, oliguria or anuria, and intractable nausea and/or vomiting are frequently present. Creatinine levels are above 1.6 mg/dL. Reduced liver perfusion affects its function; anticlotting factors are among the first to be depleted, and transaminases are increased [42]. Other laboratory findings include a hematocrit >55 percent, WBC >25,000/microL, and electrolyte imbalance (hyponatremia, hyperkalemia) [43-45]. Hemoconcentration increases the risk for thromboembolism.

In a study of 20 cases of OHSS, intraabdominal pressure (IAP) was measured and was increased in all of them, including cases of moderate OHSS [46]. Based upon these data, the study authors proposed that OHSS should be managed as a secondary abdominal compartment syndrome (ACS) [46]. ACS is defined as a persistently elevated intraabdominal hypertension that leads to compromised end-organ function.

Critical OHSS – In critical OHSS, the function of vital organs and systems is seriously compromised. Anuria with acute renal failure, cardiac arrhythmia, respiratory insufficiency, and disseminated intravascular coagulation (venous and arterial thrombosis) may result in death. Pleural effusion becomes a massive hydrothorax, accompanied by pericardial effusion. Sepsis and acute respiratory distress syndrome (ARDS) may further complicate the clinical picture. In one study of 209 patients with severe/critical OHSS, eight (4 percent) had pneumonia, four (2 percent) ARDS, and four (2 percent) had pulmonary thromboembolism (table 1) [47].

Investigators doing clinical trials in this area have proposed a different set of criteria for the diagnosis and classification of OHSS as follows:

Mild OHSS – Women presenting with mild OHSS signs/symptoms are classified as "ovarian hyperresponders."

Moderate, severe, or critical OHSS – Those presenting with moderate or more severe OHSS signs/symptoms are classified as "OHSS," which can be further classified into:

"Self-limited OHSS" – No catastrophic events

"OHSS with significant comorbidities" – At least one of the following events: venous thromboembolism; acute respiratory distress syndrome; cerebral edema, acute ischemia, encephalopathy; kidney injury; liver failure [48]

The prevention, and management of OHSS are reviewed separately. (See "Prevention of ovarian hyperstimulation syndrome" and "Management of ovarian hyperstimulation syndrome".)

Specific complications — Other potential complications that may be seen in the setting of OHSS include:

Ovarian torsion – Whenever ovarian volume is increased, there is a risk of ovarian torsion. This complication is characterized by ovarian enlargement, abdominal pain, nausea, vomiting, hypotension, progressive leukocytosis, and anemia. Ovarian torsion may demand surgical correction [49].

Thromboembolism – Thromboembolic events are infrequent, but among the most serious, complications of OHSS. Thromboses can be either arterial (25 percent) or venous (75 percent) and may lead to permanent neurologic injury or death [50-52].

The occurrence of these events is likely related not only to hemoconcentration but also to hypercoagulation associated with elevated serum estrogen concentrations. In one report, high levels of factor V, platelets, fibrinogen, profibrinolysin, fibrinolytic inhibitors, and increased thromboplastin generation were observed in women with OHSS [53].

Thromboembolic complications of OHSS have been reported in the internal jugular, subclavian, axillary, and mesenteric vessels [41,54]. In one series of five cases of internal jugular vein thrombosis presenting at 7 to 10 weeks gestation after IVF, two occurred in women who had not had OHSS but had an underlying thrombophilia, while three occurred in women with severe OHSS and no underlying thrombophilia [55]. Cerebrovascular thrombosis typically presents as an ischemic infarct.

Some experts advise that women with an underlying thrombophilia (eg, antithrombin III deficiency, factor V mutation, and protein C or S deficiency) should receive prophylaxis (such as low-dose heparin therapy) prior to ovulation induction, to prevent thromboembolic complications [56]. (See "Overview of the causes of venous thrombosis" and "Prevention of venous thromboembolic disease in adult nonorthopedic surgical patients", section on 'Selecting thromboprophylaxis'.)

Because thromboembolic complications are rare, we do not suggest routine screening for thrombophilia in women planning to undergo ovarian stimulation.

DIAGNOSIS — The diagnosis of OHSS is made by clinical history and transvaginal ultrasound (table 1) (see 'Classification' above). There should be a history of ovarian stimulation followed by administration of human chorionic gonadotropin (hCG). The number of collected oocytes, peak serum estradiol, and number of transferred embryos are predictors of the presence of OHSS.

Once the diagnosis of OHSS is made, disease severity should be classified as mild, moderate, severe, or critical (table 1). (See 'Classification' above.)

Differential diagnosis — The diagnosis of OHSS is usually straightforward, as the syndrome occurs in a specific setting: ovarian stimulation with exogenous gonadotropins followed by hCG injection. However, other disorders resulting in pelvic pain and possibly free fluid include ectopic pregnancy, hemorrhagic cyst, ruptured ovarian cyst, and ovarian torsion. These disorders, when associated with hemoperitoneum (or hemoperitoneum due to oocyte retrieval) may be similar to OHSS (enlarged ovaries, free fluid [blood], abdominal distension, and pain). However, hemoconcentration is not present (there is a fall in hemoglobin and hematocrit). (See "Ectopic pregnancy: Clinical manifestations and diagnosis" and "Ovarian and fallopian tube torsion".)

SOCIETY GUIDELINE LINKS — Links to society and government-sponsored guidelines from selected countries and regions around the world are provided separately. (See "Society guideline links: Ovarian hyperstimulation syndrome".)

INFORMATION FOR PATIENTS — UpToDate offers two types of patient education materials, "The Basics" and "Beyond the Basics." The Basics patient education pieces are written in plain language, at the 5th to 6th grade reading level, and they answer the four or five key questions a patient might have about a given condition. These articles are best for patients who want a general overview and who prefer short, easy-to-read materials. Beyond the Basics patient education pieces are longer, more sophisticated, and more detailed. These articles are written at the 10th to 12th grade reading level and are best for patients who want in-depth information and are comfortable with some medical jargon.

Here are the patient education articles that are relevant to this topic. We encourage you to print or e-mail these topics to your patients. (You can also locate patient education articles on a variety of subjects by searching on "patient info" and the keyword(s) of interest.)

Beyond the Basics topics (see "Patient education: Infertility treatment with gonadotropins (Beyond the Basics)" and "Patient education: In vitro fertilization (IVF) (Beyond the Basics)")

SUMMARY AND RECOMMENDATIONS

Definition – Ovarian hyperstimulation syndrome (OHSS) is an exaggerated ovarian response to ovulation induction, particularly in the setting of in vitro fertilization (IVF). It can be strictly defined as the shift of serum from the intravascular space to the third space, mainly to the abdominal cavity, in the context of enlarged ovaries due to follicular stimulation. In its very severe form, OHSS is a life-threatening condition (table 1).

Epidemiology – The incidence of moderate and severe OHSS while undergoing IVF has decreased in the last decade due to modern approaches in prevention strategies: use of gonadotropin-releasing hormone (GnRH) agonist triggering, dopamine agonists, and others. (See 'Epidemiology' above.)  

Pathogenesis – OHSS occurs almost exclusively in the setting of ovarian stimulation with exogenous gonadotropins, and only if human chorionic gonadotropin (hCG) is administered to trigger ovulation (algorithm 1). A number of substances have been proposed as the cause of increased vascular permeability post-hCG administration, but vascular endothelial growth factor (VEGF) appears to play the main role. (See 'Pathogenesis' above and 'VEGF/vascular permeability' above.)

Risk factors – Risk factors include the presence of polycystic ovary syndrome (PCOS), previous OHSS, luteal phase hCG support, number of follicles, and high serum estradiol concentrations. Pregnancy increases the risk, duration, and severity of OHSS (due to the persistent stimulation by endogenous hCG) (table 2). (See 'Risk factors' above.)

Clinical manifestations and classification – OHSS may be classified into mild, moderate, severe, and critical based upon the severity of symptoms, signs, and laboratory findings (table 1). (See 'Classification' above.)

Diagnosis – The diagnosis of OHSS is based upon clinical history and transvaginal ultrasound. There should be a history of ovarian stimulation followed by ovulation or administration of hCG (see 'Diagnosis' above). The signs and symptoms of mild, moderate, severe, and critical OHSS are described above. (See 'Classification' above.)

ACKNOWLEDGMENT — The UpToDate editorial staff acknowledges Bruno Lunenfeld, MD and the late Vaclav Insler, MD, who contributed to earlier versions of this topic review.

  1. Schenker JG, Weinstein D. Ovarian hyperstimulation syndrome: a current survey. Fertil Steril 1978; 30:255.
  2. Kuroda K, Nagai S, Ikemoto Y, et al. Incidences and risk factors of moderate-to-severe ovarian hyperstimulation syndrome and severe hemoperitoneum in 1,435,108 oocyte retrievals. Reprod Biomed Online 2021; 42:125.
  3. Sousa M, Cunha M, Teixeira da Silva J, et al. Ovarian hyperstimulation syndrome: a clinical report on 4894 consecutive ART treatment cycles. Reprod Biol Endocrinol 2015; 13:66.
  4. Fernández-Sánchez M, Fatemi H, García-Velasco JA, et al. Incidence and severity of ovarian hyperstimulation syndrome (OHSS) in high responders after gonadotropin-releasing hormone (GnRH) agonist trigger in "freeze-all" approach. Gynecol Endocrinol 2023; 39:2205952.
  5. Rizk B, Smitz J. Ovarian hyperstimulation syndrome after superovulation using GnRH agonists for IVF and related procedures. Hum Reprod 1992; 7:320.
  6. Mozes M, Bogokowsky H, Antebi E, et al. Thromboembolic phenomena after ovarian stimulation with human gonadotrophins. Lancet 1965; 2:1213.
  7. Roberts WG, Palade GE. Neovasculature induced by vascular endothelial growth factor is fenestrated. Cancer Res 1997; 57:765.
  8. Schenker JG. Prevention and treatment of ovarian hyperstimulation. Hum Reprod 1993; 8:653.
  9. Aboulghar MA, Mansour RT. Ovarian hyperstimulation syndrome: classifications and critical analysis of preventive measures. Hum Reprod Update 2003; 9:275.
  10. Soares SR, Gómez R, Simón C, et al. Targeting the vascular endothelial growth factor system to prevent ovarian hyperstimulation syndrome. Hum Reprod Update 2008; 14:321.
  11. Yen SS, Llerena O, Little B, Pearson OH. Disappearance rates of endogenous luteinizing hormone and chorionic gonadotropin in man. J Clin Endocrinol Metab 1968; 28:1763.
  12. McClure N, Healy DL, Rogers PA, et al. Vascular endothelial growth factor as capillary permeability agent in ovarian hyperstimulation syndrome. Lancet 1994; 344:235.
  13. Kamat BR, Brown LF, Manseau EJ, et al. Expression of vascular permeability factor/vascular endothelial growth factor by human granulosa and theca lutein cells. Role in corpus luteum development. Am J Pathol 1995; 146:157.
  14. Yan Z, Weich HA, Bernart W, et al. Vascular endothelial growth factor (VEGF) messenger ribonucleic acid (mRNA) expression in luteinized human granulosa cells in vitro. J Clin Endocrinol Metab 1993; 77:1723.
  15. Neulen J, Yan Z, Raczek S, et al. Human chorionic gonadotropin-dependent expression of vascular endothelial growth factor/vascular permeability factor in human granulosa cells: importance in ovarian hyperstimulation syndrome. J Clin Endocrinol Metab 1995; 80:1967.
  16. Wang TH, Horng SG, Chang CL, et al. Human chorionic gonadotropin-induced ovarian hyperstimulation syndrome is associated with up-regulation of vascular endothelial growth factor. J Clin Endocrinol Metab 2002; 87:3300.
  17. Yamamoto S, Konishi I, Tsuruta Y, et al. Expression of vascular endothelial growth factor (VEGF) during folliculogenesis and corpus luteum formation in the human ovary. Gynecol Endocrinol 1997; 11:371.
  18. Pellicer A, Albert C, Mercader A, et al. The pathogenesis of ovarian hyperstimulation syndrome: in vivo studies investigating the role of interleukin-1beta, interleukin-6, and vascular endothelial growth factor. Fertil Steril 1999; 71:482.
  19. Rizk B, Aboulghar M, Smitz J, Ron-El R. The role of vascular endothelial growth factor and interleukins in the pathogenesis of severe ovarian hyperstimulation syndrome. Hum Reprod Update 1997; 3:255.
  20. Chen CD, Wu MY, Chen HF, et al. Prognostic importance of serial cytokine changes in ascites and pleural effusion in women with severe ovarian hyperstimulation syndrome. Fertil Steril 1999; 72:286.
  21. Agrawal R, Tan SL, Wild S, et al. Serum vascular endothelial growth factor concentrations in in vitro fertilization cycles predict the risk of ovarian hyperstimulation syndrome. Fertil Steril 1999; 71:287.
  22. Abramov Y, Barak V, Nisman B, Schenker JG. Vascular endothelial growth factor plasma levels correlate to the clinical picture in severe ovarian hyperstimulation syndrome. Fertil Steril 1997; 67:261.
  23. Alvarez C, Martí-Bonmatí L, Novella-Maestre E, et al. Dopamine agonist cabergoline reduces hemoconcentration and ascites in hyperstimulated women undergoing assisted reproduction. J Clin Endocrinol Metab 2007; 92:2931.
  24. Pau E, Alonso-Muriel I, Gómez R, et al. Plasma levels of soluble vascular endothelial growth factor receptor-1 may determine the onset of early and late ovarian hyperstimulation syndrome. Hum Reprod 2006; 21:1453.
  25. Villasante A, Pacheco A, Ruiz A, et al. Vascular endothelial cadherin regulates vascular permeability: Implications for ovarian hyperstimulation syndrome. J Clin Endocrinol Metab 2007; 92:314.
  26. Bates DO, Lodwick D, Williams B. Vascular endothelial growth factor and microvascular permeability. Microcirculation 1999; 6:83.
  27. Villasante A, Pacheco A, Zúñiga A, Pellicer A, Garcia-Velasco JA. Ovarian hyperstimulation syndrome: the role of vascular endothelial cadherin. Hum Reprod 2003;18:35 (Abstract).
  28. Practice Committee of American Society for Reproductive Medicine. Ovarian hyperstimulation syndrome. Fertil Steril 2008; 90:S188.
  29. Delvigne A, Rozenberg S. Epidemiology and prevention of ovarian hyperstimulation syndrome (OHSS): a review. Hum Reprod Update 2002; 8:559.
  30. Delvigne A, Dubois M, Battheu B, et al. The ovarian hyperstimulation syndrome in in-vitro fertilization: a Belgian multicentric study. II. Multiple discriminant analysis for risk prediction. Hum Reprod 1993; 8:1361.
  31. Soave I, Marci R. Ovarian stimulation in patients in risk of OHSS. Minerva Ginecol 2014; 66:165.
  32. Navot D, Relou A, Birkenfeld A, et al. Risk factors and prognostic variables in the ovarian hyperstimulation syndrome. Am J Obstet Gynecol 1988; 159:210.
  33. Asch RH, Li HP, Balmaceda JP, et al. Severe ovarian hyperstimulation syndrome in assisted reproductive technology: definition of high risk groups. Hum Reprod 1991; 6:1395.
  34. Tummon I, Gavrilova-Jordan L, Allemand MC, Session D. Polycystic ovaries and ovarian hyperstimulation syndrome: a systematic review*. Acta Obstet Gynecol Scand 2005; 84:611.
  35. Ocal P, Sahmay S, Cetin M, et al. Serum anti-Müllerian hormone and antral follicle count as predictive markers of OHSS in ART cycles. J Assist Reprod Genet 2011; 28:1197.
  36. Navot D, Bergh PA, Laufer N. Ovarian hyperstimulation syndrome in novel reproductive technologies: prevention and treatment. Fertil Steril 1992; 58:249.
  37. Enskog A, Henriksson M, Unander M, et al. Prospective study of the clinical and laboratory parameters of patients in whom ovarian hyperstimulation syndrome developed during controlled ovarian hyperstimulation for in vitro fertilization. Fertil Steril 1999; 71:808.
  38. Delvigne A. Symposium: Update on prediction and management of OHSS. Epidemiology of OHSS. Reprod Biomed Online 2009; 19:8.
  39. Lewis CG, Warnes GM, Wang XJ, Matthews CD. Failure of body mass index or body weight to influence markedly the response to ovarian hyperstimulation in normal cycling women. Fertil Steril 1990; 53:1097.
  40. Delvigne A, Rozenberg S. Review of clinical course and treatment of ovarian hyperstimulation syndrome (OHSS). Hum Reprod Update 2003; 9:77.
  41. Abramov Y, Elchalal U, Schenker JG. Pulmonary manifestations of severe ovarian hyperstimulation syndrome: a multicenter study. Fertil Steril 1999; 71:645.
  42. Fábregues F, Balasch J, Ginès P, et al. Ascites and liver test abnormalities during severe ovarian hyperstimulation syndrome. Am J Gastroenterol 1999; 94:994.
  43. Whelan JG 3rd, Vlahos NF. The ovarian hyperstimulation syndrome. Fertil Steril 2000; 73:883.
  44. Elchalal U, Schenker JG. The pathophysiology of ovarian hyperstimulation syndrome--views and ideas. Hum Reprod 1997; 12:1129.
  45. Practice Committe of the American Society for Reproductive Medicine. Ovarian hyperstimulation syndrome. Fertil Steril 2003; 80:1309.
  46. Grossman LC, Michalakis KG, Browne H, et al. The pathophysiology of ovarian hyperstimulation syndrome: an unrecognized compartment syndrome. Fertil Steril 2010; 94:1392.
  47. Abramov Y, Elchalal U, Schenker JG. Febrile morbidity in severe and critical ovarian hyperstimulation syndrome: a multicentre study. Hum Reprod 1998; 13:3128.
  48. Humaidan P, Nelson SM, Devroey P, et al. Ovarian hyperstimulation syndrome: review and new classification criteria for reporting in clinical trials. Hum Reprod 2016; 31:1997.
  49. Mashiach S, Bider D, Moran O, et al. Adnexal torsion of hyperstimulated ovaries in pregnancies after gonadotropin therapy. Fertil Steril 1990; 53:76.
  50. Aboulghar MA, Mansour RT, Serour GI, Amin YM. Moderate ovarian hyperstimulation syndrome complicated by deep cerebrovascular thrombosis. Hum Reprod 1998; 13:2088.
  51. Stewart JA, Hamilton PJ, Murdoch AP. Thromboembolic disease associated with ovarian stimulation and assisted conception techniques. Hum Reprod 1997; 12:2167.
  52. Cluroe AD, Synek BJ. A fatal case of ovarian hyperstimulation syndrome with cerebral infarction. Pathology 1995; 27:344.
  53. Phillips LL, Gladstone W, vande Wiele R. Studies of the coagulation and fibrinolytic systems in hyperstimulation syndrome after administration of human gonadotropins. J Reprod Med 1975; 14:138.
  54. Tang OS, Ng EH, Wai Cheng P, Chung Ho P. Cortical vein thrombosis misinterpreted as intracranial haemorrhage in severe ovarian hyperstimulation syndrome: case report. Hum Reprod 2000; 15:1913.
  55. Arya R, Shehata HA, Patel RK, et al. Internal jugular vein thrombosis after assisted conception therapy. Br J Haematol 2001; 115:153.
  56. Dulitzky M, Cohen SB, Inbal A, et al. Increased prevalence of thrombophilia among women with severe ovarian hyperstimulation syndrome. Fertil Steril 2002; 77:463.
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