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Special Features: Global Medicine |

Lung Cancer in ChinaLung Cancer in China: Challenges and Interventions FREE TO VIEW

Jun She, MD, PhD; Ping Yang, MD, PhD; Qunying Hong, MD, PhD; Chunxue Bai, MD, PhD, FCCP
Author and Funding Information

From the Department of Pulmonary Medicine (Drs She, Hong, and Bai), Zhongshan Hospital, Fudan University, Shanghai, China; and Department of Health Sciences Research (Dr Yang), Mayo Clinic, Rochester, MN.

Correspondence to: Chunxue Bai, MD, PhD, FCCP, Department of Pulmonary Medicine, Zhongshan Hospital, Fudan University, 180 Feng Lin Rd, Shanghai, 200032, China; e-mail: bai.chunxue@zs-hospital.sh.cn


Funding/Support: Supported in part by the Shanghai Leading Academic Discipline Project [Project Number B115]; the third program of “973”: “Early detection of lung cancer”; and the third program of “985”: “Research on cancer metastases and the clinical translation.” Dr Yang was supported by the Mayo Foundation for Medical Education and Research.

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


Chest. 2013;143(4):1117-1126. doi:10.1378/chest.11-2948
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In 2008, lung cancer replaced liver cancer as the number one cause of death among people with malignant tumors in China. The registered lung cancer mortality rate increased by 464.84% in the past 3 decades, which imposes an enormous burden on patients, health-care professionals, and society. We performed a systematic review of the published data on lung cancer in China between 1990 and 2011 to analyze the incidence and mortality rates, economic burden, and risk factors of cancer and the effectiveness of interventions. Lung cancer incidence varies within China. People in eastern China, especially women, likely have a higher risk of developing lung cancer than those in western China. The crude mortality rates from lung cancer in 2008 were 47.51 per 100,000 men and 22.69 per 100,000 women. The crude mortality rate was highest in Shanghai (76.49 per 100,000 men and 35.82 per 100,000 women) and lowest in Tibet (25.14 per 100,000 men) and Ningxia (12.09 per 100,000 women). Smoking and environmental pollution are major risk factors for lung cancer in China. Continuous efforts should be concentrated on education of the general public regarding lung cancer to increase prevention and early detection. Specific interventions need to be implemented to reduce smoking rates and environmental risk factors. Standardized treatment protocols should be adapted in China.

Figures in this Article

Lung cancer, a leading cause of cancer-related mortality in men and women throughout the world, is responsible for approximately 1.4 million deaths annually.1,2 According to statistics from the National Office on Tumor Cure and Prevention,3 about 600,000 people die of lung cancer each year in China. The World Health Organization estimates that the annual lung cancer mortality rate in China may reach 1 million by 2025.2

Lung cancer has replaced liver cancer as the number one cause of death among patients with malignant tumors in China.4 In the past 3 decades, mortality rates of esophageal, stomach, and cervical cancers have steadily declined. However, there has been a corresponding increase in lifestyle-related cancers, such as lung, liver, colon, breast, and bladder.3 Of these cancers, lung cancer mortality increased by 464.84% during the past 30 years.5 The morbidity and mortality rates of lung cancer in both urban and rural Chinese populations are higher than the worldwide average, presenting a major public health issue and imposing an enormous burden on patients, health-care professionals, and society.4,5 The aim of this review is to increase public awareness of the impact of lung cancer and, particularly, to accelerate the implementation of short- and long-term lung cancer prevention strategies.

Using a Web-based search strategy, we analyzed the published data on lung cancer in China from January 1990 to September 2011, including incidence and mortality rates, economic burden, risk factors, and effectiveness of interventions. We restricted the study time because the pre-1990 literature often did not have relevant and complete data in most Chinese journals; the common practice of contacting the corresponding authors was not effective before 1990 in China; therefore, we relied on the resources where a full-text article could be retrieved.

Selection Criteria

We searched PubMed, Web of Knowledge, Chinese National Knowledge Infrastructure, ChinaInfo, and Google for all types of articles published with the key words “lung cancer in China” plus “incidence” or “prevalence”; “mortality” or “death”; “economic burden” or “disease burden”; and “risk factors,” “prevention,” or “interventions” (Fig 1). In addition, we performed a manual search of references cited in the selected articles and searches for publicly available reports from official websites of Chinese government resources, such as the National Office for Cancer Prevention and Control, National Center for Cancer Registry, Disease Prevention and Control Bureau, Ministry of Health.4,5 Publications that did not provide relevant or complete data and simple case reports, case analyses, and comments were excluded.

Figure Jump LinkFigure 1. Literature search algorithm. The scope of this review focused on chronological and regional data within China that are based on facts and trends of lung cancer from 1990 to 2011. PubMed, Web of Knowledge, Google, Chinese National Knowledge Infrastructure, ChinaInfo, and Official websites of the Chinese government were used for the published literature search. A total of 502 articles were found, and 53 were analyzed, synthesized, and summarized.Grahic Jump Location
Data Review and Analysis Process

All records retrieved were in English or Chinese, although few abstracts had been translated from other Asian languages, including Japanese, Korean, and Hindi. The literature search, data retrieval, and content inspection were performed independently and in duplicate by two authors (J. S. and Q. H.). After reviewing records against the inclusion and exclusion criteria and removing duplicates, 428 records of interest were identified. Discrepancies were resolved by two authors (P. Y. and C. B.). Because all the data retrieved for the review have been drawn from studies reporting lung cancer facts and trends in China without intervention, the potential for publication bias was considered to be minimal.

Data collection and analysis were performed nationwide or for specific provinces targeted for cancer surveillance and monitoring. Studies often used different reference populations for age adjustment of incidence and mortality rates, whereas some data did not report age adjustment, using, instead, crude rates6; we describe these differences. Total cost of lung cancer inpatient care in China was reported for 6 years (1999, 2001, 2002, 2003, 2004, 2005)7; 2000 data were missing but were not likely to have changed the overall trends. The majority of the data regarding the world and the United States were obtained from the American Cancer Society and World Health Organization through published reports.1,2

Incidence

At present, population-based cancer registries are not well established nationwide in China, and epidemiologic data for cancer are limited at the province level. Using data collected between 1988 and 2005 from 10 cancer registries, Chen et al6 investigated lung cancer incidence rates in Beijing; Shanghai; Wuhan, Hubei; Harbin, Helongjiang; Cixian, Hebei; Qidong, Jiangsu; Jiashan, Zhejiang; Futuo, Guangxi; ChangLe, Fujian; and Linzhou, Henan. In 2005, the crude incidence rate was 49.35 per 100,000 population (63.7 per 100,000 men and 35.0 per 100,000 women) in these areas. The total new cases of lung cancer were 536,407, of which 264,249 were from urban areas (182,173 men and 82,076 women) and 272,158 were from rural areas (189,020 men and 83,138 women),6 whereas an estimated 172,570 new cases of lung cancer in the United States were expected in the same year.1 Lung cancer incidence rates in women increased faster than that in men, with an average annual increase of 1.63% from 1988 to 2005 (1.3% in men and 2.34% in women) (Fig 2). However, the rate of lung cancer in women has begun to decrease after a long period of increase in the United States.1 There were regional variations in the incidence of lung cancer across the China.8 According to a cross-sectional study in 2000, people living in eastern China, particularly women, had a higher lung cancer risk than those living in western China, and people living in urban areas had a higher risk than those living in rural areas.9 In Tianjin, lung cancer was the most common cancer in women. The age-adjusted incidence rates in men and women, respectively, were 56.1 and 18.2 per 100,000 in Shanghai; 55.9 and 37.0 per 100,000 in Tianjin, and 35.0 and 11.0 per 100,000 in Qidong, an eastern rural area in China.

Figure Jump LinkFigure 2. Incidence rate for lung cancer in China from 1988 to 2005. Data were collected from the National Office for Cancer Prevention and Control, National Center for Cancer Registry, Disease Prevention and Control Bureau, Ministry of Health.4,6Grahic Jump Location
Mortality

A population based cross-sectional study estimated the mortality profile of lung cancer in 31 provinces in China.10 In 2008, the crude mortality rate from lung cancer was 35.1 per 100,000 population (47.51 per 100,000 men and 22.69 per 100,000 women). The total estimated deaths from lung cancer were 493,348 (338,346 men and 155,002 women), whereas only 156,940 deaths from lung cancer were estimated in 2011 in the United States.1 The crude mortality rates were the highest in Shanghai (76.49 per 100,000 men and 35.82 per 100,000 women), and the lowest rates were in Tibet (25.14 per 100,000 men) and Ningxia (12.09 per 100,000 women) (Fig 3A). Lung cancer mortality varied widely among provinces. People living in eastern China had a higher mortality rate for lung cancer than those living in western China, and rates were higher in men than in women.11 However, the distribution of mortality rates in men and women was not always consistent (Fig 3B).12 These differences may correlate with extensive burning of biomass fuels in the home.13

Figure Jump LinkFigure 3. A, Distribution of lung cancer mortality in China according to province. B, Distribution of lung cancer mortality in China according to sex. Data were collected from the Ministry of Health of the People’s Republic of China Third National Retrospect Spot-check of Death-Causation.5,10Grahic Jump Location

Lung cancer mortality rate increased with age.13 In urban areas, it peaked in the 80- to 84-year age group, reaching 716.86 per 100,000 men and 318.26 per 100,000 women. In rural areas, the mortality rate in men peaked at 400.06 per 100,000 in 80- to 84-year-olds, whereas in women, the rate peaked at 205.92 per 100,000 in those the aged ≥ 85 years (Fig 4).5 Patients with lung cancer living in urban areas typically were 5 to 10 years younger.13 Compared with the lung cancer data collected in the 1970s in Beijing, the age at death has decreased by 5 to 20 years, and this phenomenon is expected to continue over the next 20 to 30 years. This trend was also noticed in other cities, such as Shanghai; Shenyang, Liaoning; and Guangzhou, Guangdong,13 predicting an increase of lung cancer mortality in the near future of China.

Figure Jump LinkFigure 4. Age-adjusted mortality rates for lung cancer. Lung cancer mortality rate increased with age.6Grahic Jump Location
Economic Burden

Currently, lung cancer imposes an enormous economic burden on both families and society.1 Based on data from the China Statistical Yearbook regarding the direct economic burden of lung cancer on medical services, the total number of inpatients with lung cancer rapidly increased from 174,066 in 1999 to 364,484 in 2005.7 The total cost of inpatients increased annually from $2.16 to $6.33 billion (Fig 5A), the average annual increase in total expenditures was 16.15%, and the distribution of costs changed from 1999 to 2005 (Fig 5B and 5C).7 These data reflect improvements in technology and treatment, which were associated with increases in the costs of diagnosis and therapy. A cross-sectional survey from the Shandong province showed that the total cost of lung cancer was $616.9 million in 2006, which accounted for 0.17% of the gross domestic product.14 However, the 5-year survival rate of lung cancer is only 10% to 14% in China.15 Given the substantial economic burden of lung cancer, it is important to reduce both the incidence and the treatment-related costs of this disease.

Figure Jump LinkFigure 5. Direct economic burden of inpatients with lung cancer between 1999 and 2005 in China. A, With the rapid increase of total number of inpatients with lung cancer, the total cost rose annually from $2.16 billion to $6.33 billion between 1999 and 2005. B, The proportion of drug, therapy, diagnostic, and assay costs in 1999. C, The proportion of drug, therapy, diagnostic, and assay costs in 2005. Data were collected from the China Statistical Yearbook.7Grahic Jump Location
Smoking and Exposure to Secondhand Smoke

Smoking is a well-established global health issue and a principal risk factor for lung cancer. The mortality rate of lung cancer is about 23 times higher in current male smokers and 13 times higher in current female smokers than in lifelong nonsmokers.16 The number of smokers in the world is expected to increase to at least 1.7 billion (1.2 billion men and 500 million women) by 2025.17 In China, about 30% of the world’s cigarettes are manufactured and consumed by an estimated 350 million smokers.18 In 2002, a population-based cohort study (n = 16,056) showed that there were no obvious geographic differences in male smokers but a marked difference in female smokers.12 High smoking rates were seen in northern and northeastern China. In addition, the prevalence of smoking in Chinese men had reached its peak; although no increase in female smoking rates were seen from 1996 to 2002,12,19 the incidence of lung cancer in women increased. These data suggest that the increased number of lung cancer cases in women may be secondhand smoke in the home, among other exposures. Indeed, the rate of passive smoking among female nonsmokers was 82.5% in 2006.20

Air Pollution

A meta-analysis of 12 case-control studies suggested that cooking smoke and secondhand smoke were the main risk factors for lung cancer in Chinese women.21 Rapid industrialization in China has led to increased energy consumption and industrial waste while at the same time improving health and quality of life.22 However, with the increased release of chemical toxins into the environment and the rate of environmental disasters,23,24 air quality in China is among the worst in the world.2224

Environmental or occupational exposure to substances such as arsenic, radon, asbestos, chromium, nickel, and tar can increase the risk for lung cancer.1,25 Polycyclic aromatic hydrocarbons (PAHs) are cancer-causing chemical compounds that are released into the air when fuels such as oil and coal are burned in factories and homes.26 A cross-sectional study showed that PAH levels were higher in eastern China, particularly in the North China Plain, eastern Sichuan Basin, and Guizhou province.27 For instance, in the Shanxi province, a major coal producing area, high levels of PAH emissions have resulted from the presence of thousands of small-scale coke ovens that operate without any restrictions.28 Although these provinces account for only 12% of China’s land area, they make up 48% of the nation’s fossil fuel and biomass consumption and 66% of industrial-coking coal use. In 2004, China’s PAH emission rate was about 114,000 metric tons, or 29% of the world’s total.27

Genetics

Many chromosomal changes have been identified in lung cancer, such as numerical abnormalities and structural aberrations, including deletions and translocations.29 A genome-wide association study was conducted in China30 that identified two new loci (13q12.12 and 22q12.2) in the Chinese population and several genetic variants (3q28, 5p15.33, 13q12.12, and 22q12.2) that contribute to lung cancer susceptibility in Han Chinese. In addition, women with the same number of smoking pack-years or rates of passive smoking as men appear to be more susceptible to developing lung cancer,31 suggesting a difference in functional genetics between the sexes at the molecular level. A high epidermal growth factor receptor mutation rate has been found in lung cancer tissue from Asian female nonsmokers.32 The impact of XRCC1 (x-ray repair cross-complementing group 1), XRCC3 (x-ray repair cross-complementing group 3), and NBS1 (Nijmegen breakage syndrome 1) polymorphisms on lung cancer incidence in women is also different than that in men.33 Estrogen and related compounds can increase the expression of cytochrome genes and the efficiency of tobacco metabolism, but the detoxification of PAH activates carcinogenesis.34 Given that there is no comprehensive database on lung cancer in China, it will be necessary to increase investment in organizing high-quality research and large-scale clinical trials.

Chronic Pulmonary Disease

Accumulating evidence supports chronic pulmonary disease as an independent risk factor for lung cancer. A population-based case-control study of 886 patients with lung cancer (656 men and 230 women) in the Gansu province showed that previous TB, chronic bronchitis, and emphysema were causally related to lung cancer.35 A study from the Yunnan province showed that previous chronic bronchitis correlates with increased lung cancer risk, especially for squamous cell carcinoma (adjusted hazard ratio, 1.57; 95% CI, 1.19-2.09). From the same study, asthma was associated with increased risk of small cell lung carcinoma (adjusted hazard ratio, 2.56; 95% CI, 1.38-4.75).36

Although the precise mechanism remains unclear, overlapping genetic susceptibility may be mediated through receptors expressed on the bronchial epithelium that implicate molecular pathways underlying both chronic pulmonary disease and lung cancer.37 A variety of oncogenic viruses in lung cancer (eg, human papilloma virus, John Cunningham virus, BK virus, cytomegalovirus) may affect cell cycling to prevent apoptosis or programmed cell death, thereby increasing gene mutation and promoting uncontrolled proliferation.38 Cancer formation combined with inflammation and remodeling, which creates the stromal tumor microenvironment that acts as a barrier for immune attack to tumor growth. Indeed, a stromal cell type that expresses fibroblast activation protein cells was identified as an immunosuppressive component of the tumor microenvironment.39

Smoking Cessation

Cigarette smoking is highly prevalent and associated with substantially increased morbidity and mortality as well as increased health-care expenditures in China. A large prospective cohort study (n = 169,871) showed a significant dose-response association between pack-years smoked and death from all causes in both men and women.40 The study estimated that across China, a total of 673,000 deaths (538,200 men and 134,800 women) was attributable to smoking in persons aged ≥ 40 years in 2005.40 However, the study did not estimate the effect of passive smoking on mortality in China.

Smoking is related to education level. Individuals who are less educated, poorer, and employed in stressful jobs are more likely to be heavy smokers and less likely to quit smoking than those with higher income and better education, which was defined as > 9 years of schooling.12 Despite an increasing smoking cessation rate from 9.4% in 1996 to 11.5% in 2002, equating to an increase of 10 million quitters, the proportion of smokers who had no intention to quit remained high at 74%.12 Based on the current patterns, it is expected that global tobacco-related mortality will increase to about 10 million deaths per year by 2030, with 70% of these deaths occurring in developing countries, including China.41 This is higher than the combined mortality from malaria, pneumonia, TB, and diarrheal diseases.42 These data suggest the urgent need for continued development of national programs on smoking cessation in China.

Smoking cessation programs have been relatively uncommon in China, and most smokers quit cigarette smoking because of chronic illness.43 Fortunately, the number of tobacco control activities is on the rise. The government is moving forward with the implementation of tobacco control measures and has strengthened its tobacco control capacity within the Chinese Center for Disease Control and Prevention.44 However, the government’s role in tobacco control is in conflict with the sale of tobacco products through its state-owned company and reliance on tobacco revenues.45 In addition, mortality and morbidity will not be reduced in the short term without the adoption of measures to increase smoking cessation among the about 300 million current smokers in China.41 Therefore, authorities should take responsibility for developing effective tobacco control policies and plans to decrease disease burden caused by smoking and passive smoking.12

Reducing Air Pollution

Environmental risk factors, especially air pollution, are a major source of lung cancer-related morbidity and mortality in China.23 Although some Chinese families have switched to cleaner fuels, > 75% of households continue to burn biomass fuels, such as coal, wood, and dung, for cooking and heating in open stoves in poorly ventilated homes, leading to severe indoor air pollution (Fig 6A, 6B) in almost all rural and many urban households and greatly contributing to the burden of disease.13 Indoor air pollution leads to concentrations of inhalable particles and carbon monoxide that frequently are 10 times higher than health standards and to about 420,000 premature deaths every year.46 It accounts for 20% of all deaths in China.47

Figure Jump LinkFigure 6. Air pollution in China. A and B, Biomass and coal use in almost all rural and many urban households causes indoor air pollution. C and D, Outdoor air pollution in China originates from many sources, including chemical releases from industry and a growing transportation sector. Photographs provided by Hao Jiamao, PhD.Grahic Jump Location

Coal and biomass smoke have been associated with a variety of negative health outcomes, the most notable being lung cancer. Therefore, reducing exposure to coal and biomass smoke is a major public health objective. For instance, adding chimneys to stoves has led to a > 50% reductions in risk of lung cancer in the Yunnan province.46,47 Despite significant investment by the National Improved Stove Program, improved indoor air quality remains an elusive goal in China. Since the early 1980s, the National Improved Stove Program has introduced > 180 million stoves. Compared with traditional stoves, the improved stoves were intended to have higher combustion efficiencies and to be coupled with chimneys for diversion of pollutants outdoors, thus leading to reduced indoor pollutant concentrations.47 Pollutant concentration reduction varies substantially with the type of improved stove.22,46 Piped gas and liquefied petroleum gas offer some hope, but widespread use of these clean fuels in rural households is unlikely to occur within the near future because of cost-and-supply issues.22 Hence, policies and technical interventions to reduce pollution are still of prime importance to public health.

In China, outdoor air pollution originates from many sources, including residential and industrial coal combustion; a growing transportation sector; chemical emissions from industry; outdoor burning of agricultural waste; and dust from construction, roads, and the desert (Fig 6C, 6D).22 Approximately 70% of electricity is generated by burning coal, and there are more motor vehicle emissions containing respirable particles not only within the cities but also in the adjacent regions. In 2000, outdoor air pollution led to roughly 470,000 premature deaths in China.45 Exposure to air pollutants is associated with lung cancer. The economic cost of mortality and morbidity that results from air pollution in a typical Chinese city is about 10% of that city’s gross domestic product.45 China’s efforts to reduce outdoor air pollution have focused on reduction of dust concentrations from the energy and industrial sectors. Media reports of industrial emissions of lead have increased, which has raised public awareness and occupation protection measures.22 The Chinese Ministry of Environmental Protection will invest roughly $410 million for environmental and health projects in the 12th Five-Year Plan.48 However, the concentrations of air pollutants in many Chinese cities are currently several times higher than that in cities in developed countries, and it is a long-term challenge to improve air quality in China.

Increasing Public Awareness

Education on a healthy life style, including smoking abstinence, a balanced diet, scientifically planned physical exercises, avoidance of repeated infection, and an optimistic attitude toward life (which might not directly prevent lung cancer but could make a person more likely to stop smoking and practice other healthy behaviors), could reduce the risk of lung cancer.49 In China, the general population lacks awareness of lung cancer risk factors. A population-based study showed that overall, 60% of individuals support banning smoking in public places, and 45% support banning all cigarette advertisements.13 Although there is no health education program available in rural areas, all patients are willing to read information about lung cancer.

The Chinese population also lacks general knowledge about lung cancer. Cough is the most common symptom, but many patients with cough neglect it. Most individuals living in rural areas are willing to seek Chinese traditional medicine when they have initial symptoms; however, traditional medicine does not enable early detection of substantial lesions. More than 80% of patients with lung cancer in China miss the optimal time for treatment, and as a result, they generally present with terminal disease.50 The problem of delayed diagnosis is serious, and it is important to increase awareness of lung cancer among the public to enhance prevention and ensure early detection.

Early Detection and Standard Treatment

Early screening and proper treatment may be the key to improving the prognosis of patients with lung cancer.51 Because lung cancer shows significant heterogeneity in clinical and pathologic aspects, there is a lack of ideal measures for early diagnosis. Chest radiograph, sputum examination, and fiberoptic examination of the bronchial passages have shown limited effectiveness in improving survival.1,52 A large, prospective, randomized screening trial sponsored by National Institutes of Health showed that a 20% decrease in mortality from lung cancer was associated with the use of low-dose CT scanning, although false-positive results were high.53 In the future, molecular markers in sputum and blood may offer a promising method for detecting lung cancers at earlier, more-operable stages.

Although the standard of National Comprehensive Cancer Network clinical practice guidelines in oncology is updated annually, physicians commonly do not follow these guidelines in China. The lack of appropriate clinical training may result in delayed diagnosis and improper treatment. A population-based cohort study in patients with stage I lung cancer (n = 19,702) found that 82% underwent surgical resection, and their 5-year overall survival rate was 54%, whereas for untreated stage I disease, the 5-year overall survival rate was only 6%.50 In patients who did not receive surgery, 78% died of lung cancer within 5 years.50 In some primary hospitals, physicians often choose treatment according to their preference rather than the patient’s condition. For example, patients with stage I lung cancer receive chemotherapy whether the margin is negative or positive after surgical resection; patients with stage IV lung cancer are given only traditional herbs, not chemotherapy or procedures for controlling symptoms or improving quality of life. Greater attention to standardizing the clinical management of lung cancer is required, particularly regarding diagnosis and treatment.

Lung cancer morbidity and mortality have increased rapidly in China over the past 30 years, especially in women, with tobacco consumption and environmental pollution being the major risk factors. For the general population, continuous efforts should be concentrated on health education to increase awareness, prevention, and early detection of lung cancer. For the Chinese government, specific and timely interventions need to be implemented to reduce smoking rates and air pollution in China. For medical care providers, standardized clinical management protocols based on well-acknowledged professional guidelines should be enforced in treating patients with lung cancer and helping them to maintain a good quality of life.

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.

Role of sponsors: The sponsor had no role in the design of the study, the collection and analysis of the data, or in the preparation of the manuscript.

Other contributions: We thank Hao Jiamao, PhD, for his help in the search of related references and for providing photographs.

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Sun Y, Ren Y, Fang Z, et al. Lung adenocarcinoma from East Asian never-smokers is a disease largely defined by targetable oncogenic mutant kinases. J Clin Oncol. 2010;28(30):4616-4620. [CrossRef] [PubMed]
 
Ryk C, Kumar R, Thirumaran RK, Hou SM. Polymorphisms in the DNA repair genesXRCC1,APEX1,XRCC3andNBS1, and the risk for lung cancer in never- and ever-smokers. Lung Cancer. 2006;54(3):285-292. [CrossRef] [PubMed]
 
Ben-Zaken Cohen S, Paré PD, Man SF, Sin DD; BEN-Zaken CS BEN-Zaken CS. The growing burden of chronic obstructive pulmonary disease and lung cancer in women: examining sex differences in cigarette smoke metabolism. Am J Respir Crit Care Med. 2007;176(2):113-120. [CrossRef] [PubMed]
 
Brenner AV, Wang Z, Kleinerman RA, et al. Previous pulmonary diseases and risk of lung cancer in Gansu province, China. Int J Epidemiol. 2001;30(1):118-124. [CrossRef] [PubMed]
 
Fan YG, Jiang Y, Chang RS, et al. Prior lung disease and lung cancer risk in an occupational-based cohort in Yunnan, China. Lung Cancer. 2011;72(2):258-263. [CrossRef] [PubMed]
 
Young RP, Hopkins RJ. How the genetics of lung cancer may overlap with COPD. Respirology. 2011;16(7):1047-1055. [CrossRef] [PubMed]
 
Giuliani L, Jaxmar T, Casadio C, et al. Detection of oncogenic viruses SV40, BKV, JCV, HCMV, HPV and p53 codon 72 polymorphism in lung carcinoma. Lung Cancer. 2007;57(3):273-281. [CrossRef] [PubMed]
 
Kraman M, Bambrough PJ, Arnold JN, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-α. Science. 2010;330(6005):827-830. [CrossRef] [PubMed]
 
Gu D, Kelly TN, Wu X, et al. Mortality attributable to smoking in China. N Engl J Med. 2009;360(2):150-159. [CrossRef] [PubMed]
 
Ezzati M, Lopez AD. Estimates of global mortality attributable to smoking in 2000. Lancet. 2003;362(9387):847-852. [CrossRef] [PubMed]
 
World Health OrganizationWorld Health Organization. Policy recommendations for smoking cessation and treatment of tobacco dependence: tools for public health. 2003. World Health Organization website.http://apps.who.int/iris/handle/10665/42708?locale=zh. Accessed September 10, 2011.
 
International Tobacco Control Policy Evaluation ProjectInternational Tobacco Control Policy Evaluation Project. Mainland China summary overview. February 2009. International Tobacco Control Policy Evaluation Project website.http://www.itcproject.org/countries/china. Accessed February 8, 2012.
 
Wright AA, Katz IT. Tobacco tightrope—balancing disease prevention and economic development in China. N Engl J Med. 2007;356(15):1493-1496. [CrossRef] [PubMed]
 
Pope CA III, Burnett RT, Thun MJ, et al. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA. 2002;287(9):1132-1141. [CrossRef] [PubMed]
 
Zhang JJ, Smith KR. Household air pollution from coal and biomass fuels in China: measurements, health impacts, and interventions. Environ Health Perspect. 2007;115(6):848-855. [CrossRef] [PubMed]
 
Lan Q, Chapman RS, Schreinemachers DM, Tian LW, He XZ. Household stove improvement and risk of lung cancer in Xuanwei, China. J Natl Cancer Inst. 2002;94(11):826-835. [CrossRef] [PubMed]
 
Ministry of Environmental Protection of the People’s Republic of ChinaMinistry of Environmental Protection of the People’s Republic of China. Environment and health project in 12th 5-year plan. 2011. Ministry of Environmental Protection of the People’s Republic of China website.http://www.mep.gov.cn. Accessed September 10, 2011.
 
Shen HB, Yu SZ. Epidemiological status of lung cancer in China and strategies for prevention [in Chinese]. Bull Chin Cancer. 2004;13(5):283-285.
 
Yang CY, Yang SY. The status quo, confusion and prospect of early diagnosis for lung cancer [in Chinese]. J Xi’an Jiaotong University (Med Sci). 2011;32(1):1-5.
 
St John TM. Chapter 4: lung cancer diagnosis and staging. LungCancerGuidebook.org website.http://www.lungcancerguidebook.org/lcguidebook_aug05/ch4_0605.pdf. Accessed September 10, 2011.
 
Marcus PM, Bergstralh EJ, Fagerstrom RM, et al. Lung cancer mortality in the Mayo Lung Project: impact of extended follow-up. J Natl Cancer Inst. 2000;92(16):1308-1316. [CrossRef] [PubMed]
 
Aberle DR, Adams AM, Berg CD, et al;; The National Lung Screening Trial Research Team The National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):365-409.
 

Figures

Figure Jump LinkFigure 1. Literature search algorithm. The scope of this review focused on chronological and regional data within China that are based on facts and trends of lung cancer from 1990 to 2011. PubMed, Web of Knowledge, Google, Chinese National Knowledge Infrastructure, ChinaInfo, and Official websites of the Chinese government were used for the published literature search. A total of 502 articles were found, and 53 were analyzed, synthesized, and summarized.Grahic Jump Location
Figure Jump LinkFigure 2. Incidence rate for lung cancer in China from 1988 to 2005. Data were collected from the National Office for Cancer Prevention and Control, National Center for Cancer Registry, Disease Prevention and Control Bureau, Ministry of Health.4,6Grahic Jump Location
Figure Jump LinkFigure 3. A, Distribution of lung cancer mortality in China according to province. B, Distribution of lung cancer mortality in China according to sex. Data were collected from the Ministry of Health of the People’s Republic of China Third National Retrospect Spot-check of Death-Causation.5,10Grahic Jump Location
Figure Jump LinkFigure 4. Age-adjusted mortality rates for lung cancer. Lung cancer mortality rate increased with age.6Grahic Jump Location
Figure Jump LinkFigure 5. Direct economic burden of inpatients with lung cancer between 1999 and 2005 in China. A, With the rapid increase of total number of inpatients with lung cancer, the total cost rose annually from $2.16 billion to $6.33 billion between 1999 and 2005. B, The proportion of drug, therapy, diagnostic, and assay costs in 1999. C, The proportion of drug, therapy, diagnostic, and assay costs in 2005. Data were collected from the China Statistical Yearbook.7Grahic Jump Location
Figure Jump LinkFigure 6. Air pollution in China. A and B, Biomass and coal use in almost all rural and many urban households causes indoor air pollution. C and D, Outdoor air pollution in China originates from many sources, including chemical releases from industry and a growing transportation sector. Photographs provided by Hao Jiamao, PhD.Grahic Jump Location

Tables

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Straif K, Baan R, Grosse Y, Secretan B, El Ghissassi F, Cogliano V; WHO International Agency for Research on Cancer Monograph Working Group WHO International Agency for Research on Cancer Monograph Working Group. Carcinogenicity of household solid fuel combustion and of high-temperature frying. Lancet Oncol. 2006;7(12):977-978. [CrossRef] [PubMed]
 
Guo XL, Sun JD, Ma JX, et al. Economic burden of malignant neoplasms in Shandong province [in Chinese]. Chin J Publ Health. 2010;26(6):813-816.
 
Nie YK, Cai ZL, Zhao SH. Early lung cancer baseline screening: preliminary study with low-dose spiral CT [in Chinese]. Zhonghua Fang She Xue Za Zhi. 2002;36(3):437-442.
 
US Department of Health and Human Services, Public Health Service, Centers for Disease Control and Prevention, Center for Chronic Disease Prevention and Health Promotion, Office on Smoking and Health.The Health Consequences of Smoking: A Report of the Surgeon General. Rockville, MD: US Department of Health and Human Services; 2004.
 
Shafey O, Eriksen M, Ross H. The Tobacco Atlas.3rd ed. Atlanta, GA: American Cancer Society; 2009.
 
Fang XC, Wang XD, Bai CX. COPD in China: the burden and importance of proper management. Chest. 2011;139(4):920-929. [CrossRef] [PubMed]
 
Anderson Johnson C, Palmer PH, Chou CP, et al. Tobacco use among youth and adults in Mainland China: the China Seven Cities Study. Public Health. 2006;120(12):1156-1169. [CrossRef] [PubMed]
 
Han JX, Ma L, Zhang HW, et al. A cross sectional study of passive smoking of non-smoking women and analysis of influence factors on women passive smoking [in Chinese]. Wei Sheng Yan Jiu. 2006;35(5):609-611. [PubMed]
 
Wang DM, Chen BJ, Li WM, Li Jiang CWB. Risk factors on lung cancer: a meta-analysis [in Chinese]. Chin J Evid-Based Med. 2010;10(12):1446-1449.
 
Zhang JF, Mauzerall DL, Zhu T, Liang S, Ezzati M, Remais JV. Environmental health in China: progress towards clean air and safe water. Lancet. 2010;375(9720):1110-1119. [CrossRef] [PubMed]
 
Pruss-Ustun A, Corvalan C. Preventing Disease Through Healthy Environments. Geneva, Switzerland: World Health Organization; 2006;
 
Bulletin of China’s Environmental Conditions. Beijing, China: Ministry of Environmental Protection; 2009.
 
World Health OrganizationWorld Health Organization. Quantification of the Disease Burden Attributable to Environmental Risk Factors. China Country Profile. Geneva, Switzerland: World Health Organization; 2009.
 
Zhang J, Smith KR. Indoor air pollution: a global health concern. Br Med Bull. 2003;68:209-225. [CrossRef] [PubMed]
 
Zhang Y, Tao S, Shen H, Ma J. Inhalation exposure to ambient polycyclic aromatic hydrocarbons and lung cancer risk of Chinese population. Proc Natl Acad Sci U S A. 2009;106(50):21063-21067. [CrossRef] [PubMed]
 
Huangpu G, Qiu M, Liang XP, Li YE. Relationship between atmospheric polycyclic aromatic hydrocarbons pollution and lung cancer incidence in Datong City, China [in Chinese]. Shanxi Pre Med. 2002;11(2):132-134.
 
Broderick P, Wang YF, Vijayakrishnan J, et al. Deciphering the impact of common genetic variation on lung cancer risk: a genome-wide association study. Cancer Res. 2009;69(16):6633-6641. [CrossRef] [PubMed]
 
Hu Z, Wu C, Shi Y, et al. A genome-wide association study identifies two new lung cancer susceptibility loci at 13q12.12 and 22q12.2 in Han Chinese. Nat Genet. 2011;43(8):792-796. [CrossRef] [PubMed]
 
Henschke CI, Yip R, Miettinen OS; International Early Lung Cancer Action Program Investigators International Early Lung Cancer Action Program Investigators. Women’s susceptibility to tobacco carcinogens and survival after diagnosis of lung cancer. JAMA. 2006;296(2):180-184. [CrossRef] [PubMed]
 
Sun Y, Ren Y, Fang Z, et al. Lung adenocarcinoma from East Asian never-smokers is a disease largely defined by targetable oncogenic mutant kinases. J Clin Oncol. 2010;28(30):4616-4620. [CrossRef] [PubMed]
 
Ryk C, Kumar R, Thirumaran RK, Hou SM. Polymorphisms in the DNA repair genesXRCC1,APEX1,XRCC3andNBS1, and the risk for lung cancer in never- and ever-smokers. Lung Cancer. 2006;54(3):285-292. [CrossRef] [PubMed]
 
Ben-Zaken Cohen S, Paré PD, Man SF, Sin DD; BEN-Zaken CS BEN-Zaken CS. The growing burden of chronic obstructive pulmonary disease and lung cancer in women: examining sex differences in cigarette smoke metabolism. Am J Respir Crit Care Med. 2007;176(2):113-120. [CrossRef] [PubMed]
 
Brenner AV, Wang Z, Kleinerman RA, et al. Previous pulmonary diseases and risk of lung cancer in Gansu province, China. Int J Epidemiol. 2001;30(1):118-124. [CrossRef] [PubMed]
 
Fan YG, Jiang Y, Chang RS, et al. Prior lung disease and lung cancer risk in an occupational-based cohort in Yunnan, China. Lung Cancer. 2011;72(2):258-263. [CrossRef] [PubMed]
 
Young RP, Hopkins RJ. How the genetics of lung cancer may overlap with COPD. Respirology. 2011;16(7):1047-1055. [CrossRef] [PubMed]
 
Giuliani L, Jaxmar T, Casadio C, et al. Detection of oncogenic viruses SV40, BKV, JCV, HCMV, HPV and p53 codon 72 polymorphism in lung carcinoma. Lung Cancer. 2007;57(3):273-281. [CrossRef] [PubMed]
 
Kraman M, Bambrough PJ, Arnold JN, et al. Suppression of antitumor immunity by stromal cells expressing fibroblast activation protein-α. Science. 2010;330(6005):827-830. [CrossRef] [PubMed]
 
Gu D, Kelly TN, Wu X, et al. Mortality attributable to smoking in China. N Engl J Med. 2009;360(2):150-159. [CrossRef] [PubMed]
 
Ezzati M, Lopez AD. Estimates of global mortality attributable to smoking in 2000. Lancet. 2003;362(9387):847-852. [CrossRef] [PubMed]
 
World Health OrganizationWorld Health Organization. Policy recommendations for smoking cessation and treatment of tobacco dependence: tools for public health. 2003. World Health Organization website.http://apps.who.int/iris/handle/10665/42708?locale=zh. Accessed September 10, 2011.
 
International Tobacco Control Policy Evaluation ProjectInternational Tobacco Control Policy Evaluation Project. Mainland China summary overview. February 2009. International Tobacco Control Policy Evaluation Project website.http://www.itcproject.org/countries/china. Accessed February 8, 2012.
 
Wright AA, Katz IT. Tobacco tightrope—balancing disease prevention and economic development in China. N Engl J Med. 2007;356(15):1493-1496. [CrossRef] [PubMed]
 
Pope CA III, Burnett RT, Thun MJ, et al. Lung cancer, cardiopulmonary mortality, and long-term exposure to fine particulate air pollution. JAMA. 2002;287(9):1132-1141. [CrossRef] [PubMed]
 
Zhang JJ, Smith KR. Household air pollution from coal and biomass fuels in China: measurements, health impacts, and interventions. Environ Health Perspect. 2007;115(6):848-855. [CrossRef] [PubMed]
 
Lan Q, Chapman RS, Schreinemachers DM, Tian LW, He XZ. Household stove improvement and risk of lung cancer in Xuanwei, China. J Natl Cancer Inst. 2002;94(11):826-835. [CrossRef] [PubMed]
 
Ministry of Environmental Protection of the People’s Republic of ChinaMinistry of Environmental Protection of the People’s Republic of China. Environment and health project in 12th 5-year plan. 2011. Ministry of Environmental Protection of the People’s Republic of China website.http://www.mep.gov.cn. Accessed September 10, 2011.
 
Shen HB, Yu SZ. Epidemiological status of lung cancer in China and strategies for prevention [in Chinese]. Bull Chin Cancer. 2004;13(5):283-285.
 
Yang CY, Yang SY. The status quo, confusion and prospect of early diagnosis for lung cancer [in Chinese]. J Xi’an Jiaotong University (Med Sci). 2011;32(1):1-5.
 
St John TM. Chapter 4: lung cancer diagnosis and staging. LungCancerGuidebook.org website.http://www.lungcancerguidebook.org/lcguidebook_aug05/ch4_0605.pdf. Accessed September 10, 2011.
 
Marcus PM, Bergstralh EJ, Fagerstrom RM, et al. Lung cancer mortality in the Mayo Lung Project: impact of extended follow-up. J Natl Cancer Inst. 2000;92(16):1308-1316. [CrossRef] [PubMed]
 
Aberle DR, Adams AM, Berg CD, et al;; The National Lung Screening Trial Research Team The National Lung Screening Trial Research Team. Reduced lung-cancer mortality with low-dose computed tomographic screening. N Engl J Med. 2011;365(5):365-409.
 
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