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The Use of Chest Wall Muscle Flaps to Close Bronchopleural Fistulas:

Experience with 21 Patients


John R. Hankins, John E. Miller and Joseph S. McLaughlin
Ann Thorac Surg 1978;25:491-499
DOI: 10.1016/S0003-4975(10)63596-5

The online version of this article, along with updated information and services, is
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The Annals of Thoracic Surgery is the official journal of The Society of Thoracic Surgeons and
the Southern Thoracic Surgical Association. Copyright 1978 by The Society of Thoracic
Surgeons. Print ISSN: 0003-4975; eISSN: 1552-6259.

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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., J o h n 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 combined with a limited thoracoplasty in 13 patients.
The initial myoplasty produced prompt fistula closure 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, cauterization, 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 bronchopleural fistulas by myoplasty.
Material and Methods

Twenty-one patients with bronchopleural fistulas underwent a total of 23 muscle flap procedures at the Thoracic Surgical Services of the
Mt. Wilson State Hospital for Pulmonary Disease 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 following pulmonary resection in 15 of these 19
patients. The following types of resection were
employed: pneumonectomy in 1patient, lobectomy 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 tuberculous 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 patient 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 tuberculosis but in whom the disease was no longer
active, the fistula occurred following pulmonary resection for posttuberculosis bronchiectasis. 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 accurately, the interval between onset and myoplasty ranged from just under 3 months to 10
years, with the median interval being 6
months. The time interval was difficult to determine in 4 patients in whom fistulas developed before they were admitted to our institutions.

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

19
15a
1

Resection

Decortica tion
Plombage
Intrapleural cavity
rupture
Bronchiectasis
Resection

1
2
2b

"The following types of resection were performed in these


patients: pneumonectomy in 1, lobectomy in 4, bilobectomy in 1, lobectomy plus segmental or wedge resection in
6, segmental resection in 2, and subsegmental resection in
1.

patient underwent lobectomy plus segmental resection and the other, segmental resection.

and pyogenic organisms were grown. In 3 patients M. tuberculosis was grown from the empyema 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 determine 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 conjunction with the myoplasty.
Myoplasty was not considered an emergency
procedure. It was performed only when the active infection in the cavity was under control
and the patient was in optimal nutritional condition.

Operative Management
The presence of a fistula creates special problems for the anesthesiologist. The loss of anesthetic gases and oxygen through the fistula and
drainage of infected material from the empyema cavity through the fistula into the dependent part of the tracheobronchial tree constitute real hazards. Although there are some
advantages in the use of double-lumen endotracheal tubes, these have the disadvantages of
being difficult to position accurately and of having such narrow lumens that thick secretions
cannot be readily removed through them. We
prefer to occlude the fistula by tight gauze packing 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 thoracotomy. When a thoracoplasty was to be included 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 anteriorly.
The incision was developed through the extracostal 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 resected subperiosteally, the number being determined by the size of the empyema space as
shown on the sinogram (Table 2). A thoracoplasty 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'

No. of
Patients

Indication
Failure of previous

thoracoplasty
Anticipated thoracoplasty
failure
To obviate thoracoplasty

11
5

Table 3 . Thoracoplasty or Unroofing of Empyema


Performed in Conjunction with 23 Myoplasties
No. of

Procedures

Procedure
Limited, first-stage
thoracoplasty
Second-stage thoracoplasty
(after previous
thoracoplasty)
Unroofing (removal of short
segments, 1 to 3 ribs)
~

~~

11

3
9a

"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 associated 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 divided anteriorly near the costochondral junction 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 situations 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 serious air leakage. The cavity was cleansed of any
necrotic or purulent material and the infected
granulation tissue lining was removed by curettage.

Fig I. Method of developing and transferring to the


bronchus an intercostal muscle graft.

The bronchus from which the fistula originated 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 postpneumonectomy fistula or to the main bronchus for a postlobectomy fistula. An excessively long bronchial 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 suture 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 sufficiently 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 dissected. 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 tacking 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 fistula also could not be located in a patient with
postpneumonectomy empyema, although the
preoperative bronchogram had clearly demonstrated 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
Procedures

Method
Suture closure plus covering
with muscle flap
Flap sutured over open
bronchus
Combination procedurea
Fistulous opening not
located (muscle used to
fill empyema cavity)
~

14
3

4
2

aMultiple fistulas present: some sutured closed then covered with flap, others simply covered with flap.

It is essential that the muscle flap completely


fill the empyema cavity. If one or two intercostal muscle grafts did not suffice, then other
muscles in the vicinity of the thoracotomy, such
as serratus anterior, latissimus dorsi, or sacrospinalis, 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 with


the muscle flap, used when the bronchus cannot be dissected 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 shrinkage 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 cavity but superficial to the graft. If a thoracoplasty
was performed in conjunction with the myoplasty, the second tube was left in the subscapu-

Table 5 . Types of Muscle Used in 23 Myoplasties


~~

Type of Muscle Used


Intercostal muscles only
Extracostal muscles only
Both intercostal and
extracostal muscles

No. of

Procedures
14
4

lar space. If extensive dissection of the lung was


required, the second tube was left intrapleurally. 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 continued 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

fistula. A pleuropneumonectomy was performed but a fistula again followed. Although


No. of
the sputum was still positive, a myoplasty comOutcome
Patients
bined with a 5-rib thoracoplasty was performed, but this again was followed by recurSuccessful closure
15
rence. Two weeks later a second thoracoplasty
Partial successa
2
4b
Failure
with removal of an additional 3% ribs was carried out and resulted in prompt closure of the
aEmpyema cavity and fistula reduced in size; ultimate clofistula.
The fourth patient had severe chronic
sure occurred after hospital discharge.
"Includes 1 hospital death; 2 patients whose fistulas were lung disease, which led to respiratory failure
successfully closed by subsequent myoplasties; and 1 closed
after the myoplasty. Tracheal intubation with
by second stage thoracoplasty.
mechanical ventilation was required, and this
undoubtedly contributed to reopening of the
more gradually. Generally, this tube was han- fistula and recurrence of the empyema. Ultidled as an empyema tube. It was cut off after mately, renal failure supervened and led to the
approximately three weeks and the space was patient's death 1 month after the operation.
allowed to fill with granulation tissue. This required usually 1to 3 months, but in 2 patients 4 Comment
and 6 months, respectively, were required be- The development of improved chemotherapy
fore final tube removal.
and better suture techniques and materials, as
well as use of the automatic stapler, have lowResults
ered the incidence of bronchopleural fistula folMyoplasty was considered successful if the fis- lowing pulmonary resection from 28% two or
tula was obliterated and chest tubes could be three decades ago [6] to 3% or less in recent
removed without further operative interven- years [8,101. Nevertheless, postresection fistula
tion. By these criteria the myoplasty was suc- remains an important problem for the thoracic
cessful initially in 15 of the 21 patients (Table 6, surgeon. Also, there is a not-insignificant inciFig 4).
dence of nonsurgical spontaneously occurring
In 2 patients myoplasty was only partially bronchopleural fistula associated with such
successful. Although the fistulas eventually diseases as lung abscess or empyema [2,10,121.
closed without reoperation, the closure took an Patients with nonsurgical fistulas comprised 14
inordinately long time. Myoplasty reduced the (27%) of the 52 patients with fistulas reported
size of both the empyema space and the fistula, by Malave and associates [lo]. Further, the morallowing the patients to be discharged with tality rate from bronchopleural fistula remains
empyema tubes in place. In 1, the air leak high. Twelve, or 23.1%, of those 52 patients
ceased after 4 years and the tube was removed 3 died [lo].
months later. The other patient was readmitted
Adequate dependent surgical drainage is the
4% months postoperatively with a severe head sine qua non of the treatment of bronchopleural
injury which proved rapidly fatal. At the time fistula. But drainage alone results in closure of
of readmission the chest tube was still in place less than 20% of fistulas [8, 10, 121. In the rebut there was no mention of air leakage.
mainder, further surgical procedures are reIn 4 patients the myoplasty failed to close the quired. Decortication with revision of the emfistula. In 2, repeat myoplasties after intervals pyema space may at times succeed [lo, 121. For
of 2 and 13 months, respectively, brought about patients with postpneumonectomy fistulas,
closure. The reason for primary failure in 1 of reamputation of a long bronchial remnant will
these patients was probably an excessively long often effect closure [ll]. But traditionally, the
bronchial stump, but there was no apparent secondary procedures advocated when draincause in the other. The third patient was admit- age alone fails have included thoracoplasty
ted with a destroyed right lung accompanied by first, and if this does not succeed, then either a
positive sputum cultures and a bronchopleural further thoracoplasty or a further pulmonary re-

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497 Hankins, Miller, and McLaughlin: Chest Wall Muscle Flaps to Close Bronchopleural Fistulas

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 thoracoplasty, 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 operations sacrifice potentially salvageable lung tissue. 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 additional lung tissue and with the removal of few,
if any, additional ribs.
Abrashanoff [l] with his report in 1911 described the use of muscle flaps to close bronchopleural 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 fistulas unite firmly with the interior of the bronchus and become covered by bronchial epithelium. 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 modification 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 postresection 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 thoracoplasty 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 pneumonectomy or a large Lucite sphere plombage or, in
certain instances, an upper lobectomy and
superior segmentectomy. The addition of myoplasty 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 pulmonary 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 successful 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. myoplasty and limited, first-stage thoracoplasty
compare favorably with those of Barkers series.
If the 2 patients who were admitted with fistulas 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 although myoplasty failed initially in 3 patients,
all 3 subsequently achieved successful closure
through other operations after intervals ranging from 1 to 17 months.
It could be argued that in some of these 11
patients, fistula obliteration would have occurred with thoracoplasty alone. This will remain 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 reduced hospital stay.
A third indication for myoplasty is the situation in which a myoplasty would likely obviate
the need for a thoracoplasty altogether. In patients with a fistula associated with a small empyema 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 compromise of pulmonary function than would
occur if enough ribs were removed to collapse
such a space. Five of the myoplasties in the present 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 necessarily comparable to the point of statistical validity, 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 obliteration occurred in 17 of the 21 patients in the
myoplasty group, but in only 27 of the 52 patients 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 continue using the procedure in patients in whom
it is indicated.

References
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von Fistelgangen Welche von inneren Organen
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4. Demos NJ, Timmes JJ: Myoplasty for closure of


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The Use of Chest Wall Muscle Flaps to Close Bronchopleural Fistulas:


Experience with 21 Patients
John R. Hankins, John E. Miller and Joseph S. McLaughlin
Ann Thorac Surg 1978;25:491-499
DOI: 10.1016/S0003-4975(10)63596-5
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