Comparative study evaluating outcomes of lobectomy
and extended segmentectomy used in the treatment of
primary non- small cell bronchial carcinoma*
AIRTON SCHNEIDER(TE SBPT), PAULO ROBERTO KRIESE, LUIZ AUGUSTO LOPES DA COSTA,
TIAGO JOSÉ REFOSCO, CAROLINE BUZZATTI
Background: The use of partial lobectomy for primary tumors remains controversial.
Method: During the period from 1995 to 2000, we treated 733 cases of non- small cell bronchial carcinoma. Aft er clin ical evalu at ion an d su rgical st agin g, 191 pat ien t s were su bmit t ed t o su rgical resect ion . Of t hose 191 su rgeries, 63 were for locally advan ced t u mors an d 128 (69 segmen t ect omies an d 59 lobect omies) for
primary tumors. Post- operative FEV1 of at least 800 ml was used as a measure of surgical success. Extended
segmen t ect omies, in which t he resect ion passes t he in t ersegmen t al lin e, in clu din g t he paren chyma of t he adjoin in g segmen t , were u sed.
Results: Among the 128 patients with primary tumors, there were 3 deaths and 10 patients fell out of contact. Therefore, 62 segmentectomies and 53 lobectomies were evaluated. There were 72 adenocarcinomas and 43 epidermoid carcinomas. The 5- year survival of lobectomy patients was 80% (T1N0), 72.7% (T2N0), 50% (T1N1) and 31.8% (T2N1), whereas that of segmentectomy patients was 80% (T1N0), 66.6% (T2N0), 41.1% (T1N1) and 30% (T2N1) (p > 0.05). Tumor size and enlarged interlobar lymph nodes were prognostically significant (p < 0.001), although method of resection influenced neither survival nor local or remote recurrence (p > 0.05).
Conclusion: Extended segmentectomy represents an alternative treatment for primary tumors in patients with limited lung reserve.
Key words: Lung Neoplasms, surgery. Pulmonary Surgical Procedures. Carcinoma, Non- Small- Cell Lung.
* St u d y ca rried o u t in t h e Serviço d e Ciru rg ia To rá cica o f t h e Un iversid a d e Lu t era n a d o Bra sil.
Co rre sp o n d e n ce t o : Airt o n Sch n e id e r. Ru a Ce l. Bo rd in i 8 9 6 / 4 0 4 . CEP 9 0 4 4 0 - 0 0 3 Po rt o Ale g re , RS. Ph o n e : 5 5 - 51 - 3 3 3 0 9 8 5 4 . E- m a il: a irt o n sc@ t e rra .co m .b r
Abbreviations used in this paper:
NSCBC – No n - sm a ll cell b ro n ch o g en ic ca rcin o m a FEV1 – Fo rced exp ira t o ry vo lu m e in o n e seco n d CNS – Cen t ra l n ervo u s syst em
DNA – Deo xyrib o n u cleic a cid
INTRODUCTION
The in ciden ce of n on - small cell bron chogen ic c a rc in o m a (NSCBC) in t h e Un it e d St a t e s is a p p ro xim a t e ly 1 4 0 ,0 0 0 n e w c a s e s p e r ye a r. Approximately 14% of those new cases may be cured, principally those in which the carcinoma is localized (stages 1 and 2)(1). It is known that lobectomy is the
only curative treatment for early-stage NSCBC. However, a recommendation for lobectomy is made based not only on the extent of the disease but also on the potential resultant postoperative lung capacity(2). Since
most NSCBC patients present pulmonary comorbidities t h at rest rict t h eir fu n ct io n al reserve, lo b ect o m y becomes limited as a therapeutic option.
Co m p ared t o lo b ect o m y, lim it ed resect io n m ay o ffer less lo ss o f fu n ct io n fo r NSCBC p a t ien t s, red u cin g p o st o p erat ive m o rb id it y an d en h an cin g t h e ch an ces fo r a seco n d resect io n t o t reat a n ew prim ary carcin om a or pu lm on ary m et ast asis(3 ). The
o b ject ive o f t h e p resen t st u d y was t o p resen t t h e resu lt s o b t ain ed fro m reviewin g o u r exp erien ce in t h e c lin ic , c o m p a r in g lim it e d r e s e c t io n t o lobect omy for t he t reat men t of early- st age NSCBC.
METHOD
Du rin g t he period from 1995 t o 2000, 733 cases of NSCBC were diagn osed. Pat ien t s were su bmit t ed t o det ailed physical examin at ion , laborat ory an d cardiologic evalu at ion , pu lmon ary fu n ct ion t est s, c o m p u t e d t o m o g r a p h y s c a n s o f t h e c h e s t , mediast in u m, an d u pper abdomen , an d fiber- opt ic b ro n ch o sco py. All m et a st a t ic lesio ns, id en t ified t h ro u g h clin ica l e va lu a t io n o r im a g in g , we re confirmed by anatomopathological examination. All pat ien t s eligible for resect ion were su bmit t ed t o ce rvica l m e d ia st in o sco p y a n d le ft p a ra st e rn a l mediast in ost omy for t u mors in t he u pper left lobe. Only 199 patients could be treated surgically. Of those, 6 9 we re su b m it t e d t o se g m e n t e ct o m y, 5 9 t o lobect omy, 52 t o lobect omy in volvin g resect ion of t h e ch est wa ll, a rt ery o r b ro n ch u s, a n d 1 9 t o pneumonectomy. In 128 patients, tumors in the initial s t a g e s (T1 - 2 N0 1 M 0 ) w e re t re a t a b le (6 9 segmentectomies and 59 lobectomies). The criterion for deciding between lobectomy and segmentectomy was based on predict ive post operat ive FEV1 valu es of at least 800 mL. The differen t ial in t he presen t st u dy was t he t ype of segmen t ect omy performed. We u sed t he ext en ded segmen t ect omy t echn iqu e described by Tsubota et al.(4) In this type of resection,
the bronchus and the segmental artery were isolated. Aft er in flat in g t he lu n g, segmen t al bron chi were st apled, an d t he remain in g n on - affect ed segmen t s were collapsed. At this moment, the inflated portion was iden t ified, correspon din g t o t he in t ersegmen t al line. The resection line was taken beyond the affected segmen t (i.e. resect ion in clu ded part of t he adjacen t s e g m e n t ) b y m e a n s o f s u r g ic a l s t a p le o r electrocauterization. Samples of hilar and mediastinal lymph n odes were also obt ain ed du rin g t he su rgical procedu re. When ever possible, frozen biopsy of t he lymph n ode in t o which t he segmen t drain ed was performed. That lymph n ode was defin ed as t he segmen t al sen t in el lymph n ode. In order for t he segmen t ect omy t o be con sidered complet e du rin g t he in t raoperat ive period, biopsy resu lt s for t his sen t in el lymph n ode shou ld be n egat ive, as shou ld t hose for t he resect ion margin s. When t he sen t in el lymph n ode was posit ive an d t he reserve preven t ed lobect omy, t he resect ion lin e also in clu ded t he local lymph node draining zone. The resected material was st u died an d classified in accordan ce wit h t he World Health Organization classification(5). Surgical staging
was performed in accordan ce wit h t he in t ern at ion al syst em for st agin g lu n g can cer(6). Su rgery mort alit y
was defined as death within 30 days following surgery. Local recurrence was defined as any cancer recurrence adjacent to the resected area that presented the same h is t o lo g ic a l r e s u lt s . P a t ie n t s s u b m it t e d t o chemot herapy or radiot herapy were exclu ded from t he st u dy. Aft er hospit al discharge, pat ien t s had periodical visits with their attending physicians every 3 months during the first year, every 4 months during t he secon d year an d every 6 mon t hs from t he t hird ye a r o n . Pa t ie n t s we re su b m it t e d t o p h ysica l examin at ion an d chest X- ray in every visit .
Su rvival was est im at ed an d calcu lat ed u sin g Ka p la n - Me ie r su rviva l cu rve s(7 ), in wh ich t h e
st a rt in g p o in t w a s t h e d a t e o f t h e su rg ic a l p ro ced u re an d t h e en d p o in t was eit h er m o rt alit y o r t h e last d ay o f t h e year 2 0 0 0 . Th e in flu en ce o f each variab le o n su rvival was calcu lat ed u sin g t h e ch i- sq u are t est an d Co x m u lt ivariat e an alysis(8 ).
Fig ure 1 – Five- yea r (6 0 - m o n t h ) su rviva l cu rves fo r a ll p a t ien t s in clu d ed in t h e st u d y. *Neg a t ive o u t co m e wa s d esig n a t ed a s eit h er d ea t h o r lo ss o f co n t a ct .
Wilco xo n t est(9 ) an d p aired variab les were st u d ied
u sin g Fish er’s exact t est . In t h ese cases, st at ist ical sig n ifican ce was also set at p < 0 .0 5 .
RESULTS
Th ere were 3 d ea t h s (2 ca ses o f ven t ila t o ry in su fficien cy cau sed b y in fect io n an d 1 case o f m yo card ial in farct io n ) an d 1 0 p at ien t s fell o u t o f co n t a ct . Sixt y- t wo p a t ien t s were su b m it t ed t o seg m en t ect o m y an d 5 3 p at ien t s were su b m it t ed t o lo b ect o m y. Seven t y- t wo p at ien t s (6 2 .6 %) were d ia g n o se d wit h a d e n o ca rcin o m a , wh e re a s 4 3 p at ien t s (3 7 .4 %) were d iag n o sed wit h ep id erm o id carcin oma. The proport ion of bot h t ypes of t u mors was t h e sam e b et ween t h e t wo g ro u p s (lo b ect o m y a n d s e g m e n t e c t o m y) (p < 0 .0 5 ). Fo llo w - u p exam in at io n s were p erfo rm ed fro m t h e su rg ical p ro ced u re eit h er t o m o rt alit y o r u n t il t h e en d o f t h e year 2 0 0 0 . In t h e seg m en t ect o m y g ro u p , t h e 5 - year su rvival am o n g t h e 1 0 T1 N0 p at ien t s was 8 0 %. Th ere were 2 d eat h s in t h is g ro u p : 1 cau sed b y lo cal recu rren ce an d 1 d u e t o m et ast asis in t h e cen t ral n ervo u s syst em (CNS). Th e 5 - year su rvival am o n g t h e 1 5 T2 N0 p at ien t s was 6 6 .6 %. Of t h e 5 d ea t h s o ccu rrin g in t h is g ro u p , 3 were d u e t o causes u n relat ed t o t h e can cer, 1 was d u e t o lo cal recu rren ce, an d 1 was at t rib u t ed t o m et ast asis t o t h e CNS. Th e 5 - year su rvival am o n g t h e 1 7 T1 N1 p at ien t s su b m it t ed t o st ag in g was 41 .1 %. Of t h e
1 0 d eat h s o ccu rrin g in t h is g ro u p , 2 were fro m lo cal recu rren ce, 3 fro m m et ast asis, an d 5 fro m o t h er cau ses. Th e 5 - year su rvival am o n g t h e 2 0 T2 N1 p a t ie n t s w a s 3 0 % . Of t h e 1 4 d e a t h s o c c u rrin g in t h is g ro u p , 5 w e re f ro m lo c a l recu rren ce, 5 fro m d issem in at io n o f t h e d isease, an d 4 fro m o t h er cau ses. Wh en co m p ared wit h in t he sample, t u mor size an d t he presen ce of posit ive lym p h n o d es were p red ict ive o f wo rse p ro g n o sis (p < 0 .0 5 ). In t h e lo b ect o m y g ro u p (n = 5 3 ), t h e 5 - year su rvival am o n g t h e 1 0 T1 N0 p at ien t s was 8 0 %; 1 o f t h e d eat h s was cau sed b y m et ast asis t o t h e CNS an d t h e o t h er by lu n g can cer. Th e 5 - year su rvival am o n g t h e 11 T2 N0 p at ien t s was 7 2 .8 %; 2 o f t h e d eat h s were u n relat ed t o t h e d isease an d 1 was d u e t o g en eralized rem o t e recu rren ce. Th e 5 - year su rvival am o n g t h e 1 0 T1 N1 p at ien t s was 5 0 %. Of t h e 5 p at ien t s in t h is g ro u p wh o d ied , 2 had ot her t u m ors, 1 died of m yocardial in farct ion , 1 d ied d u e t o m et ast asis t o t h e CNS, an d 1 d ied d u e t o m u lt ip le m et ast ases. Th e su rvival o f t h e 2 2 T2 N1 p a t ien t s wa s 31 .8 % (n = 7 ). Th e 5 - yea r su rvival o f t h e 2 2 T2 N1 p at ien t s was 31 .8 %. Of t he 15 deat hs occu rrin g in t his grou p, 3 were from o t h er t yp es o f t u m o rs, 3 fro m lo cal recu rren ce, 3 fro m m et ast asis t o t h e CNS, 1 fro m g en eralized m et ast asis, an d 5 fro m o t h er cau ses. Tu m o r size an d t h e p resen ce o f p o sit ive lym p h n o d es were ag ain p ro g n o st ically sig n ifican t fo r su rvival (p < 0 .0 5 ). Fig u re 1 su m m arizes 5 - year- su rvival resu lt s fro m t h e g ro u p s o f p at ien t s su b m it t ed t o eit h er lo b ect o m y o r seg m en t ect o m y.
When we compared the results, we observed that su rvival, st age by st age, showed n o st at ist ically sign ifican t differen ces (p > 0.05; Fig. 2). Type of recu rren ce, cau se of deat h an d t ime in t ervals du rin g wh ich p a t ie n t s we re d ise a se - f re e sh o we d n o st at ist ically sign ifican t differen ces (p > 0.05). Table 1 co m p a res lo ca l recu rren ce in seg m en t ect o m y p a t ie n t s t o t h a t se e n in lo b e ct o m y p a t ie n t s. In ciden ce of met ast ases is shown in Table 2.
DISCUSSION
wh ich are p o t en t ial recu rren ce sit es(1 0 ). So m e o f
ju s t if ic a t io n s f o r lim it e d r e s e c t io n a r e t h e p reserva t io n o f p a ren ch ym a l fu n ct io n , red u ced morbidity and mortality, and shorter hospital stays(10).
Since the time that Jensik et al.(3) reported promising
segmen t ect omy resu lt s for t he t reat men t of early-st age bron chial carcin oma, it has been eearly-st ablished that segmentectomy should be used in patients with impaired ven t ilat ory reserve. These au t hors report ed t he 5- year su rvival amon g 69 pat ien t s t o be 56.4%. Va r io u s o t h e r s t u d ie s h a ve r e p o r t e d t h a t segmen t ect omy was n ot t he on ly cu lprit respon sible for the poor results obtained from surgical treatment of bron chial carcin oma. Macchiarin i et al. report ed n o correlat ion bet ween t u mor size an d su rvival(11 ).
The au t hors fou n d vascu lar in vasion an d mit ot ic in dex t o be more import an t . In a similar st u dy, Ichin ose et al. report ed t hat t he differen t iat ion degree an d DNA ploidy were more import an t as prognostic factors than was tumor size(12). In a study
coordin at ed by t he Lu n g Can cer St u dy Grou p, t he au t hors recommen ded t hat resect ion more limit ed t han lobect omy shou ld n ot be an opt ion for t he su rgical t reat men t of early- st age NSCBC becau se local recurrence was more frequent and survival was lower when compared t o lobect omy(10 ). However,
t he au t hors performed wedge resect ion , which is rat her differen t from segmen t ect omy, in 32.8% of t he cases. Lan dren eau et al. report ed t hat local recu rren ce a ft er lim it ed resect io n wa s h ig h er,
TABLE 1
Incidence of postoperative recurrence in relation to resection technique used
Recu rren ce
Yes No
n (% ) n (% )
Treat m en t Segmen t ect omy 9 (1 4 ,5 ) 5 3 (8 5 ,5 )
Lobect om y 3 (5 ,7 ) 5 0 (9 4 ,3 )
Tot al 1 2 (1 0 ,4 ) 103 (89,6)
TABLE 2
Incidence of postoperative remote metastasis in relation to resection technique used
Rem o t e m et ast asis
Yes No
n (% ) n (% )
Treat m en t Segmen t ect omy 1 0 (1 6 ,1 ) 5 2 (8 3 ,9 )
Lobect om y 8 (1 5 ,1 ) 4 5 (8 4 ,9 )
Tot al 1 8 (1 5 ,7 ) 9 7 (8 4 ,3 )
alt hou gh t he defin it ive progn ost ic fact or in t heir st u d y w a s t u m o r b io lo g y. Th e sa m e a u t h o rs su ggest ed t hat t u mors smaller t han 2 cm cou ld be t reat ed wit h limit ed resect ion procedu res(1 3 ). Warren
& Faber con clu ded t hat lobect omy did n ot improve su rvival for pat ien t s diagn osed wit h t u mors of less t han 3 cm in diamet er(1 4 ). These au t hors highlight ed
t he fact t hat local recu rren ce in pat ien t s su bmit t ed t o segmen t ect omy was 4.6 t imes higher, bu t , sin ce most pat ien t s t hat presen t ed recu rren ce died of remot e met ast ases, local recu rren ce did n ot act u ally affect su rvival in t heir st u dy.
The first cause of local recurrence must be attributed to incomplete resection in the margins or in interlobular lymph nodes. Affected interlobular lymph nodes are present in approximately 10% to 20% of peripheral lung tumors. Yamanaka et al. reported that 11.7% of patients with tumors smaller than 3 cm presented affect ed in t rapu lmon ary or in t ersegmen t al lymph nodes(15). These findings explain the high recurrence
rates after wedge resection. Wedge resection would have resulted in incomplete resection in approximately 6 .4 % o f t h e se p a t ie n t s, wh e re a s co n se rva t ive segmentectomy would have resulted in incomplete resection in approximately 11.7%.
There is n o dou bt t hat , if resect ion is an yt hin g less t han lobect omy, local recu rren ce is great er. In t he presen t st u dy, 14.5% of t he pat ien t s su bmit t ed
t o segmen t ect omy presen t ed local recu rren ce. At t he t ime of diagn osis, man y of t hese pat ien t s (38%) we re a lso d ia g n o se d wit h re m o t e re cu rre n ce . Alt hou gh less local recu rren ce (on ly 5.7%) was seen in lobect omy pat ien t s, su rvival an d t he in ciden ce of hemat ogen ou s met ast asis were t he same when compared t o segmen t ect omy pat ien t s (p > 0.05).
In order t o evalu at e limit ed resect ion in pat ien t s wit h lim it ed fu n ct io n a l reserve, Ko d a m a et a l. compared in t en t ion al segmen t ect omy (in pat ien t s wit h su fficien t reserve for lobect omy) t o obligat ory seg m en t ect o m y (in p a t ien t s wit h o u t su fficien t r e s e r ve )(1 6 ). Th e re s u lt s re ve a le d t h a t , w h e n
segmentectomy was performed in patients that could have been su bmit t ed t o lobect omy, su rvival was better, although there was no statistically significant differen ce when compared t o t hose su bmit t ed t o lobect omy (93% vs. 88%; p > 0.05). However, t here was a statistically significant difference in comparison t o t he grou p of segmen t ect omy pat ien t s presen t in g in su fficien t reserve (in which lobect omy was n ot an opt ion ). The 5- year su rvival of t hese pat ien t s was 48%. Local recu rren ce was comparable bet ween t he in t en t ion al segmen t ect omy an d lobect omy grou ps (2.2% an d 1.3%, respect ively), bu t differed in t he obligat ory segmen t ect omy grou p (11.8%)(16). These
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AC, Mo rr J , Riva rd MJ . Lim it ed resect io n fo r n o n - sm a ll c e l l l u n g c a n c e r : o b s e r v e d l o c a l c o n t r o l w i t h im p la n t a t io n o f I- 1 2 5 b ra ch yt h era p y seed s. An n Th o ra c Su rg . 2 0 0 3 ; 7 5 : 2 3 7 - 4 2 .
t u m o rs, even if t h ere is su fficien t reserve fo r lobectomy.
Variou s prot ocols have been u sed in at t empt s t o redu ce local recu rren ce aft er limit ed resect ion p ro ce d u re s. Mille r & Ha t ch e r re p o rt e d lo we r in cid en ce o f recu rren ce (6 .2 5 % vs. 3 5 %) wh en compared t o ot her cases of limit ed resect ion when co m b in e d wit h ra d io t h e ra p y in p a t ie n t s t h a t presen t ed FEV1 < 1 lit er(1 7 ). Mc Grat h et al. report ed
t h a t recu rren ce wa s 5 t im es less wh en lim it ed resect io n wa s co m b in ed wit h io d in e- 1 2 5 seed implan t at ion(18). In a recen t stu dy, Lee et al. reported
a 47% 5- year su rvival amon g pat ien t s su bmit t ed t o limit ed resect ion combin ed wit h brachyt herapy(1 9 ).
Expan ded or ext en ded segmen t ect omy differs fro m co n serva t ive seg m en t ect o m y b eca u se t h e resect ion lin e su rpasses t he in t ersegm en t al lin e, including the parenchyma of the adjoining segment. This t echn iqu e, described by Tsu bot a et al. in 1998, essen t ia lly u ses t h e sa m e st ep s a s co n serva t ive segmen t ect omy. Aft er isolat in g t he bron chi of t he segment to be resected, the anesthesiologist is asked t o in flat e t he lu n g, t he bron chi are clamped an d t he lu n g is allowed t o collapse. This delimit s t he in t e rse g m e n t a l lin e , wh ich is in clu d e d in t h e resect io n , u su a lly clo sed wit h su rg ica l st a p les. Intersegmental and intrapulmonary lymph nodes can t hu s also be resect ed.
In co n clu sio n , t h e fin d in g s rep o rt ed in t h is st u dy su ggest ed t hat ext en ded segmen t ect omy can b e an efficacio u s t o o l in t h e su rg ical t reat m en t o f p a t ie n t s wit h e a rly- st a g e t u m o rs wh e n t h e ir fu n ct io n al reserve is insu fficien t fo r lo b ect o m y. Survival was not statistically different among stages, alt h o u g h lo cal recu rren ce was h ig h er in p at ien t s su b m it t e d t o se g m e n t e ct o m y. A m u lt ice n t e r, ran d o m ized p ro sp ect ive st u d y sh o u ld b e carried out so that extended segmentectomy can be offered t o p a t ie n t s w h o s e r e s e r ve is s u f f ic ie n t f o r lobect om y.
