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肺泡细胞癌

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肺泡细胞癌 ORIGINAL ARTICLES: GENERAL THORACIC B m C m A H ki M H , K an Sec , Un B the inc of Health Organization (WHO) classification in 1999. The clinical features of patients with BAC diagnosed accord- ing to the recently revised WHO classification have not yet been cla...
肺泡细胞癌
ORIGINAL ARTICLES: GENERAL THORACIC B m C m A H ki M H , K an Sec , Un B the inc of Health Organization (WHO) classification in 1999. The clinical features of patients with BAC diagnosed accord- ing to the recently revised WHO classification have not yet been clarified. In this retrospective study, we inves- tig for com no M we cm Jap we no tum les no acc R BA no pa Lymph node involvement was seen for 30 lesions (36%) of adenocarcinoma other than BAC, but not for any BAC lesions. The median duration of follow-up after surgery was 5.1 years. There was no recurrence in the postoper- ati fre su C de WH ev pa cu pa B its ma been distinct from those of other adenocarcinomas [1–3]. Bronchioloalveolar carcinoma has shown aerogenous, rat sit tha aft ap 16] acc (W O his W an adenocarcinoma with no evidence of stromal, vascu- lar, or pleural invasion. An excellent prognosis would justifiably be expected for BACs, which are noninvasive noma other than BAC, as evaluated by a repeat pathology review. Acc Ad Fac cho, Nakakoma-gun, Yamanashi 409–3898, Japan; e-mail: sakuraihm@ ybb.ne.jp. © 2 Pu G EN ER A L T H O R A C IC 004 by The Society of Thoracic Surgeons 0003-4975/04/$30.00 blished by Elsevier Inc doi:10.1016/j.athoracsur.2004.05.017 her than lymphatic, spread [4–9], and radiologic diver- y from focal to diffuse disease [10–12]. It was reported t there was an increase in the incidence of BAC year er year [13, 14]. In a recent series, BAC accounted for proximately 20% of adenocarcinomas of the lung [15, . However, the definition of BAC has been revised ording to the most recent World Health Organization HO) classification in 1999 [17]. adenocarcinomas. However, it is difficult to compare the results across many previous studies because of the changes in the WHO definition of BAC. Consequently, there is little information available on the clinicopatho- logic significance of BAC defined as a pathologic nonin- vasive lesion. Therefore, we retrospectively examined the pattern of recurrence and survival outcome in patients with re- sected BAC, which was defined as a noninvasive adeno- carcinoma based on the revised WHO classification, compared with the pattern in patients with adenocarci- epted for publication May 4, 2004. dress reprint requests to Dr Sakurai, Second Department of Surgery, ulty of Medicine, University of Yamanashi, 1110, Shimokato, Tamaho- ated the pattern of recurrence and survival outcome patients with resected BAC by pathology review, pared with those in patients who had adenocarci- ma other than BAC. ethods. From 1985 through 2002, 108 patients under- nt surgical resection for pulmonary adenocarcinoma 3 or less in diameter at the University of Yamanashi, an. All of the resected specimens of these 108 patients re pathologically reviewed again to confirm the diag- sis as BAC or adenocarcinoma other than BAC. The or was defined as BAC when the adenocarcinoma ion had a pure bronchioloalveolar growth pattern and evidence of stromal, vascular, or pleural invasion ording to the WHO classification (third edition). ronchioloalveolar carcinoma (BAC) of the lung is a subtype of adenocarcinoma that is characterized by unique growth pattern along the alveolar wall. So far ny of the clinical and radiologic features of BAC have ve course in patients with BAC for a 5-year disease- e survival rate of 100%, whereas the 5-year disease-free rvival rate for other adenocarcinoma was 63.5%. onclusions. The patients with resected BAC, which is fined as a noninvasive adenocarcinoma by the revised O classification, had an excellent prognosis. How- er, these results may depend on a strictly accurate thology diagnosis as BAC. Limited resection might be rative in patients with focal BAC based on evidence of thologic noninvasive features. (Ann Thorac Surg 2004;78:1728–33) © 2004 by The Society of Thoracic Surgeons n the other hand, the most recent revision of the tologic classification of lung and pleural tumors by HO [17] has clearly limited the designation of BAC to ronchioloalveolar Carcino entimeters or Less in Dia ssessment iroyuki Sakurai, MD, Yoh Dobashi, MD, Ei irochika Matsubara, MD, Shoji Suzuki, MD d Masahiko Matsumoto, MD, PhD ond Department of Surgery and First Department of Pathology ackground. Bronchioloalveolar carcinoma (BAC) of lung is a subtype of adenocarcinoma for which the idence is actually rising, but the histologic definition BAC has been recently changed by the revised World a of the Lung 3 eter: A Prognostic izutani, MD, unio Takano, MD, Shunya Shindo, MD, iversity of Yamanashi, Yamanashi, Japan esults. Twenty-five patients (23%) had a diagnosis of C, and 83 (77%) had a diagnosis of other adenocarci- ma. There was a female predominance among both tients with BAC and those with other adenocarcinoma. M Pa Fo 200 lun Su cou no Am ha dia pa tio Th or stu ter ad his rec sta the ser me for Op the Pa Fo sta aci cu by mi (th cin wa ha ev inv wa ve Th exp dis sli og car his tio vid ad lar su an na ev tum lym Ple tum tum lar pre lum A sh 79 (33 op 7 p tec su Su Sta A Ta cm Ch No Ag M R Sex M F Op L S Lym M H Su C I His B A P S M Pat S S S BA niz 1729Ann Thorac Surg SAKURAI ET AL 2004;78:1728–33 BRONCHIOLOALVEOLAR CARCINOMA PROGNOSIS G EN ER A L T H O R A C IC aterial and Methods tients r the 18-year period from January 1985 to December 2, there were 210 pulmonary resections for primary g adenocarcinoma at the Department of Thoracic rgery, University of Yamanashi, Japan. These ac- nted for 61% of all resections for primary lung carci- mas resected during the same period (344 resections). ong the 210 patients with adenocarcinoma, 108 (51%) d adenocarcinoma that measured 3.0 cm or less in meter and was located in the periphery of the lung renchyma, excluding patients with a history of resec- n of other malignancy or preoperative treatment. ese 108 patients with peripheral adenocarcinoma 3 cm less in diameter were the focus of this retrospective dy. Clinicopathologic records were reviewed to charac- ize patients with BAC compared with patients who had enocarcinoma other than BAC, and included age, sex, tory, serum tumor marker level, mode of resection, urrence, and survival. The surgical and postsurgical ges were determined according to the TNM system of UICC (Union Internationale Conte le Cancer) [18]. The um tumor marker carcinoembryonic antigen (CEA) was asured preoperatively in all patients. The normal range the CEA level at our institute was 5.0 ng/mL or less. erative death was defined as any death within 30 days of operation or during hospitalization. thology Examinations rmaldehyde-fixed, paraffin-embedded blocks were ined using hematoxylin-eosin, elastica, and periodic d-Schiff, and the entire nodule, including the largest t surface of the tumor, was retrospectively examined light microscopy. The histologic subtype was deter- ned based on the WHO classification revised in 1999 ird edition) as BAC, acinar, papillary, solid with mu- , or adenocarcinoma with mixed subtypes. The tumor s defined as BAC when the adenocarcinoma lesion d a pure bronchioloalveolar growth pattern and no idence of stromal, vascular, or pleural invasion. If asive foci were present within the tumor, the tumor s classified as adenocarcinoma mixed bronchioloal- olar subtype (adenocarcinoma with mixed subtypes). ese findings were independently investigated by two erienced pulmonary pathologists (Y.D., H.S.), and crepancies were resolved by joint examination of the des under a two-headed microscope. The two pathol- ists were masked with respect to outcomes when they ried out the classification of adenocarcinoma into the tologic subtype based on the revised WHO classifica- n. For the purpose of comparison, patients were di- ed into two groups: those with BAC and those with enocarcinoma other than BAC, such as acinar, papil- y, solid, or mixed subtypes. In addition, BAC was bdivided into three groups: nonmucinous, mucinous, d mixed mucinous and nonmucinous or indetermi- te. The following histopathologic findings were also aluated in the same slides: tumor size (maximum or dimension), pleural involvement, vascular/ fre phatic permeation, and lymph node involvement. ural involvement was classified as positive when the or was exposed on the pleural surface or when the or invaded the parietal pleura or chest wall. Vascu- /lymphatic permeation was evaluated according to the sence of identifiable tumor cells in the blood vessel en or lymphatic lumen, respectively. clinicopathologic summary of all 108 patients is own in Table 1. The patients ranged in age from 34 to years with a mean age of 65.3 years. Thirty-six patients %) were male and 72 (67%) were female. The mode of eration was lobectomy in 101 patients (94%). The other atients underwent limited resection such as segmen- tomy or wedge resection because of being at poor risk ch as impaired pulmonary or cardiovascular disease. rgical curability was complete in all patients. tistics �2 test or Fisher’s exact test was used to compare the ble 1. Characteristics of Patients With Adenocarcinoma 3 or Less in Diameter aracteristic Data . of patients 108 e (years) ean 65.3 ange 34–79 ale 36 (33%) emale 72 (67%) erative mode obectomy 101 (94%) egmentectomy/partial 7 (6%) ph node dissection ediastinohilar 98 (91%) ilar only/none 10 (9%) rgical curability omplete 108 (100%) ncomplete 0 (0%) tologic subtype by the WHO classification AC 25 (23%) cinar 9 (8%) apillary 10 (9%) olid with mucin 7 (7%) ixed subtypes 57 (53%) hological stage by TNM category tage I Total � 77 T1N0M0 73 (67%) T2N0M0 4 (4%) tage II Total � 14 T1N1M0 13 (12%) T2N1M0 1 (1%) tage III Total � 17 T1N2M0 14 (13%) T2N2M0 2 (2%) T4N1M0 1 (1%) C � bronchioloalveolar carcinoma; WHO � World Health Orga- ation. quencies between subgroups. A survival curve was est ini rec be tes con Re Cl Tw 83 na mi cla BA sh be ag na CE BA oth en cin ple wh me Ly in gro the ad the No Pr Th ye ea cin 5-y an 100 BA cou ad un no pa en cau les Ta Cli Ch Ag M R Sex M F CE � � Tu M R Ple N P Va p N P Lym i N N Pat I I BA oni Ta WH Cy No Mu Mi BA niz Fig 1730 SAKURAI ET AL Ann Thorac Surg BRONCHIOLOALVEOLAR CARCINOMA PROGNOSIS 2004;78:1728–33 G EN ER A L T H O R A C IC imated by the Kaplan-Meier method using the date of tial resection as the starting point and the date of urrence or last follow-up as the endpoint. Differences tween survival curves were assessed by the log-rank t. Deaths by causes other than lung cancer were sidered censored. sults inicopathologic Features enty-five patients (23%) had a diagnosis of BAC, and (77%) had a diagnosis of other adenocarcinoma (aci- r, n � 9; papillary, n � 10; solid with mucin, n � 7; xed subtypes, n � 57), according to the 1999 WHO ssification. The clinicopathologic characteristics of C compared with those of other adenocarcinomas are own in Table 2. There were no significant differences tween BAC and other adenocarcinoma with regard to e (p � 0.423) or sex (p � 0.519). There was a predomi- nce of female patients in both groups. An elevated A level was not observed in any of the patients with C, although this was observed in 18% of patients with ble 2. Relationship Between Histologic Subtype and nicopathologic Factors in Pulmonary Adenocarcinoma aracteristic Adenocarcinoma p Value BAC (n � 25) Other Adenocarcinoma (n � 83) e (years) 0.423 ean 64.0 65.7 ange 47–78 34–79 0.519 ale 7 (28%) 29 (35%) emale 18 (72%) 54 (65%) A (ng/mL) 0.022 5.0 25 (100%) 68 (82%) 5.0 0 (0%) 15 (18%) mor size (cm) 0.086 ean 1.9 2.1 ange 0.5–3.0 0.9–3.0 ural involvement 0.001 egative 25 (100%) 56 (67%) ositive 0 (0%) 27 (33%) scular/lymphatic ermeation 0.000 egative 25 (100%) 48 (58%) ositive 0 (0%) 35 (42%) ph node nvolvement 0.000 0 25 (100%) 53 (64%) 1–3 0 (0%) 30 (36%) hological stage 0.000 25 (100%) 53 (64%) I–IV 0 (0%) 30 (36%) C � bronchioloalveolar carcinoma; CEA � serum carcinoembry- c antigen level. er adenocarcinoma. There were no significant differ- nom rat ces in tumor size between BACs and other adenocar- omas (p � 0.086). None of the BAC lesions showed ural involvement or vascular/lymphatic permeation, ereas other adenocarcinomas showed pleural involve- nt in 33%, and vascular/lymphatic permeation in 42%. mph node involvement was seen for 30 lesions (36%) the other adenocarcinoma group, but not in the BAC up. The pathologic stage was IA in all of the lesions in BAC group, whereas 50 lesions (60%) in the other enocarcinoma group were stage IA. The distribution of cytologic subtype for BAC lesions is shown in Table 3. nmucinous subtype accounted for 82% of all BACs. ognosis e postoperative median duration of follow-up was 5.1 ar. There were no operative deaths. The 5-year dis- se-free survival rate in all 108 patients with adenocar- oma 3 cm or less in diameter was 70.0% (Fig 1). The ear disease-free survival rates for patients with BAC d those with adenocarcinoma other than BAC were % and 63.5%, respectively (Fig 2). No patients with C had recurrence in their postoperative clinical rse. One of the patients with BAC had a contralateral enocarcinoma 16 years after the initial resection and derwent a second resection. This lesion was an ade- carcinoma with a mainly bronchioloalveolar growth ttern. Although we could not morphologically differ- tiate second primary from pulmonary metastasis be- se of the histologic growth pattern similar to BAC, this ion was diagnosed as second primary adenocarcinoma ble 3. Cytologic Subtype of 25 BACs According to the O Classification tologic subtype No. of Patients nmucinous 21 (84%) cinous 2 (8%) xed mucinous and nonmucinous 2 (8%) C � bronchioloalveolar carcinoma; WHO � World Health Orga- ation. 1. Survival among all 108 patients with pulmonary adenocarci- a 3.0 cm or less in diameter. The 5-year disease-free survival e was 70.0% (95% confidence interval, 57.6% to 82.3%). ba [19 Co Be no (ac ina as gro ter ev W A of be gro mu typ un an If cla (an BA exc mo vis ne rep 83% pa rec cla BA ho for as cri ne pre be I sio log aci bla Tu me fin og joi mi the les gro inv tum cin or W wi bu the int ing de Se str tec [25 mo erv 3, wo cin of we les pa gio C be Fig nom veo BA Ta Wi Au Bre Vo Eb Re Fu Pre BA Ov 1731Ann Thorac Surg SAKURAI ET AL 2004;78:1728–33 BRONCHIOLOALVEOLAR CARCINOMA PROGNOSIS G EN ER A L T H O R A C IC sed on the previous report by Martini and Melamed ]. mment fore the 1999 revised WHO classification, adenocarci- mas of the lung were classified into four subtypes inar, papillary, BAC, or solid) based on their predom- nt histologic growth pattern. Then, BAC was regarded an adenocarcinoma with a striking alveolar replacing wth pattern, and so far its clinicopathologic charac- istics had been discussed in many researches. How- er, the definition of BAC was changed by the 1999 HO classification [1–8, 10–13, 15]. ccording to the revised WHO histologic classification lung and pleural tumors in 1999, adenocarcinoma can grouped into five subtypes according to the histologic wth pattern, ie, acinar, papillary, BAC, solid with cin formation, and adenocarcinoma with mixed sub- es. Among these, BAC is an adenocarcinoma with a ique replacing growth pattern along the alveolar wall d no evidence of stromal, vascular, or pleural invasion. an invasive component is identified, the tumor is ssified as adenocarcinoma mixed bronchioloalveolar d acinar or papillary, if present) subtype rather than C. Patients with BAC should be expected to have an ellent prognosis because BACs are noninvasive tu- rs. Nevertheless, in recent reports based on the re- ed WHO classification, resected stage I BACs were not cessarily associated with excellent 5-year survival. The orted 5-year disease-free survival rates were 73% to (Table 4) [14, 16, 20–22]. These reports included tients with distant metastasis as well as locoregional urrence. Perhaps these tumors should have been ssified as invasive adenocarcinoma rather than as C. These reports did not provide pathologic details on w closely they followed the WHO criteria. The issue a rigorous pathologic evaluation of tumors regarded 2. Survival according to the histologic subtype of adenocarci- a (Ad). The 5-year survival rates were 100% for bronchioloal- lar carcinoma (BAC) and 63.5% for adenocarcinoma other than C. BAC must be addressed. A standardized morphologic ae teria defining what constitutes invasive features are eded now. Unless the pathologic diagnosis as BAC is cise, the true clinicopathologic characteristics would equivocal. n the present study, the diagnosis of histologic inva- n was based on the 1999 WHO classification. Histo- ic invasion was suggested by tumor cells arranged in nic, papillotubular structures or solid nests in a fibro- stic stroma, often accompanied by collagenization. mors were classified as BAC only if the entire lesion t the WHO description. In the present study, these dings were independently investigated by two pathol- ists (Y.D., H.S.), and discrepancies were resolved by nt examination of the slides under a two-headed croscope. Thus, with respect to the tumor histology, all tumors without any invasive features within the ion, ie, the tumors showing a pure bronchioloalveolar wth pattern, had no pleural, vascular, or lymphatic olvement. In other words, an adenocarcinoma with or histology showing a pure bronchioloalveolar car- oma could be regarded as having no pleural, vascular, lymphatic invasion, although BAC according to the HO classification was defined as an adenocarcinoma th not only a pure bronchioloalveolar growth pattern t also no evidence of vascular or pleural invasion. On other hand, several reports have supposed that the erobserver concordance was poor for pathologic find- s in lung adenocarcinoma [23, 24]. The prevalent finition of histologic “invasion” would be essential. veral investigators have reported that disruption of the omal elastic framework, which is the supporting archi- tural structure of the lung, indicated tumor invasion , 26]. We pathologically examined not only the tumor rphology by hematoxylin-eosin staining but also pres- ation of the elastic framework by elastic staining (Fig A and B). Elastic staining highlights the elastic frame- rk quite well. The tumors were regarded as adenocar- omas other than BAC based on evidence of disruption the elastic framework. Consequently, it seemed that could accurately diagnose BAC as a noninvasive ion from a prognostic perspective, since none of the tients with BAC in our study had postoperative locore- nal recurrence or distant metastasis. onversely, mucinous BACs have been suggested to more likely than nonmucinous BACs to develop an ble 4. Postoperative 5-Year Survival Rates for Patients th Stage I BAC thor (Year) Prognosis athnach et al (2001) 74%, DFS lpino et al (2001) 74.9% (stage IA), DFS right et al (2002) 83.3%, Overall na et al (2003) 81%, DFS rak et al (2003) 71%/77% (stage IA/IB), Overall sent study 100%, DFS C � bronchioloalveolar carcinoma; DFS � disease-free survival; erall � overall survival. rogenous spread, which leads to an unfavorable prog- no de de oth sis wa les tha dif BA mu occ F tre can a p req wi res an con T1 be res Lu tha wa rec su siv res fea mi in tha sec inv fib ev sec fea sec fro as fea res iss T no pro a l cla ad pr “m alt im exp go R su gro att ma (C pa cou GG an pa his no wi I BA pa wh cor Lim Fig lin sta bro 1732 SAKURAI ET AL Ann Thorac Surg BRONCHIOLOALVEOLAR CARCINOMA PROGNOSIS 2004;78:1728–33 G EN ER A L T H O R A C IC sis [3, 5, 6, 27–29]. Immunohistochemical studies have monstrated that mucinous BAC was more likely to tach from the underlying basement membrane than er subtypes [30, 31]. In the present study, the progno- of resected BAC, whether mucinous or nonmucinous, s excellent although the number of mucinous BAC ions was quite small. Many reports have s
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