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Case report

Minimally invasive thoracoscopic surgery as a diagnostic and therapeutic approach in bilateral pneumothorax in pregnancy caused by lymphangioleiomyomatosis – a case report

Željko Garabinović1, Nikola Čolić2, Jelena Vasić Madžarević1, Milan Savić1,3

ABSTRACT

Introduction: Lymphangioleiomyomatosis (LAM) is a rare disease which mainly occurs in women in the generative period, as well as during pregnancy, while only a few individual cases have been described in men. It occurs in sporadic form or is associated with tuberous sclerosis complex. The diagnosis can be made on the basis of high-resolution computed tomography (HRCT) findings, or histo- pathological analysis is required. Clinical manifestations of the disease include the following: progressive dyspnea on exertion, recurrent pneumothorax, chy- lothorax, angiomyolipomas and lymphangiomyomas.

Case report: A 32-year-old female patient was admitted to our clinic, in her third trimester of pregnancy, after a left-sided pneumothorax was verified on chest X-ray. Initial treatment included needle aspiration, followed by thoracic drainage of the left pleural cavity. Due to the prolonged air leak through the thoracic drain and the advanced stage of the pregnancy, a caesarean section was performed. After delivery, chest X-ray revealed complete right-sided pneumothorax, which required thoracic drainage, as well as an insufficiently reexpanded left lung. HRCT was performed and cystic bullous changes in the lungs were noted; LAM was histopathologically verified through a minimally invasive thoraco-surgical approach, first on the left and then on the right side, while bilateral pneumothorax was surgically treated.

Conclusion: Pneumothorax is a common complication of LAM. Due to the high recurrence rate, definitive early surgical intervention should be performed. Current guidelines recommend chemical pleurodesis and surgery for the first pneumothorax. When treating pneumothorax in pregnancy, the appropriate therapeutic procedure should be applied, taking into account the safety of the pregnancy and of the delivery.


INTRODUCTION

Lymphangioleiomyomatosis (LAM) is a progressive and rare multisystem disease of unknown etiology, which predominantly affects women, causing damage to the function of the lungs [1]. An epidemiological study, car- ried out in seven countries, showed the incidence of LAM to be 3.4 – 7.8 cases per one million women [2]. LAM mainly manifests in the form of cystic destruction of the lung parenchyma, as well as in the form of extrapul- monary disease, consisting of angiomyolipoma, lymph tumors (lymphangioleiomyoma) and chylous effusions [3]. Lymphangioleiomyomatosis is rare in the general population but is frequent in women with tuberous scle- rosis complex (TSC). It occurs in 30 – 40% of cases (TSC- LAM) [4]. It is present in women between menarche and menopause, of the average age of 34 years [5].

A significant number of patients with LAM devel- ops initial symptoms during pregnancy. It has been re- corded that pregnancy in cases of lymphangioleiomy- omatosis is linked to an increased incidence of pneu- mothorax, although some of the patients have an un- complicated pregnancy [6]. Most frequently, patients have shortness of breath, coughing, and pneumotho- rax. Less frequently, there are chylous pleural effusions and hemoptysis are present [7],[8].

The aim of this paper is to present the case of a preg- nant woman who developed spontaneous bilateral pneumothorax during the third trimester of her preg- nancy and immediately after childbirth, as well as to point out the importance of minimally invasive video-as- sisted thoracoscopic surgery (VATS) in the diagnosis of LAM and in treating pneumothorax caused by LAM.

CASE REPORT

A thirty-two-year-old female patient was admitted to our hospital in the 36th week of gestation of her second pregnancy, two days after experiencing sudden pain in the left hemithorax, which was followed by acute short- ness of breath. The patient had no previous history of chronic pulmonary disease or other comorbidities. Her first pregnancy was without complications. On physi- cal examination, she displayed tachypnea, tachycardia, and hyperresonance with percussion of the chest, with reduced breathing movements of the left hemithorax. Examination of the cardiovascular system did not yield a pathological finding nor was organomegaly verified. The blood count results, as well as the test of liver func- tion and kidney function were normal. The radiograph- ic image of the thorax confirmed the presence of com- plete left-sided pneumothorax (Figure 1).

Figure 1. Chest X-ray at hospital admission verifying left-sided pneumothorax

Figure 1. Chest X-ray at hospital admission verifying left-sided pneumothorax

Initial treatment included exsufflation of the left pleural cavity, and after this procedure yielded no im- provement, thoracic drainage of the left pleural cavity using under water sealed drainage (UWSD). Since re- expansion of the left lung did not occur, the thoracic drain was subsequently connected to active aspiration. Due to prolonged air loss via the thoracic drain and the advanced stage of pregnancy (37th week of gestation), a C-section was performed and a girl weighing 3,130 grams with a good Apgar score (9) was born.

After the delivery, an X-ray of the patient’s chest revealed complete right-sided pneumothorax, which required thoracic drainage, in addition to the thoracic drain previously placed due to left-sided pneumotho- rax (Figure 2).

02

 Figure 2. Chest X-ray after delivery verifying right-sided pneumothorax, with a previously placed thoracic drain – left ax

The high-resolution computed tomography (HRCT) chest scan showed bilateral multiple diffuse thin-walled cystic lesions, scattered throughout the lung parenchy- ma, which measured up to 22 mm in diameter (Figure 3). Computed tomography (CT) of the abdomen and the lesser pelvis showed no abnormalities.

Figure 3. Axial and coronal sections of the HRCT images of the thorax verifying cystic diffuse bilateral lesions in the lung parenchyma

Figure 3. Axial and coronal sections of the HRCT images of the thorax verifying cystic diffuse bilateral lesions in the lung parenchyma

In such circumstances, we decided on surgical treatment of the pneumothorax.

Initially, on the seventh day after delivery, we per- formed left-sided VATS. Intraoperatively, pleural adhe- sions were discovered in the region of the left superior lobe. After the separation of the pleural adhesions, a number of blisters and bullae were found in the su- perior and inferior lobe, predominantly in the lingular segment of the superior lobe and the apical segment of the inferior lobe (Figure 4). Using an endostapler, we performed wedge resection of the apical segment of the inferior lobe and the lingular segment of the su- perior lobe. Chemical pleurodesis was performed with 30 ml of 50% glucose solution, as well as mechanical pleurodesis with abrasion of the costal parietal pleura.

  Slika 4. Intraoperativni nalaz difuznih cističnih promena u plućnom parenhimu

Figure 4. Intraoperative finding of diffuse cystic lesions in the lung parenchyma

The histopathological finding revealed enlarged alveolar space with smooth muscle tissue in its walls, perivascular proliferation of smooth muscles, aggre- gates of lymphoid cells, and enlarged lymph spaces. Granuloma or malignancy was not found. The culti- vated cells of smooth muscle tissue proved positive to human melanoma block-45 (HMB-45). Thereby, the di- agnosis of lymphangioleiomyomatosis was confirmed.

Surgical treatment of the right-sided pneumothorax with the VATS approach was performed on the 15th day after delivery. Intraoperatively, we detected a number of blisters and bullae, predominantly in the middle lobe. Wedge resection of the middle lobe was performed with the use of the endostapler, followed by chemical and mechanical pleurodesis, in the same way as in the previous operation. The histopathological finding was in keeping with the one from the previous surgery.

Postoperative recovery, after both surgeries, was uneventful and full reexpansion of both the right and the left lung was achieved, with the reexpansion per- sisting after the removal of the thoracic drains.

The patient was discharged form hospital on the 20th day after delivery. On the day of discharge, the chest X-ray showed a completely reexpanded left and right lung.

Pulmonary function tests performed three, six, and twelve months upon delivery, showed results that were within the reference range.

Repeated HRCT scans of the abdomen and pelvis, six and twelve months after delivery, showed no abnor- malities. X-rays of the chest made one, three, six, and twelve months after delivery, showed a completely re- expanded left and right lung. Repeated HRCT scans of the chest, six and twelve months after delivery, showed no progression of the disease. Both the patient and her child remained healthy after a year of follow-up.

DISCUSSION

Lymphangioleiomyomatosis is a progressive cystic pulmonary disease, occurring mainly in women in their thirties [1],[5]. LAM rarely occurs in the general popula- tion. It usually develops in women with TSC (30 – 40% of cases), or it may occur as a sporadic form. There are specific criteria for diagnosing TSC [9]. In the case of our patient, the TSC criteria were not met.

Pneumothorax is frequent in patients with lymph- angioleiomyomatosis. The study of the National Heart, Lung, and Blood Institute(NHLBI) registry (USA), involv- ing 230 patients with LAM, registered pneumothorax in 55.5% of cases [10]. Other studies have shown that the incidence of pneumothorax in LAM is 1,000 great- er than in the general female population [11]. More- over, 50 – 80% of patients will develop pneumothorax during the illness. The recurrence of pneumothorax is frequent, with the average number of pneumothorax episodes being around four [10],[11],[12],[13],[14].

Nonspecific clinical characteristics with unremark- able chest X-rays on presentation lead to delayed diag- nosis or misdiagnosis [7],[8].

Complications connected to LAM, including pneu- mothorax and chylothorax, may occur in pregnancy, and the possible connection between pregnancy and the progression of LAM is cause for serious concern. Also, it has been recorded that women with LAM have a poorer outcome of pregnancy, including a greater number of premature births and miscarriages [6],[15],[16].

Pneumothorax caused by LAM in the third trimes- ter of pregnancy and shortly after delivery has been described in literature. This phenomenon is explained by the fact that hormone stimulation during pregnan- cy leads to the increase in cystic structures in the lungs, and subsequently, at the end of pregnancy or soon after delivery, hormone stimulation drops, and consequent- ly, some of the thin-walled cystic structures rupture, leading to pneumothorax. This also explains the fact that LAM is, almost typically, a female disease [17],[18].

It has been found earlier that dyspnea on exertion, as a symptom, is connected with increased mortality in LAM [19]. Conversely, it used to be believed that patients with pneumothorax had a more favorable prognosis [1]. More recent studies have not shown a link between pneumothorax and the long-term outcome [20],[21].

If a patient with confirmed LAM has pneumotho- rax, this patient should be treated in keeping with the standard guidelines for treating secondary pneumo- thorax [22]. Treatment of pneumothorax in pregnancy depends on the degree and phase of progression. Usu- ally, thoracic drainage is used, but without active aspi- ration [16]. In the case of our patient, the diagnosis of LAM was not known at the time when the decision was made on initial pneumothorax treatment, which is why we applied the recommendations of the official guide- lines for treating pneumothorax in pregnancy [23].

The American Thoracic Society/Japanese Respira- tory Society Clinical Practice Guidelines support the clinical diagnosis of LAM based on HRCT findings that are typical for lymphangioleiomyomatosis (e.g., dif- fuse, thin-walled, spheric cysts/blisters) accompanied by any of the following characteristics: TSC, renal angi- omyolipoma, cystic lymphangioleiomyoma, or chylous effusion in the thorax and/or abdomen. The guidelines strongly recommend the use of the VEGF-D test (vas- cular endothelial growth factor D test) for establishing the diagnosis of LAM, before considering lung biopsy in patients with cystic abnormalities characteristic of LAM present on the HRCT scan, but without other pos- itive clinical characteristics [24].

Histopathological confirmation of LAM may be obtained in different ways, including transbronchial, percutaneous or VATS biopsy. The risk from pneumo- thorax after transbronchial biopsy is 1 – 6 %, and it is even higher after percutaneous biopsy. The advantag- es of VATS are reflected in minimal surgical trauma, as well as in the fact that it enables the obtaining of an adequate sample for pathological confirmation, when bullectomy and pleurodesis or pleurectomy are per- formed [25]. Some retrospective studies suggest that transbronchial lung biopsy may be safe and efficient in some of the patients with suspected LAM. In a study by Meraj et al., amongst 63 patients who underwent transbronchial lung biopsy at the time when LAM was initially suspected, in 35 (56%) patients LAM was con- firmed in this way. The rate of reported complications of transbronchial biopsy was approximately 14% (6% with pneumothorax, 4% with bleeding, 2% with chest pain, and 2% with pneumonia) [26].

However, surgical biopsy of the lungs with the ap- plication of VATS is believed to be the golden standard for obtaining histopathological confirmation of LAM.

When a definitive diagnosis is necessary in patients with parenchymal cysts characteristic of LAM present on the HRCT finding, but without additional positive characteristics of LAM, the American Thoracic Society/ Japanese Respiratory Society Clinical Practice Guide- lines suggest a diagnostic approach which includes transbronchial lung biopsy, before surgical lung bi- opsy [27]. In our patient, the diagnosis of LAM was es- tablished with the VATS approach, which was also the treatment procedure for pneumothorax.

Since the recurrence rate is high, current guide- lines recommend pleurodesis at the time of the first episode of pneumothorax, in patients with confirmed LAM [22],[27]. However, pleurodesis in patients with LAM has limited efficiency, and it has been recorded that recurrence rates for pneumothorax range from 18% to 32% [27],[28]. Clear guidelines are lacking as to whether chemical or mechanical pleurodesis is opti- mal, but it is definitively important to include thorac- ic surgeons into the process early on, as some of the patients will need a lung transplant, in the long-term. European Respiratory Society Guidelines for the Diag- nosis and Management of Lymphangioleiomyomato- sis (LAM) and the American Thoracic Society/Japanese Respiratory Society Clinical Practice Guidelines recom- mend chemical pleurodesis and surgery, for the first pneumothorax [22],[26]. In the case of our patient, we performed chemical and mechanical pleurodesis. Pre- vious pleural procedures are not a contraindication for a future lung transplant [29].

  • Conflict of interest:
    None declared.

Informations

Volume 3 No 2

June 2022

Pages 241-248
  • Keywords:
    pneumothorax, pregnancy, lymphangioleiomyomatosis
  • Received:
    27 April 2022
  • Revised:
    11 May 2022
  • Accepted:
    17 May 2022
  • Online first:
    25 May 2022
  • DOI:
Corresponding author

Željko Garabinović
Clinic for Thoracic Surgery, University Clinical Center of Serbia
26 Koste Todorovića Street, 11000 Belgrade, Serbia
E-mail: This email address is being protected from spambots. You need JavaScript enabled to view it.


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    2. Harknett EC, Chang WY, Byrnes S, Johnson J, Lazor R, Cohen MM, et al. Use of variability in national and regional data to estimate the prevalence of lymp- hangioleiomyomatosis. QJM. 2011 Nov;104(11):971-9. doi: 10.1093/qjmed/hcr116.[CROSSREF]

    3. Ferrans VJ, Yu ZX, Nelson WK, Valencia JC, Tatsuguchi A, Avila NA, et al. Lymphangioleiomyomatosis (LAM): a review of clinical and morphological features. J Nippon Med Sch. 2000 Oct;67(5):311-29. doi: 10.1272/jnms.67.311.[CROSSREF]

    4. Aubry MC, Myers JL, Ryu JH, Henske EP, Logginidou H, Jalal SM, et al. Pulmo- nary lymphangioleiomyomatosis in a man. Am J Respir Crit Care Med. 2000 Aug;162(2 Pt 1):749-52. doi: 10.1164/ajrccm.162.2.9911006.[CROSSREF]

    5. Brunelli A, Catalini G, Fianchini A. Pregnancy exacerbating unsuspected me- diastinal lymphangioleiomyomatosis and chylothorax. Int J Gynaecol Obstet. 1996 Mar;52(3):289-90. doi: 10.1016/0020-7292(95)02619-3.[CROSSREF]

    6. Johnson SR, Tattersfield AE. Clinical experience of lymphangioleiomyo- matosis in the UK. Thorax. 2000 Dec;55(12):1052-7. doi: 10.1136/thorax.55.12.1052.[CROSSREF]

    7. Mitra S, Ghosal AG, Bhattacharya P. Pregnancy unmasking lymphangioleio- myomatosis. J Assoc Physicians India. 2004 Oct;52:828-30.[HTTP]

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REFERENCES

1. Cohen MM, Pollock-BarZiv S, Johnson SR. Emerging clinical picture of lymphangioleiomyomatosis. Thorax. 2005 Oct;60(10):875-9. doi: 10.1136/thx.2004.035154.[CROSSREF]

2. Harknett EC, Chang WY, Byrnes S, Johnson J, Lazor R, Cohen MM, et al. Use of variability in national and regional data to estimate the prevalence of lymp- hangioleiomyomatosis. QJM. 2011 Nov;104(11):971-9. doi: 10.1093/qjmed/hcr116.[CROSSREF]

3. Ferrans VJ, Yu ZX, Nelson WK, Valencia JC, Tatsuguchi A, Avila NA, et al. Lymphangioleiomyomatosis (LAM): a review of clinical and morphological features. J Nippon Med Sch. 2000 Oct;67(5):311-29. doi: 10.1272/jnms.67.311.[CROSSREF]

4. Aubry MC, Myers JL, Ryu JH, Henske EP, Logginidou H, Jalal SM, et al. Pulmo- nary lymphangioleiomyomatosis in a man. Am J Respir Crit Care Med. 2000 Aug;162(2 Pt 1):749-52. doi: 10.1164/ajrccm.162.2.9911006.[CROSSREF]

5. Brunelli A, Catalini G, Fianchini A. Pregnancy exacerbating unsuspected me- diastinal lymphangioleiomyomatosis and chylothorax. Int J Gynaecol Obstet. 1996 Mar;52(3):289-90. doi: 10.1016/0020-7292(95)02619-3.[CROSSREF]

6. Johnson SR, Tattersfield AE. Clinical experience of lymphangioleiomyo- matosis in the UK. Thorax. 2000 Dec;55(12):1052-7. doi: 10.1136/thorax.55.12.1052.[CROSSREF]

7. Mitra S, Ghosal AG, Bhattacharya P. Pregnancy unmasking lymphangioleio- myomatosis. J Assoc Physicians India. 2004 Oct;52:828-30.[HTTP]

8. Taylor JR, Ryu J, Colby TV, Raffin TA. Lymphangioleiomyomatosis. Clinical co- urse in 32 patients. N Engl J Med. 1990 Nov 1;323(18):1254-60. doi: 10.1056/NEJM199011013231807.[CROSSREF]

9. Northrup H, Krueger DA; International Tuberous Sclerosis Complex Con- sensus Group. Tuberous sclerosis complex diagnostic criteria update: recommendations of the 2012 Iinternational Tuberous Sclerosis Complex Consensus Conference. Pediatr Neurol. 2013 Oct;49(4):243-54. doi: 10.1016/j. pediatrneurol.2013.08.001.[CROSSREF]

10. Ryu JH, Moss J, Beck GJ, Lee JC, Brown KK, Chapman JT, et al.; NHLBI LAM Registry Group. The NHLBI lymphangioleiomyomatosis registry: characte- ristics of 230 patients at enrollment. Am J Respir Crit Care Med. 2006 Jan 1;173(1):105-11. doi: 10.1164/rccm.200409-1298OC.[CROSSREF]

11. Gonano C, Pasquier J, Daccord C, Johnson SR, Harari S, Leclerc V, et al. Air travel and incidence of pneumothorax in lymphangioleiomyomatosis. Orp- hanet J Rare Dis. 2018 Dec 13;13(1):222. doi: 10.1186/s13023-018-0964-6.[CROSSREF]

12. Johnson SR, Whale CI, Hubbard RB, Lewis SA, Tattersfield AE. Survival and disease progression in UK patients with lymphangioleiomyomatosis. Thorax. 2004 Sep;59(9):800-3. doi: 10.1136/thx.2004.023283.[CROSSREF]

13. Taylor JR, Ryu J, Colby TV, Raffin TA. Lymphangioleiomyomatosis. Clinical co- urse in 32 patients. N Engl J Med. 1990 Nov 1;323(18):1254-60. doi: 10.1056/ NEJM199011013231807.[CROSSREF]

14. Urban T, Lazor R, Lacronique J, Murris M, Labrune S, Valeyre D, et al. Pulmo- nary lymphangioleiomyomatosis. A study of 69 patients. Groupe d'Etudes et de Recherche sur les Maladies "Orphelines" Pulmonaires (GERM"O"P). Medicine (Baltimore). 1999 Sep;78(5):321-37. doi: 10.1097/00005792-199909000-00004.[CROSSREF]

15. Cohen MM, Freyer AM, Johnson SR. Pregnancy experiences among women with lymphangioleiomyomatosis. Respir Med. 2009 May;103(5):766-72. doi: 10.1016/j.rmed.2008.11.007.[CROSSREF]

16. Shen L, Xu W, Gao J, Wang J, Huang J, Wang Y, He Y, Yang Y, Tian X, Xu KF. Pre- gnancy after the diagnosis of lymphangioleiomyomatosis (LAM). Orphanet J Rare Dis. 2021 Mar 17;16(1):133. doi: 10.1186/s13023-021-01776-7.[CROSSREF]

17. Crawford TC, Grimm JC, Magruder JT, Stephens RS, Sciortino CM, Vaught AJ, et al. A curious case of acute respiratory distress syndrome. J Surg Case Rep. 2015 Nov 9;2015(11):rjv140. doi: 10.1093/jscr/rjv140.[CROSSREF]

18. Grzegorek I, Lenze D, Chabowski M, Janczak D, Szolkowska M, Langfort R, et al. Immunohistochemical evaluation of pulmonary lymphangioleiomyoma- tosis. Anticancer Res. 2015 Jun;35(6):3353-60.[HTTP]

19. Hayashida M, Seyama K, Inoue Y, Fujimoto K, Kubo K; Respiratory Failure Research Group of the Japanese Ministry of Health, Labor, and Welfare. The epidemiology of lymphangioleiomyomatosis in Japan: a nationwide cross-sectional study of presenting features and prognostic factors. Respiro- logy. 2007 Jul;12(4):523-30. doi: 10.1111/j.1440-1843.2007.01101.x.[CROSSREF]

20. Gupta N, Lee HS, Ryu JH, Taveira-DaSilva AM, Beck GJ, Lee JC, et al.; NHLBI LAM Registry Group. The NHLBI LAM Registry: Prognostic Physiologic and Radiologic Biomarkers Emerge From a 15-Year Prospective Longitudinal Analysis. Chest. 2019 Feb;155(2):288-96. doi: 10.1016/j.chest.2018.06.016.[CROSSREF]

21. Oprescu N, McCormack FX, Byrnes S, Kinder BW. Clinical predictors of mor- tality and cause of death in lymphangioleiomyomatosis: a population-based registry. Lung. 2013 Feb;191(1):35-42. doi: 10.1007/s00408-012-9419-3.[CROSSREF]

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21. Oprescu N, McCormack FX, Byrnes S, Kinder BW. Clinical predictors of mor- tality and cause of death in lymphangioleiomyomatosis: a population-based registry. Lung. 2013 Feb;191(1):35-42. doi: 10.1007/s00408-012-9419-3.[CROSSREF]

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23. MacDuff A, Arnold A, Harvey J; BTS Pleural Disease Guideline Group. Ma- nagement of spontaneous pneumothorax: British Thoracic Society Pleural Disease Guideline 2010. Thorax. 2010 Aug;65 Suppl 2:ii18-31. doi: 10.1136/thx.2010.136986.[CROSSREF]

24. McCormack FX, Gupta N, Finlay GR, Young LR, Taveira-DaSilva AM, Glasgow CG, et al.; ATS/JRS Committee on Lymphangioleiomyomatosis. Official Ame- rican Thoracic Society/Japanese Respiratory Society Clinical Practice Guide- lines: Lymphangioleiomyomatosis Diagnosis and Management. Am J Respir Crit Care Med. 2016 Sep 15;194(6):748-61. doi: 10.1164/rccm.201607-1384ST.[CROSSREF]

25. Tsai CF, Hsiao CH, Lee JM, Chen KC, Shieh MJ, Lai HS, et al. Video-assisted thoracoscopic surgery for recurrent pneumothorax in pulmonary lymphan- gioleimyomatosis with tuberous sclerosis complex. J Cardiothorac Surg. 2013 Apr 18;8:101. doi: 10.1186/1749-8090-8-101.[CROSSREF]

26. Meraj R, Wikenheiser-Brokamp KA, Young LR, Byrnes S, McCormack FX. Uti- lity of transbronchial biopsy in the diagnosis of lymphangioleiomyomatosis. Front Med. 2012 Dec;6(4):395-405. doi: 10.1007/s11684-012-0231-5.[CROSSREF]

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28. Almoosa KF, Ryu JH, Mendez J, Huggins JT, Young LR, Sullivan EJ, et al. Ma- nagement of pneumothorax in lymphangioleiomyomatosis: effects on recu- rrence and lung transplantation complications. Chest. 2006 May;129(5):1274- 81. doi: 10.1378/chest.129.5.1274.[CROSSREF]

29. Weill D, Benden C, Corris PA, Dark JH, Davis RD, Keshavjee S, et al. A consensus document for the selection of lung transplant candidates: 2014--an update from the Pulmonary Transplantation Council of the International Society for Heart and Lung Transplantation. J Heart Lung Transplant. 2015 Jan;34(1):1- 15. doi: 10.1016/j.healun.2014.06.014.[CROSSREF]


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