Aula 1 - Tracheobronchial Branching

You might also like

Download as pdf or txt
Download as pdf or txt
You are on page 1of 16

This copy is for personal use only. To order printed copies, contact reprints@rsna.

org
358
CHEST IMAGING

Tracheobronchial Branching
Abnormalities: Lobe-based
Classification Scheme1
Guillaume Chassagnon, MD
Baptiste Morel, MD Boyden’s nomenclature, which was based on postmortem speci-
Elodie Carpentier, MD mens and published in 1955 prior to the advent of computed
Hubert Ducou Le Pointe, MD, PhD tomography (CT), is commonly used to describe the normal seg-
Dominique Sirinelli, MD, PhD mental bronchial anatomy and various abnormalities. However,
several additional anomalies have been recognized since that time,
Abbreviations: ACB = accessory cardiac bron- and there is some confusion over the names used to describe
chus, LMB = left main bronchus, LPAS = left these anomalies. Several congenital branching anomalies affect-
pulmonary artery sling, MLB = middle lobe
bronchus, RMB = right main bronchus, 3D = ing the trachea, main bronchi, and intermediate bronchus have
three-dimensional, ULB = upper lobe bronchus, been reported, all of which can be recognized at chest CT but are
VACTERL = vertebral defects, anal atresia,
cardiac defects, tracheoesophageal fistula, renal
often overlooked. These anomalies, which probably occur early in
anomalies, and limb abnormalities fetal life, can be either supernumerary, with defects occurring at
RadioGraphics 2016; 36:358–373
29–30 days gestation, or displaced, with defects occurring later.
Tracheobronchial positional anomalies are often associated with
Published online 10.1148/rg.2016150115
other congenital abnormalities but may be isolated. They often are
Content Codes: asymptomatic but can be responsible for pulmonary symptoms
1
From the Department of Radiology, Hôpital such as dyspnea, recurrent pneumonia, and hemoptysis. It is essen-
Clocheville–CHU Tours, 49 Boulevard Béranger,
37044 Tours, France (G.C., E.C., D.S.); and De-
tial that these anomalies are recognized prior to lung resection to
partment of Radiology, Hôpital Armand Trous- avoid complications, especially when video-assisted thoracoscopic
seau, Paris, France (B.M., H.D.L.P.). Presented surgery is performed. In addition, bronchoscopists should be aware
as an education exhibit at the 2014 RSNA An-
nual Meeting. Received April 14, 2015; revision of these anomalies before performing diagnostic or therapeutic
requested June 26 and received July 14; accepted bronchoscopic procedures. Awareness of a few key bronchial ana-
July 31. For this journal-based SA-CME activity,
the authors, editor, and reviewers have disclosed
tomic principles and use of a lobe-based classification scheme will
no relevant relationships. Address correspon- facilitate recognition of tracheobronchial positional anomalies.
dence to G.C. (e-mail: gchassagnon@gmail.com).
©
©
RSNA, 2016 • radiographics.rsna.org
RSNA, 2016

SA-CME LEARNING OBJECTIVES


After completing this journal-based SA-CME Introduction
activity, participants will be able to: Numerous major congenital bronchial branching anomalies have
■■List the main differences between the been described, with a reported prevalence of 0.1%–2% in the general
right and left bronchial trees.
population (1–4). Most of these anomalies were described in the out-
■■Discuss situations in which the radiolo- standing work by Boyden (5) published in 1955, before the advent of
gist must search for congenital branching
abnormalities. computed tomography (CT), with additional anomalies having been
■■Describe congenital branching abnor-
recognized since that time (6,7). There is some confusion in the litera-
malities affecting the trachea, main bron- ture over the names used to describe these anomalies. For example,
chi, and intermediate bronchus. the terms tracheal bronchus and eparterial bronchus may designate simi-
See www.rsna.org/education/search/RG. lar or different anomalies depending on the authors. Thus, the use of
a uniform comprehensive classification scheme is essential in describ-
ing congenital positional anomalies of the tracheobronchial tree. All
congenital branching anomalies affecting the trachea, main bronchi,
and intermediate bronchus can be recognized at routine chest CT, but
they frequently are overlooked (8). Their recognition is essential prior
RG  •  Volume 36  Number 2 Chassagnon et al  359

TEACHING POINTS
■■ Normally, the carina is at the level of thoracic vertebrae T4
and T5.
■■ Most of these anomalies are either displaced or supernumer-
ary bronchi. The term displaced bronchus is used to describe
a bronchus with an abnormal origin, when the normal bron-
chus ventilating the corresponding parenchyma is absent. In
contrast, a supernumerary anomaly is seen in addition to the
normal bronchus. A supernumerary bronchus may end blind-
ly in the parenchyma of the corresponding normal bronchus
or may be associated with ventilated parenchyma, which is
thus considered to be additional lung tissue.
■■ At CT, the relationship of the ULB to the ipsilateral pulmonary
artery is the most reliable marker of bronchial situs.
■■ ACB is the only bronchus originating from the medial wall of
either the RMB or the intermediate bronchus, but it can oc-
casionally occur on the left side.
■■ In bridging bronchus, the carina is located at the normal level,
facing thoracic vertebrae T4 and T5, whereas the pseudoca-
rina is at the T6-T7 level and has an inverted T appearance due Figure 1.  Drawing illustrates the segmental bronchial anat-
to an increased angle. omy according to Boyden’s nomenclature. On the right side,
B1 = apical bronchus, B2 = anterior bronchus, B3 = posterior
bronchus, B4 = lateral bronchus, B5 = medial bronchus, B6 =
superior bronchus, B7 = medial basal bronchus, B8 = anterior
to lung surgery to avoid complications during basal bronchus, B9 = lateral basal bronchus, and B10 = poste-
rior basal bronchus. On the left side, B1 and B3 arise from the
lung resection (8,9). Tracheobronchial branching
same trunk and form the apicoposterior bronchus (B1 + 3), B4 =
anomalies may also have important implications superior lingular bronchus, and B5 = inferior lingular bronchus.
during tracheal intubation (4,10). The other left segmental bronchi have the same designations
In this article, we review the embryologic as their right-sided counterparts.
development and normal anatomy of the tra-
cheobronchial tree; describe various congenital
branching anomalies affecting the trachea, main during the embryonic phase (weeks 5–7) and
bronchi, and intermediate bronchus, including pseudoglandular phase (weeks 5–17). Pulmonary
abnormal bronchi directed toward the middle vessel organogenesis occurs simultaneously with
and the lower lobes that arise (or should have tracheobronchial development. Thus, at the end
arisen) from the main bronchi and intermediate of the pseudoglandular stage, all preacinar airways
bronchus; and propose a lobe-based classifica- as well as corresponding arteries and veins are
tion scheme for these anomalies to facilitate their present (13). Lung parenchyma develops during
recognition. Bronchial agenesis, aplasia, hypopla- the canalicular stage (17–26 weeks) and sacular
sia, and bronchial atresia are not discussed in this stage (24 weeks–birth). At birth, development of
article because they should not be considered as the lung parenchyma remains incomplete because
branching anomalies involving the trachea, main most alveoli are formed during the first 3 years of
bronchi, or intermediate bronchus. postnatal life.
The pathogenesis of congenital branching
Embryologic Development anomalies remains unknown, but these anomalies
Tracheobronchial development begins early in probably occur early in fetal life. Several hypoth-
fetal life. The trachea and bronchi develop as a eses have been proposed (11). Evans (3) hy-
diverticulum of the ventral wall of the foregut at pothesized that defects involving supernumerary
24–26 days gestation (3,11). Shortly thereafter, bronchi may occur at about 29–30 days gestation,
primary bronchi bud off and grow, while the whereas displaced bronchi are more likely to oc-
trachea separates from the esophagus. On days cur after 32 days. The term supernumerary refers
30–34, five growing points are identified that cor- to an abnormal bronchus that arises in addition
respond to lobar buds: three on the right side and to the normal corresponding bronchus.
two on the left (5). Bronchial buds undergo stages
of dichotomous and lateral branching that give rise Normal Tracheobronchial Anatomy
to the conducting airways (12). By days 36–38, all In radiology and thoracic surgery, Boyden’s
segmental bronchi are present, and by the end of nomenclature is commonly used to describe
the 6th week, branching up to the subsegmental segmental bronchial anatomy (Fig 1) (5). In
portions of the bronchial tree has occurred (3,12). each lung, segmental bronchi (B) are assigned a
The development of bronchial arborization occurs number from 1 to 10, similar to the number of
360  March-April 2016 radiographics.rsna.org

the corresponding segment (S). These numbers Most of these anomalies are either displaced
differ from those in the endoscopists’ nomen- or supernumerary bronchi. The term displaced
clature, in which anterior bronchi of the upper bronchus is used to describe a bronchus with an
lobes are labeled B3 (B2 in Boyden’s nomencla- abnormal origin, when the normal bronchus ven-
ture) and posterior bronchi of the upper lobes tilating the corresponding parenchyma is absent.
are labeled B2 (B3 in Boyden’s nomenclature) In contrast, a supernumerary anomaly is seen in
(5,14). Variations in the prevailing pattern of addition to the normal bronchus. A supernumer-
segmental bronchial distribution are common. ary bronchus may end blindly in the parenchyma
For example, the typical trifurcation of the right of the corresponding normal bronchus or may
upper lobe bronchus (ULB) is seen in only be associated with ventilated parenchyma, which
30%–38% of the population (5,11). To under- is thus considered to be additional lung tissue
stand tracheobronchial positional anomalies, (15). This additional lung tissue is more often
three points must be emphasized: ventilated and may be delineated by an accessory
1. Normally, the carina is at the level of tho- fissure. Blind-ended bronchi are termed congenital
racic vertebrae T4 and T5. bronchial diverticula and should not be confused
2. The relationship of the bronchi to the with acquired bronchial diverticula, which can be
pulmonary arteries differs between the lungs. observed in chronic obstructive pulmonary disease.
The right ULB lies behind and beneath the right There can be associated abnormal distribution of
pulmonary artery, whereas the left main bron- the pulmonary vasculature (eg, a left pulmonary
chus (LMB) passes beneath the left pulmonary artery sling [LPAS] in the case of a bridging bron-
artery before it gives rise to the left ULB. Thus, chus) (16,17).
the right ULB is said to be eparterial, since it Most congenital tracheobronchial anomalies
arises above the point where the right pulmonary are asymptomatic and are discovered incidentally.
artery crosses the right main bronchus (RMB), Inverted pulmonary situs in cases of situs inver-
whereas the left ULB is said to be hyparterial, sus, as well as tracheal bronchus and preepar-
since it originates below the point where the left terial bronchus, can be recognized easily at
pulmonary artery crosses the LMB. On the right chest CT, but other tracheobronchial branching
side, the normally situated right ULB (eparte- anomalies are often overlooked, and preoperative
rial bronchus) serves as a point of reference to recognition of these variations is important, es-
describe the position of the abnormally located pecially in cases involving video-assisted thoraco-
bronchus directed toward the upper lobe terri- scopic surgery (8,9).
tory, whereas on the left side, the point of refer- Tracheobronchial branching anomalies can
ence is the crossing point of the left pulmonary be isolated. However, some of these anomalies,
artery and the LMB. such as bronchial situs anomalies, tracheobron-
3. Bronchovascular distribution to the lungs is chial branching anomalies of the upper lobes,
asymmetric. The RMB is shorter than the LMB. and bridging bronchus, are often associated with
The right ULB arises alone, several centimeters other tracheobronchial branching anomalies and/
above the middle lobe bronchus (MLB), and the or congenital heart disease, lung abnormalities, or
right superior bronchus (B6) arises just inferior foregut malformations (3,4,7,18). In an autopsy
to the orifice of the MLB, nearly opposite to it. study, Evans (3) found that three of four infants
In the left lung, the superior and inferior divi- with a displaced or supernumerary bronchus had
sions (lingular bronchi) arise together from the congenital heart disease and other malformations.
left ULB, and B6 arises at a distance. Indeed, Similarly, Ming and Lin (4) reported that tra-
the common trunk of the left lower lobe is longer cheal bronchi occurred 13 times more frequently
than that of the right lower lobe and extends for a in children with congenital heart disease than in
distance of 10–12 mm (5). those without this disease entity. Congenital heart
diseases associated with tracheobronchial branch-
Congenital Tracheo­- ing anomalies include ventricular septal defects,
bronchial Branching Anomalies conotruncal heart defects, aortic coarctation, and
Numerous tracheobronchial branching anoma- atrioventricular canal defects (3,4,19). Down
lies have been described. In this article, we focus syndrome also appears to be overrepresented
on anomalous branching of the trachea, main among patients with tracheal bronchus (10).
bronchi, and intermediate bronchus. These
tracheobronchial branching anomalies can be cat- Tracheobronchial Branching
egorized into five groups: (a–d) those involving Anomalies of the Entire Lung
(a) the entire lung, (b) the upper lobes, (c) the Bronchial situs is one aspect of visceroatrial situs,
middle lobe, or (d) the lower lobes; and (e) other which refers to the position of the cardiac atria,
tracheobronchial branching anomalies. lungs, liver, stomach, and spleen relative to the
RG  •  Volume 36  Number 2 Chassagnon et al  361

Figure 2.  Drawings illustrate the rela-


tionship of the ULB to the pulmonary
arteries as a marker of bronchial situs.
(a) In situs solitus, the right ULB is in an
eparterial position (arrow) and the left
ULB is in a hyparterial position (arrow-
head). In situs inversus, just the oppo-
site is true. (b) When both ULBs are in
the same position, bronchial situs corre-
sponds either to right isomerism in cases
of bilateral eparterial bronchi or to left
isomerism in cases of bilateral hyparte-
rial bronchi.

midline (20,21). Situs solitus corresponds to the mon in right isomerism, which is associated with
usual arrangement of these organs, whereas situs an 80%–90% mortality rate during the first year of
inversus is the mirror image arrangement and life (26). Patients with left isomerism have a bet-
situs ambiguus (or heterotaxy) includes other ter outcome and a less frequent association with
arrangements that cannot be categorized as either congenital heart disease (27). Left isomerism is as-
situs solitus or situs inversus. Among types of sociated with a 60% mortality rate during the first
situs ambiguus, right isomerism describes a bilat- year of life (19), and, in autopsy series, congenital
eral right-sidedness and left isomerism describes heart diseases have been reported to occur in 50%
a bilateral left-sidedness (19,21). or more of cases (28). However, these percentages
Right isomerism (formerly known as asplenia are probably overestimated because the number
syndrome) is typically associated with right bron- of cases of left isomerism without congenital heart
chial isomerism, bilateral right morphologic atria, disease diagnosed during adulthood has increased
asplenia, midline liver, and variably located stom- with use of cross-sectional imaging (25).
ach. In contrast, left visceroatrial isomerism (for- At CT, the relationship of the ULB to the
merly known as polysplenia syndrome or Ivemark ipsilateral pulmonary artery is the most reliable
syndrome) is usually associated with left bronchial marker of bronchial situs (Fig 2) (22). A lung with
isomerism, bilateral left morphologic atria, poly- an eparterial bronchus is morphologically a right
splenia, midline liver, and variably located stom- lung, whereas a lung with a hyparterial bronchus is
ach. However, these features are variably associ- morphologically a left lung. Thus, bilateral eparterial
ated, and bronchial situs does not always correlate ULBs characterize right bronchial isomerism (Fig
with atrial and abdominal situs (22). 3), whereas bilateral hyparterial ULBs characterize
Situs anomalies can be associated with con- left bronchial isomerism (Fig 4). Other features such
genital heart diseases, primary ciliary dyskinesia as the number of lobes, ratio of left to right main
(including Kartagener syndrome), and intesti- bronchial lengths, and branching pattern are less re-
nal malrotation and other abdominal anomalies liable markers (22). The main differential diagnosis
(23–25). Congenital heart diseases are quite com- of right isomerism is a left eparterial bronchus.
362  March-April 2016 radiographics.rsna.org

Figure 3.  Right bronchial isomerism in a 4-month-old female infant with double outlet ventricle. (a) On
a contrast material–enhanced three-dimensional (3D) reconstructed CT image of the tracheobronchial
tree, the left bronchial tree has the same morphologic features as the right bronchial tree, with the early
rise of the ULB at a distance from the MLB. LLB = lower lobe bronchus, RLLB = right lower lobe bronchus,
RULB = right ULB. (b) On a 3D reconstructed CT image of the tracheobronchial tree and pulmonary
arteries, both ULBs are eparterial, since they originate behind the ipsilateral pulmonary arteries. These
findings are consistent with right bronchial isomerism. The patient also had right atrial isomerism and an
ambiguous visceral situs associated with asplenia and cavoazygos continuation.

Figure 4.  Left bronchial isomerism in an asymptomatic 61-year-old man. LULB = left ULB. (a) Contrast-
enhanced 3D reconstructed CT image of the tracheobronchial tree shows that, similar to the left ULB,
B4 and B5 on the right side arise with the ULB. (b) Superimposed 3D reconstructed CT images of the
tracheobronchial tree and pulmonary arteries show that both ULBs are hyparterial, since they arise below
the crossing of the ipsilateral pulmonary artery and main bronchi. These findings are consistent with left
bronchial isomerism. The patient also had left atrial isomerism and an ambiguous visceral situs associated
with polysplenia and truncated pancreas.

Tracheobronchial Branching the upper lobe territory (5,11,29); thus, the term
Anomalies of the Upper Lobes tracheal bronchus may seem inappropriate (29).
A bronchus abnormally originating directly from
Tracheal Bronchus.—Tracheal bronchus was de- the trachea is exposed to additional risks during
scribed for the first time by Sandifort in 1785 as a tracheal intubation, such as lobar or segmental
right ULB originating from the trachea (5). Since atelectasis due to luminal occlusion by the tube or
then, several authors have expanded this defini- respiratory failure due to inadvertent intubation of
tion to include any bronchus originating from the tracheal bronchus (4,10). Thus, in accordance
the trachea or main bronchi and directed toward with the original definition given by Sandifort and
RG  •  Volume 36  Number 2 Chassagnon et al  363

Figure 5.  Drawing illustrates tra-


cheobronchial branching anoma-
lies of the upper lobes. A = right tra-
cheal bronchus, B = right preeparte-
rial bronchus, C = right posteparte-
rial bronchus, D = left tracheal bron-
chus, E = left eparterial bronchus,
F = left prehyparterial bronchus.

Figure 6.  Recurrent pneumonia in a 16-month-old boy with displaced right tracheal bronchi and tetralogy of
Fallot. (a) Supine chest radiograph shows consolidation in the right upper lobe (*) with associated retrocardiac
consolidation in the left lower lobe (arrowhead). (b) Contrast-enhanced chest CT image obtained 3 days later
shows areas of consolidation in both the right upper lobe (black arrows) and left lower lobe (arrowhead). Red
arrow = displaced right tracheal bronchus ventilating consolidated parenchyma.

others (4,15), we suggest restricting the defini- The frequency of occurrence of right tracheal
tion of a tracheal bronchus to any bronchus that bronchus is debated. According to various bron-
abnormally originates directly from the trachea or choscopic, bronchographic, and CT studies, right
carina. ULB originating from the main bronchi tracheal bronchus is seen in 0.1%–1.3% of adults
and intermediate bronchus should be labeled dif- and in 1.5%–2% of the pediatric population (2,4).
ferently to avoid confusion (Fig 5). Associated conditions have been reported in 78% of
Tracheal bronchus is almost invariably located children with a right tracheal bronchus. These condi-
on the right side. Almost all reported cases of left tions include Down syndrome; malformations of the
tracheal bronchus have originated from the LMB thoracic cage, foregut, or lung; tracheal stenosis; and
and thus correspond to left eparterial or left pre- other tracheobronchial branching anomalies (2,16).
hyparterial bronchi. Ming and Lin (4) observed a 13-fold increase in the
To our knowledge, 12 cases of bronchi origi- frequency of occurrence of right tracheal bronchi in
nating from the trachea and directed toward the children with congenital heart disease.
left upper lung have been reported in the English Clinically, tracheal bronchus may be associ-
language literature (4,18,30–35). Among these ated with recurrent pneumonia (Fig 6), stridor,
bronchi, 11 were bilateral tracheal bronchi and at or respiratory distress in children (36). Adults are
least three should be considered as bilateral right almost invariably asymptomatic.
tracheal bronchi because they were associated At CT, tracheal bronchus is easily recognized.
with right pulmonary isomerism. It usually arises from the distal part of the trachea,
364  March-April 2016 radiographics.rsna.org

Figure 7.  Displaced right tracheal bronchus in a Figure 8.  Displaced right preeparterial bronchus in an
15-year-old boy. Three-dimensional reconstructed chest 18-year-old man with tetralogy of Fallot. Three-dimen-
CT image of the tracheobronchial tree shows an aber- sional reconstructed CT image of the tracheobronchial
rant right tracheal bronchus arising from the right wall tree shows an aberrant right preeparterial bronchus aris-
of the trachea, less than 2 cm above the carina. The B1 ing from the RMB and corresponding to a displaced B1
and B2 segmental bronchi arise from the tracheal bron- segmental bronchus. These findings are consistent with
chus, which is associated with proximal stenosis of the a displaced right preeparterial bronchus. RLLB = right
right ULB (arrow). The right ULB gives rise to B3 only. lower lobe bronchus.

less than 2 cm above the carina (Fig 7). The dis- owing to the absence of contribution of the right
tance between the tracheal bronchus and the ca- upper lobe to the development of the RMB dur-
rina should be stated in the report for the anesthe- ing fetal life (15).
siologist. In some cases, the abnormally branched A left tracheal bronchus is usually associated
bronchus may be tiny or manifest with proximal with a right tracheal bronchus, forming true bilat-
stenosis (4,15,36,37). A blind-ended right tracheal eral tracheal bronchi, in contrast to the bilateral
bronchus is also possible and is referred to as a right tracheal bronchi that can be observed in
congenital right tracheal diverticulum. cases of right isomerism (4). In all reported cases
Tracheal bronchi are more frequently dis- of true bilateral tracheal bronchi, the left tracheal
placed than supernumerary bronchi. Of the bronchus originated opposite to the right tracheal
eight right tracheal bronchi reported by Ghaye bronchus (31,33). Bilateral tracheal bronchi can
et al (11), 75% were displaced bronchi, whereas be associated with a decrease in the diameter of
only 25% were supernumerary bronchi. A right the downstream trachea (31).
tracheal bronchus may ventilate the entire right
upper lobe, one or two segments, a subsegment, Right Preeparterial Bronchus.—The term right
or a subsubsegment. A displaced tracheal bron- preeparterial bronchus refers to any bronchus
chus often supplies at least a portion of the apical directed toward the right upper lobe that arises
segment. When the entire right ULB is displaced abnormally from the RMB, above the level of
on the trachea, the right tracheal bronchus is the right ULB (eparterial bronchus) (Fig 5). The
classically termed “pig bronchus” because it cor- term eparterial bronchus was introduced by Boy-
responds to normal anatomy in swine. den (5) and originally described both right preep-
Lung parenchyma ventilated by a supernumer- arterial bronchus and right tracheal bronchus.
ary tracheal bronchus has been referred to as a The frequency of occurrence of right preeparte-
tracheal lobe by several authors and may be delin- rial bronchus is almost twice that of right tracheal
eated by an accessory fissure (38). This tracheal bronchus (0.9% versus 0.4% in a study of 1200
lobe may be intra- or extralobar and is not related bronchograms by Atwell [1]), and both share the
to the azygos lobe, seen in cases of azygos pseudo- same predisposing conditions. Right preeparterial
fissure due to an anomalous pathway of the azygos bronchus is often asymptomatic (1,11).
vein (16). Only a few cases of double right tracheal At CT, right preeparterial bronchus arises from
bronchus have been described (36,39). the lateral wall of the RMB (Fig 8). Displaced
In cases of an entirely displaced right ULB, forms represent 82% of cases, and a blind-ended
the underlying RMB can be stenotic, possibly bronchus may rarely be encountered (11). The
RG  •  Volume 36  Number 2 Chassagnon et al  365

Figure 9.  Displaced right posteparterial bronchus in a 15-year-old boy with a surgically corrected aber-
rant left pulmonary artery and partial anomalous pulmonary venous return. RULB = right ULB. (a) Coronal
3D reconstructed CT image of the tracheobronchial tree shows that the B2 and B3 segmental bronchi
arise from the MLB. (b) Oblique reconstructed CT image shows that B1 is the only segmental bronchus
to originate from the right ULB, whereas B3 originates directly from the MLB, and B2 arises from B4.

main differential diagnosis in cases of an abnor- eparterial bronchus does not expose the patient
mally branched bronchus arising from the RMB to additional risk during tracheal intubation. An
is an accessory cardiac bronchus (ACB), which association with congenital malformations such
always arises from the medial wall and is directed as VACTERL (vertebral defects, anal atresia,
toward the heart. cardiac defects, tracheoesophageal fistula, renal
anomalies, and limb abnormalities), congenital
Right Posteparterial Bronchus.—The term right heart diseases, and other airway malformations
posteparterial bronchus refers to any bronchus has been reported (8,18,41).
directed toward the right upper lobe that arises At CT, a left eparterial bronchus originates
from the right bronchial tree at a level below from the posterolateral or lateral wall of the
that of the right ULB (eparterial bronchus) (Fig LMB above the level where the left pulmonary
5) (5). artery crosses the left MLB (Fig 10). Most of
Segmental and subsegmental right ULB origi- the reported cases in the literature are displaced
nating from the MLB are considered by some au- eparterial bronchi (5,8,11,42). The anomalous
thors to be minor variants (37,40) but correspond bronchus usually ventilates at least the apico-
to the initial description of posteparterial bronchus posterior segment (segments S1 + 3) and may
proposed by Boyden (5) (Fig 9). Another variant also ventilate the anterior (S2) or superior (S6)
is a gross downward displacement of the ULB that segment of the left lower lobe (8). A trilobed
originates at the same level as the MLB. To our left lung due to an accessory fissure is often
knowledge, only one case of this variant has been observed (8,42). The accessory fissure may cor-
reported in the English language literature (5). respond to a left minor fissure similar to that en-
countered in 8%–18% of the general population
Left Eparterial Bronchus.—The term left eparte- and that separates the anterior (S2) and superior
rial bronchus refers to any bronchus directed (S4) lingular segments (8,42–45). It may also be
toward the left upper lobe that arises from the different from left minor fissure and be situated
LMB above the level where the left pulmonary between the apicoposterior (S1 and S3) and
artery crosses the LMB (Fig 5). It represents anterior (S2) segments (5,8). Hyperinflation,
the most common left-sided bronchial branch- air trapping, bronchiectasis, or lymphangiecta-
ing anomaly. In a study by Ghaye et al (11), left sia can also be encountered, probably related
eparterial bronchus occurred 1.7 times more to vascular compression by the left pulmonary
frequently than left prehyparterial bronchus but artery (29).
five times less frequently than right preeparte- Left eparterial bronchus is often overlooked.
rial bronchus. In a study by Oshiro et al (8), eight of 10 cases
Affected patients are usually asymptomatic. of left eparterial bronchi were surgical findings
Similar to right preeparterial bronchus, left that were retrospectively visible at preoperative
366  March-April 2016 radiographics.rsna.org

Figure 10.  Displaced left eparterial bronchus in an asymptomatic 69-year-old man. (a) Coronal contrast-
enhanced 3D reconstructed CT image of the tracheobronchial tree shows a displaced left B1 bronchus arising
from the LMB and directed toward the left upper lobe (arrow), as well as a displaced right tracheal bronchus
(B1). LULB = left ULB, RULB = right ULB. (b) Superimposed 3D reconstructed CT images of the tracheobron-
chial tree and pulmonary arteries (oblique posterior view) show that the displaced left B1 bronchus (arrow)
arises above the level where the left pulmonary artery crosses the left MLB (LULB). (c) On an axial CT image,
the displaced left B1 bronchus (arrow) passes behind the interlobar artery (*). These findings are consistent
with a displaced left eparterial bronchus associated with a right tracheal bronchus.

Figure 11.  Double displaced left prehyparterial bronchi (left isomerism) in a 2-year-old girl with tetral-
ogy of Fallot. (a) Coronal contrast-enhanced 3D reconstructed CT image of the tracheobronchial tree and
pulmonary arteries shows bilateral hyparterial bronchi consistent with left isomerism. On the right side
(morphologically left bronchial tree), displaced B1 + 3 and B2 bronchi originate independently from the
ULB that gives rise to B4 + 5. These displaced bronchi arise below the crossing artery. (b) On an axial CT im-
age, the displaced B2 bronchus (arrow) passes anterior to the interlobar artery (*), as do B1 + 3 and B4 + 5.

CT. The main differential diagnosis is pulmonary In the study by Ghaye et al (11), left prehyp-
right isomerism. arterial bronchus was less common than left
eparterial bronchus. There may be other associ-
Left Prehyparterial Bronchus.—Left prehyparte- ated airway anomalies, such as right preeparterial
rial bronchus is defined as an anomalous bronchus bronchus and left isomerism (Fig 5).
directed toward the left upper lobe that arises from At CT, left prehyparterial bronchus is seen as
the LMB between the level where the left pulmo- a supernumerary or displaced bronchus origi-
nary artery crosses the LMB and the level of the nating from the lateral wall of the LMB, below
left ULB (hyparterial bronchus) (Fig 5). Few data the arch of the left pulmonary artery but above
are available about this rare anomaly. the normally positioned left ULB (Fig 11). The
RG  •  Volume 36  Number 2 Chassagnon et al  367

Figure 12.  Displaced left eparterial bronchus in a 7-month-old boy with tetralogy of Fallot. (a) Posterior
oblique contrast-enhanced 3D reconstructed CT image of the tracheobronchial tree shows a displaced B1 bron-
chus (arrow) that arises at the same level as the left ULB (LULB). LLLB = left lower lobe bronchus. (b) Posterior
oblique 3D reconstructed CT image of the tracheobronchial tree and pulmonary arteries shows a supernumerary
bronchus (arrow) that seems to arise below the level where the left pulmonary artery crosses the main bron-
chus. (c) On an axial CT image, the supernumerary bronchus (arrow) passes behind the interlobar artery (*),
similar to the (eparterial) right ULB. Thus, the displaced B1 bronchus (cf a) should be considered a displaced
left eparterial bronchus.

level of the origin of the bronchus relative to the Tracheobronchial Branching


crossing of the bronchi and the left pulmonary Anomalies of the Middle Lobe
artery is important for distinguishing between
left eparterial and left prehyparterial bronchi but Gross Upward Displacement of the MLB.—Gross
may be difficult to establish, especially on axial upward displacement of the MLB corresponds
images. Thus, we suggest that bronchi taking a to an MLB arising at the level of the right ULB.
path behind the pulmonary arteries, similar to The MLB may arise from the right ULB, or even
the right ULB, should be considered left eparte- from B2. This variation is very rare and has been
rial bronchi, whereas bronchi taking a path in reported only once (5). We have encountered two
front of these arteries should be considered left such cases in our experience; in both cases, the
prehyparterial bronchi (Fig 12). As in left ep- patient had congenital heart disease.
arterial bronchus, an accessory fissure may also At CT, a displaced MLB arises with or from
be present (11,46). Although having a similar the right ULB at a distance from the origin of B6.
appearance, left eparterial and left prehyparte- Its appearance is similar to that of normal left lung
rial bronchi probably have different pathoge- anatomy, in which the left ULB gives rise to supe-
netic features because the former is usually a rior and inferior divisions (lingular bronchi) (Fig
displaced bronchus, whereas the latter is usually 13). However, the right ULB remains eparterial
supernumerary (11). and is not displaced downward. The main differ-
ential diagnoses are left bronchial isomerism and
Left Posthyparterial Bronchus.—Left posthyp- displaced posteparterial bronchus. In the latter con-
arterial bronchus has previously been defined dition, the right upper lobe is displaced downward
as an anomalous bronchus directed toward the and originates at almost the same level as B6.
left upper lobe that arises below the left ULB.
It has been included in a previous classification Tracheobronchial Branching
scheme for abnormally positioned ULB (11); Anomalies of the Lower Lobes
to our knowledge, however, no cases have been
reported in the English language literature. This Suprasuperior Bronchus.—Suprasuperior
variant is not included in the present classifica- bronchus is defined as a displaced subsegmental
tion scheme because it would arise from the left bronchus of the superior segment of the lower
lower lobe bronchus. lobe (S6) that arises from the main bronchus or
368  March-April 2016 radiographics.rsna.org

Figure 13.  Gross upward displacement of the MLB in a 4-year-old girl with tetralogy of Fallot. (a) An-
terior oblique contrast-enhanced 3D reconstructed CT image of the tracheobronchial tree shows that
the MLB is displaced and arises with the right ULB (RULB) from a common trunk, at a distance from B6.
RLLB = right lower lobe bronchus. (b) Posterior 3D reconstructed CT image shows that the bronchial
situs is solitus type because the right ULB (RULB) is eparterial and the left ULB (LULB) is hyparterial.

Figure 14.  Suprasuperior bronchus in an 80-year-old man. (a) Oblique anterior contrast-enhanced 3D reconstructed
CT image shows an aberrant bronchus (arrow) arising from the posterior wall of the intermediate bronchus, above B6.
(b) On an axial CT image, the aberrant bronchus (arrow) is directed toward the superior segment (S6) and corresponds
to a suprasuperior bronchus. (c) Axial CT image obtained at a lower level than b reveals that the B6 bronchus originates
at almost the same level as the MLB.

the intermediate bronchus (5,47). Six cases of bronchus is rare. Subsuperior and suprasuperior
right suprasuperior bronchi have been reported bronchi have been described as different enti-
by Boyden (5), all of which corresponded to ties by Boyden (5). In contrast to a subsuperior
displaced subsegmental bronchi involving at bronchus, which is always displaced, a suprasupe-
least the B6a subsegmental bronchus. At CT, a rior bronchus, which is supernumerary in nature,
suprasuperior bronchus originates above the level suggests a different pathogenesis.
where the MLB arises (Fig 14). It must be differ-
entiated from a subsuperior bronchus (B*) cor- Other Tracheo-­
responding to a supernumerary bronchus that is bronchial Branching Anomalies
directed toward the superior segment and arises
below B6. Subsuperior bronchus is very common Accessory Cardiac Bronchus.—ACB is a supernu-
and has been observed in 56% of right lungs and merary bronchus that originates from the medial
26% of left lungs (11), whereas suprasuperior wall of the main bronchus or intermediate bronchus
RG  •  Volume 36  Number 2 Chassagnon et al  369

Figure 15.  Bilateral ACB in an asymptomatic 70-year-old woman. LULB = left ULB, RULB = right ULB.
(a) Coronal contrast-enhanced minimum intensity projection reformatted CT image shows bilateral
supernumerary bronchi (arrows) arising from the medial wall of the intermediate bronchus and LMB.
(b) Three-dimensional reconstructed CT image shows that the right ACB is intermediate type, appear-
ing as a long diverticulum without arborization, whereas the left ACB is short diverticular type (arrows).

and is directed caudally toward the heart. ACB is arborization. At CT, lung tissue associated with
the only bronchus originating from the medial wall the supernumerary bronchus may appear as a
of either the RMB or the intermediate bronchus, tissue mass around the tip of the bronchus or as
but it can also occasionally occur on the left side a ventilated lobule that can be delineated by an
(48,49). First described in 1946 by Brock (50), accessory fissure. The tissue mass, which is seen
ACB is seen in 0.07%–0.5% of the general popu- in 35.7%–50% of patients, can show enhance-
lation (48). It usually ends blindly but may also ment after contrast material injection and has
supply ventilated parenchyma (48,51,52). been attributed to vestigial or rudimentary lung
ACB is usually asymptomatic, but patients parenchyma (11,52). In the same CT studies,
may experience symptoms such as recurrent the prevalence of lobules delineated by an acces-
pneumonia, hemoptysis, cough, or dyspnea (52). sory fissure was 28.5%–66%, with some patients
Cases of lung tumors arising from ACB have presenting with both a tissue mass and at least a
also been reported (53,54). ACB is not always ventilated lobule (11,52).
isolated. Patients with double ACB or other as- The main differential diagnosis is the medial
sociated bronchial anomalies such as preeparte- basal bronchus (B7), which is the only bron-
rial bronchus and left or right tracheal bronchus chus to arise from the inner wall of the lower
have been encountered (51,55–57), and the lobe bronchus (48). ACB has no relationship to
prevalence of ACB among patients with other anatomic variations and anomalies of B7 that are
major tracheobronchial positional anomalies is restricted to the lower lobe bronchus (51).
reported to be higher (52).
At chest CT, ACB is easily recognized as Bridging Bronchus.—Bridging bronchus is an ab-
the only bronchus arising from the medial wall errant bronchus that partially or totally supplies
of the main bronchus or intermediate bron- the right lung but that originates from the LMB
chus (Fig 15). The abnormal bronchus most (58). It is an extremely rare bronchial malforma-
frequently originates from the medial wall of tion and was named by Gonzalez-Crussi et al (6)
the proximal third of the intermediate bron- in 1976. Wells et al (7) reported a second variant
chus, almost directly opposite the origin of the in 1988. Thus, bridging bronchi can be divided
right ULB. Median length is 12 mm (11) and into two main subtypes (Fig 16):
mainly depends on the morphologic features of 1. In type 1, the RMB ends in the right ULB,
the bronchus. Indeed, Mangiulea and Stinghe and the intermediate bronchus abnormally arises
(51) have recognized three types of ACB at from the LMB, forming a pseudocarina (Fig 17)
bronchoscopy: (a) a short diverticular type, (59). The middle lobe is supplied by either the
(b) a long type ventilating a small undeveloped right bronchus or the bridging bronchus.
lobule, and (c) an intermediate type with a 2. In type 2, the RMB ends in a diverticu­lum or
long diverticulum but no bronchial or alveolar is absent (59). The entire right lung is ventilated
370  March-April 2016 radiographics.rsna.org

Figure 16. Drawings il-


lustrate type 1 and type 2
bridging bronchi.

Figure 17.  Type 1 bridging bronchus in a 6-year-old girl with pulmonary atresia and a ventricular septal defect. (a) On
a coronal contrast-enhanced minimum intensity projection reformatted CT image, the RMB ends in the right ULB, and
the intermediate bronchus arises from the LMB, forming a pseudocarina (arrowhead). (b) Three-dimensional recon-
structed CT image superimposed on a coronal reformatted image shows the pseudocarina at the T6 level (arrowhead),
with the carina remaining at the T4 level (arrow). IB = intermediate bronchus.

by a displaced RMB arising from the LMB, form- patients with LPAS, type 1 bridging bronchus
ing a pseudocarina (Fig 18). (LPAS type II-A) has been reported in 22%–27%
One probable case of left bridging bronchus of patients, whereas type 2 bridging bronchus
arising from the RMB and supplying the left lower (LPAS type II-B) was encountered in 30%–57%
lobe has also been reported, but autopsy confirma- (7,17). Rare cases of bridging bronchi without
tion was not obtained (60). In bridging bronchus, LPAS have been reported, and almost all were
the carina is located at the normal level, facing type 1 bridging bronchi (59,61–63). This entity
thoracic vertebrae T4 and T5, whereas the pseudo- is probably underdiagnosed or misdiagnosed as
carina is at the T6-T7 level and has an inverted T a tracheal bronchus. Congenital cardiovascular,
appearance due to an increased angle (7). vascular, abdominal, genitourinary, and gastroin-
Most cases of bridging bronchus have been testinal malformations are also frequently associ-
reported in association with LPAS. Bridging ated, as well as airway stenosis or bronchomalacia
bronchus has been reported in 52%–78% of (63,64). In bridging bronchus type 2, the right
patients with LPAS, and the association has been lung is frequently hypoplastic (17).
termed “left pulmonary artery sling type II” in Bridging bronchus is often but not exclusively
the classification scheme of Wells et al (7,17). In discovered in infants. Patients with bridging
RG  •  Volume 36  Number 2 Chassagnon et al  371

Figure 18.  Type 2 bridging bronchus in a 14-year-old girl with chronic dyspnea and wheezing. (a) Coronal
contrast-enhanced minimum intensity projection reformatted CT image shows that the normally located
RMB is diverticular, at the level of the carina (arrow). The right lung is ventilated by a displaced RMB arising
from the LMB, forming a pseudocarina (arrowhead). (b) Three-dimensional reconstructed CT image with
superimposition of the tracheobronchial tree and pulmonary arteries shows the absence of an LPAS. (c) Three-
dimensional reconstructed CT image superimposed on a coronal reformatted image shows the pseudocarina
at the T6 level (arrowhead), with the carina remaining at the T4 level (arrow). The stenosis of the LMB explains
the patient’s wheezing.

bronchus may experience wheezing or respira- chus are often overlooked but can have important
tory distress because of tracheal and/or LMB implications, especially in cases involving surgery.
stenosis (64). These stenoses may be related to These anomalies are related to defects occurring
the presence of cartilage in the posterior wall early in fetal life and often are associated with
of the narrowed airways (cartilage rings) and/or other congenital malformations. Thus, several con-
absence of the pars membranacea (7). genital malformations such as Down syndrome,
Chest CT is an ideal diagnostic tool in diagnos- congenital heart diseases, VACTERL syndrome,
ing bridging bronchus and in searching for associ- and tracheal stenosis, as well as the presence of
ated tracheobronchial stenosis or LPAS (17,59). other tracheobronchial positional anomalies,
It allows differentiation of the various subtypes. should prompt the radiologist to search for associ-
The main differential diagnosis of type 1 bridging ated tracheobronchial branching anomalies that
bronchus is a displaced tracheal bronchus. In some may otherwise be overlooked.
cases, the CT appearance of entirely displaced right Even if most tracheobronchial branching
tracheal bronchus may mimic that of type 1 bridg- anomalies are incidentally discovered, they can
ing bronchus because of the decreased diameter also be symptomatic, especially in children,
of the trachea downstream from the origin of the leading to recurrent pneumonia, hemoptysis,
right tracheal bronchus. However, in right tracheal or dyspnea. Knowledge of several anatomic
bronchus, the carina remains at the T4-T5 level, principles, such as the eparterial position of the
compared with the T6-T7 level of the pseudoca- right ULB, hyparterial position of the left ULB,
rina in bridging bronchus. In addition, the angle and T4-T5 level of the trachea, are critical for
of the carina helps differentiate between the two recognizing these anomalies. With use of a lobe-
diagnoses: In displaced tracheal bronchus, this based classification scheme (Fig 19), congenital
angle remains normal, whereas the pseudocarina branching anomalies affecting the trachea, main
in bridging bronchus has an increased angle with bronchi, and intermediate bronchus can easily
an inverted T appearance (7). Chest CT cannot be categorized.
help determine the presence or absence of tracheal
or bronchial cartilage rings, and bronchoscopy Acknowledgment.—The authors thank John Scatarige, MD,
for English language assistance.
remains necessary in cases of stenosis (59).
References
Conclusion 1. Atwell SW. Major anomalies of the tracheobronchial tree:
Congenital branching anomalies affecting the with a list of the minor anomalies. Dis Chest 1967;52(5):
trachea, main bronchi, and intermediate bron- 611–615.
372  March-April 2016 radiographics.rsna.org

Figure 19.  Chart illustrates the lobe-based classification scheme for congenital branching anomalies affecting the trachea, main
bronchi, and intermediate bronchus.

2. McLaughlin FJ, Strieder DJ, Harris GB, Vawter GP, Eraklis 9. Read R, St Cyr J, Marek J, Whitman G, Hopeman A. Bron-
AJ. Tracheal bronchus: association with respiratory morbidity chial anomaly of the right upper lobe. Ann Thorac Surg
in childhood. J Pediatr 1985;106(5):751–755. 1990;50(6):980–981.
3. Evans JA. Aberrant bronchi and cardiovascular anomalies. Am 10. O’Sullivan BP, Frassica JJ, Rayder SM. Tracheal bronchus:
J Med Genet 1990;35(1):46–54. a cause of prolonged atelectasis in intubated children. Chest
4. Ming Z, Lin Z. Evaluation of tracheal bronchus in Chinese children 1998;113(2):537–540.
using multidetector CT. Pediatr Radiol 2007;37(12):1230–1234. 11. Ghaye B, Szapiro D, Fanchamps JM, Dondelinger RF.
5. Boyden EA. Segmental anatomy of the lungs. New York, NY: Congenital bronchial abnormalities revisited. RadioGraphics
McGraw-Hill, 1955. 2001;21(1):105–119.
6. Gonzalez-Crussi F, Padilla LM, Miller JK, Grosfeld JL. “Bridging 12. Hutchins GM, Haupt HM, Moore GW. A proposed mechanism
bronchus”: a previously undescribed airway anomaly. Am J Dis for the early development of the human tracheobronchial tree.
Child 1976;130(9):1015–1018. Anat Rec 1981;201(4):635–640.
7. Wells TR, Gwinn JL, Landing BH, Stanley P. Reconsideration of 13. Burri PH. Fetal and postnatal development of the lung. Annu
the anatomy of sling left pulmonary artery: the association of one Rev Physiol 1984;46:617–628.
form with bridging bronchus and imperforate anus―anatomic 14. Beder S, Küpeli E, Karnak D, Kayacan O. Tracheobronchial
and diagnostic aspects. J Pediatr Surg 1988;23(10):892–898. variations in Turkish population. Clin Anat 2008;21(6):
8. Oshiro Y, Murayama S, Ohta M, Teruya T. CT findings of 531–538.
a displaced left upper division bronchus in adults: its impor- 15. Doolittle AM, Mair EA. Tracheal bronchus: classification, en-
tance for performing safe left pulmonary surgery. Eur J Radiol doscopic analysis, and airway management. Otolaryngol Head
2013;82(8):1347–1352. Neck Surg 2002;126(3):240–243.
RG  •  Volume 36  Number 2 Chassagnon et al  373

16. Barat M, Konrad HR. Tracheal bronchus. Am J Otolaryngol 39. Iannaccone G, Capocaccia P, Colloridi V, Roggini M. Double
1987;8(2):118–122. right tracheal bronchus: a case report in an infant. Pediatr Radiol
17. Zhong YM, Jaffe RB, Zhu M, Gao W, Sun AM, Wang Q. CT 1983;13(3):156–158.
assessment of tracheobronchial anomaly in left pulmonary artery 40. Desir A, Ghaye B. Congenital abnormalities of intrathoracic
sling. Pediatr Radiol 2010;40(11):1755–1762. airways. Radiol Clin North Am 2009;47(2):203–225.
18. Chen SJ, Lee WJ, Wang JK, et al. Usefulness of three-dimensional 41. Papaioannou G, Young C, Owens CM. Multidetector row CT
electron beam computed tomography for evaluating tracheobron- for imaging the paediatric tracheobronchial tree. Pediatr Radiol
chial anomalies in children with congenital heart disease. Am J 2007;37(6):515–529.
Cardiol 2003;92(4):483–486. 42. Wells JA. A left eparterial bronchus and a tri-lobed left lung: a
19. Applegate KE, Goske MJ, Pierce G, Murphy D. Situs re- case report. Dis Chest 1960;37:129–131.
visited: imaging of the heterotaxy syndrome. RadioGraphics 43. Austin JH. The left minor fissure. Radiology 1986;161(2):
1999;19(4):837–852; discussion 853–854. 433–436.
20. Van Praagh R. The importance of segmental situs in the diagnosis of 44. Berkmen T, Berkmen YM, Austin JH. Accessory fissures of the
congenital heart disease. Semin Roentgenol 1985;20(3):254–271. upper lobe of the left lung: CT and plain film appearance. AJR
21. Schallert EK, Danton GH, Kardon R, Young DA. Describing Am J Roentgenol 1994;162(6):1287–1293.
congenital heart disease by using three-part segmental notation. 45. Ariyürek OM, Gülsün M, Demirkazik FB. Accessory fissures of
RadioGraphics 2013;33(2):E33–E46. the lung: evaluation by high-resolution computed tomography.
22. Calder AL. Thoracic situs as an indicator of atrial append- Eur Radiol 2001;11(12):2449–2453.
age morphology: a postmortem study of 306 specimens with 46. Boonsarngsuk V, Suwatanapongched T. Puzzling bronchial
situs solitus in 250 and heterotaxy in 56 cases. Pediatr Cardiol trifurcation. Respir Care 2011;56(8):1206–1208.
2011;32(7):875–884. 47. Adamczyk M, Tomaszewski G, Naumczyk P, Kluczewska E,
23. Fulcher AS, Turner MA. Abdominal manifestations of situs Walecki J. Usefulness of computed tomography virtual bron-
anomalies in adults. RadioGraphics 2002;22(6):1439–1456. choscopy in the evaluation of bronchi divisions. Pol J Radiol
24. Raman R, Al-Ali SY, Poole CA, Dawson BV, Carman JB, Calder 2013;78(1):30–41.
L. Isomerism of the right atrial appendages: clinical, anatomical, 48. Ghaye B, Kos X, Dondelinger RF. Accessory cardiac bronchus:
and microscopic study of a long-surviving case with asplenia and 3D CT demonstration in nine cases. Eur Radiol 1999;9(1):45–48.
ciliary abnormalities. Clin Anat 2003;16(3):269–276. 49. Lachowicz D, Trzebińska-Korniszewska A. Unusual left-side
25. Tawfik AM, Batouty NM, Zaky MM, Eladalany MA, Elmoka- bronchial anomaly [in German]. Rofo 1978;129(2):271–272.
dem AH. Polysplenia syndrome: a review of the relationship with 50. Brock RC. The anatomy of the bronchial tree. London, England:
viscero-atrial situs and the spectrum of extra-cardiac anomalies. Oxford University Press, 1946.
Surg Radiol Anat 2013;35(8):647–653. 51. Mangiulea VG, Stinghe RV. The accessory cardiac bronchus:
26. Balan A, Lazoura O, Padley SP, Rubens M, Nicol ED. Atrial bronchologic aspect and review of the literature. Dis Chest
isomerism: a pictorial review. J Cardiovasc Comput Tomogr 1968;54(5):433–436.
2012;6(2):127–136. 52. McGuinness G, Naidich DP, Garay SM, Davis AL, Boyd AD,
27. Rose V, Izukawa T, Moës CA. Syndromes of asplenia and Mizrachi HH. Accessory cardiac bronchus: CT features and
polysplenia: a review of cardiac and non-cardiac malformations clinical significance. Radiology 1993;189(2):563–566.
in 60 cases with special reference to diagnosis and prognosis. Br 53. Miyahara R, Hasegawa S, Yoshimura T, Wada H. A case of
Heart J 1975;37(8):840–852. squamous cell carcinoma arising from accessory cardiac bronchus.
28. Peoples WM, Moller JH, Edwards JE. Polysplenia: a review of Eur J Cardiothorac Surg 2002;22(2):309.
146 cases. Pediatr Cardiol 1983;4(2):129–137. 54. Leo F, Galetta D, Borri A, Spaggiari L. Segmentectomy for
29. Rémy J, Smith M, Marache P, Nuyts JP. Pathogenetic left carcinoid arising from an accessory cardiac bronchus. Eur J
tracheal bronchus: a review of the literature in connection with Cardiothorac Surg 2009;35(3):537.
four cases (author’s transl) [in French]. J Radiol Electrol Med 55. Stinghe R, Mangiulea V. An unpublished bronchial anomaly:
Nucl 1977;58(10):621–630. double cardiac accessory bronchus [in French]. Bronches
30. Holinger PH, Johnston KC, Parchet VN, Zimmermann AA. 1969;19(3):239–242.
Congenital malformations of the trachea, bronchi and lung. Ann 56. Bolla A, Zanotelli F. Considerations on simple bronchial diver-
Otol Rhinol Laryngol 1952;61(4):1159–1180. ticuli and those associated with other malformations [in French].
31. Cope R, Campbell JR, Wall M. Bilateral tracheal bronchi. J Bronches 1967;17(2):125–132.
Pediatr Surg 1986;21(5):443–444. 57. Yildiz H, Ugurel S, Soylu K, Tasar M, Somuncu I. Accessory
32. Kumagae Y, Jinguji M, Tanaka D, Nakajo M. An adult case cardiac bronchus and tracheal bronchus anomalies: CT-bron-
of bilateral true tracheal bronchi associated with hemoptysis. J choscopy and CT-bronchography findings. Surg Radiol Anat
Thorac Imaging 2006;21(4):293–295. 2006;28(6):646–649.
33. Watabnabe K, Uese K, Higuchi O, et al. Three-dimensional 58. Wooten C, Patel S, Cassidy L, et al. Variations of the tracheo-
computed tomographic findings of bilateral tracheal bronchus. bronchial tree: anatomical and clinical significance. Clin Anat
Pediatr Cardiol 2009;30(1):87–88. 2014;27(8):1223–1233.
34. Ho K, Ulualp SO, Swischuk L. Left tracheal bronchus in an 59. Baden W, Schaefer J, Kumpf M, et al. Comparison of imaging
infant with laryngeal cleft. J Bronchology Interv Pulmonol techniques in the diagnosis of bridging bronchus. Eur Respir J
2009;16(1):52–54. 2008;31(5):1125–1131.
35. Lee EY, Restrepo R, Dillman JR, Ridge CA, Hammer MR, Boiselle 60. Hawass ND, Badawi MG, al-Muzrakchi AM, et al. Horse-
PM. Imaging evaluation of pediatric trachea and bronchi: system- shoe lung: differential diagnosis. Pediatr Radiol 1990;20(8):
atic review and updates. Semin Roentgenol 2012;47(2):182–196. 580–584.
36. Panigada S, Sacco O, Girosi D, Tomà P, Rossi GA. Recurrent 61. Starshak RJ, Sty JR, Woods G, Kreitzer FV. Bridging bronchus:
severe lower respiratory tract infections in a child with abnormal a rare airway anomaly. Radiology 1981;140(1):95–96.
tracheal morphology. Pediatr Pulmonol 2009;44(2):192–194. 62. Rishavy TJ, Goretsky MJ, Langenburg SE, Klein MD. Anterior
37. Beigelman C, Howarth NR, Chartrand-Lefebvre C, Grenier P. bridging bronchus. Pediatr Pulmonol 2003;35(1):70–72.
Congenital anomalies of tracheobronchial branching patterns: 63. Topcu S, Liman ST, Sarisoy HT, Babaoglu A, Ozker E. Stenotic
spiral CT aspects in adults. Eur Radiol 1998;8(1):79–85. bridging bronchus: a very rare entity. J Thorac Cardiovasc Surg
38. Wu JW, White CS, Meyer CA, Haramati LB, Mason AC. Variant 2006;131(5):1200–1201.
bronchial anatomy: CT appearance and classification. AJR Am 64. Schnabel A, Glutig K, Vogelberg C. Bridging bronchus: a rare
J Roentgenol 1999;172(3):741–744. cause of recurrent wheezy bronchitis. BMC Pediatr 2012;12:110.

TM
This journal-based SA-CME activity has been approved for AMA PRA Category 1 Credit . See www.rsna.org/education/search/RG.

You might also like