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Ann Thorac Surg 2009;87:849-853. doi:10.1016/j.athoracsur.2008.11.010
© 2009 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Multidisciplinary Management of Life-Threatening Massive Hemoptysis: A 10-Year Experience

Norihisa Shigemura, MD, PhDa, Innes Y. Wan, FRCSa, Simon C.H. Yu, FRCRb, Randolph H. Wong, FRCSa, Michael K.Y. Hsin, FRCSa, Hoi K. Thung, FRCSa, Tak-Wai Lee, FRCSa, Song Wan, MD, FRCSa, Malcolm J. Underwood, MD, FRCSa,*, Anthony P.C. Yim, MD, FRCSa

a Division of Cardiothoracic Surgery, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, People's Republic of China
b Department of Radiology and Organ Imaging, Prince of Wales Hospital, The Chinese University of Hong Kong, Hong Kong, People's Republic of China

Accepted for publication November 3, 2008.

* Address correspondence to Dr Underwood, Division of Cardiothoracic Surgery, The Chinese University of Hong Kong, Prince of Wales Hospital, Shatin, Hong Kong, People's Republic of China (Email: mjunderwood{at}surgery.cuhk.edu.hk).


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   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Life-threatening massive hemoptysis requires prompt action and thoracic surgical input. Although there are a number of reports regarding each therapeutic modality for medical or surgical treatment, the significance of a multidisciplinary strategy remains undetermined.

Methods: From January 1995 to December 2005, 120 patients were referred to our cardiothoracic center with massive hemoptysis. We retrospectively reviewed and compared the outcomes of a recent 5-year period (2000 to 2005) with those from the previous 5 years (1995 to 1999), as we made major changes in our practice in 2000. We currently try to avoid surgery within 48 hours after onset of active hemoptysis and adopt bronchial artery embolization as a first-line therapy. Treatment decisions are made after discussions among intensive care unit physicians, thoracic surgeons, and interventional radiologists.

Results: The former group had 49 patients (57.9 ± 14.1 years old, 41 males), and the recent group, 71 (62.2 ± 23.5 years old, 52 males). There were no significant differences for any characteristics studied between the groups. In analyses of short-term complications after surgery, the former had a higher in-hospital mortality rate than the recent group (15% versus 0%). Furthermore, postoperative complications were seen in 8 patients (30%) in the former, whereas those occurred in 3 patients (18%) in the recent group.

Conclusion: Bronchial artery embolization is an effective therapeutic tool and plays a pivotal role in management of life-threatening massive hemoptysis. Surgery is indicated when bronchial artery embolization is not suitable and can be safely performed in combination with a rigid bronchoscopy or bronchial artery embolization procedure. Our results indicate that a multidisciplinary approach should be adopted for management of life-threatening massive hemoptysis.

Massive hemoptysis is a life-threatening condition with a mortality rate greater than 50% in patients not treated adequately [1]. Treatment options include conservative medical therapy, surgery (pulmonary resection), and bronchial artery embolization (BAE) as well as others, with each treatment modality well described in the literature [2–4]. The decision for adopting a specific modality is affected by the underlying cause of the hemoptysis as well as the expertise of the cardiothoracic center providing care; thus the treatment may be biased toward a certain modality. Unless the physicians in charge are familiar with all treatment modalities available as well as their pros and cons, single-modality management is bound to fail in the majority of cases and is considered inadequate.

Our institution is a tertiary cardiothoracic surgical center that is accessible to a population of approximately 3 million people. As for our treatment strategy for massive hemoptysis, decision-making is a multidisciplinary process involving critical care physicians, thoracic surgeons, and interventional radiologists. In addition, cardiothoracic surgeons are familiar with all of the available modalities and conduct adequate, unbiased decision-making for the benefits of patients in a critical condition.

We reviewed the records of our single center for the past 10 years, part of which have been reported [5], and compared the outcomes of a recent 5-year period (2000 to 2005) with those from the previous 5 years (1995 to 1999). The main reason that we separated the patients into two different time frames is that there was a major change in our practice from before the year 2000 and from 2000 onward; specifically, we try to avoid having surgery within 48 hours from the onset of active hemoptysis. This is a new approach that we adopted in 2000, and it showed that the surgical mortality is markedly reduced if we can temporize the bleeding with a less-invasive interventional approach and delay surgery for at least 48 hours. Based on our findings, we propose that a multidisciplinary strategy is important for the management of life-threatening massive hemoptysis.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Selection of Patients and Management
From January 1995 to December 2005, 120 patients (93 males; mean age, 60.3 years; range, 16 to 89 years) were admitted to our emergency center with life-threatening massive hemoptysis. At our institution, life-threatening massive hemoptysis is defined as the expectoration of 600 mL or more of blood over the course of 24 hours, and all patients included in this study satisfied that criterion. To compare the contemporary outcomes with previous years, the patients were divided into two groups solely based on the era. Former group represents the first half from 1995 to 1999 and recent group represents the second half from 2000 to 2005.

All patients with massive hemoptysis were assessed by cardiothoracic surgeons and transferred to the intensive care unit for further management, where intensive medical treatment was started, including antibiotics if there was evidence of possible infection. Flexible bronchoscopy was performed at bedside as soon as possible for assessment, airway toilet, and identification of the bleeding source. All possible endobronchial interventions such as adrenaline flush, cold-saline lavage, and balloon tamponade using balloon bronchial blockers, were routinely attempted during the flexible bronchoscopy procedure. Pulmonary isolation with a double-lumen endotracheal tube was then used as the last resort in refractory cases. If there was evidence of airway obstruction by blood clots, rigid bronchoscopy treatment was indicated, in which we attempted to achieve hemostasis and evacuate any blood clots blocking the major airway. Furthermore, if possible, the exact location of the bleeding source was identified. Because suctioning and visualization remain poor with flexible bronchoscopy used for the patients with massive hemoptysis in an airway full of blood, we basically did not hesitate to proceed with rigid bronchoscopy in the operating theater if needed. In the presence of pulmonary soiling that resulted from the hemoptysis, we generally tried to avoid emergency surgical treatment (pulmonary resection) when feasible. Computed tomography of the thorax was performed for patients who were hemodynamically stable.

Under the recent therapeutic strategies from 2000 to 2005, after confirming hemodynamic stabilization, bronchial arteriography and BAE were attempted in all of the patients. Bronchial artery embolization was performed routinely using a Seldinger technique through femoral access. The surgical option of pulmonary resection was only considered when the patient continued to bleed after BAE and was considered to have sufficient pulmonary reserve based on clinical findings, with localized pathology and the bleeding source clearly identified by computed tomographic scanning. The algorithm used for management of life-threatening massive hemoptysis at our institution is shown in Figure 1.


Figure 1
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  		Fig 1. Algorithm for management of life-threatening massive hemoptysis. (BAE = bronchial artery embolization; CT = computed tomography; HPT = hemoptysis.)

 
Assessment of Outcome of Bronchial Artery Embolization
The success of BAE was categorized into 5 stages: (1) technical success, ie, complete embolization followed by immediate control of hemoptysis; (2) control of hemoptysis within 48 hours of BAE; (3) control within 30 days; (4) control within 180 days; and (5) control within 1 year.

Surgical management was indicated when there was evidence of persistent pulmonary lesions, failure of BAE, or recurrence of hemoptysis after BAE. An adequate bronchial toilet procedure was performed with either a flexible or rigid bronchoscope before attempting a pulmonary resection.

Data Analysis
Data are expressed as the mean ± standard deviation. A Mann-Whitney U test was used to compare continuous variables between the two groups. Differences were considered significant when the probability value was less than 0.05.

This study was approved by the Prince of Wales Hospital Institutional Review Board. Patients who did not authorize the use of their medical records for research were excluded from this study.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Characteristics of Patients Who Underwent Bronchial Artery Embolization and Outcomes From 2000 to 2005
Of the 120 patients who were admitted to our center with life-threatening massive hemoptysis between January of 1995 and December of 2005, the recent group (2000 to 2005) had 71 patients. Of the 71 patients in whom conservative treatment failed, 62 (52 males, 10 females; mean age, 58.4 years; range, 32 to 89 years) underwent a bronchial arteriography examination, which showed that the cause of the massive hemoptysis was old tuberculosis in 34, bronchiectasis in 14, mycetoma in 5, lung cancer in 4, necrotizing pneumonia in 4, and arteriovenous malformation in 1 (Table 1). Rigid bronchoscopy treatment was applied before angiography for hemostasis or identification of the exact location of the bleeding source in 24 (39%) of 62 patients. The bleeding source could be delineated by angiography in 55 patients based on the presence of abnormal vessels in the area of radiologically apparent parenchymal disease. Five patients had no abnormal findings shown by angiography and 2 had cannulation difficulties in their bronchial arteries, of whom 4 proceeded to surgery.


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  		Table 1 Characteristics of Patients Undergoing Bronchial Artery Embolization (BAE) for Life-Threatening Haemoptysis From 2000 to 2005
 
Of the 71 patients, 55 patients in whom the bleeding source could be identified by angiography proceeded to the treatment of embolization. Bronchial artery embolization was successful in controlling hemoptysis immediately in 48 (88%) of 55 patients and in 45 (81%) at 48 hours after the procedure. Seven of 10 patients in whom control of hemoptysis could not be achieved within 48 hours of BAE proceeded to surgery. Although 5 of 55 patients were lost to follow-up, 12 (24%) of the other 50 patients had recurrent hemoptysis within 1 month after BAE. Four of these 12 patients died of bleeding as a result of succumbing to respiratory failure 2 to 6 months after the initial treatment. Our final follow-up findings revealed that a total of 14 (25%) of the 55 patients died within 1 year, 8 because of bleeding, possibly as a result of disease progression, whereas there was no follow-up information available for 15 patients. None of these 8 patients who died with relapse of massive hemoptysis received pulmonary resection. Twenty-eight patients (70%) were followed up for 1 year after BAE without evidence of hemoptysis (Table 2).


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  		Table 2 Outcomes of Bronchial Artery Embolization (BAE) for Life-Threatening Haemoptysis Under Recent Therapeutic Strategy (2000–2005)
 
Surgical Treatment for Life-Threatening Hemoptysis and Outcomes From 2000 to 2005
Surgical treatment was offered to 16 patients (Table 3) in the recent group (2000 to 2005), with a rigid bronchoscopy performed before pulmonary resection in 12 (75%), and then the operation was performed after confirming hemostasis and hemodynamic stabilization. Hemostasis was secured in the other 4 patients (2 with lung cancer, 1 with mycetoma, 1 with arteriovenous malformation); thus the pulmonary resection was performed without rigid bronchoscopy in those patients after considering their original disease characteristics. In 7 patients (43%), BAE was performed before a secondary operation. None of the patients underwent an operation on the day of admission, as all surgical procedures were planned after a delay of 1 to 8 days. Rigid bronchoscopy or BAE procedures were performed before surgery. None of the patients who underwent surgical treatment had recurrent hemoptysis at the time of follow-up examinations conducted from 5 to 48 months (mean, 26.4 months) after the operation. Two patients had postoperative pneumonia, of whom 1 experienced empyema and 1 patient with left lung cancer had vocal cord paralysis possibly caused by nerve manipulation. No patient died during the in-hospital follow-up period (Table 3).


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  		Table 3 Characteristics and Outcomes of Patients Undergoing Surgery for Life-Threatening Haemoptysis From 2000 to 2005
 
Comparison of Therapeutic Outcomes for Life-Threatening Hemoptysis Between Former (1995 to 1999) and Recent (2000 to 2005) Therapeutic Strategies
Patients' characteristics and preoperative data that may be closely correlated with high morbidity as well as mortality rate were analyzed and compared in patients treated for life-threatening massive hemoptysis between former (1995 to 1999) and recent (2000 to 2005) therapeutic strategies. There were major changes we made in our practice in the year 2000. From 2000 onward, we try other interventional means as the first-line therapy to avoid surgery within 48 hours from the onset of active hemoptysis.

There were no significant differences for any of the variables studied as shown in Table 4A. Blood transfusion was required in 25 patients (35%) in the current group and in 20 patients (41%) in the former group, although this was not statistically different.


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  		Table 4 Comparison of Characteristics and Preoperative Factors, and Therapeutic Outcomes in Patients Treated for Life-Threatening Haemoptysis Between Former (1995–1999) and Recent (2000–2005) Therapeutic Strategies
 
In contrast, in regard to the short-term clinical complications after the surgery, the former group had a higher in-hospital mortality rate than the recent group (former group, 15%; recent group, 0%; Table 4B). The procedures performed in those patients who died related to surgery in the former group included pneumonectomy in 2, bilobectomy in 1, and lobectomy in 1, whereas the cause of death was respiratory failure that required an extended period of ventilatory support in 2, bronchopleural fistula in 1, and acute myocardial infarction in 1. Postoperative morbidity occurred in 8 patients (30%) in the former group including prolonged ventilatory support because of respiratory failure, empyema, and acute myocardial infarction, whereas only 3 (18%) patients in the recent group had postoperative complications as shown in Table 3.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
The recent emergence of BAE as a therapeutic modality for life-threatening massive hemoptysis has revolutionized management of the disease, as it is a less invasive but reliable procedure that leads to excellent therapeutic outcomes [6–8]. Nevertheless, surgical management of massive hemoptysis still plays an important role as a therapeutic strategy. A number of studies have addressed the management of massive hemoptysis by focusing on a single treatment modality, such as BAE or pulmonary resection, and outcomes. However, it is important for attending physicians in charge of patients with life-threatening massive hemoptysis to be familiar with the merits and limitations of each therapeutic modality, and make adequate decisions promptly during diagnosis and treatments. The findings in the present study first revealed excellent patient outcomes with our current multidisciplinary strategy for treatment of life-threatening massive hemoptysis as compared with the protocol used in the previous 5-year period before 2000.

Since the first report by Remy and colleagues in 1973 [9], the use of BAE for management of life-threatening massive hemoptysis has become widespread. Furthermore, developments and application of superselective BAE with a coaxial microcatheter system [10] have accelerated that trend. According to recent outcomes reported by the Mayo Clinic group [11], immediate control of bleeding was reached successfully in 94% of the cases, with 30-day control obtained in 85% of the remaining patients. Also, the Singaporean group [12], working in a region where most hemoptysis cases are related to tuberculosis with pleural abnormalities that may require repeated difficult embolization [13], also reported excellent outcomes in patients who underwent BAE, with an overall success rate of 81.6%. As demonstrated in our algorithm of management for massive hemoptysis presented in Figure 1, we consider BAE to be an interim procedure used to stabilize the patient before definitive management is instituted, although BAE on its own can be the definitive modality. Our recent results of BAE also showed excellent success in the immediate control of massive hemoptysis with 88% of the cases, which was better than 71% in the former group. We consider BAE is an operator-dependent technique, and there was always a learning curve, which could explain the improvement in the results of BAE together with the progress in the catheter techniques with more refined technologies. Although there is a trend that more patients with massive hemoptysis currently undergo BAE as a first-line therapy, accumulated lines of evidence lead us to think that the thoracic surgeons should first consider application of this effective therapeutic tool, which can be repeated in patients who have a recurrence of hemoptysis.

Unlike other modalities, surgery for massive hemoptysis is definitely curative. However, surgical mortality rates, especially in an emergency setting, remain high, ranging from 10% to 38% [5, 14, 15]. The reasons for such a high mortality may be related to ongoing bleeding in unstable hemodynamic conditions, together with soiling of other healthy bronchopulmonary segments before and during the operation.

We found that the outcome of surgery was better in our recent series of patients as compared with those treated under the previous management protocol in the period from 1995 to 1999 (Table 4). There was a major change we made in our practice beginning in the year 2000. We are more conservative in the sense that we are still performing surgery for patients with persistent bleeding, but from 2000 onward we try other less-invasive interventional means to buy time so as to delay surgery for at least 48 hours. In the recent series, BAE was used as a first-line therapy, whereas surgery was the first-line therapy in our previous protocol. Furthermore, our results demonstrated that the routine use of a rigid bronchoscopy procedure for airway clearance before surgery may contribute to improving surgical outcome, as the mortality rate was 0%, which we considered to be assisted by stabilization of hemodynamics and performance of an airway toilet as well as identification of bleeding source before surgery. In the difficult cases with a nonlocalized source of bleeding in an airway full of blood, rigid bronchoscopy may pave the way to the next action. In addition, BAE may have contributed to the excellent outcome rate in the recent surgical group, because cessation of hemorrhaging by BAE helps delay surgery and enables the patient to be more prepared for surgery with a stabilized cardiopulmonary function. From results of their comparative study between emergency surgery and delayed (planned) surgery for massive hemoptysis, Jougon and the colleagues [16] suggested that surgical treatment is best performed at a later date in cases with bronchial vessel hemorrhaging. In addition to their findings, it is important to emphasize that both rigid bronchoscopy and BAE may play a pivotal role, based on their less invasive and reliable features, in surgical management for life-threatening massive hemoptysis for obtaining a successful outcome. With those, the location and source of bleeding can be well delineated before surgery, which likely contribute to a better surgical outcome.

Although a multidisciplinary strategy for life-threatening massive hemoptysis appears to be difficult in many clinical settings because of the limited expertise and available modalities in the institution, our results suggest that reliance on a single modality may limit the opportunity to achieve a successful outcome. Thus, a multidisciplinary approach should be adopted for management of patients with life-threatening massive hemoptysis.

In conclusion, in experienced hands, BAE is an effective therapeutic tool and plays a pivotal role in the management of life-threatening massive hemoptysis. Surgery is the only curative treatment and is especially effective for localized lesions, and should be considered when BAE is unavailable or bleeding is unlikely to be controlled by that approach. Before the critical decision to perform surgery, the surgeons should make sure that available interventional modalities such as balloon bronchial blockers, rigid bronchoscopy, or BAE be used in an optimal manner to buy time so as to delay surgery for a better surgical outcome. Our results demonstrated that a multidisciplinary team approach for management of life-threatening massive hemoptysis is able to achieve good outcomes in affected patients.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

  1. Jean-Baptiste E. Clinical assessment and management of massive hemoptysis Crit Care Med 2000;28:1642-1647.[Medline]
  2. Lordan JL, Gascoigne A, Corris PA. The pulmonary physician in critical care Thorax 2003;58:814-819.[Free Full Text]
  3. Wong ML, Szkup P, Hopley MJ. Percutaneous embolotherapy for life-threatening hemoptysis Chest 2002;121:95-102.[Medline]
  4. Ayed A. Pulmonary resection for massive hemoptysis of benign etiology 2003;24:689-693.
  5. Lee TW, Wan S, Choy DK, et al. Management of massive hemoptysis: a single institution experience Ann Thorac Cardiovasc Surg 2000;6:232-235.[Medline]
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  7. Ramakantan R, Bandekar VG, Gandhi MS, et al. Massive hemoptysis due to pulmonary tuberculosis: control with bronchial artery embolization Radiology 1996;200:691-694.[Abstract/Free Full Text]
  8. Haponik EF, Fein A, Chin R. Managing life-threatening hemoptysis: has anything really changed? Chest 2000;118:1431-1435.[Medline]
  9. Remy J, Arnaud A, Fardou H, et al. Treatment of hemoptysis by embolization of bronchial arteries Radiology 1977;122:33-37.[Abstract]
  10. Tanaka N, Yamakado K, Murashima S, et al. Superselective bronchial artery embolization for hemoptysis with a coaxial microcatheter system J Vasc Interv Radiol 1997;8:65-70.[Medline]
  11. Swanson KL, Johnson M, Prakash UBS, et al. Bronchial artery embolization: experience with 54 patients Chest 2002;121:789-795.[Medline]
  12. Goh P, Lin M, Teo N, et al. Embolization for hemoptysis: a six-year review Cardiovasc Interv Radiol 2002;25:17-25.[Medline]
  13. Tamura S, Kodama T, Otsuka N, et al. Embolotherapy for persistent hemoptysis: the significance of pleural thickening Cardiovasc Interv Radiol 1993;16:85-88.[Medline]
  14. Knott-Craig CJ, Oostuizen JG, Rossouw G, et al. Management and prognosis of massive hemoptysis. Recent experiences with 120 patients. J Thorac Cardiovasc Surg 1993;105:394-397.[Abstract]
  15. Endo S, Otani S, Saito N, et al. Management of massive hemoptysis in a thoracic surgical unit Eur J Cardiothorac Surg 2003;23:467-472.[Abstract/Free Full Text]
  16. Jougon J, Ballester M, Delcambre F, et al. Massive hemoptysis: what place for medical and surgical treatment Eur J Cardiothorac Surg 2002;22:345-351.[Abstract/Free Full Text]



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Ann. Thorac. Surg., November 1, 2009; 88(5): 1565 - 1565.
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