Professional Documents
Culture Documents
Hemoptysis
Hemoptysis
a Department of Respiratory and Critical Care Medicine, Tangdu Hospital, Air Force Medical University, Xi’an, China;
b Department
of Respiratory and Critical Care Medicine, Dongfang Hospital, Tongji University, Shanghai, China;
c Department of Respiratory Medicine, Changhai Hospital, Naval Medical University, Shanghai, China; d Department
of Respiratory Medicine, Meitan General Hospital, Beijing, China; e Guangzhou Institute of Respiratory Health, State
Key Laboratory of Respiratory Disease, The First Affiliated Hospital of Guangzhou Medical University, Guangzhou,
China; f Department of Respiratory Medicine, Jinling Hospital, Nanjing University School of Medicine, Nanjing,
China; g Department of Respiratory Pulmonary and Critical Care Medicine, The Second Hospital of Fujian Medical
University, Quanzhou, China; h Department of Respiratory Medicine, The Second Xiangya Hospital, Central South
University, Changsha, China; i Department of Respiration, Central South University Xiangya Hospital, Changsha,
China; j Department of Respiration, Beijing Tiantan Hospital, Capital Medical University, Beijing, China; k Department
The lungs have a dual blood supply from the pulmo- Infection
nary and bronchial arteries [14]. The pulmonary artery In the middle of the 20th century before the advent of
originates from the right ventricle, branches into the left anti-TB drugs, TB and its associated complications are
and right pulmonary artery, and the pulmonary artery the most common cause of hemoptysis. Currently, the
eventually forming a wide capillary network to complete rate of massive hemoptysis caused by pulmonary tuber-
the gas exchange. The pulmonary artery is a low-pressure, culosis decreased, but it is still common that pulmonary
low-resistance system with a large blood volume. The tuberculosis complicated with bronchial tuberculosis re-
blood pressure will not increase significantly even if the sults in bronchial damage or bronchiectasis results in he-
blood flow increases. If the pulmonary capillary network moptysis [15].
ruptures, the amount of bleeding will not be too large, and Bronchiectasis and chronic infection are pathological
it is easy to stop bleeding; however, if large pulmonary features of bronchiectasia. Repeated bacterial infections,
arteries or branches rupture, hemorrhage often occurs especially Staphylococcus aureus, Pseudomonas aerugino-
due to large blood volume and short distance from right sa, and so on, lead to bronchial artery hypertrophy, dis-
ventricular, and the success rate of rescue is low. The tortion, aneurysm formation, and systemic circulation –
bronchial artery originates from the aorta, and a few are pulmonary vascular anastomosis or arterial fistula forma-
from the intercostal artery to provide nutrients to the tion. The above arterial rupture can cause massive, rapid,
lung parenchyma. Unlike the pulmonary artery, the bron- and fatal massive hemoptysis [16].
chial artery is a high-pressure system that closely follows In recent years, the proportion of massive hemoptysis
the bronchial movement and eventually forms a capillary caused by fungal infections has gradually increased, espe-
130.238.7.40 - 9/15/2019 11:30:47 AM
2 Respiration Jin/Li/Bai/Wang/Li/Song/Zeng/Zhou/Li/
DOI: 10.1159/000502156 Hu/Zhang/Zhou/Zhang
Uppsala Universitetsbibl.
Downloaded by:
cially in patients with cavitary lung disease or with sig- Table 1. Common causes of massive hemoptysis
nificant immunosuppression. Most of the cavity forma-
tions combined with mold infections are Aspergillus in- Classification Disease
fection, and the dilated bronchial artery or intercostal Infection Tuberculosis/nontuberculous mycobacterial
artery is often surrounded by the cavity, which is highly infection
susceptible to rupture and massive bleeding. It has been Bronchiectasis (including cystic fibrosis)
reported that 50–90% of Aspergillus infections compli- Invasive pulmonary fungal disease
cated with cavity can cause massive hemoptysis [17–19]. Lung abscess
Paragonimiasis
In addition, mucormycosis infection can also result in Necrotizing pneumonia
massive hemoptysis, mainly because of the characteristics Pulmonary embolism (septic)
of mucormycosis, which can easily damage the pulmo- Tumor Primary lung cancer
nary artery and cause fatal massive hemoptysis [20–22]. Intratracheal metastatic cancer
In immunodeficient patients, massive hemoptysis caused Intrapulmonary metastatic carcinoma
by invasive fungal infection is rare, but after the recov- Autoimmune Diffuse alveolar hemorrhage
ery of neutrophil deficiency, increased inflammatory re- disease Granulomatous polyangiitis
sponse due to local infection will cause rupture of blood Microscopic polyangiitis
vessels and cause massive hemoptysis [23, 24]. Hemopty- Goodpasture syndrome
sis can also be caused by other lung infections, especially Nodular polyangiitis
Systemic lupus erythematosus
those with lung abscess, and necrotizing pneumonia Rheumatoid arthritis
caused by various infections [25]. Systemic sclerosis
Cardiovascular Arteriovenous malformation
Tumor diseases Mitral stenosis
Hemoptysis can occur due to any type of lung cancer, Pulmonary embolism/infarction
and the probability of massive hemoptysis in patients Congenital heart disease (such as atrial septal
with central airway lumen and tumor cavity formation is defect, patent ductus arteriosus, etc.)
high [5, 13, 26]. Squamous cell carcinoma often occurs in Primary pulmonary hypertension
Aortic aneurysm
the central airway, so the resulting massive hemoptysis is Bronchial arterial fistula
more common than adenocarcinoma, small cell carcino- Congestive heart failure
ma, or large cell carcinoma. Any tumor that is transferred Localized pulmonary venous stenosis after
to the bronchial cavity or the lung parenchyma can lead atrial fibrillation ablation
to massive hemoptysis. Some new antiangiogenic drugs, Iatrogenic Bronchoscopy-related operations
such as bevacizumab, can cause tumor necrosis and cav- Percutaneous lung biopsy
ity leading to massive hemoptysis [27]. Pulmonary catheter implantation
Trachea – innominate artery fistula
Radiotherapy
Autoimmune Diseases Antiangiogenic drug applications (e.g.,
Autoimmune diseases can also result in massive he- bevacizumab)
moptysis. The vasculitis also accounts for a proportion of Trauma Lung blunt injury
hemorrhage, which can manifest as massive hemoptysis Chest wall penetrating injury
or diffuse alveolar hemorrhage (DAH), and may be ac- Pseudo-hemoptysis
companied by progressive hypoxemia and respiratory Bone marrow transplantation
failure, some patients may not have much hemoptysis, Hematological Coagulopathy (congenital, acquired, or
even without hemoptysis symptom, but progressive ane- diseases iatrogenic)
mia and hypoxemia may occur, with higher mortality Platelet disease
[28]. Thrombotic thrombocytopenic purpura
Cardiovascular Disease
Cardiac hemoptysis is caused by underlying cardio- when venous pressure suddenly rises for some reason, it
vascular diseases. In diseases that can cause primary car- may trigger rupture. Massive hemoptysis may also occur
diogenic hemoptysis, elevated pulmonary venous pres- in patients with localized elevation of pulmonary venous
sure can lead to venous dilatation/varicose formation, pressure caused by local stenosis of the pulmonary vein
130.238.7.40 - 9/15/2019 11:30:47 AM
4 Respiration Jin/Li/Bai/Wang/Li/Song/Zeng/Zhou/Li/
DOI: 10.1159/000502156 Hu/Zhang/Zhou/Zhang
Uppsala Universitetsbibl.
Downloaded by:
Fig. 1. Tumor resection under rigid bron-
choscopy. The patient was diagnosed with
hemoptysis and found a new spherical neo-
plasm in the upper segment of the trachea,
which grew into the lumen, and the surface
was rich in blood supply, which caused
bleeding. Rigid argon knife cauterization
was used to stop bleeding.
ogy. Bronchoscopy is an important tool for the diagnosis tracheal intubation should be performed immediately.
and treatment of massive hemoptysis [47, 48]. The flexi- Large (8–8.5 mm) catheters used in tracheal intubation
ble bronchoscope is convenient to use, but the suction with large side holes may be considered for bronchosco-
ability is limited, the visual field is easy to be blurred, and py. If necessary, use a rigid bronchoscope for treatment
for the rapid treatment of massive hemoptysis is limited. (Fig. 1).
The rigid bronchoscope allows for rapid suction while
maintaining airway open and ventilated [49]. However, Isolation of Bleeding Source
the rigid bronchoscope needs to be performed under gen- Quickly clean up the hematocele in the airway by tra-
eral anesthesia, and the operation is complicated, and it cheal intubation or rigid bronchoscope, isolate the bleed-
is impossible to reach the airway other than the trachea, ing source as soon as possible to prevent the blood from
the bulge, and the main bronchus. Therefore, there are overflowing into the contralateral to form a blood clot to
conditions that can be used in combination to achieve block the airway and affect the alveolar gas exchange, and
optimal diagnosis, evaluation, and control of bleeding ef- keep the airway unobstructed as well. Therefore, in the
fects. case of nonbilateral lung bleeding, the first step should be
to quickly determine the side of the lung and the lobe
Emergency Treatment Methods from which the bleeding comes and prevent blood from
The principle of emergency treatment of massive he- entering the contralateral of the lung, and the most basic
moptysis is to ensure airway unobstructed and isolate method is to let the patient have a lateral position. After
bleeding sources [13, 50–54]. finding the source of bleeding, there are several ways to
isolate the source of bleeding as much as possible: (1) se-
Keep the Airway Unobstructed lect a unilateral tracheal intubation under bronchoscopy
When acute active hemorrhage complicated with mas- and insert the distal end of the catheter into the main
sive hemoptysis, the best way to clean up the blood and bronchus of the contralateral lung. The balloon is filled to
secretions in the airway is the patient’s cough reflex. Pa- prevent blood permeation, and the affected side lung is
tients should be encouraged to clear the airway hemato- treated under the condition of contralateral lung ventila-
cele through the cough. If the patient’s cough reflex can- tion. (2) After tracheal intubation, the source of bleeding
not effectively remove airway hemorrhage, relieve as- was identified under bronchoscopy. The Fogarty balloon
phyxia, and develop progressive dyspnea or hypoxemia, was placed into the hemorrhagic airway through a bron-
130.238.7.40 - 9/15/2019 11:30:47 AM
choscope, and the airway was filled after inflation. Its pur- spraying of ice normal saline, diluted adrenaline, throm-
pose is to quickly control bleeding and protect the con- bin or fibrin complex to contract blood vessels to stop
tralateral airway from being obstructed. The 6 F or 7 F bleeding. (5) When the petechia is directly observed un-
balloon is often used to block the main bronchus on the der the bronchoscope, hemostasis can be performed by
bleeding side. It is best not to pass the bronchoscope laser, electric knife, argon knife, or freezing technique
working hole, but to insert the balloon under the bron- (Fig. 2, 3). (6) If the patients are suspected as tracheal-
choscope. It can not only block the bleeding airway but innominate artery fistula, emergency surgery should be
also continue to suctioning and keep the airway unob- performed by cardiothoracic surgery. Before the surgical
structed. (3) Double-lumen tracheal catheter intubation, repair, try to cut the trachea, inflate the balloon, or replace
lung ventilation, and airway dredging can be operated the tracheostomy tube with a tracheal intubation cathe-
separately through the double-lumen tube, but accurate ter, place the distal end of the catheter under the petechia,
double-lumen tracheal intubation is time-consuming and inflate the balloon. At the same time, put your finger
and laborious, and the independent lumen of the double- into the sinus of the tracheotomy and press the anterior
lumen tube is too small to hinder operation, requires spe- wall of the trachea forward to the sternum to help stop
cial suction tube and the need to use muscle relaxants, bleeding, which will give you time and opportunity for
which led to limited application of the double-lumen surgery.
tube. (4) If hemorrhage occurs under bronchoscopy, local
130.238.7.40 - 9/15/2019 11:30:47 AM
6 Respiration Jin/Li/Bai/Wang/Li/Song/Zeng/Zhou/Li/
DOI: 10.1159/000502156 Hu/Zhang/Zhou/Zhang
Uppsala Universitetsbibl.
Downloaded by:
Fig. 4. Freezing and removing thrombus
through bronchoscopy. Patients with mas-
sive hemoptysis and respiratory failure
were given tracheal intubation and ventila-
tor-assisted breathing. Emergency bron-
choscopy revealed that the left main bron-
chus was blocked by thrombus, the cryo-
probe entered the thrombus, pulled out
the thrombus, and the removed material
showed a bronchial tree-like change. After
the removal of 2 thrombus trees, the left
main bronchus and the bronchial lumens
at all levels were unobstructed.
Remove the Blood Clot remain suctioning when retracting the endoscope. (3) Re-
Blood clots formed after massive hemoptysis can block move blood clots using machine: blood clots can be re-
the central airway, leading to hypoxemia or asphyxia. At moved using biopsy forceps, trigeminal grasping forceps,
this time, trying to remove blood clots to improve ventila- snares, Dormia basket, and so on (4) remove blood clots
tion is the first consideration. Rigid bronchoscopy or soft by freezing: insert the cryoprobe into the blood clot, start
bronchoscopy can be used according to the conditions, the freezing mode, keep the frozen state, and pull the en-
the rigid bronchoscopy can be used preferentially or com- doscope body and probe together with the frozen blood
bined with soft and rigid bronchoscopy, or soft bronchos- clots out of the airway [55], as seen in Figure 4.
copy can be used under the guidance of tracheal intuba- Removing the blood clot from the trachea can relieve
tion. There are 4 methods: (1) remove blood clots direct- airway obstruction and improve ventilation. And also,
ly: place the front end of the endoscope at the basilar part due to the removal of the blood clot and the alleviation of
of the blood clot, pull out the endoscope and remain suc- the compression of the bleeding site, the bleeding is
tioning, thus giving the opportunity to remove the entire caused again. Thus, when removing a blood clot, the op-
blocked blood clot. (2) Remove blood clots using balloon: erator must be prepared to treat acute massive hemopty-
place the balloon at the distal end of the central airway sis. For blood clots in the lung lobe, pulmonary segments
clot, then inflate, pull out the endoscope and balloon, and or side of the bronchi, if there is no life-threatening dys-
130.238.7.40 - 9/15/2019 11:30:47 AM
8 Respiration Jin/Li/Bai/Wang/Li/Song/Zeng/Zhou/Li/
DOI: 10.1159/000502156 Hu/Zhang/Zhou/Zhang
Uppsala Universitetsbibl.
Downloaded by:
References
1 Burke CT, Mauro MA. Bronchial artery em- 17 Kokkonouzis I, Athanasopoulos I, Doulgera- 31 Tellapuri S, Park HS, Kalva SP. Pulmonary ar-
bolization. Semin Intervent Radiol. 2004 Mar; kis N, Tsonis G, Lampaditis I, Saridis N, et al. teriovenous malformations. Int J Cardiovasc
21(1):43–8. Fatal Hemoptysis due to Chronic Cavitary Imaging. 2019 Aug;35(8):1421–8.
2 Kalva SP. Bronchial artery embolization. Pulmonary Aspergillosis Complicated by 32 Mall S, Sharma RK, Prajapat D, Gupta SK,
Tech Vasc Interv Radiol. 2009 Jun;12(2):130– Nontuberculous Mycobacterial Tuberculosis. Talwar D. Hemoptysis: beyond routine chest
8. Case Rep Infect Dis. 2011;2011:837146. computed tomography and bronchoscopy.
3 Corey R, Hla KM. Major and massive hemop- 18 Sabayev V, Savel RH, Schiteanu A, Asnis D, Lung India. 2017 Jul-Aug;34(4):368–71.
tysis: reassessment of conservative manage- Veloudios A. Invasive Aspergillosis-Associat- 33 Kim H, Kwon D, Yoon SH, Kim H, Park CM,
ment. Am J Med Sci. 1987 Nov;294(5):301–9. ed Pulmonary Artery Pseudoaneurysm: A Goo JM, et al. Bronchovascular injury associ-
4 Noë GD, Jaffé SM, Molan MP. CT and CT Rare Cause of Hemoptysis in an HIV-Infect- ated with clinically significant hemoptysis af-
angiography in massive haemoptysis with ed Patient. Clin Pulm Med. 2005; 12(5): 297– ter CT-guided core biopsy of the lung: Radio-
emphasis on pre-embolization assessment. 300. logic and histopathologic analysis. PLoS One.
Clin Radiol. 2011 Sep;66(9):869–75. 19 Caulet S, Capron F, Laaban JP, Prudent J, Ro- 2018 Sep;13(9):e0204064.
5 Radchenko C, Alraiyes AH, Shojaee S. A sys- chemaure J, Diebold J. [Fatal hemoptysis dur- 34 Wang Y, Jiang F, Tan X, Tian P. CT-guid-
tematic approach to the management of mas- ing bronchial aspergillosis with multiple pul- ed percutaneous transthoracic needle biopsy
sive hemoptysis. J Thorac Dis. 2017 Sep; 9 monary artery aneurysms]. Ann Pathol. 1990; for paramediastinal and nonparamediastinal
(Suppl 10):S1069–86. 10(3):177–80. lung lesions: diagnostic yield and complica-
6 Hurt K, Bilton D. Haemoptysis: diagnosis and 20 Feng J, Sun X. Characteristics of pulmonary tions in 1484 patients. Medicine (Baltimore).
treatment. Acute Med. 2012;11(1):39–45. mucormycosis and predictive risk factors for 2016 Aug;95(31):e4460.
7 Fartoukh M, Khoshnood B, Parrot A, Khalil the outcome. Infection. 2018 Aug;46(4):503– 35 Zhang S, Zheng Y, Yu P, Yu F, Zhang Q, Lv Y,
A, Carette MF, Stoclin A, et al. Early predic- 12. et al. The combined treatment of CT-guid-
tion of in-hospital mortality of patients with 21 Brown RB, Johnson JH, Kessinger JM, Sealy ed percutaneous 125I seed implantation and
hemoptysis: an approach to defining severe WC. Bronchovascular mucormycosis in the chemotherapy for non-small-cell lung cancer.
hemoptysis. Respiration. 2012;83(2):106–14. diabetic: an urgent surgical problem. Ann J Cancer Res Clin Oncol. 2011 Dec; 137(12):
8 Hirshberg B, Biran I, Glazer M, Kramer MR. Thorac Surg. 1992 May;53(5):854–5. 1813–22.
Hemoptysis: etiology, evaluation, and out- 22 Lee FY, Mossad SB, Adal KA. Pulmonary mu- 36 Zhu JC, Yan TD, Glenn D, Morris DL. Radio-
come in a tertiary referral hospital. Chest. cormycosis: the last 30 years. Arch Intern frequency ablation of lung tumors: feasibility
1997 Aug;112(2):440–4. Med. 1999 Jun;159(12):1301–9. and safety. Ann Thorac Surg. 2009 Apr;87(4):
9 Knott-Craig CJ, Oostuizen JG, Rossouw G, 23 Paya CV. Fungal infections in solid-organ 1023–8.
Joubert JR, Barnard PM. Management and transplantation. Clin Infect Dis. 1993 May; 37 Sano Y, Toyooka S, Okabe K, Aoe M, Date H,
prognosis of massive hemoptysis. Recent ex- 16(5):677–88. Mukai T, et al. O-144 Feasibility of the percu-
perience with 120 patients. J Thorac Cardio- 24 Albelda SM, Talbot GH, Gerson SL, Miller taneous radiofrequency ablation (RFA) for
vasc Surg. 1993 Mar;105(3):394–7. WT, Cassileth PA. Pulmonary cavitation and intrathoracic malignancies. Lung Cancer.
10 Mal H, Rullon I, Mellot F, Brugière O, Slei- massive hemoptysis in invasive pulmonary 2005;49 Suppl 2:S49.
man C, Menu Y, et al. Immediate and long- aspergillosis. Influence of bone marrow re- 38 Siobal M, Kallet RH, Kraemer R, Jonson E,
term results of bronchial artery embolization covery in patients with acute leukemia. Am Lemons D, Young D, et al. Tracheal-innomi-
for life-threatening hemoptysis. Chest. 1999 Rev Respir Dis. 1985 Jan;131(1):115–20. nate artery fistula caused by the endotracheal
Apr;115(4):996–1001. 25 Carteaux G, Contou D, Voiriot G, Khalil A, tube tip: case report and investigation of a fa-
11 Ong TH, Eng P. Massive hemoptysis requir- Carette MF, Antoine M, et al. Severe Hemop- tal complication of prolonged intubation.
ing intensive care. Intensive Care Med. 2003 tysis Associated with Bacterial Pulmonary Respir Care. 2001 Oct;46(10):1012–8.
Feb;29(2):317–20. Infection: Clinical Features, Significance of 39 Friduss M, Hoover LA, Alessi D, Robertson J.
12 Lee TW, Wan S, Choy DK, Chan M, Arifi A, Parenchymal Necrosis, and Outcome. Lung. Traumatic innominate pseudoaneurysm rup-
Yim AP. Management of massive hemoptysis: 2018 Feb;196(1):33–42. ture during laryngeal dilatation. Ann Otol
a single institution experience. Ann Thorac 26 Miller RR, McGregor DH. Hemorrhage from Rhinol Laryngol. 1987 Nov-Dec;96(6):695–7.
Cardiovasc Surg. 2000 Aug;6(4):232–5. carcinoma of the lung. Cancer. 1980 Jul;46(1): 40 Madden BP. Evolutional trends in the man-
13 Jean-Baptiste E. Clinical assessment and 200–5. agement of tracheal and bronchial injuries. J
management of massive hemoptysis. Crit 27 Goto K, Endo M, Kusumoto M, Yamamoto Thorac Dis. 2017 Jan;9(1):E67–70.
Care Med. 2000 May;28(5):1642–7. N, Ohe Y, Shimizu A, et al. Bevacizumab for 41 Broderick SR. Hemothorax: Etiology, diagno-
14 Jiang S. Human sectional anatomy. People’s non-small-cell lung cancer: A nested case sis, and management. Thorac Surg Clin. 2013
Medical Publishing House. PMPH; 2008. p. control study of risk factors for hemoptysis. Feb;23(1):89–96.
109. Cancer Sci. 2016 Dec;107(12):1837–42. 42 Mo XD, Xu LP, Liu DH, Zhang XH, Chen H,
15 Zhang Y, Chen C, Jiang GN. Surgery of mas- 28 Zandman-Goddard G. Diffuse alveolar hem- Chen YH, et al. High-dose cyclophosphamide
sive hemoptysis in pulmonary tuberculosis: orrhage in autoimmune diseases. Isr Med As- therapy associated with diffuse alveolar hem-
immediate and long-term outcomes. J Thorac soc J. 2002 Jun;4(6):461–2. orrhage after allogeneic hematopoietic stem
Cardiovasc Surg. 2014 Aug;148(2):651–6. 29 Cheng S, Lu X, Wang J, Liu T, Zhang X. Tho- cell transplantation. Respiration. 2013; 86(6):
16 Gupta K, Saggar K, Goyal A, Banerjee A. racoscopic lobectomy for massive hemoptysis 453–61.
Anomalies of Pulmonary Circulation as a caused by complete pulmonary vein occlu- 43 Coucke L, Marcelis L, Deeren D, Van Dorpe
Cause of Hemoptysis: A Series of Unusual sion after radiofrequency ablation for atrial J, Lambein K, Devreese K. Lymphoplasma-
Cases and Review of the Literature. Oman fibrillation. J Thorac Dis. 2018 Apr; 10(4): cytic lymphoma exposed by haemoptysis and
Med J. 2015 May;30(3):208–11. E296–300. acquired von Willebrand syndrome. Blood
30 Zhang G, Yu H, Chen L, Li Y, Liang Z. Pulmo- Coagul Fibrinolysis. 2014 Jun;25(4):395–7.
nary veins stenosis after catheter ablation of 44 Padhi P, Parihar G, Stepp J, Kaplan R. Post-
atrial fibrillation as the cause of haemoptysis: transfusion purpura: a rare and life-threaten-
three cases and a literature review. Clin Respir ing aetiology of thrombocytopenia. BMJ Case
J. 2018 Jan;12(1):3–9. Rep. 2013 May;2013:pii:bcr2013008860.
130.238.7.40 - 9/15/2019 11:30:47 AM
10 Respiration Jin/Li/Bai/Wang/Li/Song/Zeng/Zhou/Li/
DOI: 10.1159/000502156 Hu/Zhang/Zhou/Zhang
Uppsala Universitetsbibl.
Downloaded by: