- Email: [email protected]
Successful Lobectomy for Pulmonary Arteriovenous Malformation Causing Recurrent Massive Haemoptysis
Case Reports
3. Hirst Jr AE, Johns Jr VJ, Kime Jr SW. Dissecting aneurysm of the aorta: a review of 505 cases. Medicine (Baltimore) 1958;37:217–79. 4. Linsay Jr J, Hurst JW. Clinical features and prognosis in dissecting aneurysm of the aorta: a re-appraisal. Circulation 1967;35:880–8. 5. Jamieson WR, Munro AI, Miyagishima RT, Allen P, Tyers GF, Gerein AN. Aortic dissection: early diagnosis and surgical management are the keys to survival. Can J Surg 1982;25:145– 9. 6. Meszaros I, Morocz J, Szlavi J, Schmidt J, Tornoci L, Nagy L, Szep L. Epidemiology and clinicopathology of aortic dissection. Chest 2000;117:1271–8. 7. Bickerstaff LK, Pairolero PC, Hollier LH, Melton LJ, Van Peenen HJ, Cherry KJ, Joyce JW, Lie JT. Thoracic aortic aneurysms: a population-based study. Surgery 1982;92: 1103–8. 8. Spittell PC, Spittell Jr JA, Joyce JW, Tajik AJ, Edwards WD, Schaff HV, Stanson AW. Clinical features and differential
9.
10.
11. 12. 13.
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diagnosis of aortic dissection: experience with 236 cases (1980 through 1990). Mayo Clin Proc 1993;68:642–51. Hagan PG, Nienaber CA, Isselbacher EM, Bruckman D, Karavite DJ, Russman PL, Evangelista A, Fattori R, Suzuki T, Oh JK, Moore AG, Malouf JF, Pape LA, Gaca C, Sechtem U, Lenferink S, Deutsch HJ, Diedrichs H, Marcos y Robles J, Llovet A, Gilon D, Das SK, Armstrong WF, Deeb GM, Eagle KA. The International Registry of Acute Aortic Dissection (IRAD): new insights into an old disease. JAMA 2000;283:897–903. Bourland MD. Aortic dissection. In: Rosen P, Barkin RM, editors. Emergency medicine-concepts and clinical practice. 3rd ed. St. Louis, MO: Mosby-Year Book Inc; 1992. p. 1384–90. Zull DN, Cydulka R. Acute paraplegia: a presenting manifestation of aortic dissection. Am J Med 1988;84:765–70. Rosen SA. Painless aortic dissection presenting as spinal cord ischemia. Ann Emerg Med 1988;17:840–2. Weisman AD, Adams RD. The neurological complication of dissection aortic aneurysm. Brain 1944;67:6–91.
Successful Lobectomy for Pulmonary Arteriovenous Malformation Causing Recurrent Massive Haemoptysis Ujjwal K. Chowdhury, M.Ch., Diplomate N.B. a,∗ , Shyam S. Kothari, DM, FACC b and Arvind K. Bishnoi, MS a Ruchika Gupta, MD c Chander M. Mittal, MS a Srikrishna Reddy, MS a a
Department of Cardiothoracic Surgery, AIIMS, New Delhi, India b Department of Cardiology, AIIMS, New Delhi, India c Department of Cardiac Pathology, AIIMS, New Delhi, India
A 6-year-old child with pulmonary arteriovenous malformation (PAVM) of the lower lobe of left lung was successfully treated by left lower lobectomy and the case is reported for its rarity. The exact diagnosis is relatively easy to make by contrast echocardiography and pulmonary angiocardiography, provided the possibility is entertained. Because of recurrent episodes of massive haemoptysis from a single pulmonary lobe, surgical resection was deemed the best curative option to avoid further episodes and recurrence. Published reports detailing coil embolisation therapy for PAVMs are also discussed. (Heart, Lung and Circulation 2009;18:133–162) © 2008 Published by Elsevier Inc on behalf of Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Keywords. Pulmonary arteriovenous malformation; Polycythaemia; Lobectomy
Introduction Received 13 August 2007; received in revised form 14 November 2007; accepted 21 November 2007; available online 21 February 2008 ∗ Corresponding author at: Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, New Delhi 110029, India. Tel.: +91 11 26588700/26588500x4835; fax: +91 11 26588663/26588641. E-mail addresses: [email protected], [email protected] (U.K. Chowdhury)
C
ongenital pulmonary arteriovenous malformation (PAVM) is a rare entity and is different from right pulmonary artery-to-left atrium communication. They may occur as an isolated anomaly or in association with hereditary haemorrhagic telangiectasia.1 Patients with PAVMs may be asymptomatic or present with hypoxaemia, paradoxical thromboembolism, brain abscess or massive haemoptysis.1–6
© 2008 Published by Elsevier Inc on behalf of Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand.
1443-9506/04/$30.00 doi:10.1016/j.hlc.2007.11.142
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Figures 1–2. A selective pulmonary angiogram (Fig. 1A–C) and computerised tomographic pulmonary angiogram (Fig. 2A–C) showing pulmonary arteriovenous malformations involving all segments of the lower lobe of the left lung with a dilated, tortuous left pulmonary artery (LPA) and a single draining pulmonary vein (PV) into the left atrium (LA). There are multiple feeding arteries originating from the left lower lobar division of the left pulmonary artery supplying the pulmonary malformation (PAVM) and there are no intra-or-extrathoracic vascular communications.
We report a patient who presented with recurrent episodes of massive haemoptysis from a bleeding left lower lobe PAVM that was successfully treated by left lower lobectomy. The extreme rarity of the disease entity, the usage of contrast echocardiography, and pulmonary angiography for diagnosis, the successful surgical correction using left lower lobectomy, and a brief literature review of the long-term outcome after surgical repair forms the basis of the present study.
Case Report A 6-year-old child was referred to our institute with progressively increasing symptoms of shortness of breath (NYHA functional class III), non-resolving pneumonia, and recurrent haemoptysis of 4 months duration. He received three courses of antibiotic treatment during this period. The significant clinical findings included central cyanosis, digital clubbing, and a bruit which increased its
Figure 3. (A and B) Surgical specimen (excised left lower lobe (LLL)) illustrating ecstatic bronchioles and dilated vessels near the visceral pleural surface.
pitch and volume on inspiration, best heard on the infrascapsular and infraaxillary regions. Remarkable signs on laboratory work up included low systemic arterial oxygen saturation (SaO2 ) of 65% and haemoglobin of 18.0 g%. Chest radiography revealed a lobulated mass in lower lobe of left lung. Chest contrast computed tomography demonstrated a 12 cm × 10 cm lobulated mass in the lower lobe of left lung with brilliant contrast enhancement in the arterial phase and its appearance was consistent with a PAVM. Contrast echocardiography showed microbubbles in left atrium after 5 s, thus confirming an intrapulmonary shunt. A selective pulmonary angiogram and computerised tomographic pulmonary angiogram showed PAVM involving all segments of the lower lobe of left lung with dilated, tortuous left pulmonary artery (LPA) measuring >2 cm in diameter. There were multiple feeding arteries supplying the PAVM and there were no intra-or extra-thoracic vascular communications (Fig. 1(A–C) and 2(A–C)). There were no additional PAVM on either side of the lung. Considering the multiplicity of the feeder vessels, localisation to the isolated lobe and massive dilatation of LPA at the lobar fissure, the patient was considered for resectional therapy through left muscle sparing thoracotomy. Intra-operatively, a large pulsating complex of PAVM, measuring 12 cm × 10 cm almost completely occupying the left lower lobe was supplied by superior segmental and main basal pulmonary arteries. There was no aberrant
Case Reports
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Figure 4. Photomicrograph of lung biopsy of the patient with pulmonary arteriovenous malformation (light microscopy 40×; Haematoxylin and Eosin stain). A shows parenchymal haemorrhages, abnormally dilated vascular channels (→) close to bronchiolar structure. B depicts multiple dilated vascular channels (→) with irregular lumen and variable wall thicknesses in the lung parenchyma in place of normal corner vessels.
blood supply. The pulmonary artery and vein were ecstatic measuring almost 2 cm in diameter (Fig. 3A and B). Lower lobectomy was performed. The SaO2 improved from 65 to 100% immediately after ligation of LPA. Histo-pathological examination of the specimen revealed a plexiform mass of dilated vessels with feeding vessels. Dilated bronchi and bronchioles were apparent and contained blood clots and inflammatory exudates. Vessels in apposition with these ecstatic bronchioles were also dilated with irregular lumen and variable wall thicknesses. There was parenchymal haemorrhage and oedema. An increased number of irregular vessels were also noted at the peripheries of the lung (Fig. 4A and B). The postoperative course was uneventful and patient was discharged after 6 days. Follow-up visit at 14 months showed no cyanosis, no dyspnoea and room air SaO2 of 98%.
Discussion Since the first description of PAVM at autopsy by Churton in 1897,2 these abnormal communications have been given various names, including pulmonary arteriovenous aneurysms, haemangiomas of the lung, cavernous angiomas of the lung, and pulmonary telangiectases.3
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PAVM may be simple (single pulmonary artery-topulmonary vein communication) or complex (multiple feeding arteries and draining veins), and single (40%), multiple (40%), or bilateral (20%). Most PAVMs are congenital but acquired causes include infections (tuberculosis, actinomyocosis, and schistosomiasis), metastatic carcinoma, chest trauma, modified Fontan operations and iatrogenic.4,5 Thirty-six percent of single lesions and 57% of multiple lesions are associated with hereditary haemorrhagic telangiectasia (Osler–Weber–Rendu syndrome), an autosomal dominant disorder with mutations localised to chromosome locus 9q and 12.6,7 Fifty-three to 70% of PAVMs are found in lower lobes. Females are affected twice or often as males but there is a male predominance in newborns.6,7 No definite pathogenetic explanation has been described for this anomaly. The postulated theories include a defect in the terminal arterial loops, which allows dilatation of the thin-walled capillary sacs, incomplete resorption of the vascular septae that separate the arterial and venous plexuses, which normally anastomose during foetal development and a failure of capillary development in the foetus.8 PAVMs exhibit a wide range of histology from diffuse telangiectasia to large complex structures consisting of a bulbous aneurysmal sac between dilated feeding arteries and draining veins. Approximately 95% of these feeding arteries originated from the pulmonary rather than the systemic circulation.9 The most common systemic arterial supplies to PAVMs reported in the literature originated from the bronchial artery, less so from the internal mammary artery or even directly from the descending thoracic aorta.10 The disease entity should be suspected when the following combination of symptoms and signs co-exist: central cyanosis, digital clubbing, exertional dyspnoea, haemoptysis, epistaxis, telangiectasia, history of cerebral abscess/embolism, silent precordium, normally split second heart sound, non-specific bruit over the right or left infraaxillary region, static hypoxaemia (orthodeoxia), platypnoea (improvement of dyspnoea on reclining) and one or more pulmonary nodules associated with typical roentgenographic findings (round or oval mass of uniform density, frequently lobulated but sharply defined, located commonly in lower lobes, ranging from 1 to 5 cm in diameter). Diagnosis of this anomaly is difficult. A plain chest radiography shows abnormalities in about 98% of patients. The 100% oxygen method, contrast echocardiography, and radionuclide imaging are nearly 100% sensitive for the detection of clinically significant PAVMs. The specificity of contrast echocardiography and radionuclide imaging is higher than 100% oxygen method.3–7 Contrast echocardiography using agitated saline into a peripheral vein is perhaps the most sensitive method for detection of PAVMs. Appearance of bubbles in left atrium after 3–5 cardiac cycles in the absence of intracardiac shunt (where bubbles appear in less than 3 cardiac cycles) gives a clue to the possibility of PAVMs. Although it does not quantify shunt fraction, it allows assessment of
Heart, Lung and Circulation 2009;18:133–162
the efficiency of embolotherapy and as a screening tool in family members of patients with hereditary haemorrhagic telangiectasia.5–7 Radionuclide imaging is also a sensitive method and can quantify the shunt fraction, but it cannot differentiate between a cardiac or pulmonary source of shunt.3–7 Like contrast echocardiography, it does not provide accurate anatomical details of PAVM. Ultrafast contrast enhanced, computed tomography has been shown to be more sensitive than conventional pulmonary angiograms for PAVMs and better in defining the architecture. Three-dimensional helical computed tomography has also been shown to be very accurate in analysing the PAVMs especially if combined with cross-sectional images.3–7,12 Its main advantage is non-invasiveness and avoidance of contrast injection. The disadvantage is false positive results with vascular tumours. The use of magnetic resonance imaging (MRI) in PAVMs is limited. Recently, phase contrast cine sequences have been shown to be the most accurate of MRI techniques.4,5 PAVMs and aneurysms with rapid blood flow in the region results in a signal void and produce low intensity signals. Despite isolated case reports of successful diagnosis, the main limitations of MRI are limited availability, relative expense, and the need for highly specialised staff for data interpretation.3–5 Pulmonary angiography remains the gold standard especially when a therapeutic intervention is planned.3–5 Subtraction angiography has largely replaced the conventional angiogram for PAVMs. Angiography provides detailed information on the location and size of PAVMs, the angioarchitecture and mapping of the feeding vessels, which are necessary before surgery or embolotherapy. Angiography should be performed on all portions of the lung to look for any unsuspected PAVMs, source of intrathoracic or extrathoracic vascular communications.3,5,13 Published reports recommend the screening of patients with hereditary haemorrhagic telangiectasia for PAVM with chest X-ray and contrast echocardiography.6,7 If either is positive, a contrast and helical computed tomography scanning of chest with three-dimensional reconstructions should be performed. The natural history of PAVMs is such that they tend to increase in size, especially if multiple, and rarely regress spontaneously. The mortality rate in historical reviews of untreated but symptomatic patients with PAVMs over periods of 15 years ranges from 4 to 22% and in severe cases up to 40%. The abnormal vessels may bleed into a bronchus or the pleural cavity, sometimes with a fatal outcome.14 Early surgical intervention or embolotherapy is recommended to prevent chronic arterial hypoxaemia, systemic thromboembolic complications, congestive cardiac failure, shunt-derived pulmonary hypertension, pulmonary haemorrhage and cerebral embolism or abscess.3,6,10,12 Treatment of PAVMs should be based on the size, number, and location of the lesions and the specific complications as well as patients’ general condition.
Therapeutic transcatheter embolisation offers an effective therapy for patients who are poor surgical candidates, whose lesions are too numerous to resect, and patients who decline surgical intervention.3–5,11,12 Reports of embolisation therapy do not adequately document long-term follow-up with serial chest roentgenograms, oxymetry to evaluate the incidence of delayed balloon deflation and recurrence.3–5,12,15 However, even with good initial control (80–100%), embolisation is associated with higher subsequent recurrent haemoptysis compared with surgery.16 The risks of balloon embolisation include balloon migration, clot propagation, recurrence, systemic embolisation and pulmonary infarction.15 Simple ligation has been abandoned as a surgical procedure for PAVMs because of the difficulty of feeding of all feeder vessels and the high incidence of recanalisation of PAVMs through accessory vessels.9 Published literature documents surgical resection as the treatment of choice for patients who can tolerate surgery, who fail embolotherapy, develop serious complication despite embolotherapy, have intrapleural rupture of PAVMs, have untreatable contrast allergy, lesions not amenable to embolotherapy (e.g. large centrally localised lesions) and in neonates presenting with early neurologic symptoms.3–5,11,17 Conservative lung resection, local resection, segmentectomy or lobectomy are the procedures of choice whenever possible.3–5,11,17 Brown and associates performed staged bilateral thoracotomies in case of extensive bilateral PAVMs.18 Recently, video assisted thoracoscopy has been employed in the resection of a small PAVM.8 The reported perioperative mortality has varied from 0 to 9.1% with only rare postoperative recurrences.3–5,11,17 The current case serves to emphasise that surgical resection is a safe method of treatment of PAVM in selected patients i.e. when PAVM is solitary and large (more than 2 cm) in diameter and the risk of embolotherapy is high.
References 1. Vase P, Holm M, Arendrup H. Pulmonary arteriovenous fistulas in heridatary haemorrhagic telangiectasia. Acta Med Scand 1985;218:105–9. 2. Churton T. Multiple aneurysms of pulmonary artery. Br Med J 1897;1:1223. 3. Dines DE, Seward JB, Bernatz PE. Pulmonary arteriovenous fistulas. Mayo Clin Proc 1983;58:176–81. 4. Khurshid I, Downie GH. Pulmonary arteriovenous malformation. Postgrad Med J 2002;78:191–7.
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5. Iqbal M, Rossoff LJ, Steinberg HN, Marzouk KA, Siegel DN. Pulmonary arteriovenous malformations: a clinical review. Postgrad Med J 2000;76:390–4. 6. Cottin V, Plauchu H, Bayle JY, Barthelet M, Revel D, Cordier JF. Pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. Am J Respir Crit Care Med 2004;169:994–1000. 7. Shovlin CL, Guttmacher AE, Buscarini E, Faughnan ME, Hyland RH, Westermann CJ, Kjeldsen AD, Plauchu H. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu–Osler–Weber syndrome). Am J Med Genet 2000;91:66–7. 8. Watanabe N, Munakata Y, Ogiwara M, Miyatake M, Nakagawa F, Hirayama J. A case of pulmonary arteriovenous malformation in a patient with brain abscess successfully treated with video-assisted thoracoscopic resection. Chest 1995;108:1724–7. 9. Bosher LH, Blake A, Byrd BR. An analysis of the pathologic anatomy of pulmonary arteriovenous aneurysms with particular reference to the applicability of local excision. Surgery 1959;45:91–104. 10. Kuwahara T, Ida M, Hamada T. A case of systemic arterial supply to the normal left basal segments with anomalous return to the left inferior pulmonary vein. Nihon Kyobu Shikkan Gakkiai Sushi 1995;33:733–7. 11. Puskas JD, Allen MS, Moncure AC, Wain Jr JC, Hilgenberg AD, Wright C, Grillo HC, Mathisen DJ. Pulmonary arteriovenous malformations, therapeutic options. Ann Thorac Surg 1993;56:253–7. 12. Lee DW, White RI, Egglin TK, Pollak JS, Fayad PB, Wirth JA, Rosenblatt MM, Dickey KW, Burdge CM. Embolotherapy of large pulmonary arteriovenous malformations: long-term results. Ann Thorac Surg 1997;64:930–40. 13. Thung KH, Sihoe ADL, Wan IYP, Lee TW, Wong R, Yim AP. Hemoptysis from an unusual pulmonary arteriovenous malformation. Ann Thorac Surg 2003;76:1730–3. 14. Sluiter-Eringa H, Orie NGM, Sluiter HJ. Pulmonary arteriovenous fistula. Diagnosis and prognosis in noncomplaint patients. Am Rev Respir Dis 1969;100:177–88. 15. White Jr RI, Lynch-Nyhan A, Terry P, Buescher PC, Farmlett EJ, Charnas L, Shuman K, Kim W, Kinnison M, Mitchell SE. Pulmonary arteriovenous malformations: techniques and long-term outcome of embolotherapy. Radiology 1988;169:663–9. 16. Wispelaere JE, Trigaux JP, Weynants P, Delos M, Coene BD. Systemic supply to a pulmonary arteriovenous malformation: potential explanation for recurrence. Cardiovasc Intervent Radiol 1996;19:285–9. 17. Georghiou GP, Berman M, Vidne BA, Saute M. Pulmonary arteriovenous malformation treated by lobectomy. Eur J Cardiothoracic Surg 2003;24:328–30. 18. Brown SE, Wright PW, Renner JW, Riker JB. Staged bilateral thoracotomies for multiple pulmonary arteriovenous malformations complicating hereditary hemorrhagic telangiectasia. J Thorac Cardiovasc Surg 1982;83:285–9.
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3. Hirst Jr AE, Johns Jr VJ, Kime Jr SW. Dissecting aneurysm of the aorta: a review of 505 cases. Medicine (Baltimore) 1958;37:217–79. 4. Linsay Jr J, Hurst JW. Clinical features and prognosis in dissecting aneurysm of the aorta: a re-appraisal. Circulation 1967;35:880–8. 5. Jamieson WR, Munro AI, Miyagishima RT, Allen P, Tyers GF, Gerein AN. Aortic dissection: early diagnosis and surgical management are the keys to survival. Can J Surg 1982;25:145– 9. 6. Meszaros I, Morocz J, Szlavi J, Schmidt J, Tornoci L, Nagy L, Szep L. Epidemiology and clinicopathology of aortic dissection. Chest 2000;117:1271–8. 7. Bickerstaff LK, Pairolero PC, Hollier LH, Melton LJ, Van Peenen HJ, Cherry KJ, Joyce JW, Lie JT. Thoracic aortic aneurysms: a population-based study. Surgery 1982;92: 1103–8. 8. Spittell PC, Spittell Jr JA, Joyce JW, Tajik AJ, Edwards WD, Schaff HV, Stanson AW. Clinical features and differential
9.
10.
11. 12. 13.
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diagnosis of aortic dissection: experience with 236 cases (1980 through 1990). Mayo Clin Proc 1993;68:642–51. Hagan PG, Nienaber CA, Isselbacher EM, Bruckman D, Karavite DJ, Russman PL, Evangelista A, Fattori R, Suzuki T, Oh JK, Moore AG, Malouf JF, Pape LA, Gaca C, Sechtem U, Lenferink S, Deutsch HJ, Diedrichs H, Marcos y Robles J, Llovet A, Gilon D, Das SK, Armstrong WF, Deeb GM, Eagle KA. The International Registry of Acute Aortic Dissection (IRAD): new insights into an old disease. JAMA 2000;283:897–903. Bourland MD. Aortic dissection. In: Rosen P, Barkin RM, editors. Emergency medicine-concepts and clinical practice. 3rd ed. St. Louis, MO: Mosby-Year Book Inc; 1992. p. 1384–90. Zull DN, Cydulka R. Acute paraplegia: a presenting manifestation of aortic dissection. Am J Med 1988;84:765–70. Rosen SA. Painless aortic dissection presenting as spinal cord ischemia. Ann Emerg Med 1988;17:840–2. Weisman AD, Adams RD. The neurological complication of dissection aortic aneurysm. Brain 1944;67:6–91.
Successful Lobectomy for Pulmonary Arteriovenous Malformation Causing Recurrent Massive Haemoptysis Ujjwal K. Chowdhury, M.Ch., Diplomate N.B. a,∗ , Shyam S. Kothari, DM, FACC b and Arvind K. Bishnoi, MS a Ruchika Gupta, MD c Chander M. Mittal, MS a Srikrishna Reddy, MS a a
Department of Cardiothoracic Surgery, AIIMS, New Delhi, India b Department of Cardiology, AIIMS, New Delhi, India c Department of Cardiac Pathology, AIIMS, New Delhi, India
A 6-year-old child with pulmonary arteriovenous malformation (PAVM) of the lower lobe of left lung was successfully treated by left lower lobectomy and the case is reported for its rarity. The exact diagnosis is relatively easy to make by contrast echocardiography and pulmonary angiocardiography, provided the possibility is entertained. Because of recurrent episodes of massive haemoptysis from a single pulmonary lobe, surgical resection was deemed the best curative option to avoid further episodes and recurrence. Published reports detailing coil embolisation therapy for PAVMs are also discussed. (Heart, Lung and Circulation 2009;18:133–162) © 2008 Published by Elsevier Inc on behalf of Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand. Keywords. Pulmonary arteriovenous malformation; Polycythaemia; Lobectomy
Introduction Received 13 August 2007; received in revised form 14 November 2007; accepted 21 November 2007; available online 21 February 2008 ∗ Corresponding author at: Department of Cardiothoracic and Vascular Surgery, All India Institute of Medical Sciences, New Delhi 110029, India. Tel.: +91 11 26588700/26588500x4835; fax: +91 11 26588663/26588641. E-mail addresses: [email protected], [email protected] (U.K. Chowdhury)
C
ongenital pulmonary arteriovenous malformation (PAVM) is a rare entity and is different from right pulmonary artery-to-left atrium communication. They may occur as an isolated anomaly or in association with hereditary haemorrhagic telangiectasia.1 Patients with PAVMs may be asymptomatic or present with hypoxaemia, paradoxical thromboembolism, brain abscess or massive haemoptysis.1–6
© 2008 Published by Elsevier Inc on behalf of Australasian Society of Cardiac and Thoracic Surgeons and the Cardiac Society of Australia and New Zealand.
1443-9506/04/$30.00 doi:10.1016/j.hlc.2007.11.142
CASE REPORTS
Heart, Lung and Circulation 2009;18:133–162
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Heart, Lung and Circulation 2009;18:133–162
Figures 1–2. A selective pulmonary angiogram (Fig. 1A–C) and computerised tomographic pulmonary angiogram (Fig. 2A–C) showing pulmonary arteriovenous malformations involving all segments of the lower lobe of the left lung with a dilated, tortuous left pulmonary artery (LPA) and a single draining pulmonary vein (PV) into the left atrium (LA). There are multiple feeding arteries originating from the left lower lobar division of the left pulmonary artery supplying the pulmonary malformation (PAVM) and there are no intra-or-extrathoracic vascular communications.
We report a patient who presented with recurrent episodes of massive haemoptysis from a bleeding left lower lobe PAVM that was successfully treated by left lower lobectomy. The extreme rarity of the disease entity, the usage of contrast echocardiography, and pulmonary angiography for diagnosis, the successful surgical correction using left lower lobectomy, and a brief literature review of the long-term outcome after surgical repair forms the basis of the present study.
Case Report A 6-year-old child was referred to our institute with progressively increasing symptoms of shortness of breath (NYHA functional class III), non-resolving pneumonia, and recurrent haemoptysis of 4 months duration. He received three courses of antibiotic treatment during this period. The significant clinical findings included central cyanosis, digital clubbing, and a bruit which increased its
Figure 3. (A and B) Surgical specimen (excised left lower lobe (LLL)) illustrating ecstatic bronchioles and dilated vessels near the visceral pleural surface.
pitch and volume on inspiration, best heard on the infrascapsular and infraaxillary regions. Remarkable signs on laboratory work up included low systemic arterial oxygen saturation (SaO2 ) of 65% and haemoglobin of 18.0 g%. Chest radiography revealed a lobulated mass in lower lobe of left lung. Chest contrast computed tomography demonstrated a 12 cm × 10 cm lobulated mass in the lower lobe of left lung with brilliant contrast enhancement in the arterial phase and its appearance was consistent with a PAVM. Contrast echocardiography showed microbubbles in left atrium after 5 s, thus confirming an intrapulmonary shunt. A selective pulmonary angiogram and computerised tomographic pulmonary angiogram showed PAVM involving all segments of the lower lobe of left lung with dilated, tortuous left pulmonary artery (LPA) measuring >2 cm in diameter. There were multiple feeding arteries supplying the PAVM and there were no intra-or extra-thoracic vascular communications (Fig. 1(A–C) and 2(A–C)). There were no additional PAVM on either side of the lung. Considering the multiplicity of the feeder vessels, localisation to the isolated lobe and massive dilatation of LPA at the lobar fissure, the patient was considered for resectional therapy through left muscle sparing thoracotomy. Intra-operatively, a large pulsating complex of PAVM, measuring 12 cm × 10 cm almost completely occupying the left lower lobe was supplied by superior segmental and main basal pulmonary arteries. There was no aberrant
Case Reports
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Figure 4. Photomicrograph of lung biopsy of the patient with pulmonary arteriovenous malformation (light microscopy 40×; Haematoxylin and Eosin stain). A shows parenchymal haemorrhages, abnormally dilated vascular channels (→) close to bronchiolar structure. B depicts multiple dilated vascular channels (→) with irregular lumen and variable wall thicknesses in the lung parenchyma in place of normal corner vessels.
blood supply. The pulmonary artery and vein were ecstatic measuring almost 2 cm in diameter (Fig. 3A and B). Lower lobectomy was performed. The SaO2 improved from 65 to 100% immediately after ligation of LPA. Histo-pathological examination of the specimen revealed a plexiform mass of dilated vessels with feeding vessels. Dilated bronchi and bronchioles were apparent and contained blood clots and inflammatory exudates. Vessels in apposition with these ecstatic bronchioles were also dilated with irregular lumen and variable wall thicknesses. There was parenchymal haemorrhage and oedema. An increased number of irregular vessels were also noted at the peripheries of the lung (Fig. 4A and B). The postoperative course was uneventful and patient was discharged after 6 days. Follow-up visit at 14 months showed no cyanosis, no dyspnoea and room air SaO2 of 98%.
Discussion Since the first description of PAVM at autopsy by Churton in 1897,2 these abnormal communications have been given various names, including pulmonary arteriovenous aneurysms, haemangiomas of the lung, cavernous angiomas of the lung, and pulmonary telangiectases.3
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PAVM may be simple (single pulmonary artery-topulmonary vein communication) or complex (multiple feeding arteries and draining veins), and single (40%), multiple (40%), or bilateral (20%). Most PAVMs are congenital but acquired causes include infections (tuberculosis, actinomyocosis, and schistosomiasis), metastatic carcinoma, chest trauma, modified Fontan operations and iatrogenic.4,5 Thirty-six percent of single lesions and 57% of multiple lesions are associated with hereditary haemorrhagic telangiectasia (Osler–Weber–Rendu syndrome), an autosomal dominant disorder with mutations localised to chromosome locus 9q and 12.6,7 Fifty-three to 70% of PAVMs are found in lower lobes. Females are affected twice or often as males but there is a male predominance in newborns.6,7 No definite pathogenetic explanation has been described for this anomaly. The postulated theories include a defect in the terminal arterial loops, which allows dilatation of the thin-walled capillary sacs, incomplete resorption of the vascular septae that separate the arterial and venous plexuses, which normally anastomose during foetal development and a failure of capillary development in the foetus.8 PAVMs exhibit a wide range of histology from diffuse telangiectasia to large complex structures consisting of a bulbous aneurysmal sac between dilated feeding arteries and draining veins. Approximately 95% of these feeding arteries originated from the pulmonary rather than the systemic circulation.9 The most common systemic arterial supplies to PAVMs reported in the literature originated from the bronchial artery, less so from the internal mammary artery or even directly from the descending thoracic aorta.10 The disease entity should be suspected when the following combination of symptoms and signs co-exist: central cyanosis, digital clubbing, exertional dyspnoea, haemoptysis, epistaxis, telangiectasia, history of cerebral abscess/embolism, silent precordium, normally split second heart sound, non-specific bruit over the right or left infraaxillary region, static hypoxaemia (orthodeoxia), platypnoea (improvement of dyspnoea on reclining) and one or more pulmonary nodules associated with typical roentgenographic findings (round or oval mass of uniform density, frequently lobulated but sharply defined, located commonly in lower lobes, ranging from 1 to 5 cm in diameter). Diagnosis of this anomaly is difficult. A plain chest radiography shows abnormalities in about 98% of patients. The 100% oxygen method, contrast echocardiography, and radionuclide imaging are nearly 100% sensitive for the detection of clinically significant PAVMs. The specificity of contrast echocardiography and radionuclide imaging is higher than 100% oxygen method.3–7 Contrast echocardiography using agitated saline into a peripheral vein is perhaps the most sensitive method for detection of PAVMs. Appearance of bubbles in left atrium after 3–5 cardiac cycles in the absence of intracardiac shunt (where bubbles appear in less than 3 cardiac cycles) gives a clue to the possibility of PAVMs. Although it does not quantify shunt fraction, it allows assessment of
Heart, Lung and Circulation 2009;18:133–162
the efficiency of embolotherapy and as a screening tool in family members of patients with hereditary haemorrhagic telangiectasia.5–7 Radionuclide imaging is also a sensitive method and can quantify the shunt fraction, but it cannot differentiate between a cardiac or pulmonary source of shunt.3–7 Like contrast echocardiography, it does not provide accurate anatomical details of PAVM. Ultrafast contrast enhanced, computed tomography has been shown to be more sensitive than conventional pulmonary angiograms for PAVMs and better in defining the architecture. Three-dimensional helical computed tomography has also been shown to be very accurate in analysing the PAVMs especially if combined with cross-sectional images.3–7,12 Its main advantage is non-invasiveness and avoidance of contrast injection. The disadvantage is false positive results with vascular tumours. The use of magnetic resonance imaging (MRI) in PAVMs is limited. Recently, phase contrast cine sequences have been shown to be the most accurate of MRI techniques.4,5 PAVMs and aneurysms with rapid blood flow in the region results in a signal void and produce low intensity signals. Despite isolated case reports of successful diagnosis, the main limitations of MRI are limited availability, relative expense, and the need for highly specialised staff for data interpretation.3–5 Pulmonary angiography remains the gold standard especially when a therapeutic intervention is planned.3–5 Subtraction angiography has largely replaced the conventional angiogram for PAVMs. Angiography provides detailed information on the location and size of PAVMs, the angioarchitecture and mapping of the feeding vessels, which are necessary before surgery or embolotherapy. Angiography should be performed on all portions of the lung to look for any unsuspected PAVMs, source of intrathoracic or extrathoracic vascular communications.3,5,13 Published reports recommend the screening of patients with hereditary haemorrhagic telangiectasia for PAVM with chest X-ray and contrast echocardiography.6,7 If either is positive, a contrast and helical computed tomography scanning of chest with three-dimensional reconstructions should be performed. The natural history of PAVMs is such that they tend to increase in size, especially if multiple, and rarely regress spontaneously. The mortality rate in historical reviews of untreated but symptomatic patients with PAVMs over periods of 15 years ranges from 4 to 22% and in severe cases up to 40%. The abnormal vessels may bleed into a bronchus or the pleural cavity, sometimes with a fatal outcome.14 Early surgical intervention or embolotherapy is recommended to prevent chronic arterial hypoxaemia, systemic thromboembolic complications, congestive cardiac failure, shunt-derived pulmonary hypertension, pulmonary haemorrhage and cerebral embolism or abscess.3,6,10,12 Treatment of PAVMs should be based on the size, number, and location of the lesions and the specific complications as well as patients’ general condition.
Therapeutic transcatheter embolisation offers an effective therapy for patients who are poor surgical candidates, whose lesions are too numerous to resect, and patients who decline surgical intervention.3–5,11,12 Reports of embolisation therapy do not adequately document long-term follow-up with serial chest roentgenograms, oxymetry to evaluate the incidence of delayed balloon deflation and recurrence.3–5,12,15 However, even with good initial control (80–100%), embolisation is associated with higher subsequent recurrent haemoptysis compared with surgery.16 The risks of balloon embolisation include balloon migration, clot propagation, recurrence, systemic embolisation and pulmonary infarction.15 Simple ligation has been abandoned as a surgical procedure for PAVMs because of the difficulty of feeding of all feeder vessels and the high incidence of recanalisation of PAVMs through accessory vessels.9 Published literature documents surgical resection as the treatment of choice for patients who can tolerate surgery, who fail embolotherapy, develop serious complication despite embolotherapy, have intrapleural rupture of PAVMs, have untreatable contrast allergy, lesions not amenable to embolotherapy (e.g. large centrally localised lesions) and in neonates presenting with early neurologic symptoms.3–5,11,17 Conservative lung resection, local resection, segmentectomy or lobectomy are the procedures of choice whenever possible.3–5,11,17 Brown and associates performed staged bilateral thoracotomies in case of extensive bilateral PAVMs.18 Recently, video assisted thoracoscopy has been employed in the resection of a small PAVM.8 The reported perioperative mortality has varied from 0 to 9.1% with only rare postoperative recurrences.3–5,11,17 The current case serves to emphasise that surgical resection is a safe method of treatment of PAVM in selected patients i.e. when PAVM is solitary and large (more than 2 cm) in diameter and the risk of embolotherapy is high.
References 1. Vase P, Holm M, Arendrup H. Pulmonary arteriovenous fistulas in heridatary haemorrhagic telangiectasia. Acta Med Scand 1985;218:105–9. 2. Churton T. Multiple aneurysms of pulmonary artery. Br Med J 1897;1:1223. 3. Dines DE, Seward JB, Bernatz PE. Pulmonary arteriovenous fistulas. Mayo Clin Proc 1983;58:176–81. 4. Khurshid I, Downie GH. Pulmonary arteriovenous malformation. Postgrad Med J 2002;78:191–7.
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5. Iqbal M, Rossoff LJ, Steinberg HN, Marzouk KA, Siegel DN. Pulmonary arteriovenous malformations: a clinical review. Postgrad Med J 2000;76:390–4. 6. Cottin V, Plauchu H, Bayle JY, Barthelet M, Revel D, Cordier JF. Pulmonary arteriovenous malformations in patients with hereditary hemorrhagic telangiectasia. Am J Respir Crit Care Med 2004;169:994–1000. 7. Shovlin CL, Guttmacher AE, Buscarini E, Faughnan ME, Hyland RH, Westermann CJ, Kjeldsen AD, Plauchu H. Diagnostic criteria for hereditary hemorrhagic telangiectasia (Rendu–Osler–Weber syndrome). Am J Med Genet 2000;91:66–7. 8. Watanabe N, Munakata Y, Ogiwara M, Miyatake M, Nakagawa F, Hirayama J. A case of pulmonary arteriovenous malformation in a patient with brain abscess successfully treated with video-assisted thoracoscopic resection. Chest 1995;108:1724–7. 9. Bosher LH, Blake A, Byrd BR. An analysis of the pathologic anatomy of pulmonary arteriovenous aneurysms with particular reference to the applicability of local excision. Surgery 1959;45:91–104. 10. Kuwahara T, Ida M, Hamada T. A case of systemic arterial supply to the normal left basal segments with anomalous return to the left inferior pulmonary vein. Nihon Kyobu Shikkan Gakkiai Sushi 1995;33:733–7. 11. Puskas JD, Allen MS, Moncure AC, Wain Jr JC, Hilgenberg AD, Wright C, Grillo HC, Mathisen DJ. Pulmonary arteriovenous malformations, therapeutic options. Ann Thorac Surg 1993;56:253–7. 12. Lee DW, White RI, Egglin TK, Pollak JS, Fayad PB, Wirth JA, Rosenblatt MM, Dickey KW, Burdge CM. Embolotherapy of large pulmonary arteriovenous malformations: long-term results. Ann Thorac Surg 1997;64:930–40. 13. Thung KH, Sihoe ADL, Wan IYP, Lee TW, Wong R, Yim AP. Hemoptysis from an unusual pulmonary arteriovenous malformation. Ann Thorac Surg 2003;76:1730–3. 14. Sluiter-Eringa H, Orie NGM, Sluiter HJ. Pulmonary arteriovenous fistula. Diagnosis and prognosis in noncomplaint patients. Am Rev Respir Dis 1969;100:177–88. 15. White Jr RI, Lynch-Nyhan A, Terry P, Buescher PC, Farmlett EJ, Charnas L, Shuman K, Kim W, Kinnison M, Mitchell SE. Pulmonary arteriovenous malformations: techniques and long-term outcome of embolotherapy. Radiology 1988;169:663–9. 16. Wispelaere JE, Trigaux JP, Weynants P, Delos M, Coene BD. Systemic supply to a pulmonary arteriovenous malformation: potential explanation for recurrence. Cardiovasc Intervent Radiol 1996;19:285–9. 17. Georghiou GP, Berman M, Vidne BA, Saute M. Pulmonary arteriovenous malformation treated by lobectomy. Eur J Cardiothoracic Surg 2003;24:328–30. 18. Brown SE, Wright PW, Renner JW, Riker JB. Staged bilateral thoracotomies for multiple pulmonary arteriovenous malformations complicating hereditary hemorrhagic telangiectasia. J Thorac Cardiovasc Surg 1982;83:285–9.
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