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Anna Rita Larici, Paola Franchi, Mariaelena Occhipinti, Andrea Contegiacomo, Annemilia del Ciello,
Lucio Calandriello, Maria Luigia Storto, Riccardo Marano, Lorenzo Bonomo
I
ABSTRACT
n clinical practice hemoptysis is a common symptom, which may re-
Hemoptysis is the expectoration of blood that originates quire further investigation. It is defined as the expectoration of blood
from the lower respiratory tract. It is usually a self-limiting that originates from the lower respiratory tract (1). Bleeding from the
event but in fewer than 5% of cases it may be massive, rep-
resenting a life-threatening condition that warrants urgent upper airways is excluded from this definition.
investigations and treatment. This article aims to provide a In most cases hemoptysis is a self-limiting event but in fewer than 5%
comprehensive literature review on hemoptysis, analyzing its
causes and pathophysiologic mechanisms, and providing de-
it may be severe or massive, representing a life-threatening condition
tails about anatomy and imaging of systemic bronchial and that warrants urgent investigations and treatment (2). Massive hemop-
nonbronchial arteries responsible for hemoptysis. Strengths tysis usually refers to the expectoration of a large amount of blood and/
and limits of chest radiography, bronchoscopy, multidetector
computed tomography (MDCT), MDCT angiography and or to a rapid rate of bleeding. The blood volume expectorated over 24
digital subtraction angiography to assess the cause and lead hours is generally used for distinguishing massive and nonmassive he-
the treatment of hemoptysis were reported, with particular
emphasis on MDCT angiography. Treatment options for re-
moptysis, although the choice of a cutoff value is controversial (3). Vol-
current or massive hemoptysis were summarized, highlight- umes of 100 to 1000 mL of blood (49) have been described as indicative
ing the predominant role of bronchial artery embolization. of massive hemoptysis, but no specific volume has been universally ac-
Finally, a guide was proposed for managing massive and non-
massive hemoptysis, according to the most recent medical cepted. Furthermore, a large volume of expectorated blood alone should
literature. not define massive hemoptysis, but rather an amount of blood sufficient
to cause a condition that threatens the patients life can be a more cor-
rect and functional definition of severe hemoptysis (4, 5).
Asphyxia due to the flooding of the airways rather than exsanguina-
tion is usually the cause of death, and it is commonly accompanied by
cardiovascular collapse. The mortality rate from untreated massive he-
moptysis is more than 50% (6). Therefore, prompt recognition of severe
hemoptysis and identification of its causes are mandatory to initiate an
adequate treatment and to avoid fatal complications (6). Imaging plays
a relevant role in managing this clinical condition.
This article aims to provide a comprehensive review on massive and
nonmassive hemoptysis, with particular emphasis on the pathophys-
iologic mechanisms, the anatomy of systemic and pulmonary arteries
responsible for hemoptysis, and the role of imaging modalities in diag-
nosing causes and helping treatment. Strengths and limitations of the
various diagnostic modalities will be analyzed and a guide for managing
hemoptysis, according to the most recent medical literature, will be pro-
posed.
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(CT), particularly multidetector CT
Table 1. Causes of hemoptysis from small vessels (MDCT), a decrease in the prevalence
Immunologic and vasculitic diseases Acute lung allograft rejection of hemoptysis without known cause
Antiphospholipid antibody syndrome might be expected (17).
Behet disease
Goodpastures syndrome Anatomy of the lung arterial blood
Henoch-Schnlein purpura supply
Isolated pulmonary capillaritis Bronchial arteries are the principal
Microscopic polyarteritis sources of hemoptysis amenable to
Mixed cryoglobulinemia treatment (5). Searching the bronchial
Wegener granulomatosis arteries origin before treatment is help-
Cardiovascular diseases Mitral stenosis ful, because over 30% have an abnor-
mal origin that may lead to endovas-
Coagulatory diseases Iatrogenic (anticoagulants/thrombolytic agents)
cular treatment failure. The bronchial
Coagulopathies
arteries commonly originate from the
Others Diffuse alveolar damage upper portion of the descending tho-
Lymphangioleiomyomatosis racic aorta. The origin is defined or-
Pulmonary capillary hemangiomatosis
thotopic if the arteries arise from the
Pulmonary hemosiderosis
descending aorta at the level of the ver-
Tuberous sclerosis
tebral bodies of T5T6 (or at the carina).
Veno-occlusive disease
When the bronchial arteries originate
at other levels, including aortic branch-
es, they are referred to as ectopic (18).
tysis are bronchiectasis, tuberculosis, vascularization and pulmonary vessel Ectopic bronchial arteries commonly
fungal infections, and cancer (4, 7). remodeling, with engagement of col- arise from the inferior aspect of the
Two arterial vascular systems supply lateral systemic vessels (11). These new aortic arch, subclavian artery, brachio-
blood to the lungs: the pulmonary ar- and collateral vessels are fragile and cephalic trunk, thyrocervical trunk, in-
teries and the bronchial arteries. The prone to rupture into the airways. ternal mammary artery, costocervical
pulmonary arteries provide 99% of the In cases of severe hemoptysis requir- trunk, pericardiophrenic artery, inferi-
arterial blood to the lungs and are in- ing treatment, the source of bleeding or phrenic artery, abdominal aorta, and
volved in the gas exchange. The bron- originates from bronchial and pulmo- coronary arteries (4, 6, 18).
chial arteries supply nourishment to nary arteries in 90% and 5% of cases, Cauldwell et al. (19) reported the
the extra- and intrapulmonary airways respectively (5). In the remaining 5% most frequent types of origin of orthot-
and to the pulmonary arteries (vasa va- opic bronchial arteries in a population
of cases, hemoptysis may derive from
sorum), without being involved in the of 150 adult cadavers (Fig. 1). Usually,
nonbronchial systemic arteries (4).
gas exchange (8). Mediastinal lymph two or three branches of the bronchi-
Very rarely, hemoptysis has been re-
nodes and nerves, visceral pleura, al arteries run parallel with the major
ported originating from pulmonary
esophagus, vasa vasorum of the aorta, bronchi and generate a peribronchi-
and bronchial veins (12, 13) and cap-
and pulmonary veins are also provided al plexus by anastomosing with each
illaries (14). A recent study by No et
by the bronchial arteries (4). other (20). Arterioles from this plexus
al. (15) shows that bleeding from bron-
Complex capillary anastomoses exist perforate the muscular layer and create
chial arteries can coexist with bleeding
between the pulmonary arteries and a parallel plexus in the bronchial sub-
from nonbronchial and pulmonary ar-
the systemic bronchial arteries (9). mucosa. In normal conditions the di-
teries in the same patient. ameter of bronchial arteries is less than
When pulmonary circulation is com-
According to different authors, eti- 1.5 mm at the origin and less than 0.5
promised (e.g., in thromboembolic
disease, vasculitic disorders, or in hy- ology of hemoptysis cannot be deter- mm more distally (21). They are usu-
poxic vasoconstriction), the bronchial mined in 3% to 42% of cases and it ally considered hypertrophic and a
supply gradually increases causing a is defined as cryptogenic (7, 16, 17). potential source of hemoptysis when
hyperflow in the anastomotic vessels, Nevertheless, it has been demonstrat- larger than 2 mm at the origin (22).
which become hypertrophic with thin ed that a proportion of patients pre- Hemoptysis may also arise from
walls and tend to break into the alveoli senting with hemoptysis without any nonbronchial systemic arteries, which
and bronchi, giving rise to hemoptysis. morbidity are smokers, and bleed- enter the pulmonary parenchyma
Likewise, in chronic inflammatory dis- ing in smokers should be defined as through transpleural adhesions due
orders, such as bronchiectasis, chronic smoke-related (occurring as a result to chronic inflammatory processes
bronchitis, tuberculosis, mycotic lung of tobacco-induced bronchial wall in- (tuberculosis, mycosis) or through
diseases, and lung abscess, as well as in flammation), rather than cryptogenic pulmonary ligaments (20) and anas-
neoplastic diseases, the release of an- (17). Moreover, with a more systemat- tomose with the pulmonary arterial
giogenic growth factors promote neo- ic use of chest computed tomography circulation (8). Nonbronchial arteries
b c
Figure 7. ac. Hypertrophic nonbronchial arteries. Axial CT image at mediastinal window (a) of a 69-year-old woman with history of tuberculosis shows
right upper lobe consolidation and enlarged and tortuous right upper intercostal artery (arrows) that courses along thickened pleura and goes towards
the lesion. Coronal MIP image (b) detects a collateral hypertrophic nonbronchial vessel arising from the right intercostal artery that enters into the lung
parenchyma with a vertical course (not parallel to the bronchi) and anastomoses with a pulmonary arterial branch (arrows). In the same patient, axial
MIP reconstruction (c) demonstrates a hypertrophic nonbronchial arterial vessel originating from an enlarged right internal mammarian artery that
enters into the lung parenchyma with a horizontal course and anastomoses with the arterial pulmonary system (arrows).
(Rasmussens aneurysm) (40). The sus- sensitivity of 98.2% (vs. 59.6% of pul- tic step, nonbronchial or extrathoracic
picion of a pseudoaneurysm should monary angiography), and provides a feeders may be missed or not sought
rise when an avidly enhancing nodule reliable analysis of PAVM angioarchi- as the main source of bleeding (15).
is identified within a lesion on con- tecture that is very helpful in planning Therefore, DSA is now reserved for cas-
trast-enhanced CT scans. the treatment option, in particular for es where endovascular treatment has
Hemoptysis of pulmonary arterial managing complex lesions. to be attempted and once the other di-
origin may be associated with pulmo- agnostic studies, such as MDCTA, have
nary artery aneurysm (Behet disease) Digital subtraction angiography already been completed.
(41) or with PAVMs. Although pul- Nowadays DSA has a marginal role as Bronchial artery embolization (BAE)
monary angiography has been consid- a diagnostic tool in detecting the ori- is not free from complications. The
ered the gold standard for diagno- gin of hemoptysis. most disastrous event is spinal cord
sis of PAVM, MDCTA has assumed a Bronchial arteries are the main source ischemia. Its prevalence after BAE is
greater role in this regard (42). Inter- of hemoptysis. The recognition of all between 1.4% and 6.5% according to
estingly, Remy et al. (43) found that the possible origins of the bronchial different studies (4447). Spinal cord
contrast-enhanced CT has a better arterial supply at angiography may be ischemia can occur after inadver-
performance than pulmonary angiog- challenging (15). Moreover, if angiog- tent occlusion of the artery of Adam-
raphy in identifying PAVMs, with a raphy is performed as the first diagnos- kiewicz, which supports the anterior
Figure 9. ac. Oblique MIP image at mediastinal window setting (a) demonstrates a hypertrophic right bronchial artery (arrows) that supplies
a pulmonary neuroendocrine mass in a 45-year-old man presenting with relapsing hemoptysis. Pre-embolization DSA (b) confirms the blood
supply of the mass from the right bronchial artery (arrows). Postembolization image (c) shows the disappearance of lesion vascular supply
(arrows). A subsequent resolution of hemoptysis was observed and eventually the patient underwent surgery.
spinal artery supply in the distal tho- ered the most effective and minimal- Aside from the immediate control of
racic and lumbar regions. The Adam- ly invasive procedure for managing bleeding, Anuradha et al. (52) recent-
kiewicz artery originates from the de- massive and recurrent hemoptysis in ly demonstrated that in patients with
scending thoracic aorta at the levels almost all other cases. Endovascular massive hemoptysis due to tuberculo-
of T9T12 in 75% of cases. However, embolization may constitute a defini- sis and post-tuberculous sequelae, the
it may originate between levels of T5 tive therapy or it may be used as a tool effectiveness of BAE tends to decrease
and T8 (48), and when this vessel is to stabilize the patient before surgery over years, being 51% in the first year
visualized at angiography, emboliza- (5, 7, 50). Embolization reduces the and 39% in the second year after treat-
tion should not be carried out (4). At pressure in the fragile hypertrophic ar- ment. Nevertheless, repeated BAE in
MDCTA performed before the emboli- terial vessels supplying the pathologi- patients with early recurrence im-
zation, Adamkiewicz artery may be de- cal lung areas and decreases the risk of proves the outcome.
picted (48), even though its fine caliber perioperative bleeding (Fig. 9) (6). Also nonbronchial systemic arteries
makes certain identification difficult. As the bronchial arteries are respon- and pulmonary arteries may be subjected
On the other hand, DSA is suitable in sible for massive hemoptysis requiring to an endovascular treatment, if they are
identifying this small vessel. treatment in over 90% of cases (8), the source of the hemorrhage (15, 53).
BAE is the most frequently performed
Treatment endovascular procedure. It promptly Management
Until twenty years ago, surgery was brings the bleeding under control in In this review we attempted to cre-
considered the treatment of choice for 66% to 90% of patients (7, 49). ate a possible algorithm for managing
hemoptysis once the bleeding site was Samara et al. (51) demonstrated that hemoptysis according to the available
localized. However, surgery during an BAE is also an effective tool for man- data in the medical literature.
acute episode of hemorrhage implies a aging massive cryptogenic hemoptysis. Patients with hemoptysis should be
high risk of complications, with asso- Menchini et al. (17) observed imme- managed based on the rate and severi-
ciated mortality rate ranging from 7% diate cessation of bleeding in 85% of ty of bleeding (massive or nonmassive)
to 18%, which increases up to 40% in smoker patients with no other morbid- and the clinical condition of the patient.
emergency (49). Moreover, not all pa- ities, undergoing DSA and BAE. Mod- In case of massive bleeding in unstable
tients are candidates for surgery, such erate to marked hypertrophic bron- patients, resuscitation is mandatory be-
as those with pre-existing respiratory chial arteries were found in only 80% fore any other diagnostic investigation.
and cardiovascular comorbidities. of these patients, while the remaining
Nowadays, surgery remains the treat- 20% had angiographically normal Massive hemoptysis
ment of choice only in selected cases, bronchial arteries on the bleeding side. The flowchart for massive hemopty-
such as chest trauma and iatrogenic This result confirms that normal bron- sis is summarized in Fig. 10. An initial
pulmonary artery rupture (5), while chial arteries may also be responsible CXR is advisable in order to localize
endovascular embolization is consid- for bleeding in smokers. the bleeding site. MDCTA should be
Nonmassive hemoptysis
The flowchart for nonmassive he-
moptysis is summarized in Fig. 11. A
Figure 10. Flowchart for managing massive hemoptysis. CXR, chest radiography; MDCTA, CXR should always be performed as a
multidetector computed tomography angiography; DSA, digital subtraction angiography. first instance exam (1, 6, 8, 10). If the
underlying parenchymal or pleural ab-
normalities causing hemoptysis (i.e.,
pneumonia, mass, etc.) are identified,
the diagnostic and therapeutic man-
agement for the detected lesion should
follow (i.e., antibiotic treatment for a
young patient with fever and a pulmo-
nary opacity on CXR; further investi-
gation in case of a middle-aged, smok-
er patient with a pulmonary opacity on
CXR). If hemoptysis does not resolve
or recurs, further treatment (medical,
endovascular, and surgical) should be
considered. On the other hand, it is ad-
vised to perform a MDCTA in case of a
negative or nonlocalizing CXR, partic-
ularly when a lung cancer cannot be
excluded (30).
If MDCTA reveals the cause of he-
moptysis, the standard diagnostic
and therapeutic management for the
underlying condition should be per-
formed. If MDCTA is negative and the
Figure 11. Flowchart for managing nonmassive hemoptysis. CXR, chest radiography; MDCTA, episode of hemoptysis is resolving, it
multidetector computed tomography angiography. is possible to stop the investigation,
whereas further examination such as
bronchoscopy is warranted if the he-
executed in any case, even in emergen- ture, surgical treatment is the gold stan-
moptysis is persistent (33).
cy, regardless of CXR results, due to its dard (with the exception of patients in In case of a positive result at bronchos-
undisputed superiority in identifying whom surgery is contraindicated due to copy, the flowchart follows the same
the bleeding source and the possible comorbidities or emergency) (5) while, indication as for the above-mentioned
underlying cause, allowing for better in all other cases with positive MDC- positive diagnostic tests. If a cause can-
planning of further management and TA, DSA with arterial endovascular em- not be identified even at bronchosco-
treatment (30, 32, 35). bolization represents the procedure of py, a cryptogenic hemoptysis should be
If the underlying cause is chest trau- choice for managing massive and recur- considered. Clinicians should wait for
ma or iatrogenic pulmonary artery rup- rent hemoptysis (5, 7, 50). In emergen- a spontaneous resolution of bleeding