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DOI: 10.1016/S0003-4975(10)63596-5 1978;25:491-499 Ann Thorac
Surg
John R. Hankins, John E. Miller and Joseph S. McLaughlin
Experience with 21 Patients
The Use of Chest Wall Muscle Flaps to Close Bronchopleural
Fistulas:
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ORIGINAL ARTICLES
The Use of Chest Wall Muscle Flaps to Close Bronchopleural
Fistulas: Experience with 21 Patients John R. Hankins, M.D., John
E. Miller, M.D., and Joseph S . McLaughlin, M.D.
ABSTRACT Nineteen patients with bronchopleural fistulas
associated with tuberculosis and 2 patients with fistulas following
resection for bronchiectasis underwent closure of the fistulas with
pedicled flaps of chest wall muscle. The muscle grafting was com-
bined with a limited thoracoplasty in 13 patients. The initial
myoplasty produced prompt fistula clo- sure in 15 patients and
delayed closure in 2 others. A repeat myoplasty was successful in 2
patients in whom the initial myoplasty failed. Compared with other
methods of treating bronchopleural fistulas used during the same
period, muscle grafting carried a higher rate of successful fistula
closure and a lower mortality rate.
A number of techniques have been advocated to control persistent
bronchopleural fistulas. Scarifying agents, radium implants,
cauteriza- tion, packing, and inversion with pursestring suture
have all been used with varying degrees of success [5,7]. Pedicled
flaps or grafts of chest wall muscle (myoplasties) were introduced
by Abrashanoff [ll in 1911 and have proved to be an effective means
of closing such fistulas. This report describes our experience over
a 13-year period with the treatment of persistent bron- chopleural
fistulas by myoplasty.
Material and Methods
Twenty-one patients with bronchopleural fis- tulas underwent a
total of 23 muscle flap proce- dures at the Thoracic Surgical
Services of the Mt. Wilson State Hospital for Pulmonary Dis- ease
and the University of Maryland Hospital from 1963 to 1976. These
patients ranged from 19 to 64 years old with a median age of 48
years. Thirteen were white and 8 were black; there were 12 men and
9 women.
From the Division of Thoracic and Cardiovascular Surgery,
University of Maryland School of Medicine, Baltimore, MD.
Presented at the Twenty-fourth Annual Meeting of the Southern
Thoracic Surgical Association, Nov 3-5, 1977, Marco Island, FL.
Address reprint requests to Dr. Hankins, University of Maryland
Hospital, Baltimore, MD 21201.
Nineteen patients had active pulmonary tuberculosis (Table 1). A
fistula developed fol- lowing pulmonary resection in 15 of these 19
patients. The following types of resection were employed:
pneumonectomy in 1 patient, lobec- tomy in 4, bilobectomy in 1,
lobectomy plus segmental or wedge resection in 6, segmental
resection in 2, and subsegmental resection in 1. For 7 of these
patients, sputum cultures were positive for Mycobacterium
tuberculosis at the time of resection. Bronchopleural fistula and
empyema from spontaneous rupture of tubercu- lous cavities into the
pleural space developed in 2 patients. Initial treatment,
consisting of pleuropneumonectomy in 1 of these patients and
decortication in the other, failed to resolve these fistulas. One
patient was admitted with a fistula after having undergone rib
resection and later decortication at another hospital for an
empyema in which the underlying tuberculous cause was not
suspected. In the remaining pa- tient a fistula developed that was
accompanied by sputum positive for M . tuberculosis 21 years after
a Lucite sphere plombage. She had been asymptomatic for more than
20 years.
In 2 patients who formerly had had tuber- culosis but in whom
the disease was no longer active, the fistula occurred following
pulmo- nary resection for posttuberculosis bronchiec- tasis. These
resections were lobectomy plus segmental resection in 1 patient and
segmental resection in the other.
Among the 17 patients in whom the time of onset of the fistula
could be determined accu- rately, the interval between onset and
myo- plasty ranged from just under 3 months to 10 years, with the
median interval being 6 months. The time interval was difficult to
de- termine in 4 patients in whom fistulas de- veloped before they
were admitted to our in- stitutions.
Preoperative Evaluation and Preparation Specimens were taken
from the empyema space, and cultures for M . tuberculosis,
fungi,
491 0003-497517810025-0602$1.25 @ 1978 by John R. Hankins
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492 The Annals of Thoracic Surgery Vol25 No 6 June 1978
Table 1 . Underlying Disease or Condition Associated with
Bronchopleural Fistula in 21 Patients
Disorder No. of Patients
Tuberculosis Resection Decortica tion Plombage Intrapleural
cavity
rupture Bronchiectasis
Resection
19 15a 1 1 2
2b
"The following types of resection were performed in these
patients: pneumonectomy in 1, lobectomy in 4, bilobec- tomy in 1,
lobectomy plus segmental or wedge resection in 6, segmental
resection in 2, and subsegmental resection in 1.
patient underwent lobectomy plus segmental resec- tion and the
other, segmental resection.
and pyogenic organisms were grown. In 3 pa- tients M.
tuberculosis was grown from the em- pyema fluid. Sensitivity
studies indicated the need for a change in the antimicrobial
regimen before an attempt was made to close the fistula.
Sensitivity to antibiotics also was determined for the pyogenic
organisms found in the cavities, and appropriate antimicrobial
agents instituted. Pseudomonas aeruginosa, Proteus, and
Staphylococcus were among the more frequent organisms
encountered.
Bronchoscopy was routinely performed to rule out tuberculous
endobronchitis and to check for excessive length of the bronchial
stump.
Sinograms were made for the majority of the patients to confirm
the diagnosis of fistula, to identify the offending bronchus, and
to deter- mine the size and adequacy of dependent drainage of the
empyema cavity.
Bronchography was not routine. At times it provided useful
information about the length and condition of the bronchus giving
rise to the fistula or about the remainder of the bronchial tree in
the affected lobe or lung.
Pulmonary function tests were carried out when possible. At
times it was necessary to temporarily occlude the cutaneous opening
of the fistula to obtain accurate spirometry. Poor
pulmonary function was an indication to avoid thoracoplasty if
possible or at least to limit the number of ribs that were removed
in conjunc- tion with the myoplasty.
Myoplasty was not considered an emergency procedure. It was
performed only when the ac- tive infection in the cavity was under
control and the patient was in optimal nutritional con- dition.
Operative Management The presence of a fistula creates special
prob- lems for the anesthesiologist. The loss of anes- thetic gases
and oxygen through the fistula and drainage of infected material
from the em- pyema cavity through the fistula into the de- pendent
part of the tracheobronchial tree con- stitute real hazards.
Although there are some advantages in the use of double-lumen endo-
tracheal tubes, these have the disadvantages of being difficult to
position accurately and of hav- ing such narrow lumens that thick
secretions cannot be readily removed through them. We prefer to
occlude the fistula by tight gauze pack- ing of the sinus tract
during the initial stages of the procedure. After the sinus tract
has been dissected down to the bronchus, the latter can be occluded
by temporary sutures. In this way a single-lumen endotracheal tube
can be used with impunity in most instances.
In the majority of patients in this series, the operative
approach was simply a reopening of the previously made
posterolateral thora- cotomy. When a thoracoplasty was to be in-
cluded with the myoplasty, the posterior end of the incision was
extended cephalad almost to the level of the first rib. If it was
anticipated that the pectoralis major or pectoralis minor muscle
would be used, the incision was extended an- teriorly.
The incision was developed through the ex- tracostal muscles
down to the ribs. The fistula tract was excised from the skin
opening down to the point where the tract passed through an
intercostal space. When a thoracoplasty was performed, the upper 3,
4, or 5 ribs were re- sected subperiosteally, the number being de-
termined by the size of the empyema space as shown on the sinogram
(Table 2). A thoraco- plasty concomitant with myoplasty was
per-
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493 Hankins, Miller, and McLaughlin: Chest Wall Muscle Flaps to
Close Bronchopleural Fistulas
Table 2 . lndications for Myoplasty in 21 Patients I ) , I '
Indication No. of Patients
Failure of previous thoracoplasty
Anticipated thoracoplasty failure
To obviate thoracoplasty
5
11
5
Table 3 . Thoracoplasty or Unroofing of Empyema Performed in
Conjunction with 23 Myoplasties
Procedure No. of Procedures
Limited, first-stage 11
Second-stage thoracoplasty 3
Unroofing (removal of short 9a
thoracoplasty
(after previous thoracoplasty)
segments, 1 to 3 ribs) ~ ~~ ~
"Performed because of thoracoplasty failure in 4 instances and
to obviate thoracoplasty in 5 instances.
formed in 11 patients (Table 3). In resecting these ribs, great
care was taken to preserve at least two intercostal muscles and
their asso- ciated intercostal vessels for use as pedicled grafts
(Fig 1). The periosteum from the ribs on either side and the
underlying parietal pleura were left on the muscles to help ensure
integrity of the intercostal vessels. Each muscle was di- vided
anteriorly near the costochondral junc- tion and thus remained
based on a posterior pedicle. In patients in whom a thoracoplasty
had been performed previously and in those in whom a thoracoplasty
was to be avoided, short segments of 1 to 3 ribs overlying the
empyema cavity were resected to unroof it. In these situa- tions
the intercostal muscles on either side of the resected ribs were
again preserved for use as grafts.
The empyema cavity was thoroughly exposed and unroofed, but
extensive mobilization of the surrounding lung was avoided to
prevent seri- ous air leakage. The cavity was cleansed of any
necrotic or purulent material and the infected granulation tissue
lining was removed by curet- tage.
Fig I. Method of developing and transferring to the bronchus an
intercostal muscle graft.
The bronchus from which the fistula origi- nated was dissected
away from the wall of the empyema cavity and, where possible, up to
the main airway from which it originated-that is, to the trachea in
the case of a postpneumonec- tomy fistula or to the main bronchus
for a post- lobectomy fistula. An excessively long bron- chial
stump, even though securely sutured, predisposes to recurrence.
After reamputation, the bronchus was closed with interrupted
nonabsorbable sutures.
The muscle flap was tacked over the stump using the ends of the
bronchial closure sutures passed through the flap, plus additional
tacking sutures around the edges as indicated (Fig 2). Finally, the
muscle graft was sutured to the walls of the empyema cavity to
ensure that it would remain in place and fill the cavity as
completely as possible.
It was possible to carry out the foregoing technique-that is,
dissection of the bronchus with or without reamputation, followed
by su- ture closure and muscle flap reinforcement of the closure-in
14 of the 23 myoplasties, or in 12 of the 21 patients (Table 4). In
3 patients it was not possible to dissect the bronchus suf-
ficiently to allow suture closure, either because too short a stump
remained or because of dense scarring. In these instances, the
muscle graft was sutured to the stoma of the bronchus with
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494 The Annals of Thoracic Surgery Vol 25 No 6 June 1978
Fig 2 . Technique of suture closure and muscle f l a p coverage
used when the bronchial stump can be dis- sected. lnset shows
cross-sectional view.
interrupted sutures in such a way as to occlude it (Fig 3).
In 4 other patients the bronchial fistulas were multiple, in
some instances resembling a sieve. Here a combination of the two
methods was used. The larger openings were closed by suture and
then covered by the muscle flap, while the smaller ones were
occluded by tack- ing the same flap over them. In 1 patient who had
had a prolonged air leak in association with an empyema, the
fistula could not be found after the empyema cavity was opened. The
fis- tula also could not be located in a patient with
postpneumonectomy empyema, although the preoperative bronchogram
had clearly demon- strated one. The cavity in both patients was
simply filled with the muscle flap.
Table 4 . Method of Management of Bronchus in 23 Myoplasties
No. of Method Procedures
Suture closure plus covering 14 with muscle flap
bronchus Flap sutured over open 3
Combination procedurea 4 Fistulous opening not 2
located (muscle used to fill empyema cavity)
~ ~
aMultiple fistulas present: some sutured closed then cov- ered
with flap, others simply covered with flap.
It is essential that the muscle flap completely fill the empyema
cavity. If one or two intercos- tal muscle grafts did not suffice,
then other muscles in the vicinity of the thoracotomy, such as
serratus anterior, latissimus dorsi, or sacro- spinalis, were used
(Table 5). The muscle that is
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495 Hankins, Miller, and McLaughlin: Chest Wall Muscle Flaps to
Close Bronchopleural Fistulas
Fig 3 . Technique of occluding the open bronchus wi th the
muscle f lap , used when the bronchus cannot be dis- sected
sufficiently for direct suture closure. Inset shows cross-sectional
v i e w .
used must have an adequate blood supply and sufficient length to
reach the fistula without tension. To allow for a certain amount of
shrink- age and contracture, we believe that the length of the flap
should be at least four times its width. In this series intercostal
muscle alone was used in 14 operations and a combination of
intercostal and extracostal muscles in 5 others. In 4 myoplasties
the intercostal muscles could not be used because of excessive
scarring, and extracostal muscles alone were used. One drainage
tube was left within the empyema cav- ity but superficial to the
graft. If a thoracoplasty was performed in conjunction with the
myo- plasty, the second tube was left in the subscapu-
I
(,
Table 5 . Types of Muscle Used in 23 Myoplasties ~~
Type of Muscle Used No. of Procedures
Intercostal muscles only 14
Both intercostal and 5 Extracostal muscles only 4
extracostal muscles
lar space. If extensive dissection of the lung was required, the
second tube was left intrapleu- rally. Air leakage from the chest
tubes continued for at least several days postoperatively in nearly
all patients and was assumed to be due to superficial tears in the
lung resulting from the dissection. In 1 patient the air leak con-
tinued for more than 3 months but eventually ceased. Drainage of
exudate from the tube that had been left in the empyema cavity
declined
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496 The Annals of Thoracic Surgery Vol 25 No 6 June 1978
Table 6 . Results of 23 Myoplasties in 21 Patients
Outcome No. of Patients
Successful closure Partial successa Failure
15 2 4 b
aEmpyema cavity and fistula reduced in size; ultimate clo- sure
occurred after hospital discharge. "Includes 1 hospital death; 2
patients whose fistulas were successfully closed by subsequent
myoplasties; and 1 closed by second stage thoracoplasty.
more gradually. Generally, this tube was han- dled as an empyema
tube. It was cut off after approximately three weeks and the space
was allowed to fill with granulation tissue. This re- quired
usually 1 to 3 months, but in 2 patients 4 and 6 months,
respectively, were required be- fore final tube removal.
Results Myoplasty was considered successful if the fis- tula was
obliterated and chest tubes could be removed without further
operative interven- tion. By these criteria the myoplasty was suc-
cessful initially in 15 of the 21 patients (Table 6, Fig 4).
In 2 patients myoplasty was only partially successful. Although
the fistulas eventually closed without reoperation, the closure
took an inordinately long time. Myoplasty reduced the size of both
the empyema space and the fistula, allowing the patients to be
discharged with empyema tubes in place. In 1, the air leak ceased
after 4 years and the tube was removed 3 months later. The other
patient was readmitted 4% months postoperatively with a severe head
injury which proved rapidly fatal. At the time of readmission the
chest tube was still in place but there was no mention of air
leakage.
In 4 patients the myoplasty failed to close the fistula. In 2,
repeat myoplasties after intervals of 2 and 13 months,
respectively, brought about closure. The reason for primary failure
in 1 of these patients was probably an excessively long bronchial
stump, but there was no apparent cause in the other. The third
patient was admit- ted with a destroyed right lung accompanied by
positive sputum cultures and a bronchopleural
fistula. A pleuropneumonectomy was per- formed but a fistula
again followed. Although the sputum was still positive, a myoplasty
com- bined with a 5-rib thoracoplasty was per- formed, but this
again was followed by recur- rence. Two weeks later a second
thoracoplasty with removal of an additional 3% ribs was car- ried
out and resulted in prompt closure of the fistula. The fourth
patient had severe chronic lung disease, which led to respiratory
failure after the myoplasty. Tracheal intubation with mechanical
ventilation was required, and this undoubtedly contributed to
reopening of the fistula and recurrence of the empyema. Ulti-
mately, renal failure supervened and led to the patient's death 1
month after the operation.
Comment The development of improved chemotherapy and better
suture techniques and materials, as well as use of the automatic
stapler, have low- ered the incidence of bronchopleural fistula
fol- lowing pulmonary resection from 28% two or three decades ago
[6] to 3% or less in recent years [8, 101. Nevertheless,
postresection fistula remains an important problem for the thoracic
surgeon. Also, there is a not-insignificant inci- dence of
nonsurgical spontaneously occurring bronchopleural fistula
associated with such diseases as lung abscess or empyema [2,10,121.
Patients with nonsurgical fistulas comprised 14 (27%) of the 52
patients with fistulas reported by Malave and associates [lo].
Further, the mor- tality rate from bronchopleural fistula remains
high. Twelve, or 23.1%, of those 52 patients died [lo].
Adequate dependent surgical drainage is the sine qua non of the
treatment of bronchopleural fistula. But drainage alone results in
closure of less than 20% of fistulas [8, 10, 121. In the re-
mainder, further surgical procedures are re- quired. Decortication
with revision of the em- pyema space may at times succeed [lo, 121.
For patients with postpneumonectomy fistulas, reamputation of a
long bronchial remnant will often effect closure [ll]. But
traditionally, the secondary procedures advocated when drain- age
alone fails have included thoracoplasty first, and if this does not
succeed, then either a further thoracoplasty or a further pulmonary
re-
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497 Hankins, Miller, and McLaughlin: Chest Wall Muscle Flaps to
Close Bronchopleural Fistulas
C D
Fig 4. Serial chest roentgenograms in a 41-year-old man who
underwent right upper and middle lobectomy for cavitary
tuberculosis. (A ) On admission. (B) Three weeks postresection,
showing a large apical space. (C) Three months postoperatively.
Despite adequate tube drainage, the sinogram shows a bronchopleural
fistula. ( D ) Seven months after myoplasty and a 4-rib thoraco-
plasty, the fistula and empyema have both become o blitera ted.
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498 The Annals of Thoracic Surgery Vol 25 No 6 June 1978
section. However, both of these latter opera- tions sacrifice
potentially salvageable lung tis- sue. Many patients with fistulas
have impaired cardiopulmonary function and either fail to survive
such operations or become pulmonary cripples. Myoplasty offers the
possibility of closing the fistula without excision of addi- tional
lung tissue and with the removal of few, if any, additional
ribs.
Abrashanoff [l] with his report in 1911 de- scribed the use of
muscle flaps to close bron- chopleural fistulas. In the United
States, Eggers [5] in 1920 provided early impetus toward this use,
as did Pool and Garlock [13]. The latter authors showed through
animal experiments that muscle grafts implanted into bronchial fis-
tulas unite firmly with the interior of the bron- chus and become
covered by bronchial epi- thelium. Maier and Luomanen [9] in 1949
reported their experience using the pectoralis major muscle after
the method of Berry. In 1971, Barker and associates [2] described
their mod- ification of this technique. Shenstone [14] in 1936
popularized the use of intercostal muscles as grafts. Demos and
Timmes [4] reported in 1973 their use of this muscle, as did
Delarue and Gale a year later 131.
We believe that myoplasty is indicated when a fistula persists
despite adequate drainage and an adequate thoracoplasty (see Table
2) [21. This was the indication in 5 patients with postresec- tion
fistulas in our series, 4 of whom had undergone a thoracoplasty
before resection and 1, a thoracoplasty concomitant with
resection.
We believe a second indication for muscle grafting is
anticipated failure of a thoracoplasty. An additional surgical
procedure can be avoided if those patients in whom thoraco- plasty
alone is likely to fail are identified and undergo myoplasty as a
supplement to the thoracoplasty. Experience has shown that a
conventional 5-rib thoracoplasty is unlikely to obliterate a
fistula that follows a pneumonec- tomy or a large Lucite sphere
plombage or, in certain instances, an upper lobectomy and superior
segmentectomy. The addition of myo- plasty to the thoracoplasty in
patients with such large empyema cavities usually makes it possible
to obliterate both the cavity and the fistula by resection of fewer
ribs than would
otherwise have been necessary. Thus pulmo- nary function is
conserved. Because of the anticipated failure of thoracoplasty
alone, myoplasty concomitant with limited, first-stage
thoracoplasty was performed in 11 patients.
In 11 of the 17 patients reported by Barker and co-workers [21 a
thoracoplasty preceded the myoplasty. The initial myoplasty was
success- ful in 14 of the 17 patients. One patient died. But the
average interval between the onset of the fistula and myoplasty was
40 months. Whereas the two series are not entirely similar in other
respects, we think the results in our 11 patients who underwent
concomitant. myo- plasty and limited, first-stage thoracoplasty
compare favorably with those of Barkers series. If the 2 patients
who were admitted with fis- tulas of 6 and 10 years duration,
respectively, are excluded, the average interval from onset of
fistula to myoplasty in our patients was only 6 months. None of the
patients died, and al- though myoplasty failed initially in 3
patients, all 3 subsequently achieved successful closure through
other operations after intervals rang- ing from 1 to 17 months.
It could be argued that in some of these 11 patients, fistula
obliteration would have oc- curred with thoracoplasty alone. This
will re- main a moot point. Nevertheless, the addition of myoplasty
to thoracoplasty did not increase the operative mortality. It
appears to have saved at least some of the 11 patients an
additional operation. And it considerably re- duced hospital
stay.
A third indication for myoplasty is the situa- tion in which a
myoplasty would likely obviate the need for a thoracoplasty
altogether. In pa- tients with a fistula associated with a small
em- pyema space below the level of the posterior end of the fifth
rib, such as may occur after a lower lobectomy, myoplasty alone
will often successfully obliterate the fistula and the space.
Moreover, it will do so with far less com- promise of pulmonary
function than would occur if enough ribs were removed to collapse
such a space. Five of the myoplasties in the pres- ent series were
performed for this indication.
It is interesting to assess the results in the 21 patients
treated by myoplasty in relation to those in 52 other patients with
bronchopleural
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499 Hankins, Miller, and McLaughlin: Chest Wall Muscle Flaps to
Close Bronchopleural Fistulas
fistula treated by other methods during the same period. The two
groups are not necessar- ily comparable to the point of statistical
valid- ity, and some-selection of the more favorable cases may have
occurred in the myoplasty group. Conversely, the nonmyoplasty group
contained 9 patients whose fistulas healed after surgical drainage
alone. Ultimate fistula oblit- eration occurred in 17 of the 21
patients in the myoplasty group, but in only 27 of the 52 pa-
tients in the other group. One of the myoplasty group and 15 of the
other group died. The high rate of fistula closure and the low
mortality rate associated with myoplasty encourage us to con- tinue
using the procedure in patients in whom it is indicated.
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DOI: 10.1016/S0003-4975(10)63596-5 1978;25:491-499 Ann Thorac
Surg
John R. Hankins, John E. Miller and Joseph S. McLaughlin
Experience with 21 Patients
The Use of Chest Wall Muscle Flaps to Close Bronchopleural
Fistulas:
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