0
Original Research: Lung Cancer |

Impact of Histologic Subtyping on Outcome in Lobar vs Sublobar Resections for Lung CancerImpact of Histology on Lung Cancer Resection Type: A Pilot Study FREE TO VIEW

Francine R. Dembitzer, MD; Raja M. Flores, MD, FCCP; Michael K. Parides, PhD; Mary Beth Beasley, MD
Author and Funding Information

From the Department of Pathology (Drs Dembitzer and Beasley), Department of Cardiothoracic Surgery (Dr Flores), and Mount Sinai Center for Biostatistics (Dr Parides), Icahn School of Medicine at Mount Sinai, New York, NY.

CORRESPONDENCE TO: Francine R. Dembitzer, MD, Department of Pathology, Icahn School of Medicine at Mount Sinai, One Gustave Levy Place, New York, NY 10029; e-mail: Francine.Dembitzer@mountsinai.org


FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2014;146(1):175-181. doi:10.1378/chest.13-2506
Text Size: A A A
Published online

OBJECTIVE:  The 2011 International Association for the Study of Lung Cancer (IASLC)/American Thoracic Society (ATS)/European Respiratory Society (ERS) classification of pulmonary adenocarcinomas introduces adenocarcinoma in situ and minimally invasive carcinoma and categorizes adenocarcinoma with more extensive invasion by the predominant subtype. Data have shown that wedge or segmentectomy (W/S) may be appropriate for in situ and minimally invasive adenocarcinoma, but whether sublobar resection is appropriate for tumors with more extensive invasion is unclear. The aim of this pilot study is to evaluate whether there are any trends regarding the impact of invasion and subtypes of carcinoma regarding survival in lobectomy vs W/S procedures using a comprehensive histologic evaluation.

METHODS:  Eighty-five surgical specimens (59 lobectomies, 26 W/Ss) were reviewed. Histologic type, size, pleural, lymphovascular invasion, and necrosis were recorded. Adenocarcinomas were classified by 2011 IASLC/ATS/ERS guidelines with each histologic pattern recorded as a percentage of the total tumor. Statistical analysis was performed using SAS, version 9.2. Proportional hazards regression analysis was used to evaluate survival according to resection type (lobectomy or W/S) adjusting for tumor size and the predominant histology.

RESULTS:  Multivariate analysis did not show a statistically significant difference in survival between lobectomy and W/S specimens adjusting for tumor size, regardless of histologic subtype or other negative predictors of prognosis (P = .7704).

CONCLUSIONS:  Our findings corroborate the prognostic significance of the 2011 adenocarcinoma subtyping classification and additionally suggest that lobectomy does not offer an overall survival advantage over W/S regardless of histologic subtype. Therefore, this finding suggests that limited resection may be appropriate for small size tumors, particularly those ≤ 2 cm with invasive histology.

Figures in this Article

The surgical management of non-small cell lung carcinoma (NSCLC) has been an issue of debate since the early 1970s when anatomic segmentectomy was proposed as a possible treatment of stage I NSCLC.1 With the advent of more advanced radiographic techniques, the detection of small lesions and ground-glass opacities has increased,2 and the issue of whether to perform a lobectomy or a lesser surgical procedure, that is, segmentectomy or wedge resection, has met with renewed interest and remains controversial.35 The focus on radiographic ground glass opacities and small peripheral lesions, which largely correspond to adenocarcinomas (ADCs), prompted an intense study of this particular carcinoma subtype over the past two decades.69 The culmination of this review resulted in an updated classification of ADC issued by the International Association for the Study of Lung Cancer (IASLC)/American Thoracic Society (ATS)/European Respiratory Society (ERS), which was published in 2011 (Table 1).10 In addition to other guideline revisions from previous classification systems,11 this revision introduced the concepts of adenocarcinoma in situ (AIS) and minimally invasive adenocarcinoma (MIA). These two categories of ADC are associated with virtually 100% 5-year survival and, evidence suggests, are potentially amenable to treatment with either wedge or segmentectomy (W/S).10,1214 However, AIS and MIA account for only a small percentage of all lung carcinomas,10 with the vast majority of non-small cell carcinomas having a much poorer prognosis even at stage I.10 While the updated ADC classification scheme has been shown to correlate with prognosis, the impact of histologic subtype based on the updated classification system has not been thoroughly evaluated in regard to overall survival based on type of resection. The aim of this pilot study is to evaluate the potential significance of histologic subtype regarding survival in lobectomy vs W/S procedures, incorporating a comprehensive histologic approach.

Table Graphic Jump Location
TABLE 1  ] 2011 IASLC/ATS/ERS Classification of Pulmonary ADCs10

ADC = adenocarcinoma; AIS = adenocarcinoma in situ; ATS = American Thoracic Society; BAC = bronchioloalveolar carcinoma; ERS = European Respiratory Society; IASLC = International Association for the Study of Lung Cancer; MIA = minimally invasive adenocarcinoma.

A retrospective review of 85 surgical specimens from patients with NSCLC (59 lobectomy specimens, 19 wedge resections, and seven segmentectomy specimens) from the Department of Thoracic Surgery of The Mount Sinai Hospital obtained during the period of 2002 to 2010 were reviewed. Only node-negative tumors and resections with negative margins were included in order for the dataset to be as uniform as possible. The rationale in limiting our pilot study to patients that had node-negative results was to focus on the impact of histology and minimize confounding factors. Histologic type, tumor size, and the presence of pleural, vascular, or lymphatic invasion and necrosis were recorded. Subtypes of ADC were classified according to the 2011 IASLC/ATS/ERS guidelines with each histologic pattern recorded as a percentage of the total tumor. Non-ADC tumors were classified by current World Health Organization (WHO) criteria. All histologic sections were reviewed by two pathologists, with cases of ADC reclassified using 2011 guidelines as necessary. As there is currently no accepted grading system for lung carcinomas, grade was not separately evaluated. Tumors ≤ 3 cm were submitted entirely for histologic evaluation, and tumors > 3 cm were submitted at a minimum of one section per centimeter of tumor to ensure accurate classification of ADC in particular. Tumor size was taken from the pathology reports and verified with the findings on the histologic slides. For purposes of this study, the overall tumor size was used in the analysis to align with current American Joint Committee on Cancer (AJCC) staging guidelines. Comparison was made between patients with sublobar resections (W/S) vs patients who underwent lobectomy. Data including patient demographics, pathologic staging, and postoperative follow-up were obtained from surgical pathology reports and patients’ medical records. Pathologic staging was performed in accordance with the seventh edition of guidelines established by the AJCC.15 Mount Sinai Institutional Review Board approval was obtained and individual consent for the study waived (Mount Sinai IRB IFI322786).

Statistical Analysis

Statistical analysis was performed using SAS, version 9.2 (SAS Institute Inc). Proportional hazards regression analysis was used to determine whether survival differed according to resection type (lobectomy or W/S) adjusting for tumor size and the predominant histology. The principal question we addressed was whether survival differed according to resection type (lobectomy vs W/S) adjusting for tumor size and the predominant tumor histology. The analysis was based on 85 patients, 59 (69%) of whom underwent lobectomy. The cumulative probability of survival for each group was estimated using the Kaplan-Meier method. Results are summarized in terms of the hazard ratio (the instantaneous relative risk) and associated 95% CIs. The hazard ratio represents the relative increase (or decrease if < 1) in risk of mortality. The χ2 statistic and its associated P value are used to assess statistical significance.

Patients included 34 men and 51 women with an average age of 79 years (range, 52-96 years) and 74 years (range, 44-97 years), respectively. Mean follow-up time was 38 months (range, 11-96 months) for W/S and 64 months (range, 1-106 months) for lobectomy. Three patients in the W/S group died of disease (mean time to death, 32 months; range, 16-58 months), and 18 patients in the lobectomy group died of disease (mean time to death, 36 months; range, 1-77 months). No patients received chemotherapy or radiation therapy.

W/S cases had the following features: mean size, 1.9 cm (range, 0.8-5.2 cm); stage pT1a (17), pT1b (four), pT2a (four), pT2 (one). Histologic types included: AIS (one), MIA (eight), lepidic predominant (one), acinar predominant (four), papillary predominant (six), micropapillary predominant (zero), and solid predominant ADC (two), squamous cell (one), invasive mucinous ADC (one). In addition to the predominant subtype in ADC, the percentage of each histologic subtype present was recorded (data not shown). Regarding poor prognostic subtypes, nine tumors had a nonpredominant micropapillary component (ranging from 5% to 15% of the tumor), and one tumor had a nonpredominant solid component, comprising 10% of the tumor. Necrosis was present in three, lymphatic invasion in four, large vessel invasion in four, and visceral pleural invasion (VPI) in four.

Lobectomy cases had the following features: mean size, 2.7 cm (range, 1-6 cm); stage pT1a (22), pT1b (16), pT2a (14), pT2b (seven). Histology included AIS (two), MIA (two), lepidic predominant (four), acinar predominant (nine), papillary predominant (12), micropapillary predominant (one), solid predominant ADC (nine), squamous cell carcinoma (13), and invasive mucinous ADC (eight). In addition to the predominant subtype in ADC, the percentage of each histologic subtype present was recorded (data not shown). Twenty-one tumors had a nonpredominant micropapillary component (ranging from 2% to 35% of the tumor), and two tumors had a nonpredominant solid component (ranging from 10% to 45% of the tumor), respectively. Necrosis was present in 20, lymphatic invasion in 23, large vessel invasion in 10, and VPI in 11. The pathologic and histologic findings are summarized in Table 2.

Table Graphic Jump Location
TABLE 2  ] Summary of Pathologic/Histologic Results

VPI = visceral pleural invasion; W/S = wedge or segmentectomy. See Table 1 legend for expansion of other abbreviations.

For ADCs, subtypes AIS, MIA, and lepidic predominant tumors had the best prognosis and those with solid growth patterns had the worst prognosis (P = .0015), corroborating other studies. Solid and squamous subtypes are associated with significantly poorer prognosis compared with lepidic (a 13.6- and 5.5-fold increase, respectively), while acinar type is significant at the 0.054 level (Table 3). There were an insufficient number of micropapillary predominant ADC for analysis in this regard.

Table Graphic Jump Location
TABLE 3  ] Mortality Risk by Predominant Subtype of Invasive ADC

Histology is presented as predominant type with hazard ratios relative to lepidic subtype. See Table 1 legend for expansion of abbreviation.

Univariate analysis showed a significantly poorer prognosis with increasing tumor size (risk increases 39% for each unit increase in tumor size). Additionally, lymphatic invasion was present more often in lobectomy cases (85% vs 15%, P = .039) and was also associated with higher mortality (48% vs 14%, P < .001). No association between resection and survival was found for either pleural P = .148) or vascular (P = .091) invasion.

However, multivariate analysis did not show a statistically significant difference in survival between lobectomy and W/S specimens adjusting for tumor size, regardless of histologic subtype or other negative predictors of prognosis such as lymphatic, large vessel, or pleural invasion (P = .7704). The resulting survival curve is presented in Figure 1.

Figure Jump LinkFigure 1  Overall survival: lobectomy vs wedge or segmentectomy. resec = resection.Grahic Jump Location

Sublobar resection was first introduced in 1939 as a treatment of bronchiectasis.16 At that time, pneumonectomy was the standard treatment of NSCLC, but was associated with a 40% morbidity and mortality rate.17 By the 1970s, when clinically appropriate, the standard had shifted to the safer, less extensive, and apparently equally efficacious, lobectomy.18 In 1973, when Jensik et al1 proposed anatomic segmentectomy for the treatment of NSCLC, it was the treatment of choice particularly in high-risk patients with cardiopulmonary compromise who could not undergo lobectomy without significant morbidity and mortality.

Whether sublobar resection is in fact equivalent to lobectomy is still a matter of inquiry and debate and is the subject of several multicenter investigations, including the ongoing Cancer and Leukemia Group B study 140503. The Lung Cancer Study Group3 reported in a randomized trial a threefold increase in local recurrence rate between patients who underwent lobectomy vs those who were treated with sublobar resection (6.4% vs 17.2%) for T1N0 NSCLC. This finding was substantiated by others, who demonstrated increased local recurrence in patients undergoing a limited surgical procedure in a nonrandomized study, and better survival and fewer recurrences in patients who underwent lobectomy.4,19,20 Other studies have produced mixed results. Higher rates of local recurrence with simple wedge resection compared with lobectomy have been reported by Sienel et al,21 Okada et al,22 and El-Sherif et al.23 Others reported significant survival advantage of lobectomy compared with segmentectomy24 with yet other studies finding equivalent 5-year survival in patients with T1N0 tumors.25 Kondo et al26 found similar results in patients with < 1 cm tumors with overall 97% 5-year survivals in both groups, and others also demonstrated equivalent outcomes for less than lobectomy procedures in early stage disease.17,2729

Most of these studies did not take into account the differences in tumor subtype or histology, which is a limitation given that lung ADC consists of a heterogeneous group of neoplasms with varying biologic behavior and prognosis.10,30 Beginning with the landmark study by Noguchi et al,31 and corroborated by others, it was recognized that tumors with essentially pure lepidic growth had nearly 100% 5-year survival, an outcome markedly distinct from the majority of lung ADC. Based on this observation, the WHO in 1999 and 200411 defined what was then called bronchioloalveolar carcinoma (BAC) as a tumor with pure lepidic growth. Still, the majority of ADCs were classified as “mixed type” in the 2004 WHO classification, the category of ADC that encompassed the largest group of tumors, and which, by their diversity, possessed variable biologic behavior.32 Because these tumors have heterogeneous clinical, molecular, pathologic, and radiologic characteristics, the mixed category provided minimal practical information to the clinician regarding potential prognosis.10 To address the clinical need for a prognostic relevance, a multidisciplinary consensus classification was published jointly by the IASLC, ATS, and ERS in 2011 that included a reclassification of tumors with pure lepidic growth as AIS replacing the terminology of BAC.10 Second, a category of MIA was introduced based on data10,31 indicating that lepidic tumors with an invasive component equal to or < 5 mm have essentially the same survival as those with pure lepidic growth. The final major change was the elimination of the mixed category with the recommendation that ADC be categorized by the predominant histologic subtype (ie, lepidic, papillary, acinar, solid, or micropapillary) (Table 1). The intent was to provide clinical, that is, prognostic meaning to the former mixed category. Most studies have demonstrated the prognostic value in this classification system, with favorable (lepidic), intermediate (acinar and papillary), and poor (solid, micropapillary) prognostic categories.30,3234 The results of our pilot study corroborate prior data and demonstrated prognostic stratification based on tumor histology.

Studies have shown that W/S may be appropriate for small tumors with a ground glass or predominantly ground-glass appearance radiographically.1214,35 These tumors for the most part correspond to AIS or MIA.35 The impact of detailed histologic subtype analysis outside of these two categories has not been critically evaluated regarding resection type to date. Our study suggests that there is no difference in overall survival between sublobar (W/S) resection and lobectomy regardless of histologic subtype even in the presence of adverse prognostic features such as vascular, lymphatic, or pleural invasion. Tumor size did correlate with a worse outcome; however, for equivalent tumor size there was no difference in overall survival, even in tumors with histologic subtypes associated with a poor prognosis, that is, micropapillary and solid ADCs, regardless of whether these patterns comprised the predominant histology or any component of the tumor.

Limitations of our pilot study include the relatively small number of W/S specimens, retrospective nature of the study, the lack of uniform nodal sampling, higher percentage of pT1a tumors, and the absence of micropapillary predominant cases in our group of W/S, and data presented solely based on a pathologic staging system. Our study did demonstrate a decreased survival with increasing tumor size, although an optimal tumor size “cutoff” could not be established. Although we do not have complete information on disease-free as opposed to overall survival, all of the patient deaths in our study occurred in patients with tumors larger than 2 cm and two had lymphatic and pleural invasion. Our results combined with those of others2,26,35 support that W/S procedures are most appropriate for smaller tumors, particularly those ≤ 2.0 cm. All of our cases did have negative margins, but precise distance was not recorded in all cases so an optimal distance of clearance for the wedge resections in particular could not be calculated. Evaluation of optimal margin distance as well as expanding the study to include node-positive tumors is under way in a now ongoing, prospective study. Future studies will also address physiologic status, age, and preoperative comorbidities between the surgical groups, in addition to overall recurrence and survival rates.

The decision-making process involved in choosing a surgical procedure for any patient is a multifaceted one. The findings of this study suggest that the decision-making tree may be simplified. Our finding that there was no statistically significant difference in survival between lobectomy and W/S specimens adjusting for tumor size regardless of histologic type in both ADC and non-ADC types, even in the presence of other negative prognostic factors such as lymphovascular and pleural invasion, suggests that sublobar resection may be an acceptable surgical procedure not only for AIS and MIA, but for histologic subtypes of NSCLC with more extensive invasive components. While these results need to be replicated in larger studies and in ongoing multicenter trials, our results begin to provide the surgeon with a rationale for choosing a less extensive surgical alternative for NSCLC, regardless of histologic subtype, without compromising patient outcomes.

Author contributions: F. R. D. is guarantor and primary author of the manuscript. M. B. B. is senior author of the manuscript. F. R. D. and M. B. B. contributed to pathology review; R. M. F. contributed to review of surgical and clinical material; M. K. P. contributed to statistical analysis; and F. R. D., R. M. F., M. K. P., and M. B. B. contributed to writing and revision of the manuscript.

Financial/nonfinancial disclosures: The authors have reported to CHEST that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

Other contributions: We thank Jason Roth for assistance with data evaluation.

ADC

adenocarcinoma

AIS

adenocarcinoma in situ

ATS

American Thoracic Society

BAC

bronchioloalveolar carcinoma

ERS

European Respiratory Society

IASLC

International Association for the Study of Lung Cancer

MIA

minimally invasive adenocarcinoma

NSCLC

non-small cell lung carcinoma

VPI

visceral pleural invasion

WHO

World Health Organization

W/S

wedge or segmentectomy

Jensik RJ, Faber LP, Milloy FJ, Monson DO. Segmental resection for lung cancer. A fifteen-year experience. J Thorac Cardiovasc Surg. 1973;66(4):563-572. [PubMed]
 
Nakamura H, Saji H, Ogata A, Saijo T, Okada S, Kato H. Lung cancer patients showing pure ground-glass opacity on computed tomography are good candidates for wedge resection. Lung Cancer. 2004;44(1):61-68. [CrossRef] [PubMed]
 
Ginsberg RJ, Rubinstein LV; Lung Cancer Study Group. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Ann Thorac Surg. 1995;60(3):615-622. [CrossRef] [PubMed]
 
Landrenau RJ, Sugarbaker DJ, Mack MJ, et al. Wedge resection versus lobectomy for stage 1 (T1N0M0) non-small cell lung cancer. J Thorac Cardiovasc Surg. 1997;113:698-700.
 
El-Sherif A, Gooding WE, Santos R, et al. Outcomes of sublobar resection versus lobectomy for stage I non-small cell lung cancer: a 13-year analysis. Ann Thorac Surg. 2006;82(2):408-415. [CrossRef] [PubMed]
 
Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet. 1999;354(9173):99-105. [CrossRef] [PubMed]
 
Asamura H, Suzuki K, Watanabe S, Matsuno Y, Maeshima A, Tsuchiya R. A clinicopathological study of resected subcentimeter lung cancers: a favorable prognosis for ground glass opacity lesions. Ann Thorac Surg. 2003;76(4):1016-1022. [CrossRef] [PubMed]
 
Kodama K, Higashiyama M, Yokouchi H, et al. Prognostic value of ground-glass opacity found in small lung adenocarcinoma on high-resolution CT scanning. Lung Cancer. 2001;33(1):17-25. [CrossRef] [PubMed]
 
Suzuki K, Asamura H, Kusumoto M, Kondo H, Tsuchiya R. “Early” peripheral lung cancer: prognostic significance of ground glass opacity on thin-section computed tomographic scan. Ann Thorac Surg. 2002;74(5):1635-1639. [CrossRef] [PubMed]
 
Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244-285. [CrossRef] [PubMed]
 
Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and Genetics: Tumors of the Lung, Pleura, Thymus and Heart. World Health Organisation Classification of Tumours. Lyon, France: IARC Press; 2004.
 
Van Schil PE, Asamura H, Rusch VW, et al. Surgical implications of the new IASLC/ATS/ERS adenocarcinoma classification. Eur Respir J. 2012;39(2):478-486. [CrossRef] [PubMed]
 
Rami-Porta R, Wittekind C, Goldstraw P; International Association for the Study of Lung Cancer (IASLC) Staging Committee. Complete resection in lung cancer surgery: proposed definition. Lung Cancer. 2005;49(1):25-33. [CrossRef] [PubMed]
 
Blasberg JD, Pass HI, Donington JS. Sublobar resection: a movement from the Lung Cancer Study Group. J Thorac Oncol. 2010;5(10):1583-1593. [PubMed]
 
Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471-1474. [CrossRef] [PubMed]
 
Churchill ED, Belsey R. Segmental pneumonectomy in bronchietasis: the lingula segment of the left upper lobe. Ann Surg. 1939;109(4):481-489. [CrossRef] [PubMed]
 
Schuchert MJ, Abbas G, Pennathur A, et al. Sublobar resection for early-stage lung cancer. Semin Thorac Cardiovasc Surg. 2010;22(1):22-31. [CrossRef] [PubMed]
 
Shields TW. The fate of the patient after incomplete resection of bronchial carcinoma. Surg Gynecol Obstet Surg. 1974;139:569-574.
 
Miller DL, Rowland CM, Deschamps C, Allen MS, Trastek VF, Pairolero PC. Surgical treatment of non-small cell lung cancer 1 cm or less in diameter. Ann Thorac Surg. 2002;73(5):1545-1550. [CrossRef] [PubMed]
 
Martini N, Bains MS, Burt ME, et al. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg. 1995;109(1):120-129. [CrossRef] [PubMed]
 
Sienel W, Dango S, Kirschbaum A, et al. Sublobar resections in stage IA non-small cell lung cancer: segmentectomies result in significantly better cancer-related survival than wedge resections. Eur J Cardiothorac Surg. 2008;33(4):728-734. [CrossRef] [PubMed]
 
Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: the role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg. 2005;129(1):87-93. [CrossRef] [PubMed]
 
El-Sherif A, Fernando HC, Santos R, et al. Margin and local recurrence after sublobar resection of non-small cell lung cancer. Ann Surg Oncol. 2007;14(8):2400-2405. [CrossRef] [PubMed]
 
Whitson BA, Groth SS, Andrade RS, Maddaus MA, Habermann EB, D’Cunha J. Survival after lobectomy versus segmentectomy for stage I non-small cell lung cancer: a population-based analysis. Ann Thorac Surg. 2011;92(6):1943-1950. [CrossRef] [PubMed]
 
Okada M, Yoshikawa K, Hatta T, Tsubota N. Is segmentectomy with lymph node assessment an alternative to lobectomy for non-small cell lung cancer of 2 cm or smaller? Ann Thorac Surg. 2001;71(3):956-960. [CrossRef] [PubMed]
 
Kondo D, Yamada K, Kitayama Y, Hoshi S. Peripheral lung adenocarcinomas: 10 mm or less in diameter. Ann Thorac Surg. 2003;76(2):350-355. [CrossRef] [PubMed]
 
Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg. 2005;27(4):675-679. [CrossRef] [PubMed]
 
Schuchert MJ, Pettiford BL, Keeley S, et al. Anatomic segmentectomy in the treatment of stage I non-small cell lung cancer. Ann Thorac Surg. 2007;84(3):926-932. [CrossRef] [PubMed]
 
Carr SR, Schuchert MJ, Pennathur A, et al. Impact of tumor size on outcomes after anatomic lung resection for stage 1A non-small cell lung cancer based on the current staging system. J Thorac Cardiovasc Surg. 2012;143(2):390-397. [CrossRef] [PubMed]
 
Russell PA, Wainer Z, Wright GM, Daniels M, Conron M, Williams RA. Does lung adenocarcinoma subtype predict patient survival? A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol. 2011;6(9):1496-1504. [CrossRef] [PubMed]
 
Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer. 1995;75(12):2844-2852. [CrossRef] [PubMed]
 
Yoshizawa A, Motoi N, Riely GJ, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol. 2011;24(5):653-664. [CrossRef] [PubMed]
 
Okumura M, Goto M, Ideguchi K, et al. Factors associated with outcome of segmentectomy for non-small cell lung cancer: long-term follow-up study at a single institution in Japan. Lung Cancer. 2007;58(2):231-237. [CrossRef] [PubMed]
 
Sica G, Yoshizawa A, Sima CS, et al. A grading system of lung adenocarcinomas based on histologic pattern is predictive of disease recurrence in stage I tumors. Am J Surg Pathol. 2010;34(8):1155-1162. [CrossRef] [PubMed]
 
Okada M, Koike T, Higashiyama M, Yamato Y, Kodama K, Tsubota N. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg. 2006;132(4):769-775. [CrossRef] [PubMed]
 

Figures

Figure Jump LinkFigure 1  Overall survival: lobectomy vs wedge or segmentectomy. resec = resection.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1  ] 2011 IASLC/ATS/ERS Classification of Pulmonary ADCs10

ADC = adenocarcinoma; AIS = adenocarcinoma in situ; ATS = American Thoracic Society; BAC = bronchioloalveolar carcinoma; ERS = European Respiratory Society; IASLC = International Association for the Study of Lung Cancer; MIA = minimally invasive adenocarcinoma.

Table Graphic Jump Location
TABLE 2  ] Summary of Pathologic/Histologic Results

VPI = visceral pleural invasion; W/S = wedge or segmentectomy. See Table 1 legend for expansion of other abbreviations.

Table Graphic Jump Location
TABLE 3  ] Mortality Risk by Predominant Subtype of Invasive ADC

Histology is presented as predominant type with hazard ratios relative to lepidic subtype. See Table 1 legend for expansion of abbreviation.

References

Jensik RJ, Faber LP, Milloy FJ, Monson DO. Segmental resection for lung cancer. A fifteen-year experience. J Thorac Cardiovasc Surg. 1973;66(4):563-572. [PubMed]
 
Nakamura H, Saji H, Ogata A, Saijo T, Okada S, Kato H. Lung cancer patients showing pure ground-glass opacity on computed tomography are good candidates for wedge resection. Lung Cancer. 2004;44(1):61-68. [CrossRef] [PubMed]
 
Ginsberg RJ, Rubinstein LV; Lung Cancer Study Group. Randomized trial of lobectomy versus limited resection for T1 N0 non-small cell lung cancer. Ann Thorac Surg. 1995;60(3):615-622. [CrossRef] [PubMed]
 
Landrenau RJ, Sugarbaker DJ, Mack MJ, et al. Wedge resection versus lobectomy for stage 1 (T1N0M0) non-small cell lung cancer. J Thorac Cardiovasc Surg. 1997;113:698-700.
 
El-Sherif A, Gooding WE, Santos R, et al. Outcomes of sublobar resection versus lobectomy for stage I non-small cell lung cancer: a 13-year analysis. Ann Thorac Surg. 2006;82(2):408-415. [CrossRef] [PubMed]
 
Henschke CI, McCauley DI, Yankelevitz DF, et al. Early Lung Cancer Action Project: overall design and findings from baseline screening. Lancet. 1999;354(9173):99-105. [CrossRef] [PubMed]
 
Asamura H, Suzuki K, Watanabe S, Matsuno Y, Maeshima A, Tsuchiya R. A clinicopathological study of resected subcentimeter lung cancers: a favorable prognosis for ground glass opacity lesions. Ann Thorac Surg. 2003;76(4):1016-1022. [CrossRef] [PubMed]
 
Kodama K, Higashiyama M, Yokouchi H, et al. Prognostic value of ground-glass opacity found in small lung adenocarcinoma on high-resolution CT scanning. Lung Cancer. 2001;33(1):17-25. [CrossRef] [PubMed]
 
Suzuki K, Asamura H, Kusumoto M, Kondo H, Tsuchiya R. “Early” peripheral lung cancer: prognostic significance of ground glass opacity on thin-section computed tomographic scan. Ann Thorac Surg. 2002;74(5):1635-1639. [CrossRef] [PubMed]
 
Travis WD, Brambilla E, Noguchi M, et al. International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary classification of lung adenocarcinoma. J Thorac Oncol. 2011;6(2):244-285. [CrossRef] [PubMed]
 
Travis WD, Brambilla E, Muller-Hermelink HK, Harris CC. Pathology and Genetics: Tumors of the Lung, Pleura, Thymus and Heart. World Health Organisation Classification of Tumours. Lyon, France: IARC Press; 2004.
 
Van Schil PE, Asamura H, Rusch VW, et al. Surgical implications of the new IASLC/ATS/ERS adenocarcinoma classification. Eur Respir J. 2012;39(2):478-486. [CrossRef] [PubMed]
 
Rami-Porta R, Wittekind C, Goldstraw P; International Association for the Study of Lung Cancer (IASLC) Staging Committee. Complete resection in lung cancer surgery: proposed definition. Lung Cancer. 2005;49(1):25-33. [CrossRef] [PubMed]
 
Blasberg JD, Pass HI, Donington JS. Sublobar resection: a movement from the Lung Cancer Study Group. J Thorac Oncol. 2010;5(10):1583-1593. [PubMed]
 
Edge SB, Compton CC. The American Joint Committee on Cancer: the 7th edition of the AJCC cancer staging manual and the future of TNM. Ann Surg Oncol. 2010;17(6):1471-1474. [CrossRef] [PubMed]
 
Churchill ED, Belsey R. Segmental pneumonectomy in bronchietasis: the lingula segment of the left upper lobe. Ann Surg. 1939;109(4):481-489. [CrossRef] [PubMed]
 
Schuchert MJ, Abbas G, Pennathur A, et al. Sublobar resection for early-stage lung cancer. Semin Thorac Cardiovasc Surg. 2010;22(1):22-31. [CrossRef] [PubMed]
 
Shields TW. The fate of the patient after incomplete resection of bronchial carcinoma. Surg Gynecol Obstet Surg. 1974;139:569-574.
 
Miller DL, Rowland CM, Deschamps C, Allen MS, Trastek VF, Pairolero PC. Surgical treatment of non-small cell lung cancer 1 cm or less in diameter. Ann Thorac Surg. 2002;73(5):1545-1550. [CrossRef] [PubMed]
 
Martini N, Bains MS, Burt ME, et al. Incidence of local recurrence and second primary tumors in resected stage I lung cancer. J Thorac Cardiovasc Surg. 1995;109(1):120-129. [CrossRef] [PubMed]
 
Sienel W, Dango S, Kirschbaum A, et al. Sublobar resections in stage IA non-small cell lung cancer: segmentectomies result in significantly better cancer-related survival than wedge resections. Eur J Cardiothorac Surg. 2008;33(4):728-734. [CrossRef] [PubMed]
 
Okada M, Nishio W, Sakamoto T, et al. Effect of tumor size on prognosis in patients with non-small cell lung cancer: the role of segmentectomy as a type of lesser resection. J Thorac Cardiovasc Surg. 2005;129(1):87-93. [CrossRef] [PubMed]
 
El-Sherif A, Fernando HC, Santos R, et al. Margin and local recurrence after sublobar resection of non-small cell lung cancer. Ann Surg Oncol. 2007;14(8):2400-2405. [CrossRef] [PubMed]
 
Whitson BA, Groth SS, Andrade RS, Maddaus MA, Habermann EB, D’Cunha J. Survival after lobectomy versus segmentectomy for stage I non-small cell lung cancer: a population-based analysis. Ann Thorac Surg. 2011;92(6):1943-1950. [CrossRef] [PubMed]
 
Okada M, Yoshikawa K, Hatta T, Tsubota N. Is segmentectomy with lymph node assessment an alternative to lobectomy for non-small cell lung cancer of 2 cm or smaller? Ann Thorac Surg. 2001;71(3):956-960. [CrossRef] [PubMed]
 
Kondo D, Yamada K, Kitayama Y, Hoshi S. Peripheral lung adenocarcinomas: 10 mm or less in diameter. Ann Thorac Surg. 2003;76(2):350-355. [CrossRef] [PubMed]
 
Martin-Ucar AE, Nakas A, Pilling JE, West KJ, Waller DA. A case-matched study of anatomical segmentectomy versus lobectomy for stage I lung cancer in high-risk patients. Eur J Cardiothorac Surg. 2005;27(4):675-679. [CrossRef] [PubMed]
 
Schuchert MJ, Pettiford BL, Keeley S, et al. Anatomic segmentectomy in the treatment of stage I non-small cell lung cancer. Ann Thorac Surg. 2007;84(3):926-932. [CrossRef] [PubMed]
 
Carr SR, Schuchert MJ, Pennathur A, et al. Impact of tumor size on outcomes after anatomic lung resection for stage 1A non-small cell lung cancer based on the current staging system. J Thorac Cardiovasc Surg. 2012;143(2):390-397. [CrossRef] [PubMed]
 
Russell PA, Wainer Z, Wright GM, Daniels M, Conron M, Williams RA. Does lung adenocarcinoma subtype predict patient survival? A clinicopathologic study based on the new International Association for the Study of Lung Cancer/American Thoracic Society/European Respiratory Society international multidisciplinary lung adenocarcinoma classification. J Thorac Oncol. 2011;6(9):1496-1504. [CrossRef] [PubMed]
 
Noguchi M, Morikawa A, Kawasaki M, et al. Small adenocarcinoma of the lung. Histologic characteristics and prognosis. Cancer. 1995;75(12):2844-2852. [CrossRef] [PubMed]
 
Yoshizawa A, Motoi N, Riely GJ, et al. Impact of proposed IASLC/ATS/ERS classification of lung adenocarcinoma: prognostic subgroups and implications for further revision of staging based on analysis of 514 stage I cases. Mod Pathol. 2011;24(5):653-664. [CrossRef] [PubMed]
 
Okumura M, Goto M, Ideguchi K, et al. Factors associated with outcome of segmentectomy for non-small cell lung cancer: long-term follow-up study at a single institution in Japan. Lung Cancer. 2007;58(2):231-237. [CrossRef] [PubMed]
 
Sica G, Yoshizawa A, Sima CS, et al. A grading system of lung adenocarcinomas based on histologic pattern is predictive of disease recurrence in stage I tumors. Am J Surg Pathol. 2010;34(8):1155-1162. [CrossRef] [PubMed]
 
Okada M, Koike T, Higashiyama M, Yamato Y, Kodama K, Tsubota N. Radical sublobar resection for small-sized non-small cell lung cancer: a multicenter study. J Thorac Cardiovasc Surg. 2006;132(4):769-775. [CrossRef] [PubMed]
 
NOTE:
Citing articles are presented as examples only. In non-demo SCM6 implementation, integration with CrossRef’s "Cited By" API will populate this tab (http://www.crossref.org/citedby.html).

Some tools below are only available to our subscribers or users with an online account.

Related Content

Customize your page view by dragging & repositioning the boxes below.

Find Similar Articles
CHEST Journal Articles
PubMed Articles
  • CHEST Journal
    Print ISSN: 0012-3692
    Online ISSN: 1931-3543