OUR SURGICAL HERITAGE
Evolution of Pulmonary Resection Techniques and
Review of the Bronchus-First Method
Jerome T. Grismer, MD, and Raymond C. Read,
University of Arkansas for Medical Sciences, Little Rock, Arkansas
The dissection technique of pulmonary resection evolved
in the period 1930 to 1950. Surgeons had to cope with the
location of disease, bronchiectasis, tuberculosis, and lung
cancer, as well as associated bronchial secretions, hilar
pathology, and the status of anesthesiology. Two basic
hilar dissection methods emerged, the anterior vessel-
first sequence and the posterior bronchus-first method.
The bronchus-first method is particularly suitable for
t the beginning of the 20th century, thoracic surgery
A was in its infancy, in 1898, Murphy identified the
major p u l m o n a r y problems a m e n a b l e to operation as
suppurative bronchiectasis, e m p y e m a , lung abscess and
tuberculosis. Lung cancer was relatively rare. He, Mey-
ers, Robinson, and others initiated animal research to
explore techniques for p u l m o n a r y resection. These pio-
neer thoracic surgeons faced many hazards, which would
be c o n q u e r e d in parallel fashion with advances in under-
standing of anesthesia, cardiopulmonary pathophysiol-
ogy, and antibiotics.
In their efforts to r e m o v e suppurative bronchiectasis,
pioneer surgeons could not duplicate the successful tech-
niques of the animal laborato D' I1]. Two major problems
existed: preoperative and operative m a n a g e m e n t of the
patient's copious foul infected sputum and intraoperative
vascular control in the extensively diseased hilum. Rob-
inson, in his presidential address to the American Asso-
ciation of Thoracic Surgeons (1923), graphically cited his
experience [2]:
The patient is placed on the operating table. The posture
is uncomfortable. There may be cyanosis. It induces
coughing. The anesthetist is greeted bv an evacuation of a
large amount of pungent, purulent sputum, incident to
the posture on the table. The whole bronchial tree may be
filled with this material as the anesthetist begins. If
regional blocking and paravertebral procainization is car~
ried out, the pleura is no sooner opened and traction on
the diaphragm commenced than the need of general
anesthesia is obvious. As the secretions well toward the
trachea, the cyanosis increases. The lower lobe obsti-
nately resists being delivered; the pleural adhesions are
strong and wide spread; the attachments to the dia-
phragm are ropelike and tenacious. Finger dissection is
inadequate. Work with the knife and scissors are blind.
Cleavages are sought in vain. ]'he pericardium is danger-
ously involved in the adhesions. Meanwhile, the patient's
Address reprint requests to Dr (;risnler. \ eterans Affairs Medical Ccntt'l,
(14A-NLR),2200 Fort Roots Dr, Norlh Little Rock, AIR 72114.
© 1995 by The Society ot Thuraci¢ Sur~eoll,
MD
p n e u m o n e c t o m y , right upper lobectomy, and posterior-
apical s e g m e n t e c t o m y of this lobe as well as ease of
l y m p h node removal. This technique, as a primary
method of lung resection, does not appear to be empha-
sized in teaching curricula and supporting atlases or
texts.
(Ann Thorac Surg I995;60:1133-7)
condition may become distressing and perhaps alarming.
If open pneumothorax is adding insult to injury, the lung
cannot be used to plug the thoracic gap, because the lobe
is not deliverable. If differential pressure is being em-
ployed, that too may be acting badly. The mucopurulent
secretion may interfere with proper intratracheal air in-
sufflation. It interferes with the respiration under positive
pressure. There mav be cyanosis, even with the head
outside the negative pressure cabinet. And then the
difficulties multiply. The complete liberation at one sitting
may have to be abandoned. There is bleeding and infec-
tious leakage from the lung, and bleeding from the
diaphragm. Tight closure of the chest without drainage
seems inadvisable under these conditions, and yet neces-
sary to aw}id the ills of postoperative pneumothorax.
Suddenly, it is obviously time to return the patient to his
bed. Not much has been accomplished.
Surgeons then devised staged procedures in an effort to
control bronchial secretions, aspiration, hemorrhage, op-
erative shock, mediastinal and pleural infections, pne u-
mothorax, and bronchopleural fistula 13]. In 1929, Brunn
141 successfully advanced to " t h e ultimate goal in surgical
procedures on the chest": the single-stage lung resection.
He used the T r e n d e l e n b e r g position to "favor drainage,"
local anesthesia, and "positive pressure with gas and
o x y g e n . . . ," and " t h e patient is adjured not to c o u g h "
during the lobectomy. Through a posterolateral incision,
he obtained initial proximal vascular control of the lower
lobe pedicle using extramediastinal multiclamp hilar occlu-
sion. He then p er f o r m ed mass ligation, and amputation
of the involved lower lobe at the level of the segmental
bronchi. He e m p h a s i z e d postoperative catheter drainage
of the residual pleural space (7 patients, 1 death).
Another advance in single-stage resection took place in
1932: Shenstone and Janes [5] introduced the hilar tour-
niquet. " W i t h o u t devitalization of the tissues, it controls
the blood supply, obstructs the bronchi, and provides a
solid support during suture of the pedicle." They e m p h a -
sized preoperative postural drainage with coughing to
aw~id intraoperative "flooding of the sound lung by the
0003-4975•95•59.50
SSDI 0003-4975(95)00602-H
1134 ttERITAGE GRISMER AND R I A I )
EVOLUTION OF BRONCHLIS-FIRSI It:C~INIQLE
secretions from the diseased side" and noted the use by
others of "two p r e p a r a t o r y m e a s u r e s " (pneumothorax
and bronchial lavage) to decrease intraoperative down-
lung flooding with infected sputum. Nevertheless, post-
operative contralateral p n e u m o n i a attributed to this fac-
tor did develop in 3 patients (17 patients, 2 deaths). The
tourniquet m e t h o d also a m p u t a t e d the lobar lung tissue
distal to the bifurcation of the segmental bronchi without
o p e n i n g the mediastinal compartment. This site avoided
mediastinal dissection and r e d u c e d intraoperative hem-
orrhage along with postoperative complications of medi-
astinitis and b r o n c h o p [ e u r a l fistula. The t o u r n i q u e t
m e t h o d b e c a m e the " n e w " standard in this period of
resection for infected lung problems. Individual hilar
dissection was thwarted by inflamed hilar structures and
massive l y m p h a d e n o p a t h y .
The technique of one-stage resection used a postero-
lateral incision. This incision and the patient's lateral
position forced the surgeons and anesthesiologists to
concentrate on the p r o b l e m of intraoperafive spillage of
infected bronchial secretions into the down lung [6].
Efforts b e c a m e focused on control of the bronchus as the
first step in the technique of lung resection. Methods
were e m p l o y e d to occlude the bronchus, either by cuffed
endotracheal tubes, transoral intrabronchial tamponade,
or by posterior hilar dissection and tempora~ ligation or
external compression of the bronchus "at the earliest opportu-
nity" [71. Surgeons also evolved various operative posi-
tions, ie, the T r e n d e l e n b e r g position bv Brunn (1929), the
45-degree supine position of Rienhoff (1933), and (1940)
T r u m b l e ' s prone position as refined bv Overholt (1948).
Jeger's d e v e l o p m e n t in 1912 of a balloon-cuffed double-
lumen endotracheal tube would lie d o r m a n t until Car-
lens i n d e p e n d e n t l y d e v e l o p e d a similar prosthesis for
b r o n c h o s p i r o m e t r y in 1949 [8]. In 1950, Bjark's use of
C a r l e n ' s tube to control secretions i n t r a o p e r a t i v e l y
would prove to be the most effective method [91.
In noninfected neoplastic diseases, the surgeon was not
confronted with the p r o b l e m of spillage or the inflammed
hilum. Vascular control was a p p r o a c h e d directly. In 1912,
Davies d e m o n s t r a t e d the feasibility of Mever's experi-
mental method of single-stage vessel first hilar dissec-
tion. By lateral thoracotomy, he resected a right lower
lobe for cancer. The patient died unexpectedly on the 8th
postoperative day. Churchill [10l in 1933 was the first to
follow successfully Davies's 1912 technique of [obectomy
for cancer. He r e p o r t e d t w o one-stage resections (right
lower and middle lobes, right lower lobe) using arterial,
venous, and then bronchial amputation. Young in 1934
m a y have been the first to use the hilar dissection
vessel-first sequence in left u p p e r Iobectomv for cancer.
G r a h a m and Singer [11] in 1933 performed the first
successful one-stage p n e u m o n e c t o m y for cancer using
the "'proven" hilar tourniquet a m p u t a t i o n method. Two
months later, Rienhoff, employing an anterior thoracot-
omy, would be the first to use individual hilar vessel-first
dissection to resect the lung for cancer. Rienhoff, a skilled
general surgeon, was not k n o w l e d g e a b l e of or guided bv
the literature on the multistage approach for suppurative
diseases or with tourniquet treatment of the hilum [12].
Ann Thorac Surg
1995;60:1133 7
His s u b s e q u e n t article detailing preoperative m a n a g e -
ment p r e s e n t e d specific drawings of the operative tech-
nique [131. He, however, did not a d d r e s s the issue of
bronchial secretions. Rienhoff's p r o c e d u r e revolutionized
the thinking on surgical a p p r o a c h and dissection. In 1934,
Heur and Archibald noted that in "tumors of the bronchi
and lungs" the absence of major hilar p a t h o l o g y p e r m i t -
ted "in the direct and obvious w a y " hilar dissection in
one-stage Iobectomy and p n e u m o n e c t o m y . In the ab-
sence of infection, Overholt preferred Rienhoff's anterior
m e t h o d for p n e u m o n e c t o m y . He noted in 3937, "The
advantages of the dissection of the hilum are that (1) the
main bronchus can be divided closer to the carina; (2) the
mediastinal glands can be removed; (3) there is less
danger of h e m o r r h a g e . . . ; (4)... the d a n g e r of express-
ing infectious material into the contralateral lung is
greatly reduced . . . . "
Crafoord 1141 in 1938 p r o p o s e d a different a p p r o a c h to
down lung bronchial spillage a n d vascular control. He
advocated posterior mediastinal dissection and division
rather than t e m p o r a r y ligation of the bronchus before
dissection of the vessels. Crafoord m a y have d e v e l o p e d
this posterior hilar technique from his awareness of
European literature as d e s c r i b e d by O ' S h a u g h n e s s y
(1935). Crafoord stated, " M y p u r p o s e in this investigation
has been to work out an advantageous technique for
p n e u m o n e c t o m y in man. I have analyzed all p n e u m o -
nectomies on dogs and man in the available literature
and have c o m p a r e d the results with my own clinical
findings." Crafoord wished to identify the reason for the
high mortality and m o r b i d i t y from p n e u m o n e c t o m y . He
noted that 105 cases had been reported from 1931 to 1938,
about equally divided between cancer and bronchiectasis
in 91 completely r e p o r t e d cases. Six patients died of
a s p i r a t i o n of s e c r e t i o n s into the r e m a i n i n g lung.
Crafoord reported on 16 of his patients. In the first 8
patients, by lateral thoracotomy, he used the s t a n d a r d
vessel-first hilar dissection technique: p o s t o p e r a t i v e
complications d e v e l o p e d in 7, a n d 6 died. Crafoord was
well aware of Giertz's principles of endotracheal anes-
thesia. A i d e d by Frenker, an anesthesiologist, Crafoord
designed an internal bronchial t a m p o n a d e , which was
inserted before thoracotomy to obstruct secretions from
the involved lung. Based on this experience a n d exten-
sive autopsy dissections of the vessels, bronchi, and
lymph nodes, Crafoord devised the posterior hilar dis-
section bronchus-first method. By an extensive postero-
lateral incision, he resected the lung in the next 8 patients
(5 survivors). He s u m m a r i z e d his experience: "[it] . . . has
convinced me that total extirpation of a lung is m a r k e d l y
facilitated by free dissection of the main bronchus and
division and disposal of it before the large vessels are
cut." He noted that traction on the bronchial s t u m p
i m p r o v e d the dissection and visualization of the main
p u h n o n a r y artery and the inclusion in the dissection of
the s u r r o u n d i n g nodal c o m p o n e n t s in the hilum. He also
noted the ability to resect the pericardial sac a n d perform
intrapericardial ligation of the vessels. His article had
manv p h o t o g r a p h s and drawings of the procedure.
Crafoord's bronchus first a p p r o a c h had an initial but
A n n Thorac Surg
1995;60:1133-7
limited impact. In 1938, before Crafoord's article, Over-
holt's s u m m a r y of the literature regarding techniques of
lobectomy and p n e u m o n e c t o m y did not mention the
bronchus-first technique. The next year, he wrote that, in
select circumstances, he divided the riy,ht main bronchus bejbre
the artery and veins. On the h~ft, he isolated arid divided the h'fi
bronchus after the artery and before securing the veins. Over-
holt, however, still preferred the a r t e r y - v e i n - b r o n c h u s
sequence. Ochsner and DeBakey (1939) applied Crafoord's
posterolateral incision and posterior hilar bronchus-first
division as well as Rienhoff's anterior technique. Later,
in their series of 19 patients (1940), they wrote that they
p r e f e r r e d Rienhoff's approach as it was less traumatic
than the posterolateral incision of Crafoord for the bron-
chus-first technique of p n e u m o n e c t o m y [15].
In isolated case reports in the 1940 to 1960 era, Brown,
Cahan, and other surgeons reported their use of the
bronchus-first m e t h o d [16, 17]. Cahan noted that, after
division of the bronchus, access was facilitated to the
subcarinal nodes a n d the nodes between the bronchus
and artery especially in bulky tumors of the u p p e r lobes.
It is noteworthy that although the prone position became
established to control bronchial secretions in 1945 and
offered easy access to control of the main bronchus,
Overholt and other surgeons still p r o c e e d e d with the
vessel-first dissection. In the 1940s, the operative treat-
m e n t for lobectomy evolved to individual hilar dissec-
tion. Anatomically, resection of the lower lobes was best
suited to a vessel-first individual hilar dissection [18[. For
bronchiectasis, with the use of antibiotics, the vessel-first
sequence prevailed over tourniquet resection [191. To
prevent septic emboli, Kent reiterated Brunn's concept,
p r o m o t e d in 1929, of division of the veins before the
artery. Later, surgeons p r o m o t e d this sequence to pre-
vent t u m o r emboli. M e a d e [12] credits Blades and Kent
with popularization of individual vessel-first hilar dissec-
tion for s u p p u r a t i v e diseases.
A concerted attack to cure tuberculosis by p u l m o n a r y
resection began in the early 1940s [20]. The vessel-first
hilar dissection m e t h o d quickly became the standard.
Although surgeons practiced early bronchial occlusion to
p r e v e n t spillage, the bronchus-first amputation sequence
was not strongly advocated in this time period. Cham-
berlain and McNeill [21] described ligation and division
of the bronchus for u p p e r lobe cavitation not a m e n a b l e to
resection in 1960. Churchill and Belsey's introduction of
s e g m e n t e c t o m y for bronchiectasis (1937) p a v e d the way
for conservative resection in tuberculosis and bronchiec-
tasis. Overholt in 1947 described and d i a g r a m e d the
vessel-first, bronchus-last m e t h o d to all types of segmen-
tectomy. Overholt's extensive articles on s e g m e n t e c t o m y
p o p u l a r i z e d this sequence.
C h a m b e r l a i n b e c a m e the m o d e r n p r o p o n e n t of the
posterior hilar dissection and bronchus-first a m p u t a t i o n
for p n e u m o n e c t o m y , right u p p e r lobectomy, and seg-
m e n t e c t o m y even though Rubenstein (1949) may have
p r e c e d e d him in performing s e g m e n t e c t o m y by dividing
the b r o n c h u s before the vessels. C h a m b e r l a i n a n d
Finnerty [22] first advocated the bronchus-first method
for s e g m e n t e c t o m y in 1949. They e m p h a s i z e d that the
HERITAGE GRISMER AND READ 1135
EVOLUTION OF BRONCHUS-FIRST TECHNIQUE
first objective was the identification a n d isolation of the
bronchus serving the diseased segment, which was di-
vided before the blood vessels. In discussion of Cahan
and W a t s o n ' s article [17] in 1950, he noted his use of this
sequence in p n e u m o n e c t o m y .
In lower lobectomy, C h a m b e r l a i n used a modification
of his posterior a p p r o a c h dissection. In stepwise dissec-
tion, he, ligated the superior segmental vein, a m p u t a t e d
the superior segmental bronchus, ligated the superior
s e g m e n t arterial branches, and then dissected a n d am-
putated the lower lobe bronchus before the other vessels.
A noted European surgeon c o m m e n t e d to one of us
(R.C.R.) that he saw Chamberlain, in resecting the lower
lobe in this manner, transect the right m i d d l e lobe
bronchus. Unfazed, he reattached the b r o n c h u s a n d
continued the operation.
C h a m b e r l a i n e m p h a s i z e d the term "bronchus-first."
His n u m e r o u s articles contained few descriptions or
drawings. Even though respected for his technical ability,
C h a m b e r l a i n ' s influence on dissection techniques ulti-
mately proved limited.
In video-assisted thoracoscopic surgery, Kirby a n d
Birnbaum [23] in 1993 u n d e r s c o r e d the value of the
posterior hilar, bronchus-first a p p r o a c h to nodal a n d
vessel dissection in right u p p e r lobectomy. Doctor Kirby
indicated that Dr Paulson had taught him this m e t h o d
during residency in 1970 (personal communication). Doc-
tor Paulson occasionally used the p r o c e d u r e in concert
with Dr Shaw in their operations on patients in the prone
position (personal communication).
The decades of the 1930s and 1940s were crucial in the
evolution from mass ligation and tourniquet m e t h o d s to
individual hilar dissection. The s u r g e o n s ' a p p r o a c h to
hilar dissection r e m a i n e d consistent with their resection
of other organs (Meyers, 1910; Rienhoff, 1936; Hyed,
1941): to prevent h e m o r r h a g e and control vascular struc-
tures before " o r g a n " (lung) removal b y a m p u t a t i o n of
the bronchus. However, they practiced posterior hilar
dissection with early clamping of the main bronchus to
control secretions. Surgeons tried but did not accept or
extend Crafoord's unique continuation of this posterior
hilar dissection to a m p u t a t e the bronchus before vascular
control. Also, the fear of i n t r a p u l m o n a r y shunting a n d
desaturation m a d e anesthesiologists and surgeons hesi-
tant to discontinue ventilation to the o p e r a t e d lung by
a m p u t a t i n g the bronchus before the vessels [9]. In our
experience, this theoretic objection has not been a p r o b -
lem. Finally, by 1950 and b e y o n d in the periodicals,
cardiac surge D , d o m i n a t e d discussion of technical pro-
cesses in thoracic surgery.
Few texts d e s c r i b e d the bronchus-first approach. In the
1950 book Teclmiques in British Surgery, Sellors [24] b e a u -
tifully describes the bronchus-first sequence for p n e u -
monectomy. Cooper's atlas, The Craft of Surgery (1966 a n d
1971), contained C h a m b e r l a i n ' s classic article, his illus-
tn~ted description of bronchus-first p n e u m o n e c t o m y a n d
lobectomy [25]. In juxtaposition to C h a m b e r l a i n ' s 1971
chapter is Mayer's chapter on "vessel-first" dissection,
in which he criticizes the bronchus-first sequence as an
1136 HERITAGE GRISMER ANI) RIAI)
EVOI U~IION OF B R O N C ! I U S - H R S I I I Z t t N I Q L t
Fi,~,, 1. The instrunlcnt is first pointed dowm('ard ,rod thcH rotated 45
de~rees toward the imh'.~ fin.\~cr. (Rein'tilted witil t,vrmi>si(,t .fir(,tl
The Craft of Surgery by P. Cooper, ~.) 1971. Pubti*hcd tpV 1 #tic,
Brown, and Companq,;
"intractable" c o m m i t m e n t to resectitm ]26]. Maver max
well have w)iced the perception of most thoracic sur-
geons.
We reviewed 80 other available thoracic or cardiotho-
racic texts and atlases from 1950 to 1994. Many old and
recent texts mention but do not illustrate the early
isolation and occlusion of tile bronchus to control secre-
tions. As noted, few described or illustrated the bron-
chus-first technique. Academic writers may not consider
the bronchus-first approach as the primary method. In
our survey of directors of the 93 accredited Fhoracic
Surgery programs, 62 (66.3",) replied. All indicated that
they taught the vessel-first technique for right upper
lobectonly and pneumonectoray. We surmise that as a
primary technique, the teaching and use of the bronchus-
first method for resection never became a potent factor in
training within the United States. Experienced surgeons
recognize its value and use the method in specific cases
[27].
We agree with Crafoord, Chamberlain, and others that
the bronchus-first method provides advantages in select
lung resections, especially in removal of lymph nodes
and exposure of the vessels. Since 1966, we have taught
its use as the first choice under most circumstances in
resection of the right upper lobe, select segmentectomies,
or p n e u m o n e c t o m y . Doctor Read, while in residency at
the University of Minnesota, learned the technique from
Dr Coleman Connollv. Connollv credits his knowledge of
it from training at the Mayo Clinic in the 1950s.
We employ o n e - l u n g anesthesia, which facilitates the
posterior hilar dissection and assessment of the shunt
fraction. Careful examination of the hilar structures ob-
viates Mayer's concern of an "intractable" commitment.
In our experience, the advantages of the bronchus-first
Ann Thorac Surg
I995;60:1133-7
method are dissection of the bronchus and exposure of
the blood vessels, removal of the lymph nodes, and
sequence.
Dissection of the Bronchus and Exposure of the
Blood Vessels
Traction on the distal bronchial stump facilitates expo-
sure of the vessels in right or left p n e u m o n e c t o m y , in
right upper lobectomy, or in right apical-posterior seg-
mentectomv (Figs 1, 2). As Ginsberg stated in 1990, "By
lifting the distal bronchial stump an unusually easy
exposure of the main p u l m o n a r y arter 7 is obtained. By
these maneuvers, the surgeon is not forced to ligate the
artery in the deep well formed by the superior vena cava
anteriorly, the bronchus posteriorly, and the azygos vein
superiorly. Obviously, a clear opinion as to the resect-
ability in a patient who can tolerate the perfusion of the
nonventilated lung for a limited period of time must have
been weighed faw)rably before embarking on this ap-
proach" [281.
Removal of the Lymph Nodes
Amputation of the bronchus discloses nodal clusters in
peritracheobronchial tissue and pericardial fibrous "'en-
velnpes" ahmg the main pulmonary artery,, its branches,
and in proximity to nodal tissue between branches of the
superior p u l m o n a r y vein (Fig 3). Milloy and associates
[29] (1963) beautifully portrayed this anatomy of the right
upper lobe and the arterial branch relationships after
amputation of the bronchus and traction on the distal
bronchial stump.
.. t i~" PERIVaSCULAR
" tt -" S H E A T H ENCLOSING
o7~..~,~ ~" PU LMO,NARY ARTERY
~BRONCHUS
,!
PROXIMAL
t i~ 2. Thc t,uh,onary artery is well pn#ected by its perivascular
qlc,lth durillX t~eribronchial instrumentation. Small trianyylar
( lamps arc u~ed to occlude and protect the dishfl end qf the divided
t,om /1us. ¢Rcpriutcd with permission .from The Craft of Surgery.
t,v P. Coopcp; Q 1971. Published bV Litth,, Brown, and Company.)
Ann ]horac Surg HERITAGE GRISMERAND READ 1137
1995;60:1133 7 EVOLUTION OF BRONCHUS-FIRST TECHNIQUE

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