Lung cancer is the leading cause of cancer death in the world and in Korea [1,2]. In 2012, 1.82 million cases (12.9% of the total number of cancer cases) of lung cancer were diagnosed and it caused 1.6 million deaths worldwide. Interestingly, incidence rate among females in Eastern Asia is somewhat high, despite the low smoking rate [2,3]. In Korea, a total of 22,118 new cases of lung cancer were reported and the crude rate of lung cancer was 43.9 per 100,000 persons in 2012 [4]. It is estimated that there will be 25,640 new cases of lung cancer and a crude rate of 50.4 per 100,000 persons in 2015 [5]. In the United States, lung cancer survival has already improved and the incidence of localized lung cancer has increased [6,7]. Although surgical resection remains the treatment of choice for early-stage lung cancer, only 22% of new lung cancer cases are localized diseases in Korea [4,8,9].

The survival benefit of low-dose chest computed tomography (LDCT) related to a stage shift was reported in 2011 [10]. Additionally, differences in lung cancer incidence, smoking prevalence, and life expectancy patterns between males and females have been reported [1,11,12]. These factors related to population composition and cancer prevention policies can affect the incidence of the disease and treatment modalities.

Korea has abundant health care resources and utilization in terms of the number of hospitals, hospital beds, computed tomography scanners, and consultations with doctors per population [3]. The Korean government has operated National Health Insurance Service (NHIS), which covers over 98% of the Korean population, for over 30 years [13]. Additionally, the Korean Health and Insurance Review and Assessment Service (HIRA) collects reimbursement records from all claims made under NHIS and nation-wide information related to a specific disease, and treatment is available without patient identifiers. However, few studies have investigated national trends in lung cancer surgery, and some that have are out of date [14-17]. Thus, we investigated current trends in lung cancer surgery and identified demographic and social factors related to changes in these trends utilizing the Korean NHIS database from 2010 to 2014.

Lung cancer is the most common cancer and the leading cause of cancer death in the world [2]. In Korea, lung cancer is the third most common cancer in male patients and the fifth most common in female patients [4]. The age-standardized rate of lung cancer has not increased over the last five years; however, there has been a large change in the incidence pattern according to sex [1]. The incidence rate of lung cancer has declined in males and increased in females in Korea, as well as in Japan and the United States [7,18]. Consequently, the number of lung cancer surgeries has increased and the composition of patients has changed in terms of sex ratio and age distribution [14,15,17]. In Korea, the incidence of lung cancer was 2.3 times higher in male patients than in female patients in 2012 [4]. However, the male-to-female ratio of lung cancer surgery was 1.6 in 2012. These findings suggest that lung cancer of an operable stage is more likely in female patients than in male patients, which may result from lung cancer screening in conjunction with the distinctive characteristic of lung cancer in non-smoking Asian females.

Lung cancer is a disease that commonly afflicts the elderly and is the most common cancer in male patients and the third most common in female patients aged ≥ 65 years in Korea [1]. In 2012, patients aged ≥ 65 years accounted for 75.4% of new lung cancer cases; however, only 47.9% of patients aged ≥ 65 years underwent lung cancer surgery in Korea. Aging is a well-known definite risk factor for perioperative morbidities and mortality [19-21]. Some studies have raised concerns about the under-treatment of elderly patients [22,23], and the incidence of lung cancer surgery in elderly patients has been increasing [16].

According to the United Nations, the number of persons aged ≥ 80 years is expected to increase by a factor 10 from 2000 to 2050 in Korea [24]. Moreover, life expectancy is higher in females than in males [4,12]. Therefore, sophisticated surgical techniques and delicate perioperative management are essential to achieve successful surgical outcomes in elderly patients. Although elderly patients have commonly been considered to include patients aged ≥ 65 years [19], an increase in the number of elderly patient can result not only from the population aging, but also from an increase in the number of physically competent elderly patients who can tolerate surgical management [25,26]. A Japanese study revealed that the physical activity of healthy elderly individuals was more youthful by 7.5 years among men and by 10 years among women in the 2002 cohort than in the 1992 cohort [25]. Consequently, the proportion of female elderly patients undergoing lung cancer surgery is expected to increase steadily in the future.

The surgical procedures for lung cancer have changed over the last few years. The use of pneumonectomy for lung cancer treatment has been declining worldwide [14-16]. Our study found a decrease in the use of pneumonectomy and bilobectomy for lung cancer treatment that could be associated with stage shifts following lung cancer screening with LDCT and changes in the dominant histology type of lung cancer [10,27]. A National Lung Cancer Screening Trial found that LDCT screening decreased the proportion of advanced lung cancer [10]. Additionally, the NELSON lung cancer screening study demonstrated that lung cancers detected upon screening were often diagnosed at stage I, and that the diagnosis was made at a more favorable stage in female than male patients [28]. In a LDCT screening study of 1,520 participants conducted by the Mayo Clinic, only two bilobectomies and no pnemonectomies were performed among 53 patients found to have lung cancer upon screening [29]. The International Early Lung Cancer Action Program study reported that 85% of diagnosed lung cancer cases (412/484) were clinical stage I, and that only 10 bilobectomies (2.7%) and no pneumonectomies were performed among 375 lung cancer surgeries [30].

The centralization of lung cancer surgery is a somewhat distinctive phenomenon in Korea [17]. Although the nationwide incidence of lung cancer surgery has increased, this has only be experienced by tertiary hospitals. The case volumes in secondary hospitals have remained steady. Approximately 40% of tertiary hospitals designated by the Korean government (17/44) are located in the Seoul metropolitan area, which is home to 20% of the Korean population. However, over 60% of lung cancer surgeries were performed in tertiary hospitals in the Seoul metropolitan area over the last 5 years. Improvement in geographical accessibility and advanced transportation systems may have contributed to the centralization of lung cancer surgery in Korea. However, the primary reason is that people are opting for the most up-to-date and advanced treatments for lung cancer. Cancer management requires a multidisciplinary approach and involves surgical oncologists, pulmonologists, medical oncologists, radiologic oncologists, diagnostic radiologists, pathologists, and nursing staff as part of a well-organized team. Therefore, centralization to high-volume centers is an inevitable consequence, considering the social needs for efficient and qualified treatment. A positive relationship between hospital or surgeon volume and surgical outcomes has been established. However, efforts should be made to relieve centralization by maintaining the quality of lung cancer care in regional cancer centers to enable effective utilization of national health resources.

It should be noted that the present study has some limitations. Specifically, procedure code O1597 represents any mediastinal lymph node dissection with lung resection, regardless of the primary diagnosis. We could not identify lung cancer surgery without lymph node dissection or sampling. Although data based on the procedure code did not allow classification according to the primary diagnosis, anatomical pulmonary resection and mediastinal lymph node dissection/sampling are the standard surgical methods for primary lung cancer. Therefore, the proportion of cases not involving primary lung cancer and lung cancer surgery without lymph node evaluation was negligible in this investigation. Finally, data describing cancer stage and other co-morbidities were lacking, which influences the selection of the modalities for lung cancer treatment and surgical procedures.

This is the first study evaluating changes in lung cancer surgery trend in Korea based on national healthcare data. Remarkable findings include an increase in the use of lung cancer surgery in elderly patients and female patients, and a decrease in the proportion of patients requiring extensive pulmonary resection. Centralization of lung cancer surgery was also noted. These changes are expected to continue and should be considered in the reforming of lung cancer management systems in Korea.