Thoracic Endometriosis Syndrome
Camran Nezhat, Babak Hajhosseini, Elizabeth Buescher, Asrafjah Hussein, Georgios E. Hilaris, Michal Sellin
The purpose of this section is to provide practicing gynecologic endoscopic surgeons with up-to-date evidence on the etiopathogenesis, diagnosis, and treatment of thoracic endometriosis syndrome (TES) and to heighten the level of clinical suspicion of this pathology. This syndrome represents an underreported cause of catamenial spontaneous pneumothorax. A multidisciplinary approach by thoracic and gynecologic surgical teams offers the best chances for accurate diagnosis and treatment of women with this syndrome.
Endometriosis is defined as the presence of endometrial glands and stroma outside the uterine cavity and is usually confined to the pelvis. TES is a rare disorder characterized by the presence of functioning endometrial tissue in pleura, lung parenchyma, airways, and/or diaphragm.
TES encompasses mainly four clinical entities: catamenial pneumothorax (CP), catamenial hemothorax (CHt), catamenial hemoptysis (CH), and lung nodules. Of these, CP is by far the most common clinical presentation.1
The diagnosis of thoracic endometriosis has improved substantially over the past two decades because of advances in endoscopic techniques (video-assisted thoracoscopic surgery [VATS] as well as laparoscopy) coupled with a higher level of clinical suspicion. Its etiology and pathogenesis, however, are still not well understood. Hence, optimal management of thoracic endometriosis remains to be elucidated, with medical, surgical, or combined approaches being reported in the medical literature.
The true incidence of TES remains unclear. Since the first description of thoracic endometriosis in 1953,2 there have been more than 250 cases reported in the medical literature.3-12 In recent published series, however, up to one third of women hospitalized with a diagnosis of spontaneous pneumothorax had CP.11,13 Therefore, it is plausible that, in the subset of hormonally cycling women, thoracic endometriosis is an underreported cause of secondary spontaneous pneumothorax when the cases of pneumothorax were previously thought to be primary spontanceous pneumothorax.14
Like other sites of extragenital endometriosis, thoracic endometriosis seems to affect a slightly older population when compared to patients with pelvic disease. The mean age at presentation of women with thoracic endometriosis is 35 years, with a range from 15 to 54 years. Interestingly, pelvic endometriosis precedes thoracic endometriosis symptoms, occurring between 24 and 29 years – that is approximately 5 to 7 years earlier.1 Similar data came from a recent review of CP cases in 229 patients in whom the mean age at onset of symptoms was 34 years, with a range from 15 to 47 years.12
Fifty to 84% of women diagnosed with thoracic endometriosis have concomitant pelvic endometriosis. However, the percentage of women with pelvic disease who develop thoracic endometriosis is largely unknown.1
Most lesions are solitary, with the right hemithorax (mainly pleura, less commonly the lung parenchyma) being involved in up to 92% of cases and the left hemithorax in 5% of cases. The remaining 3% have bilateral involvement.12
CP is the most frequent clinical presentation of patients with TES, occurring in approximately 80% of the cases. CHt occurs in 14%, and CH occurs in 5%. The least common presentation is endometriotic nodules.1,15
ETIOLOGY AND PATHOGENESIS
Based on the anatomic location of the endometriotic lesions, thoracic endometriosis can be classified into pleural and bronchopulmonary (parenchymal). The former, which is the most common type, gives rise to CP and CHt, whereas the latter gives rise to CH and the exceedingly rare lung nodules.15-16
There is general agreement that thoracic endometriosis is the only cause of CHt, CH, and endometriotic lung nodules. Conversely, CP, although most frequently associated with thoracic endometriosis, may also have other etiologic mechanisms.14
A number of hypotheses have been suggested to explain the etiology of CP. According to one hypothesis, the open connection between the atmosphere and the peritoneal cavity during menstruation allows air to migrate into the thoracic cavity through diaphragmatic fenestrations and porosities. This is supported by the almost 9:1 right-sidedpredominance of endometriotic pleural implants.12,17 Another hypothesis suggests that diaphragmatic defects are caused by endometriosis. The third theory involves a metastatic spreading of endometriosis through the uterine veins into the venous system.18 Lastly, prostaglandin F2 is a potent constrictor of bronchioles and vascular structures which can be found in the plasma of some women during menstruation. It may destroy alveolar tissue due to vasospasm, leading to pneumothorax.12,17-19 Rossi and Goplerud have suggested that synchronous increases in prostaglandin F2 during menses could induce CPT.20 At peak levels during sloughing of the endometrial mucosa, the potent bronchial and vascular constrictor prostaglandin F2 may cause the rupture of preformed subpleural blebs in otherwise normal lungs. This hypothesis could explain that in 23.1% of all explored cases, bullae or blebs were the only lesions discovered, and in 8.5% no pathologic findings were found.
Lymphatic or hematogenous embolization from the uterus or pelvis could explain not only the parenchymal or bronchopulmonary endometriotic nodules, but also other extrapelvic locations.1,21 In fact, a review of autopsy data showed that cadavers with bronchopulmonary endometriosis usually had bilateral lesions, whereas pleural and diaphragmatic lesions were almost always right sided.22
During menses, the dissolving cervical mucus plug may allow the ascent of air through the fallopian tubes. The theory of transfallopian ascent of air is supported by the cure of CPT with plication of diaphragmatic perforations and tubal ligation. The theory of transdiaphragmatic passage of endometrial debris and/or air is now the most favored explanation for thoracic endometriosis. It supports both the anatomic location of endometriotic lesions (found in the right pleura in more than 90% of the cases) and the exceedingly more common presentation of CP versus other less common entities of TES.23 This theory is based on the concept that peritoneal fluid circulation within the abdomen follows a characteristic clockwise pattern that promotes the flow of fluid (air, cell aggregates, pus) from the pelvis to the right subdiaphragmatic area through the right paracolic gutter. Transdiaphragmatic passage of peritoneal fluid into the right pleural cavity may occur through congenital or acquired defects and fenestrations and may be the key pathognomonic feature of thoracic endometriosis.1,12,24 Although there are small peritoneal stomata that enable particles below 30 mm to enter diaphragmatic lacunae, a substantial defect in the continuity of the hemidiaphragm must be present to allow ascent of a sufficient quantity of air to cause a pneumothorax. Kirschner introduced the concept of the porous diaphragm syndrome in 1998, proposing preexisting diaphragmatic defects allowing gas and fluids to traverse this anatomic boundary.23 During menses, refluxed endometrial tissue or air may pass through these defects into the pleural space, favored by both the thoracoabdominal pressure gradient and the “piston-like” action of the solid liver bulk.24 Theories of both implantation and metaplasia are discussed to explain endometriosis. This phenomenon may be due to retrograde regurgitation of endometrial tissue during menstruation and secondary implantation on the pelvic peritoneal surface.25 Refluxed endometrial fragments and proliferating endometrial cells, which are capable of tissue adhesion and invasion and of angiogenesis, have been isolated from the peritoneal fluid during menses.
In vitro cultivation of ovarian surface epithelium in the presence of 17Î²-estradiol can induce endometrial transformation (coelomic tissue metaplasia).26-27 As in the case of pelvic endometriosis, heterotropic endometrial implants adhere, proliferate, and follow hormonal cyclic changes. Recurrent bleeding and subsequent fibrosis may weaken the implantation site on visceral pleura that in subsequent cycles may rupture or bleed, causing pneumothorax or hemothorax, respectively. Bronchopulmonary implants, on the other hand, may erode the parenchyma or bronchi causing hemoptysis and fibrosis as in the case of lung nodules.
Lillington and associates coined the term catamenial pneumothorax.28 They proposed a model in which the expansion of intraparenchymal subpleural endometriotic tissue during menses would cause a check-valve airway obstruction, eventually leading to alveolar rupture. Concerning the etiology of CPT, we hypothesize that transgression or erosion of the diaphragm as an anatomic boundary by endometriotic tissue represents the central pathophysiologic mechanism of CPT. This can be stimulated through a heat-stable factor from the peritoneal fluid, together with an increased proteolytic capacity. Endometriotic cells can demonstrate a higher maneuverability with an enhanced potential for local invasiveness.
Women with bronchopulmonary endometriosis tend to have a history of uterine manipulation or trauma (e.g., hysteroscopy, dilation and curettage). This supports the lymphovascular embolization theory, whereas those with pleural disease most often have a history of pelvic endometriosis.15-16
SIGNS AND SYMPTOMS
The most common presentation of TES is CP, which accounts for almost 80% of cases. Less frequent clinical entities include CHt (14%), CH (5%), and lung nodules.1,15 CP is defined as a recurrent pneumothorax occurring within 72 hours from the onset of menstruation.13 Although CP is typically cyclic, noncyclic recurrences occurring in the immediate premenstrual period18,29 or ovulatory phase30 have also been reported. In most cases, CP is right sided with the left side being rarely involved.1,12 Bilateral CP is possible but extremely rare.31-32
Patients with CP present with symptoms of spontaneous pneumothorax that are usually nonspecific, such as pleurisy, cough, and shortness of breath. Patients may also have referred peri-scapular or radiating neck pain due to diaphragmatic irritation. In most cases, symptoms are mild to moderate; severe presentations are rare.14
CHt is an uncommon manifestation of TES accounting for approximately 14% of cases. As with CP, CHt is almost always unilateral and right sided, although left-sided hemothorax has been reported.33 Again, symptoms are nonspecific and include pleuritic pain, shortness of breath, and cough. The presence of bloody effusion is variable.
Computed tomography (CT) of the chest may show multiloculated effusions, nodular lesions of the pleura, or bulky pleural masses.5
CH and lung nodules are both clinical entities of bronchopulmonary TES and are very rare manifestations. Hemoptysis is a quite variable manifestation, with neither massive hemoptysis nor deaths being described so far. An association with menses may not always be appreciated, and diagnostic delays of up to 4 years from the onset of symptoms have been reported.34 CH and lung nodules are interrelated entities. Thus, patients who present with CH frequently have associated lung nodules on imaging studies and vice versa.14
CP, CHt, CH, and lung nodules represent the main clinical entities in TES. However, they are not the only manifestations of TES. Specifically, in the diaphragmatic-only endometriosis cases, catamenial phrenic nerve irritation causing a catamenial pain-only syndrome, namely cyclic shoulder, neck, epigastric, or right upper quadrant pain, may be the only presentation of TES.35-36
Overall, a high level of clinical suspicion is of paramount importance in TES. A detailed history might make the difference in promptly establishing a correct diagnosis and avoiding delays in treatment, which are commonly reported.
The most valuable tool in the diagnosis of thoracic endometriosis is a high level of clinical suspicion.3 A cyclic (i.e., catamenial) constellation of symptoms can be considered pathognomonic for the disease. However, diagnosis is often delayed for more than 8 months from the onset of symptoms.16
Chest radiograph, CT, magnetic resonance imaging, thoracocentesis, and bronchoscopy are useful in the diagnosis of the patient presenting with pneumothorax, hemothorax, hemoptysis, or lung nodules and help rule out malignancy, infection, and other pathologies. All of them, however, have limited diagnostic yield in the diagnosis of TES per se, with variable and inconsistent findings.3,16 Interestingly, in the case of bronchopulmonary endometriosis, bronchoscopy-directed biopsies of suspected lesions usually fail to provide a tissue diagnosis, whereas brush cytology frequently shows distinctive features of endometrial cells.37
Performance of imaging studies or bronchoscopy during menses may assist in the diagnosis of pleural or bronchopulmonary disease. Repeat imaging studies or bronchoscopy during midcycle typically documents the disappearance of the previously reported findings, thus strengthening the clinical suspicion.38
VATS is the gold standard modality for both the definitive diagnosis and surgical treatment of CP.3,11-12,14 In the largest review of CP cases, more than 50% (52.1%) of patients with CP assessed with VATS were diagnosed as having thoracic endometriosis. Diaphragmatic abnormalities (fenestrations or endometriosis, alone or combined) are the most commonly described lesions (38.8%), followed by endometriosis of the visceral pleura (29.6%). In the remainder of cases, discrete lesions, such as bullae, blebs, and scarring (23.1%), or no findings (8.5%) are noted.12-13,18
Diaphragmatic fenestrations range from a few millimeters to 2 cm.13,39 Endometrial deposits in both the diaphragm and pleura have a similar appearance and range from a few millimeters to 1 cm. Their color ranges from violet to brown, depending on the day of menstrual cycle.3,14,40
Performance of a combined VATS and laparoscopy procedure in a single session is another diagnostic approach.3 This way, the thoracic cavity as well as the pelvis and subdiaphragmatic region can be assessed. The use of combined thoracoscopy and laparoscopy to treat TES was first described by the lead author in 2009, and his findings confirmed the necessity of examining the abdominal side of the diaphragm for complete treatment of TES.52 It may be particularly helpful in cases of inconclusive VATS, which may be the result of the presence of endometriosis only in the abdominal part of the diaphragm causing catamenial phrenic nerve irritation and pain.35
The authors would like to emphasize that laparoscopy, rather than laparotomy, is the preferred approach to the treatment of endometriosis. With the advent of videolaparoscopy in 1986, the surgeon is now able to comfortably stand and operate with two hands, rather than uncomfortably lean over and look through a laparoscope. In addition, the surgeon now has both hands free to operate, and the other medical personnel in the room can also see, making it easier to assist the primary surgeon. With current advances in videolaparoscopy, the surgeon is easily able to visualize endometriotic implants in the peritoneal cavity, in the upper abdomen, and on the diaphragm and resect or ablate them. In the hands of an experienced laparoscopist, the complication rate of laparoscopy is less than that with laparotomy. With the improved recovery time and decreased healing of laparoscopy, the utility of laparotomy is largely moot.
Although exploratory thoracotomy was performed extensively in the past, it is now reserved for select cases of prior VATS failure or large lesions.
Treatment of TES can be medical, surgical, or a combination of both.
Medical treatment has long been considered the first step in the management of thoracic endometriosis. Danazol, progestational agents, oral contraceptive pills, and GnRH analogues have all been widely used.14 All have equal effectiveness in alleviating symptoms, and the decision on which one to use is influenced by cost, compliance, and side effect profiles.41 Among the agents studied however, GnRH agonists have been found to be more effective in controlling recurrences of CP, particularly when used for prolonged periods of up to 1 year.42-43
Nevertheless, in the largest series of TES, which included 110 patients, medical treatment was far less effective than surgical treatment, with recurrence rates exceeding 50% regardless of the agent used. Specifically, recurrences at 6 and 12 months were 50% and 60% for medical and 5% and 25% for surgical treatment, respectively.1 This is anticipated because at best, current agents can suppress endometriotic implant growth and activity for only as long as they are being used.
Medical treatment often serves merely as a diagnostic tool. A positive response to medical treatment in women with suspected TES may be considered diagnostic, and surgical treatment may be sought.38
Thoracocentesis and chest tube placement are obviously first-step therapeutic interventions in the emergency room until further action is taken.
VATS is currently the gold standard for the surgical treatment of TES, especially CP. Laparoscopy aids in the surgical treatment of implants on the abdominal aspect of the diaphragm. VATS provides magnification and exposure of possible defects that are sometimes better than that provided by thoracotomy. Misdiagnosis may occur, especially if the patient is positioned for an axillary thoracotomy, since complete visualization of diaphragm is difficult. A better approach seems to be a VATS with the patient positioned for a postero-lateral thoracotomy.
When endometriotic implants are the sole findings during VATS and are in the range of a few millimeters, they can be carefully fulgurated using bipolar diathermy or CO2 laser, regardless of their location (i.e., parietal, visceral, or diaphragmatic pleura) Larger endometriotic implants of the visceral pleura may be excised using sharp dissection.3 Nonetheless, large lesions or deep parenchymal endometriotic nodules are best treated with parenchymal-sparing procedures such as wedge resection13 or subsegmentectomy44 via a minithoracotomy. Occasionally, lobectomy may be required.45
Diaphragmatic lesions (endometriotic implants or perforations) are probably best treated by resection using endoscopic stapler devices, provided that the resected surface is relatively small.13,24 Laparoscopic treatment of diagphragmatic endometriosis was first described by the lead author in 1992.51 Larger diaphragmatic perforations can be sutured, although significant recurrences have been reported with the use of sutures.46 The use of mesh to replace large diaphragmatic excisions has been described in three women who at 45 months follow-up suffered no recurrences,18 although other authors have not confirmed these results.47
Another important therapeutic intervention is pleurodesis (mechanical, chemical, pleurectomy, or talcum). It can be performed alone or in conjunction with implant and/or perforation excision. In a literature review of 79 VATS-treated patients, 28 underwent pleurodesis alone with a median recurrence-free interval of 61 months (10 days to 164 months).12 Pleurodesis, especially in younger patients, should always be carried out concomitantly with VATS exploration. This way, an accurate diagnosis and treatment can be instituted and recurrences avoided. Standard pleurodesis may not suffice, and it is suggested to do apical resection and apical pleurectomy associated with a diaphragmatic procedure when indicated. Hormonal treatment with GnRH agonist seems to improve the outcome.
The pleural cavity and the diaphragm should be carefully explored. Otherwise, endometriotic implants or perforations may be overlooked.
If the abdominal aspect of the diaphragm is involved with endometriotic implants, an experienced team of gynecologic and thoracic surgeons can fulgurate or excise small lesions. Hydrodissection, laser fulguration, or excision can be carried out successfully.35 However, if larger implants or defects are present, they should be approached via VATS, as the liver bulk and limited subdiaphragmatic space may not allow complete resection.36
There is limited information in the literature regarding surgical treatment of CHt and CH. Pleurectomy for CHt has been successfully reported in two cases.4,48 A single case of CH, successfully treated with bronchoscopy-directed neodymium-doped yttrium aluminium garnet (Nd:YAG) laser destruction of an endobronchial implant has also been reported.49
Finally, hysterectomy and bilateral salpingo-oophorectomy (BSO) is the treatment of last resort when other options have failed. Nonetheless, TES may recur if the intrathoracic disease has not been properly addressed and hormone replacement treatment is initiated.1
Based on the suboptimal recurrence rates following either medical or surgical treatment, some investigators prefer surgical treatment followed by hormonal suppression in the postoperative period.13,24,40,50
TES is a challenging clinical entity. A high index of clinical suspicion is of paramount importance as both diagnosis and treatment may often be delayed for years.
Endometriosis has variable and often subtle clinical and macroscopic features that can be appreciated best by experienced gynecologic endoscopic surgeons. Hence, a multidisciplinary approach by thoracic and gynecologic surgical teams carries the highest chance of making an accurate diagnosis and providing the appropriate treatment strategies.
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- Hiraoka N, Odama S, Unoura K, et al. [Five cases of female pneumothorax with endometriosis on the blebs]. Nihon Kokyuki Gakkai Zasshi. Jan 2005;43(1):53-58.
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