- Email: [email protected]
Surgical management of lung metastases
J
THORAC CARDIOVASC SURG
1991;101:901-8
Surgical management of lung metastases Usefulness of resection with the neodymium:yttrium-aluminum-garnet laser with median sternotomy Between May 1969 and September 1989,677 metastatic lesio~ were resected during 107 operations in 100 patients with pulmonary metastases from various primary sites at the Center for Adult Diseases, Osaka, Japan. Of those patients, 65 underwent conventional lateral thoracotomy, and 35 patients bad median sternotomy. No significant difference existed in actuarial survival after the first operation to remove the metastases between the two patient groups. Furthermore, local excision of 418 lesio~ was performed in 25 patients with the neodymium:yttrium-aluminum-garnet (Nd:YAG) laser. Of those, 18 patients bad undergone a one-stage operation for bilateral lesions through a median sternotomy approach. Although our study was not randomized, survival of the 25 patients treated with the Nd:YAG laser tends to be longer than survivalof the 75 patients for whom the Nd:YAG laser was not used. We concluded tbat aggressive excision and evaporation of multiple lung metastases with the Nd:YAG laser under median sternotomy is a safe and promising variation in technique and that tbis approach will expand the scope of surgical indications for metastatic lung tumors. For a clearer demo~tration of the influence of differences in surgical techniques on long-term survival it is necessary to conduct randomized prospective studies of the surgical techniques.
Ken Kodama, MD,a Osamu Doi, MD,a Masahiko Higashiyama, MD,a Masayuki Tatsuta, MD,a and Takeshi Iwanaga, MD,b Osaka, Japan
Long-term survival after resection of isolated pulmonary metastases has been documented in several series. 1-3 Recent reports indicated that the presence of unilateral or bilateral metastases did not influence survival.v" and patients with single or multiple metastases achieved prolonged survival.t" Moreover, it also has been reported? that there was no significant difference in actuarial survival between median sternotomy and lateral thoracotomy in patients with adult soft-tissue sarcomas. Conversely,an intensivechemotherapy regimen including cisplatin has been acceptable, and some series of malignant tumors respond dramatically to such a regimen.v? Despite the important achievements of multimodality treatment for
From the Department of Thoracic Surgery," The First Department of Surgery.s The Center for Adult Diseases, Osaka, Japan. Received for publication Jan. 31, 1990. Accepted for publication May 22, 1990. Address for reprints: Ken Kodama, MD, Department of Thoracic Surgery, The Center for Adult Diseases, 3 Nakamichi, l-chorne, Higashinari-ku, Osaka 537, Japan.
12/1/23663
sarcomas and some kindsof carcinoma, the occurrence of pulmonary metastases represents the most important reason for failure.'? . Recently, the neodymium:yttrium-aluminum-garnet (Nd:YAG) laser has been found to be a useful tool for endoscopic surgery, and it also would become acceptable for resection of pulmonary tumors.l"!' However, there have been no reports on the influence of aggressive excision and evaporation of multiple lung metastases with the use of the laser on long-term survival. The objectives at the present study are to retrospectively compare the results of median sternotomy and lateral thoracotomy and evaluate the usefulness of aggressive excision with the Nd:YAG laser for patients with pulmonary metastases. Moreover, we also attempt to analyze the interaction between the aggressive surgical management and the impact of intensive chemotherapy in a subset of patients with metastatic lung cancer.
Patients and methods From May 1969 to September 1989, 106 patients had operations for metastatic lung cancer from various sites. One case of unknown origin and five cases that were lost to follow-up were
901
The Journal of Thoracic and Cardiovascular
9 0 2 Kodama et al.
Surgery
Table I. Characteristics ofpatients with metastatic lung tumors Characteristic
No. of patients Age (yr) Range Mean Sex distribution Male Female Metastatic pattern Solitary Multiple Approach Median sternotomy Lateral thoracotomy Resection With Nd:YAG laser Without Nd:YAG laser Primary site Colorectal Renal Lung Head and neck Breast Testicular Ovary and uterus Bladder Soft tissuesarcoma Osteosarcoma Others
100 8-79 53 62 38 57 43 35 65 25 75 21 13 12 9 8 6 4 3 15 4 5
excluded. There were 100 patients eligible for inclusion. The characteristics of the 100 analyzed patients are summarized in Table I. The mean age at the time of the first thoracotomy was 53 years (range 8 to 79 years). Sixty-two patients were male and 38 were female (ratio 1.6:1). There were 57 solitary and 43 multiple metastases. A mean of 5.9 nodules were resected per patient (range 1 to Ill). Median sternotomy was used for 35 patients and lateral thoracotomy for 65 patients. The Nd:YAG laser was used in 25 patients. The primary tumors were located in the colorectum (n = 21), kidney (n = 13), lung (n = 12), head and/or neck (n = 9), breast (n = 8), testis (n = 6), ovary and/or uterus (n = 4), bladder (n = 3), soft tissue sarcoma (n = 15), osteosarcoma (n = 4), or other site (n = 5). The soft tissue sarcoma consisted of four synovial sarcomas, three liposarcomas, three alveolar soft part sarcomas, and one each of the following: malignant fibrous histiocytoma, leiomyosarcoma, meningioma, malignant schwannoma, and Ewing's sarcoma. The histologic classification of the primary tumor was carcinoma in 81 patients and sarcoma in 19 patients. The reason for the small number of cases of osteosarcoma was that, since the principal objective of our institution is the treatment of adult diseases, younger patients, who are more likely to have osteosarcoma, were not available for this study. Preoperative evaluation. After excision of the primary tumor, patients were evaluated by thoracic computed tomographic (CT) scanning or linear tomography, or both, every 3 to 6 months for 2 years. Patients with newly developing abnor-
Table II. Comparison of background factors between patients undergoing median sternotomy and patients undergoing lateral thoracotomy Characteristic
Median sternotomy
No. of patients 35 Laser surgery Applied 18 Not applied 17 Disease-free interval (DFI) -sr yr 19 14 I < DFI < 5 yr 2:5 yr 2 No. of metastases ::s3 II 2:4 24 Maximal tumor diameter (em) ::s3 24 >3 II
Lateral thoracotomy
x2 Test
65 7
58
p
14 35 16
p
59 6
p
32 33
< 0.01 NS
NS, Not significant.
malities consistent with pulmonary metastases were offered resection of the metastases if the primary tumor was controlled, if extrapulmonary metastases were absent, and if the amount of lung tissue remaining would provide the patient with sufficient pulmonary parenchymal reserve." Aggressive resection of multiple lung metastases was initiated in our department in 1983. Before that year routine CT scanning had not been performed, and operation was indicated only for metastases that were diagnosed as definitely solitary on the basis of a chest tomogram. Since 1983, CTscan images (resolving power) have been strikingly improved, thereby enabling us to detect small lesions, and thus CT also has come to be widely used for screening of metastatic lesions. Therefore, even if the lesion is not solitary, we use lateral thoracotomy if the lesions are unilateral, the number is no more than a few, and their size is almost uniform. Operative procedure. Lateral thoracotomy was adopted for patients whose linear tomography and/or CT scan detected only a solitary lesion or a small number of unilateral lesions and there was no change in either the size or number of primary and/or metastatic sites in the unilateral lung throughout chemotherapy. Conversely, metastases involving the bilateral lungs were resected through median sternotomy. In the treatment of testicular carcinomas, chemotherapy consisting mainly of cisplatin, vinblastine, and bleomycin was administered. For some of the soft tissue sarcomas chemotherapy consisting mainly of ifosfamide, vincristine, doxorubicin (Adriamycin), and dacarbazine was administered, whereas chemotherapy mainly consisting of doxorubicin, methotrexate, and cisplatin was administered for osteosarcoma. a-Interferon was administered in the treatment of renal cell carcinoma. The excision of the metastasis after intensive chemotherapy usually was undertaken from 4 to 8 weeks after the last course of chemotherapy to ensure optimal preoperative health and recovery of the patient. After 1986 the Nd: YAG laser was frequently used to preserve as much pulmonary function as possible and to achieve the most complete resection of the lesions. The laser equipment consisted of a MediLas 2 type 621 Nd:YAG laser (MBB-Medical Technology Ltd., Munich, Federal Republic of Germany).
Volume 101
Lung metastases
Number 5 May 1991
903
100 90
80 ..J
70
:::>
40
« > 60 ...... > 50 0::: (f)
30
20 10
00
5
20
15
10 TIME (YRS)
Fig. 1. Overall survival after resection of the primary lesion (open circles) and after excision of the metastasis (closed
circles). This device is capable of generating and delivering power up to 100 W to the operative site for up to 9.9 seconds. A focusing handpiece with an interchangeable optic was used. With this hand applicator as a noncontact mode, the energy density can be changed by altering the distance to the tissue. The beam can be focused on a small spot (0.4 mm) or used to treat large surfaces for excision, evaporation, or fulguration of the tissues. The power setting used for all resections was 45 to 50 W of continuous-wave energy. The timer of the laser was set at the maximum (9.9 seconds) and then reset repeatedly to irradiate for the necessary time. Resection was performed as follows. For tumors on the surface of the lung, the lung was inflated, and the laser beam was irradiated to the parenchyma adjacent to the tumor. This caused evaporation of the parenchyma directly exposed to the irradiation and separation of the tumor from the surrounding parenchyma, resulting in isolation of the tumor without any manipulation. Conversely, for tumors located in the parenchyma, that is, tumors in a deep region of the lung, the lung was deflated, the site of the tumor was confirmed by palpation, laser irradiation was applied to the site immediately above the tumor, and the parenchyma was evaporated. When the tumor was pushed up from the underside with a finger, into the field of irradiation, it became visible as a hemispheric shape. The tumor was isolated easily when the surrounding parenchyma was evaporated by the laser beam. Small tumors with a diameter of less than a few millimeters were evaporated by direct exposure to laser irradiation. After confirming that there was no bleeding from the punched-out parenchyma as a result of laser treatment, we sutured wounds on the lung surface to prevent postoperative air leakage. Statistical analyses. Survival duration was computed from the date of the initial excision of the metastasis or from the date of treatment of the primary tumor until the date of the last known follow-up or date of death. Survival curves were plotted with the life-table method or the Kaplan-Meier method. Estimates of median survival time and survival rates at specific time points were derived from these curves. The z test was used for
Table III. Comparison of background factors between the patients with and without laser surgery Characteristic
Laser surgery
No laser surgery
25
75
18 7
17 58
P < 0.01
13 10 2
20 39 16
p
10 15
60 15
p
17 8
39 36
NS
No. of patients Approach Median sternotomy Lateral thoracotomy Disease-free interval (OFf) ::0 I yr I yr < OFf < 5 yr 2:5 yrs No. of metastases
s3 2:4
X2 Test
< 0.05
Maximal tumor diameter (em)
::03 >3 NS. Not significant.
statistically comparing two survival curves. Statistical analysis for significant differences between the two groups in terms of the distribution of each of the patient-background factors presented in Tables II and III was performed by the x 2 test. When the p value was less than 0.05, the difference was regarded as significant.
Results There were no perioperative deaths in this series. One hundred patients underwent 107 thoracic explorations. The survival curves for the total number of patients from the time of treatment of the primary site and the time of the first excision ofthe metastasis in the lung are presented in Fig. 1. Overall survival rates after resection of the
904
The Journal of Thoracic and Cardiovascular
Kodama et al.
Surgery
100 90 80 ..J 70 <:( > 60 ......
>
0::
::>
(f)
?R
m I
I
:
::
:!
-~,
~r:l I_~! ~a(-·L.: ~-2I :
50
.._ ..
(n=13)
L-...l;.....L---------- 1
40
30 20 10 0
.---.L._J_. ....J HEAD & NECK (n=9)
:
:
~
I
BREAST (n=8) I •••••• _•••••••••••••• ~ .••• _•••J I I I I
' - - - - - - - - - ' COLO-RECTAL (n=2l)
I LUNG (n=12) I
0
3
10
5
15
TIME (YRS)
Fig. 2. Survival after excision of the metastasis in cancer patients as a function of the site of the primary lesion.
...1._---------100 I 90 'I II 80 'L ~ ..J 70 ~ 60 , I > L-'=-=+----'1 0::: 50 I , ~ I (J) 40 I, I 30 I LJ I, 20 10 I 0 0 3
TESTICULAR (n =6) OVARY & UTERUS (n =4) BLADDER (n=3)
I
I-i
I
OTHERS(n=5)
'*
5
10
15
TIME (YRS) Fig. 3. Survival after excision of the metastasis in cancer patients as a function of the site of the primary lesion.
primary tumor were 67% at 5 years and 40% at 10 years, whereas the rates after the first pulmonary operation to remove the lesion were 45% and 30%, respectively. The survival curves from the time of the first excision of the metastasis as a function of the primary site are presented in Figs. 2 to 4. The best outcome was achieved with patients who had head and neck cancer. Both the 3- and 5-year survival rates were 85%, and the median survival time has not been reached. The 3-year survival rates in colorectal, breast, renal, and lung cancers were 66%, 60%, 50%, and 43%, respectively. The 5-year survival rates in
those groups were 57%, 30%, 50%, and 43%, respectively. The median survival time in those groups were 66,38, 22, and 24 months, respectively (Fig. 2). Although the numbers of patients in other groups are too small for meaningful interpretation of the survival results, the treatment result in testicular cancer is noteworthy (Fig. 3). Four of six patients whose serum markers (o-fetoprotein and/or human chorionic gonadotropin) returned to the normal range after intensive chemotherapy had a good outcome attributable to resection of residual multiple metastases with the Nd: YAG laser. The 3- and 5-year
Volume 101
Lung metastases 9 0 5
Number 5 May 1991
100 90 80 ..J
70
« 60
> .......
> 50 0::: ::J
(/)
'*
40 30
I I I
SOFT-TISSUE SARCOMA (n=15)
I I
I
t.; --I OSTEOSARCOMA (n =4)
20 10 OL...---...,.-----,-----....-------r----o 3 5 10 15 TIME (YRS)
Fig. 4. Survival after excision of the metastasis in patients with soft tissue sarcoma and osteosarcoma.
100
90 80 ...J
70
« 60 > ....... > 0::: 50 ::J
(J)
40
'''0,
30
'0,
'0,
"0--0--0. ,
20
10 0 0
5
boo -0- -0--0- -0-
10 TIME (YRS)
15
20
Fig. 5. Comparison of survival after excision of the metastasis between patients undergoing median sternotomy (closed circles) and lateral thoracotomy (open circles).
survival rates in soft tissue sarcoma were 53% and 40%, respectively, and the median survival time was 41 months (Fig. 4). To assess the influence of the type of incision on survival, we compared the two groups of patients undergoing excision of the lesion, either by median sternotomy or by lateral thoracotomy. The patient characteristics of these two groups are summarized in Table II. Laser surgery was used significantly more often in the median sternot-
omy group than in the lateral thoracotomy group. Both the use of median sternotomy for an approach to bilaterallesions and the advent oflaser surgery have come of age concurrently. The disease-free interval of the former group was significantly shorter than that of the latter group. The number of metastases in the latter group was significantly smaller than that in the former group. When the maximal diameter of the metastatic lesions was classified at the level of 3 em, there was no significant differ-
The Journal of
9 0 6 Kodama et af.
Thoracic and Cardiovascular Surgery
100 90
80 b :i; ..J
70
2:
60
«
> 0:: 50
:::>
(/)
'*
40
.. P'<'ii.05
\~!lL 'b_ -0--0,'0.,
30 20
"0--0-0.
''0- -0-0- -0- 0- -O-.()
10
O'--------'-----.. . . . - --_I....o
5
15
......l.._ _
20
Fig. 6. Comparison of survival after excision of the metastasis between patients undergoing laser surgery (closed circles) and those without laser surgery (open circles).
ence betweenthe two groups.The median survival was 46 months for both the sternotomy group and the lateral thoracotomy group, and no significantdifference existed between the two survival curves (Fig. 5). Standard wedge resection and/or enucleation of 259 lesions by 80 operations in 75 patients were performed without the Nd:YAG laser. Conversely, local excision of 418 lesions by 27 operations in 25 patients was performed with the Nd:YAG laser. In addition to thoselesions, small lesions of less than a few millimeters in diameter were directly evaporated with the laser. If many small lesions were presentand silicoticnodulesor other granulomatous lesions were suspected on the basis of the patient's occupation or history of disease, a biopsy specimen of one of the lesions was obtained before evaporation, and we determined whether it was a metastatic lesion by intraoperative histodiagnosis with frozen sections. Excision and evaporation required 5000 to 60,000 J per patient. The clinical characteristics of the patients in the two groups, with or without laser surgery, are presented in Table III. The median sternotomy approach was used for bilateral lung metastases in 18 of 25 patients who underwent laser surgery. In the statistical analysis the 25 patients in the laser surgery group included three whose lung metastases were first excisedby conventionalwedge resection, with subsequent laser resection of recurrent metastases. Significant differences between the two groups were found with regard to the approach, diseasefree interval, and number of metastases. No significant difference was found with regard to the maximal diameter of the tumor. The 3-year and 5-year survival rates in the patients with laser surgery were 85% and 61%, whereas those in the patients without laser surgery were
54%and 42% (Fig. 6). The differencebetweenthe 2- and 3-year points in those two survival curves was significant (p < 0.05). Discussion
In 1979, McCormack and Martini I 5 reported that the overall 5-year survival rates after resectionof metastatic disease for 202 patients with sarcoma and 246 patients withcarcinoma were30%and 25%,respectively. In 1984, Mountain and colleagues' described772 resections in 556 patients who had metastatic disease, with an overall 5-year survivalrate of 35% after excision of the metastasis. To date we have performed resection of 677 metastatic lesions in 107operations in 100 patients. The overall5-year survivalrate obtained after the firstexcision was 45%.This rate is acceptable because it is superiorto overall survival achieved for resected primary lung cancer, and there was a low incidence of morbidity and mortality. In the analysisof site-specific survival results,an excellent outcome was achieved in the group of patients with head and neck cancer, with a 5-year survival of 85%. McCormack and Martini I 5 reported on 27 patients with head and neck carcinoma metastatic to the lung; these patients underwent pulmonary resection,and the overall 5-year survivalrate was 47%. This discrepancy is due to the fact that tumors from different organs or with a different histologic type within the head and neck have various tendencies to metastasize, and the outcome after excision also may be different. Median sternotomy is thought to be the best approach for bilateral surgical staging and complete one-stage resection." Roth and colleagues? reported that occult
Volume 101 Number 5 May 1991
contralateral metastases are present in about 20% of cases, and they indicate that there are bilateral metastases; one might use this as a strong argument to imply median sternotomy should be the procedure of choice rather than lateral thoracotomy. Surgery for metastatic lungdisease is localtherapy for a systemic problem. The purpose of surgical intervention for pulmonary metastasesis to decrease the tumor burden by removing maeroscopic disease in preparation for further therapy to control or eradicate microscopic foci. Thus complete resection of the lung lesion is necessary to increase the effectiveness of surgicalintervention. Mediansternotomy maximizes the role of surgeryin this context and is thus the procedure of choice whenever possible."! In comparison with the lateral thoracotomy group, the sternotomy group included significantly higher percentages of patients witha disease-free intervaloflessthan I yearand patientswith four or more metastatic lesions. The postthoracotomy survival was not significantly different for the two groups. Therefore we also recommended this approach if there were no severe pleural adhesions. If a patienthas a historyof clear pleuritis and, in addition,if chestx-rayfilms demonstratepleuralthickening and calcification, 'we inspect the respiratory movement (i.e., expiratory phaseand inspiratory phase) of the thickened pleura by visualization with x-ray films and estimate whetherpleural adhesion is present. When severe adhesion is suspected at the preoperative evaluation, we recommend staged lateral thoracotomy. Superior survival was achieved in the laser-treated group, althoughtheirclinical background wasnotas good as that of the nonlaser group.Althoughour experience is limited toonly18cases, onthe basisofthe data fromthem weconsider the combination of median sternotomy and lasersurgery to be a safe surgicalmethod and a promisingvariation in technique. We expectthat this approach will expandthe scope of surgicalindications for multiple metastaticlesions. In an early experimental study, LoCicero and colleagues!' demonstrated that the Nd:YAG lasercan be a useful adjunct to maximally preserve normal lung tissue and to seal bleeding, leaking, and raw lung surfaces. Recently, Moghissi'? reported that the Nd:YAG laser wasefficacious in eliminating pulmonarynodularlesions by local excision and evaporation in 14 patients with a solitary nodule, particularlyin high-risk patients such as thosewithlimitedrespiratory function and in the elderly. Moreover, LoCicero and colleagues':' found the laser to be an excellent adjunct for pulmonary resection on the basis of their experience with localexcision of 32 pulmonary lesions in 26 patientswhohad marginal pulmonary function or deepparenchymal lesions that werenot amenableto wedge resection.
Lung metastases
907
It has been indicated that intensive chemotherapy, including cisplatin, is capable of playing a major role in eradicatingall evidence of metastaticdiseasein testicular cancer''and osteosarcoma.l" In such casessurgicaltreatment is indicatedto eradicate and reclassify lesions that stabilize but do not disappeartotallywith chemotherapy because of a high rate of recurrenceat thosesitesof metastatic lesions. Excluding one patient with a seminoma, whom we treated before intensive chemotherapy came into wide use, the remaining five of the six patients with testicular carcinoma treated by us had nonseminomatous tumors. These five patients already had severe multiple pulmonary metastases when we performed high orchiectomy, and thus we administered intensive chemotherapy. As a result, in each case the shadows on chest x-ray films becamesmallerin both sizeand number but did not disappear completely. Thus all of these cases required surgical treatment. The serum markers did not return to their normal rangesin oneofthe five patientsbeforethe operation,and thispatientdiedofrecurrenceearlyafter resection of lung metastases. The serum markers returned to their normal ranges before the operation in the remaining four patients,and the excised tumorshad undergone complete necrosis in three of them. The remainingcase is interesting in that viable malignant cells were demonstrated in only one of 57 resected tumors. Those findings indicate that viable malignant cells may be present even if the serum markers have returned to their normal ranges so long as shadows remain on the chest x-ray films. Moreover, there alsois a possibility that tumorscontain malignant cells that do not produce any markers. Therefore, evenif the serum markers have returned to their normal ranges,it is desirable to resect residualshadows as thoroughlyas possible. Under these circumstances the surgical methodusingthe Nd:YAG laser with median sternotomy can be a suitable approach for this purpose. We encountered only four casesof osteosarcoma. For each case we performed intensive chemotherapy in the treatment of multiplelung metastases. However, despite the chemotherapy, the lung metastases increased in two cases, and the patientseventually died of recurrenceearlyafter resection of the metastaticlesions. The remaining two patients had operations after a partial response to chemotherapy was obtained, and they are now free of disease. Althoughit is tooearly to draw any hard conclusions, on the basisof these resultswe think that surgical treatment is not. indicated for patients in whom lung metastases advancedespite intensive chemotherapy. Multiplelungmetastases ofsofttissuesarcomas,which are characteristically relatively slow growing and resistant to chemotherapy, also seem to be a good indication
9 0 8 Kodama et al.
for laser surgery. Recently, Jablon and colleagues'? reported that resection of pulmonary metastasis in patients with soft tissue sarcomas is associated with longterm survival, particularly in patients with a disease-free interval of more than I year and with no more than five nodules. However, they have not performed laser-assisted resection. In our series of soft tissue sarcomas three patients with alveolar soft part sarcomas had multiple metastases numbering more than 30 nodules, and those metastases had already been present when the original diagnosis was made. In such cases survival must be influenced by those metastases after complete resection of the primary site. IS, 19 Thus it is reasonable to extend the operative indications for the Nd:YAG laser to such cases, and prolonged survival is likely. On the basis of the results of the present study, we believe that the combination of median sternotomy and Nd:YAG laser surgery is a safe technique that expands the scope of surgical indications for lung metastases, especially bilateral multiple lung metastases. However, it is necessary to carefully consider the result of preceding chemotherapy and the biologic behavior of the tumor before deciding to operate. REFERENCES 1. Thomford NR, Woolner LB, Clagett OT. The surgical treatment of metastatic tumors in the lung. J THORAC CARDIOVASC SURa 1965;49:357-63. 2. Sellors TH. Treatment of isolated pulmonary metastases. Br Med J 1970;2:253-6. 3. Choksi LB, Takita H, Vincent RG. The surgical management of solitary pulmonary metastasis. Surg Gynecol Obstet 1972;134:479-82. 4. Takita H, Edgerton F, Karakousis C, et al. Surgical management of metastases to the lung. Surg Gynecol Obstet 1981;152:191-4. 5. Mountain CF, McMurtrey MJ, Hermes KE. Surgery for pulmonary metastasis. Ann Thorac Surg 1984;38:323-30. 6. Regal A, Reese P, Antkowiak J, et al. Median sternotomy for metastatic lung lesions in 131 patients. Cancer 1985; 55:1334-9.
The Journal of Thoracic and Cardiovascular Surgery
7. Roth JA, Pass HI, Wesley MN, et al. Comparison of median sternotomy and thoracotomy for resection of pulmonary metastases in patients with adult soft-tissue sarcomas. Ann Thorac Surg 1986;42:134-8. 8. Mandelbaum I, Yaw PB, Einhorn LH, et al. The importance of one-stage median sternotomy and retroperitoneal node dissection in disseminated testicular cancer. Ann Thorac Surg 1983;36:524-8. 9. Rowland RG. Surgical management of post-chemotherapy residual testis tumor. In: Urologic oncology. Boston: Martinus Nijhoff, 1984:256-74. 10. Potter DA, Glenn J, Kinsella T, et al. Pattern of recurrence in patients with high-grade soft-tissue sarcoma. J Clin Oncol 1985;3:353-66. 11. LoCicero J III, Hartz RS, Frederiksen JW, et al. New applications of the laser in pulmonary surgery: hemostasis and sealing of air leaks. Ann Thorac Surg 1985;40:546-50. 12. Moghissi K. Local excision of pulmonary nodular (coin) lesion with noncontact yttrium-aluminum-garnet laser. J THORAC CARDIOVASC SURa 1989;97:147-51. 13. LoCicero J III, Frederiksen JW, Hartz RS, et al. Laser-assisted parenchyma-sparing pulmonary resection. J THORAC CARDIOVASC SURa 1989;97:732-6. 14. Holbert BL, Holbert JM, Libshitz HI. The chest radiograph after resection of pulmonary nodules with a neodymium-YAG laser. J Thorac Imaging 1989;4:82-6. 15. McCormack PM, Martini N. The changing role of surgery for pulmonary metastases. Ann Thorac Surg 1979;28:13945. 16. Pastorino U, Valente M, Gasparini M, et al. Lung resection for metastatic sarcomas: total survival from primary treatment. J Surg OncoI1989;40:275-80. 17. Jablon D, Steinberg SM, Roth J, et al. Metastatectomy for soft tissue sarcoma: further evidence for efficacyand prognostic indicators. J THORAC CARDIOVASC SURa 1989;97:695-705. 18. Evans HL. Alveolar soft-part sarcoma: a study of 13 typical examples and one with a histologicallyatypical component. Cancer 1985;55:912-7. 19. Lieberman PH, Brennan MF, Kimmel M, et al. Alveolar soft-part sarcoma: a clinico-pathological study of half a century. Cancer 1989;63:1-13.
THORAC CARDIOVASC SURG
1991;101:901-8
Surgical management of lung metastases Usefulness of resection with the neodymium:yttrium-aluminum-garnet laser with median sternotomy Between May 1969 and September 1989,677 metastatic lesio~ were resected during 107 operations in 100 patients with pulmonary metastases from various primary sites at the Center for Adult Diseases, Osaka, Japan. Of those patients, 65 underwent conventional lateral thoracotomy, and 35 patients bad median sternotomy. No significant difference existed in actuarial survival after the first operation to remove the metastases between the two patient groups. Furthermore, local excision of 418 lesio~ was performed in 25 patients with the neodymium:yttrium-aluminum-garnet (Nd:YAG) laser. Of those, 18 patients bad undergone a one-stage operation for bilateral lesions through a median sternotomy approach. Although our study was not randomized, survival of the 25 patients treated with the Nd:YAG laser tends to be longer than survivalof the 75 patients for whom the Nd:YAG laser was not used. We concluded tbat aggressive excision and evaporation of multiple lung metastases with the Nd:YAG laser under median sternotomy is a safe and promising variation in technique and that tbis approach will expand the scope of surgical indications for metastatic lung tumors. For a clearer demo~tration of the influence of differences in surgical techniques on long-term survival it is necessary to conduct randomized prospective studies of the surgical techniques.
Ken Kodama, MD,a Osamu Doi, MD,a Masahiko Higashiyama, MD,a Masayuki Tatsuta, MD,a and Takeshi Iwanaga, MD,b Osaka, Japan
Long-term survival after resection of isolated pulmonary metastases has been documented in several series. 1-3 Recent reports indicated that the presence of unilateral or bilateral metastases did not influence survival.v" and patients with single or multiple metastases achieved prolonged survival.t" Moreover, it also has been reported? that there was no significant difference in actuarial survival between median sternotomy and lateral thoracotomy in patients with adult soft-tissue sarcomas. Conversely,an intensivechemotherapy regimen including cisplatin has been acceptable, and some series of malignant tumors respond dramatically to such a regimen.v? Despite the important achievements of multimodality treatment for
From the Department of Thoracic Surgery," The First Department of Surgery.s The Center for Adult Diseases, Osaka, Japan. Received for publication Jan. 31, 1990. Accepted for publication May 22, 1990. Address for reprints: Ken Kodama, MD, Department of Thoracic Surgery, The Center for Adult Diseases, 3 Nakamichi, l-chorne, Higashinari-ku, Osaka 537, Japan.
12/1/23663
sarcomas and some kindsof carcinoma, the occurrence of pulmonary metastases represents the most important reason for failure.'? . Recently, the neodymium:yttrium-aluminum-garnet (Nd:YAG) laser has been found to be a useful tool for endoscopic surgery, and it also would become acceptable for resection of pulmonary tumors.l"!' However, there have been no reports on the influence of aggressive excision and evaporation of multiple lung metastases with the use of the laser on long-term survival. The objectives at the present study are to retrospectively compare the results of median sternotomy and lateral thoracotomy and evaluate the usefulness of aggressive excision with the Nd:YAG laser for patients with pulmonary metastases. Moreover, we also attempt to analyze the interaction between the aggressive surgical management and the impact of intensive chemotherapy in a subset of patients with metastatic lung cancer.
Patients and methods From May 1969 to September 1989, 106 patients had operations for metastatic lung cancer from various sites. One case of unknown origin and five cases that were lost to follow-up were
901
The Journal of Thoracic and Cardiovascular
9 0 2 Kodama et al.
Surgery
Table I. Characteristics ofpatients with metastatic lung tumors Characteristic
No. of patients Age (yr) Range Mean Sex distribution Male Female Metastatic pattern Solitary Multiple Approach Median sternotomy Lateral thoracotomy Resection With Nd:YAG laser Without Nd:YAG laser Primary site Colorectal Renal Lung Head and neck Breast Testicular Ovary and uterus Bladder Soft tissuesarcoma Osteosarcoma Others
100 8-79 53 62 38 57 43 35 65 25 75 21 13 12 9 8 6 4 3 15 4 5
excluded. There were 100 patients eligible for inclusion. The characteristics of the 100 analyzed patients are summarized in Table I. The mean age at the time of the first thoracotomy was 53 years (range 8 to 79 years). Sixty-two patients were male and 38 were female (ratio 1.6:1). There were 57 solitary and 43 multiple metastases. A mean of 5.9 nodules were resected per patient (range 1 to Ill). Median sternotomy was used for 35 patients and lateral thoracotomy for 65 patients. The Nd:YAG laser was used in 25 patients. The primary tumors were located in the colorectum (n = 21), kidney (n = 13), lung (n = 12), head and/or neck (n = 9), breast (n = 8), testis (n = 6), ovary and/or uterus (n = 4), bladder (n = 3), soft tissue sarcoma (n = 15), osteosarcoma (n = 4), or other site (n = 5). The soft tissue sarcoma consisted of four synovial sarcomas, three liposarcomas, three alveolar soft part sarcomas, and one each of the following: malignant fibrous histiocytoma, leiomyosarcoma, meningioma, malignant schwannoma, and Ewing's sarcoma. The histologic classification of the primary tumor was carcinoma in 81 patients and sarcoma in 19 patients. The reason for the small number of cases of osteosarcoma was that, since the principal objective of our institution is the treatment of adult diseases, younger patients, who are more likely to have osteosarcoma, were not available for this study. Preoperative evaluation. After excision of the primary tumor, patients were evaluated by thoracic computed tomographic (CT) scanning or linear tomography, or both, every 3 to 6 months for 2 years. Patients with newly developing abnor-
Table II. Comparison of background factors between patients undergoing median sternotomy and patients undergoing lateral thoracotomy Characteristic
Median sternotomy
No. of patients 35 Laser surgery Applied 18 Not applied 17 Disease-free interval (DFI) -sr yr 19 14 I < DFI < 5 yr 2:5 yr 2 No. of metastases ::s3 II 2:4 24 Maximal tumor diameter (em) ::s3 24 >3 II
Lateral thoracotomy
x2 Test
65 7
58
p
14 35 16
p
59 6
p
32 33
< 0.01 NS
NS, Not significant.
malities consistent with pulmonary metastases were offered resection of the metastases if the primary tumor was controlled, if extrapulmonary metastases were absent, and if the amount of lung tissue remaining would provide the patient with sufficient pulmonary parenchymal reserve." Aggressive resection of multiple lung metastases was initiated in our department in 1983. Before that year routine CT scanning had not been performed, and operation was indicated only for metastases that were diagnosed as definitely solitary on the basis of a chest tomogram. Since 1983, CTscan images (resolving power) have been strikingly improved, thereby enabling us to detect small lesions, and thus CT also has come to be widely used for screening of metastatic lesions. Therefore, even if the lesion is not solitary, we use lateral thoracotomy if the lesions are unilateral, the number is no more than a few, and their size is almost uniform. Operative procedure. Lateral thoracotomy was adopted for patients whose linear tomography and/or CT scan detected only a solitary lesion or a small number of unilateral lesions and there was no change in either the size or number of primary and/or metastatic sites in the unilateral lung throughout chemotherapy. Conversely, metastases involving the bilateral lungs were resected through median sternotomy. In the treatment of testicular carcinomas, chemotherapy consisting mainly of cisplatin, vinblastine, and bleomycin was administered. For some of the soft tissue sarcomas chemotherapy consisting mainly of ifosfamide, vincristine, doxorubicin (Adriamycin), and dacarbazine was administered, whereas chemotherapy mainly consisting of doxorubicin, methotrexate, and cisplatin was administered for osteosarcoma. a-Interferon was administered in the treatment of renal cell carcinoma. The excision of the metastasis after intensive chemotherapy usually was undertaken from 4 to 8 weeks after the last course of chemotherapy to ensure optimal preoperative health and recovery of the patient. After 1986 the Nd: YAG laser was frequently used to preserve as much pulmonary function as possible and to achieve the most complete resection of the lesions. The laser equipment consisted of a MediLas 2 type 621 Nd:YAG laser (MBB-Medical Technology Ltd., Munich, Federal Republic of Germany).
Volume 101
Lung metastases
Number 5 May 1991
903
100 90
80 ..J
70
:::>
40
« > 60 ...... > 50 0::: (f)
30
20 10
00
5
20
15
10 TIME (YRS)
Fig. 1. Overall survival after resection of the primary lesion (open circles) and after excision of the metastasis (closed
circles). This device is capable of generating and delivering power up to 100 W to the operative site for up to 9.9 seconds. A focusing handpiece with an interchangeable optic was used. With this hand applicator as a noncontact mode, the energy density can be changed by altering the distance to the tissue. The beam can be focused on a small spot (0.4 mm) or used to treat large surfaces for excision, evaporation, or fulguration of the tissues. The power setting used for all resections was 45 to 50 W of continuous-wave energy. The timer of the laser was set at the maximum (9.9 seconds) and then reset repeatedly to irradiate for the necessary time. Resection was performed as follows. For tumors on the surface of the lung, the lung was inflated, and the laser beam was irradiated to the parenchyma adjacent to the tumor. This caused evaporation of the parenchyma directly exposed to the irradiation and separation of the tumor from the surrounding parenchyma, resulting in isolation of the tumor without any manipulation. Conversely, for tumors located in the parenchyma, that is, tumors in a deep region of the lung, the lung was deflated, the site of the tumor was confirmed by palpation, laser irradiation was applied to the site immediately above the tumor, and the parenchyma was evaporated. When the tumor was pushed up from the underside with a finger, into the field of irradiation, it became visible as a hemispheric shape. The tumor was isolated easily when the surrounding parenchyma was evaporated by the laser beam. Small tumors with a diameter of less than a few millimeters were evaporated by direct exposure to laser irradiation. After confirming that there was no bleeding from the punched-out parenchyma as a result of laser treatment, we sutured wounds on the lung surface to prevent postoperative air leakage. Statistical analyses. Survival duration was computed from the date of the initial excision of the metastasis or from the date of treatment of the primary tumor until the date of the last known follow-up or date of death. Survival curves were plotted with the life-table method or the Kaplan-Meier method. Estimates of median survival time and survival rates at specific time points were derived from these curves. The z test was used for
Table III. Comparison of background factors between the patients with and without laser surgery Characteristic
Laser surgery
No laser surgery
25
75
18 7
17 58
P < 0.01
13 10 2
20 39 16
p
10 15
60 15
p
17 8
39 36
NS
No. of patients Approach Median sternotomy Lateral thoracotomy Disease-free interval (OFf) ::0 I yr I yr < OFf < 5 yr 2:5 yrs No. of metastases
s3 2:4
X2 Test
< 0.05
Maximal tumor diameter (em)
::03 >3 NS. Not significant.
statistically comparing two survival curves. Statistical analysis for significant differences between the two groups in terms of the distribution of each of the patient-background factors presented in Tables II and III was performed by the x 2 test. When the p value was less than 0.05, the difference was regarded as significant.
Results There were no perioperative deaths in this series. One hundred patients underwent 107 thoracic explorations. The survival curves for the total number of patients from the time of treatment of the primary site and the time of the first excision ofthe metastasis in the lung are presented in Fig. 1. Overall survival rates after resection of the
904
The Journal of Thoracic and Cardiovascular
Kodama et al.
Surgery
100 90 80 ..J 70 <:( > 60 ......
>
0::
::>
(f)
?R
m I
I
:
::
:!
-~,
~r:l I_~! ~a(-·L.: ~-2I :
50
.._ ..
(n=13)
L-...l;.....L---------- 1
40
30 20 10 0
.---.L._J_. ....J HEAD & NECK (n=9)
:
:
~
I
BREAST (n=8) I •••••• _•••••••••••••• ~ .••• _•••J I I I I
' - - - - - - - - - ' COLO-RECTAL (n=2l)
I LUNG (n=12) I
0
3
10
5
15
TIME (YRS)
Fig. 2. Survival after excision of the metastasis in cancer patients as a function of the site of the primary lesion.
...1._---------100 I 90 'I II 80 'L ~ ..J 70 ~ 60 , I > L-'=-=+----'1 0::: 50 I , ~ I (J) 40 I, I 30 I LJ I, 20 10 I 0 0 3
TESTICULAR (n =6) OVARY & UTERUS (n =4) BLADDER (n=3)
I
I-i
I
OTHERS(n=5)
'*
5
10
15
TIME (YRS) Fig. 3. Survival after excision of the metastasis in cancer patients as a function of the site of the primary lesion.
primary tumor were 67% at 5 years and 40% at 10 years, whereas the rates after the first pulmonary operation to remove the lesion were 45% and 30%, respectively. The survival curves from the time of the first excision of the metastasis as a function of the primary site are presented in Figs. 2 to 4. The best outcome was achieved with patients who had head and neck cancer. Both the 3- and 5-year survival rates were 85%, and the median survival time has not been reached. The 3-year survival rates in colorectal, breast, renal, and lung cancers were 66%, 60%, 50%, and 43%, respectively. The 5-year survival rates in
those groups were 57%, 30%, 50%, and 43%, respectively. The median survival time in those groups were 66,38, 22, and 24 months, respectively (Fig. 2). Although the numbers of patients in other groups are too small for meaningful interpretation of the survival results, the treatment result in testicular cancer is noteworthy (Fig. 3). Four of six patients whose serum markers (o-fetoprotein and/or human chorionic gonadotropin) returned to the normal range after intensive chemotherapy had a good outcome attributable to resection of residual multiple metastases with the Nd: YAG laser. The 3- and 5-year
Volume 101
Lung metastases 9 0 5
Number 5 May 1991
100 90 80 ..J
70
« 60
> .......
> 50 0::: ::J
(/)
'*
40 30
I I I
SOFT-TISSUE SARCOMA (n=15)
I I
I
t.; --I OSTEOSARCOMA (n =4)
20 10 OL...---...,.-----,-----....-------r----o 3 5 10 15 TIME (YRS)
Fig. 4. Survival after excision of the metastasis in patients with soft tissue sarcoma and osteosarcoma.
100
90 80 ...J
70
« 60 > ....... > 0::: 50 ::J
(J)
40
'''0,
30
'0,
'0,
"0--0--0. ,
20
10 0 0
5
boo -0- -0--0- -0-
10 TIME (YRS)
15
20
Fig. 5. Comparison of survival after excision of the metastasis between patients undergoing median sternotomy (closed circles) and lateral thoracotomy (open circles).
survival rates in soft tissue sarcoma were 53% and 40%, respectively, and the median survival time was 41 months (Fig. 4). To assess the influence of the type of incision on survival, we compared the two groups of patients undergoing excision of the lesion, either by median sternotomy or by lateral thoracotomy. The patient characteristics of these two groups are summarized in Table II. Laser surgery was used significantly more often in the median sternot-
omy group than in the lateral thoracotomy group. Both the use of median sternotomy for an approach to bilaterallesions and the advent oflaser surgery have come of age concurrently. The disease-free interval of the former group was significantly shorter than that of the latter group. The number of metastases in the latter group was significantly smaller than that in the former group. When the maximal diameter of the metastatic lesions was classified at the level of 3 em, there was no significant differ-
The Journal of
9 0 6 Kodama et af.
Thoracic and Cardiovascular Surgery
100 90
80 b :i; ..J
70
2:
60
«
> 0:: 50
:::>
(/)
'*
40
.. P'<'ii.05
\~!lL 'b_ -0--0,'0.,
30 20
"0--0-0.
''0- -0-0- -0- 0- -O-.()
10
O'--------'-----.. . . . - --_I....o
5
15
......l.._ _
20
Fig. 6. Comparison of survival after excision of the metastasis between patients undergoing laser surgery (closed circles) and those without laser surgery (open circles).
ence betweenthe two groups.The median survival was 46 months for both the sternotomy group and the lateral thoracotomy group, and no significantdifference existed between the two survival curves (Fig. 5). Standard wedge resection and/or enucleation of 259 lesions by 80 operations in 75 patients were performed without the Nd:YAG laser. Conversely, local excision of 418 lesions by 27 operations in 25 patients was performed with the Nd:YAG laser. In addition to thoselesions, small lesions of less than a few millimeters in diameter were directly evaporated with the laser. If many small lesions were presentand silicoticnodulesor other granulomatous lesions were suspected on the basis of the patient's occupation or history of disease, a biopsy specimen of one of the lesions was obtained before evaporation, and we determined whether it was a metastatic lesion by intraoperative histodiagnosis with frozen sections. Excision and evaporation required 5000 to 60,000 J per patient. The clinical characteristics of the patients in the two groups, with or without laser surgery, are presented in Table III. The median sternotomy approach was used for bilateral lung metastases in 18 of 25 patients who underwent laser surgery. In the statistical analysis the 25 patients in the laser surgery group included three whose lung metastases were first excisedby conventionalwedge resection, with subsequent laser resection of recurrent metastases. Significant differences between the two groups were found with regard to the approach, diseasefree interval, and number of metastases. No significant difference was found with regard to the maximal diameter of the tumor. The 3-year and 5-year survival rates in the patients with laser surgery were 85% and 61%, whereas those in the patients without laser surgery were
54%and 42% (Fig. 6). The differencebetweenthe 2- and 3-year points in those two survival curves was significant (p < 0.05). Discussion
In 1979, McCormack and Martini I 5 reported that the overall 5-year survival rates after resectionof metastatic disease for 202 patients with sarcoma and 246 patients withcarcinoma were30%and 25%,respectively. In 1984, Mountain and colleagues' described772 resections in 556 patients who had metastatic disease, with an overall 5-year survivalrate of 35% after excision of the metastasis. To date we have performed resection of 677 metastatic lesions in 107operations in 100 patients. The overall5-year survivalrate obtained after the firstexcision was 45%.This rate is acceptable because it is superiorto overall survival achieved for resected primary lung cancer, and there was a low incidence of morbidity and mortality. In the analysisof site-specific survival results,an excellent outcome was achieved in the group of patients with head and neck cancer, with a 5-year survival of 85%. McCormack and Martini I 5 reported on 27 patients with head and neck carcinoma metastatic to the lung; these patients underwent pulmonary resection,and the overall 5-year survivalrate was 47%. This discrepancy is due to the fact that tumors from different organs or with a different histologic type within the head and neck have various tendencies to metastasize, and the outcome after excision also may be different. Median sternotomy is thought to be the best approach for bilateral surgical staging and complete one-stage resection." Roth and colleagues? reported that occult
Volume 101 Number 5 May 1991
contralateral metastases are present in about 20% of cases, and they indicate that there are bilateral metastases; one might use this as a strong argument to imply median sternotomy should be the procedure of choice rather than lateral thoracotomy. Surgery for metastatic lungdisease is localtherapy for a systemic problem. The purpose of surgical intervention for pulmonary metastasesis to decrease the tumor burden by removing maeroscopic disease in preparation for further therapy to control or eradicate microscopic foci. Thus complete resection of the lung lesion is necessary to increase the effectiveness of surgicalintervention. Mediansternotomy maximizes the role of surgeryin this context and is thus the procedure of choice whenever possible."! In comparison with the lateral thoracotomy group, the sternotomy group included significantly higher percentages of patients witha disease-free intervaloflessthan I yearand patientswith four or more metastatic lesions. The postthoracotomy survival was not significantly different for the two groups. Therefore we also recommended this approach if there were no severe pleural adhesions. If a patienthas a historyof clear pleuritis and, in addition,if chestx-rayfilms demonstratepleuralthickening and calcification, 'we inspect the respiratory movement (i.e., expiratory phaseand inspiratory phase) of the thickened pleura by visualization with x-ray films and estimate whetherpleural adhesion is present. When severe adhesion is suspected at the preoperative evaluation, we recommend staged lateral thoracotomy. Superior survival was achieved in the laser-treated group, althoughtheirclinical background wasnotas good as that of the nonlaser group.Althoughour experience is limited toonly18cases, onthe basisofthe data fromthem weconsider the combination of median sternotomy and lasersurgery to be a safe surgicalmethod and a promisingvariation in technique. We expectthat this approach will expandthe scope of surgicalindications for multiple metastaticlesions. In an early experimental study, LoCicero and colleagues!' demonstrated that the Nd:YAG lasercan be a useful adjunct to maximally preserve normal lung tissue and to seal bleeding, leaking, and raw lung surfaces. Recently, Moghissi'? reported that the Nd:YAG laser wasefficacious in eliminating pulmonarynodularlesions by local excision and evaporation in 14 patients with a solitary nodule, particularlyin high-risk patients such as thosewithlimitedrespiratory function and in the elderly. Moreover, LoCicero and colleagues':' found the laser to be an excellent adjunct for pulmonary resection on the basis of their experience with localexcision of 32 pulmonary lesions in 26 patientswhohad marginal pulmonary function or deepparenchymal lesions that werenot amenableto wedge resection.
Lung metastases
907
It has been indicated that intensive chemotherapy, including cisplatin, is capable of playing a major role in eradicatingall evidence of metastaticdiseasein testicular cancer''and osteosarcoma.l" In such casessurgicaltreatment is indicatedto eradicate and reclassify lesions that stabilize but do not disappeartotallywith chemotherapy because of a high rate of recurrenceat thosesitesof metastatic lesions. Excluding one patient with a seminoma, whom we treated before intensive chemotherapy came into wide use, the remaining five of the six patients with testicular carcinoma treated by us had nonseminomatous tumors. These five patients already had severe multiple pulmonary metastases when we performed high orchiectomy, and thus we administered intensive chemotherapy. As a result, in each case the shadows on chest x-ray films becamesmallerin both sizeand number but did not disappear completely. Thus all of these cases required surgical treatment. The serum markers did not return to their normal rangesin oneofthe five patientsbeforethe operation,and thispatientdiedofrecurrenceearlyafter resection of lung metastases. The serum markers returned to their normal ranges before the operation in the remaining four patients,and the excised tumorshad undergone complete necrosis in three of them. The remainingcase is interesting in that viable malignant cells were demonstrated in only one of 57 resected tumors. Those findings indicate that viable malignant cells may be present even if the serum markers have returned to their normal ranges so long as shadows remain on the chest x-ray films. Moreover, there alsois a possibility that tumorscontain malignant cells that do not produce any markers. Therefore, evenif the serum markers have returned to their normal ranges,it is desirable to resect residualshadows as thoroughlyas possible. Under these circumstances the surgical methodusingthe Nd:YAG laser with median sternotomy can be a suitable approach for this purpose. We encountered only four casesof osteosarcoma. For each case we performed intensive chemotherapy in the treatment of multiplelung metastases. However, despite the chemotherapy, the lung metastases increased in two cases, and the patientseventually died of recurrenceearlyafter resection of the metastaticlesions. The remaining two patients had operations after a partial response to chemotherapy was obtained, and they are now free of disease. Althoughit is tooearly to draw any hard conclusions, on the basisof these resultswe think that surgical treatment is not. indicated for patients in whom lung metastases advancedespite intensive chemotherapy. Multiplelungmetastases ofsofttissuesarcomas,which are characteristically relatively slow growing and resistant to chemotherapy, also seem to be a good indication
9 0 8 Kodama et al.
for laser surgery. Recently, Jablon and colleagues'? reported that resection of pulmonary metastasis in patients with soft tissue sarcomas is associated with longterm survival, particularly in patients with a disease-free interval of more than I year and with no more than five nodules. However, they have not performed laser-assisted resection. In our series of soft tissue sarcomas three patients with alveolar soft part sarcomas had multiple metastases numbering more than 30 nodules, and those metastases had already been present when the original diagnosis was made. In such cases survival must be influenced by those metastases after complete resection of the primary site. IS, 19 Thus it is reasonable to extend the operative indications for the Nd:YAG laser to such cases, and prolonged survival is likely. On the basis of the results of the present study, we believe that the combination of median sternotomy and Nd:YAG laser surgery is a safe technique that expands the scope of surgical indications for lung metastases, especially bilateral multiple lung metastases. However, it is necessary to carefully consider the result of preceding chemotherapy and the biologic behavior of the tumor before deciding to operate. REFERENCES 1. Thomford NR, Woolner LB, Clagett OT. The surgical treatment of metastatic tumors in the lung. J THORAC CARDIOVASC SURa 1965;49:357-63. 2. Sellors TH. Treatment of isolated pulmonary metastases. Br Med J 1970;2:253-6. 3. Choksi LB, Takita H, Vincent RG. The surgical management of solitary pulmonary metastasis. Surg Gynecol Obstet 1972;134:479-82. 4. Takita H, Edgerton F, Karakousis C, et al. Surgical management of metastases to the lung. Surg Gynecol Obstet 1981;152:191-4. 5. Mountain CF, McMurtrey MJ, Hermes KE. Surgery for pulmonary metastasis. Ann Thorac Surg 1984;38:323-30. 6. Regal A, Reese P, Antkowiak J, et al. Median sternotomy for metastatic lung lesions in 131 patients. Cancer 1985; 55:1334-9.
The Journal of Thoracic and Cardiovascular Surgery
7. Roth JA, Pass HI, Wesley MN, et al. Comparison of median sternotomy and thoracotomy for resection of pulmonary metastases in patients with adult soft-tissue sarcomas. Ann Thorac Surg 1986;42:134-8. 8. Mandelbaum I, Yaw PB, Einhorn LH, et al. The importance of one-stage median sternotomy and retroperitoneal node dissection in disseminated testicular cancer. Ann Thorac Surg 1983;36:524-8. 9. Rowland RG. Surgical management of post-chemotherapy residual testis tumor. In: Urologic oncology. Boston: Martinus Nijhoff, 1984:256-74. 10. Potter DA, Glenn J, Kinsella T, et al. Pattern of recurrence in patients with high-grade soft-tissue sarcoma. J Clin Oncol 1985;3:353-66. 11. LoCicero J III, Hartz RS, Frederiksen JW, et al. New applications of the laser in pulmonary surgery: hemostasis and sealing of air leaks. Ann Thorac Surg 1985;40:546-50. 12. Moghissi K. Local excision of pulmonary nodular (coin) lesion with noncontact yttrium-aluminum-garnet laser. J THORAC CARDIOVASC SURa 1989;97:147-51. 13. LoCicero J III, Frederiksen JW, Hartz RS, et al. Laser-assisted parenchyma-sparing pulmonary resection. J THORAC CARDIOVASC SURa 1989;97:732-6. 14. Holbert BL, Holbert JM, Libshitz HI. The chest radiograph after resection of pulmonary nodules with a neodymium-YAG laser. J Thorac Imaging 1989;4:82-6. 15. McCormack PM, Martini N. The changing role of surgery for pulmonary metastases. Ann Thorac Surg 1979;28:13945. 16. Pastorino U, Valente M, Gasparini M, et al. Lung resection for metastatic sarcomas: total survival from primary treatment. J Surg OncoI1989;40:275-80. 17. Jablon D, Steinberg SM, Roth J, et al. Metastatectomy for soft tissue sarcoma: further evidence for efficacyand prognostic indicators. J THORAC CARDIOVASC SURa 1989;97:695-705. 18. Evans HL. Alveolar soft-part sarcoma: a study of 13 typical examples and one with a histologicallyatypical component. Cancer 1985;55:912-7. 19. Lieberman PH, Brennan MF, Kimmel M, et al. Alveolar soft-part sarcoma: a clinico-pathological study of half a century. Cancer 1989;63:1-13.