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Trends in lung cancer and smoking behavior in Italy: an alarm bell for women

Abstract

Introduction

The epidemiology of lung cancer is changing worldwide, with smoking being the key driver of lung cancer incidence and mortality. Our aim is to analyze the incidence, survival and mortality trends in Italy in the framework of the 2017 survey on smoking behavior in Italy.

Methods

AIRTUM 2017 reports on cancer survival and incidence; 2017 survey on smoking behavior in Italy.

Results

Men achieved progress in lung cancer control characterized by a decrease in incidence and mortality and an increase in survival. The decreasing use of tobacco in men (from 60% in the 1960s to 24% in 2017) was most likely responsible for the decreasing incidence and mortality. Women showed no progress: although survival improved slightly, the incidence and mortality were both on the rise. This was most likely due to the increasing smoking rates in women in the 1970s and 80s. Of major concern is the accelerated rise in the number of smoking women from 4.6 million in 2016 to 5.7 million in 2017 compared to the decrease observed in men (from 6.9 to 6 million).

Conclusions

The incidence and mortality trends in males clearly demonstrate that primary prevention is the most effective way to reduce lung cancer mortality. By contrast, a 24% increase in the prevalence of smoking among women in just 1 year is extremely worrying for the future, and calls for immediate action by targeted strategies to reduce tobacco consumption in women and avert the dreadful prospect of a lung cancer epidemic in Italy.

Post author correction

Article Type: ORIGINAL RESEARCH ARTICLE

DOI:10.5301/tj.5000684

OPEN ACCESS ARTICLE

Authors

Annalisa Trama, Roberto Boffi, Paolo Contiero, Carlotta Buzzoni, Roberta Pacifici, Lucia Mangone, AIRTUM Working Group

Article History

Disclosures

Registro Tumori ASL BT (Barletta-Andria-Trani)
Registro Tumori Toscano, Istituto per lo studio e la prevenzione oncologica (ISPO), Firenze
Registro Tumori di Popolazione della Regione Campania, ASL Napoli 3 Sud, Napoli
Registro Tumori ASL BT (Barletta-Andria-Trani)
Centro Nazionale di Epidemiologia, Sorveglianza e Promozione della Salute (CNESPS), Istituto Superiore di Sanità, Roma
Registro Tumori Piemonte: province di Biella e Vercelli, Biella
Registro Tumori Reggiano, USL di Reggio Emilia, Reggio Emilia
European Commission, DG Joint Research Center (JRC), Ispra, Varese
Registro Tumori dell’Alto Adige - Tumorregister Südtirol, Servizio di Anatomia e Istologia Patologica, Ospedale di Bolzano
Registro Tumori ASL BT (Barletta-Andria-Trani), Sezione Registro Tumori Puglia, Unità di Epidemiologia e Statistica
Registro Tumori di Basilicata, SC Registro Tumori Regionale, Epidemiologia Clinica e Biostatistica, IRCCS CROB
Registro Tumori della ATS di Bergamo, Servizio Epidemiologico Aziendale, Agenzia di Tutela della Salute di Bergamo
Registro Tumori Piemonte, Province di Biella e Vercelli, Centro di Riferimento Regionale per l’Epidemiologia e la Prevenzione Oncologica (CPO) c/o SOS di Epidemiologia, SC Programmazione e Qualità ASL BI
Registro Tumori della ATS di Brescia, UO Osservatorio Epidemiologico, Dip. Programmazione, Accreditamento, Acquisto Prestazioni, ATS Brescia
Registri Tumori Regione Lombardia - Registro Tumori dell’ATS della Brianza, Servizio di Epidemiologia
Registro Tumori della Provincia di Brindisi, Sezione Registro Tumori Puglia, Unità di Statistica ed Epidemiologia ASL Brindisi
Registro Tumori di Popolazione ASL Caserta
Registro Tumori Integrato di Catania, Messina e Enna
Registro Tumori dell’Azienda Sanitaria Provinciale (ASP) di Catanzaro, ASP di Catanzaro, Servizio di Epidemiologia e Statistica Sanitaria
Registro Tumori Provincia di Como, ATS Insubria Area Territoriale di Como, UOS Registro Tumori e Screening
Registri Tumori Regione Lombardia - Registro Tumori di Cremona, ATS della Val Padana. Paolo Ricci (staff in fase di riorganizzazione) Registro Tumori dell’Area Vasta Emilia Centrale, Azienda USL di Ferrara, Dipartimento di Sanità Pubblica
Registro Tumori del Friuli Venezia Giulia, Direzione Centrale Salute, Integrazione Sociosanitaria e Politiche Sociali, Udine c/o SOC Epidemiologia e Biostatistica, IRCCS CRO, Aviano
Registro Tumori di Latina, Dipartimento di Prevenzione AUSL Latina c/o Centro Commerciale Le Corbusier snc
Registro Tumori di Popolazione della Provincia di Lecce, UOC Epidemiologia e Statistica, Azienda ASL Lecce. UO Registro Tumori, Polo Oncologico Vito Fazzi
Registro Tumori Regione Liguria, Epidemiologia Clinica IRCCS AOU San Martino-IST
Registro Tumori della Provincia di Macerata, Scuola di Bioscienze e Medicina Veterinaria, Università di Camerino
Registri Tumori Regione Lombardia - Registro Tumori di Mantova, ATS della Val Padana
Registro Tumori di Milano, ASL di Milano, SS di Epidemiologia
Registri Tumori Regione Lombardia - Registro delle ASL della Provincia di Milano, Osservatorio Epidemiologico e Registri Specializzati
Registro Tumori della Provincia di Modena, Dipartimento di Sanità Pubblica c/o Centro Servizi AUSL di Modena
Registro Tumori di Popolazione ASL Napoli 3 Sud
Registro Tumori di Nuoro, UO Registro Tumori di Nuoro, ASL di Nuoro e ASL di Lanusei
Registro Tumori di Palermo e Provincia e Registro Tumori della Mammella di Palermo, UOC di Epidemiologia Clinica con Registro Tumori di Palermo e Provincia, Dipartimento di Scienze per la Promozione della Salute Materno-Infantile “G. D’Alessandro”
Registro Tumori della Provincia di Parma, UOC di Oncologia Medica c/o Azienda Ospedaliera Universitaria di Parma
Registro Tumori della Provincia di Pavia c/o Osservatorio Epidemiologico ATS Pavia
Registro Tumori della Provincia di Piacenza, Dipartimento di Sanità Pubblica, UO di Epidemiologia e Comunicazione del Rischio, ASL di Piacenza
Registro Tumori Piemonte, Centro di Riferimento per l’Epidemiologia e la Prevenzione Oncologica (CPO) Piemonte, AOU Città della Salute e Scienza di Torino
Registro Tumori ASP Ragusa esteso alla Provincia di Caltanissetta, Dipartimento di Prevenzione Medica, Azienda Sanitaria Provinciale (ASP7) Ragusa
Registro Tumori Reggiano, AUSL, ASMN-IRCCS, Unità di Epidemiologia, Azienda USL di Reggio Emilia
Registro Tumori della Romagna, IRCCS - Istituto Tumori della Romagna (IRST)
Registro Tumori della Provincia di Salerno
Registro Tumori Nord Sardegna e Coordinamento Regionale dei Registri della Sardegna - ATS Sardegna, Azienda Regionale per la Tutela della Salute-Direzione Generale - SC Pianificazione Strategica, Organizzazione Aziendale, Governance, Marketing Istituzionale
Registro Tumori della Provincia di Siracusa, ASP Siracusa
Registro Tumori della Provincia di Sondrio, ATS della Montagna, Osservatorio Epidemiologico
Registro Tumori ASL di Taranto, SC di Statistica Epidemiologia, Settore Registro Tumori, ASL Taranto
Registro Tumori Toscano, Istituto per lo Studio e la Prevenzione Oncologica (ISPO), SS Infrastruttura Registri, SC di Epidemiologia Clinica
Registro Tumori della Provincia di Trapani, Servizio Sanitario Regione Sicilia, Dipartimento di Prevenzione, Area Igiene e Sanità Pubblica, ASP Trapani
Registro Tumori della Provincia di Trento, Servizio Epidemiologia Clinica e Valutativa, Azienda Provinciale per i Servizi Sanitari, Centro per i Servizi Sanitari
Registro Tumori Umbro di Popolazione, Dipartimento di Specialità Medico-Chirurgiche e Sanità Pubblica, Sezione di Sanità Pubblica, Università degli Studi di Perugia
Registro Tumori della Lombardia, Provincia di Varese, Fondazione IRCCS Istituto Nazionale dei Tumori
Registro Tumori del Veneto, Sistema Epidemiologico Regionale (SER) - Regione del Veneto
Registro Tumori della Provincia di Viterbo c/o UOC PreSAL - Dipartimento di Prevenzione, ASL Viterbo, Cittadella della Salute
Registro Tumori Infantili e negli Adolescenti Regione Marche, Scuola in Scienze del Farmaco e dei Prodotti della Salute, Centro Ricerche Igienistiche e Sanitarie, Ambientali, Università di Camerino
Registro dei Tumori Infantili del Piemonte, SCDU Unità di Epidemiologia dei Tumori, Università di Torino, Centro di Riferimento per l’Epidemiologia e la Prevenzione Oncologica (CPO) Piemonte
Registro Mesoteliomi della Regione Emilia-Romagna, COR Emilia-Romagna del Registro Nazionale Mesoteliomi (ReNaM) presso AUSL di Reggio Emilia
Registro Mesoteliomi Liguria, COR Liguria del Registro Nazionale dei Mesoteliomi (ReNaM), Dip. Terapie Oncologiche, UO Epidemiologia, IRCCS AOU San Martino, Istituto Nazionale Ricerca sul Cancro (IST)
Registro dei Tumori Colorettali di Modena c/o Dipartimento di Medicine e Specialità Mediche, Medicina 1, Policlinico Universitario di Modena
Registro Tumori Specialistico del Pancreas della Provincia di Reggio Emilia, SC di Gastroenterologia ed Endoscopia Digestiva, Arcispedale Santa Maria Nuova-IRCCS, Servizio Interaziendale di Epidemiologia, AUSL Reggio Emilia
Financial support: None.
Conflict of interest: The authors declare no conflicts of interest.

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Introduction

Lung cancer cases were 1.8 million in 2012 across the globe, corresponding to 13% of all cancers (1). Lung cancer was the most common cancer in men worldwide with 1.2 million new cases per year; meanwhile, nearly 600,000 new cases were diagnosed in women in 2012. Differences were also observed between regions, with 758,000 cases occurring in the more developed areas and more than 1 million of cases diagnosed in the less developed areas. Lung cancer remains lethal everywhere in the world, with a 5-year survival rate below 20% (2). Because of the high incidence rates and low survival, lung cancer is the most common cause of death from cancer worldwide with 1.59 million deaths, more than 1 million in men and 491,000 in women (1). In Europe, it is the third most common cause of cancer, after breast and prostate cancer (1).

The epidemiology of lung cancer is changing in many areas of the world in terms of incidence by gender, age class and histological type (3, 4). Different histological subtypes are linked to different risk factors; for example, outdoor particulate matter has been recognized as a stronger risk factor for adenocarcinoma of the lung than for other histologies, while smoking has been associated in the past mainly with squamous cell carcinoma. However, because of the dissemination of low-tar filter cigarettes, smoking has been hypothesized to be linked also with adenocarcinoma (3). Lung cancer appears to have biologically different characteristics in men and women. The histological distribution of lung cancer subtypes is distinctly different and female smokers are more likely to develop adenocarcinoma of the lung than squamous cell carcinoma, which is more common in men (4). However, the differences in incidence rates between men and women are mainly attributable to the different exposure to tobacco smoking (3).

The aim of this paper is to analyze the lung cancer incidence, survival and mortality trends in Italy in the last available 15 years by using the data of the Italian Association of Cancer Registries (AIRTUM; http://registri-tumori.it/cms/).

While assessing the progress in lung cancer control in Italy, we will speculate about possible reasons for the observed changes over time and we will outline opportunities to reduce the burden of lung cancer in the discussion section of this article.

Materials and methods

Data

Formally established in 1997, AIRTUM promotes and supports activities and research programs for both general and specialized population-based Italian cancer registries (CRs). AIRTUM has developed a central database to collect and store CR data and make them available for collaborative studies and research activities after an official quality check in terms of data accuracy and completeness. Currently the AIRTUM CRs cover more than 35 million people, corresponding to 60% of the Italian population. AIRTUM has had a central database since 2005, which stores data from all accredited CRs. All CRs transfer data to the AIRTUM database in accordance with a standard protocol, performing regular updates over time. Each registry can send new data or update old records with new variables, including follow-up for vital status. The network standard protocol describes the inclusion criteria, data format, and checks. (For detailed information see http://www.registri-tumori.it/cms/files/2010.pdf).

Data published in the most recent AIRTUM reports on survival (5) and incidence (6) were selected for this paper.

Statistical analyses

For the joint analyses of incidence, mortality and survival (5), 23 CRs covering the period 1999-2010 and representing the population of 4 Italian macro-areas: Northwest Italy (Biella, Genoa, Mantua, Milan, Sondrio, Turin, Varese), Northeast Italy (Alto Adige, Ferrara, Friuli Venezia Giulia, Modena, Parma, Reggio Emilia, Romagna, Trento, Veneto), Central Italy (Umbria, Latina), and South Italy (Naples, Ragusa, Salerno, Sassari, Siracusa) were included. The study period was stratified in triennia.

Incidence and mortality rates were standardized by age with the direct method using the old (1960) European standard population. The average annual percent change of incidence and mortality rates was expressed by an indicator called annual percent change (APC), which explains synthetically the trend and the intensity of the variation in time. This model is based on linear segments connected at join points that represent the best fit of the observed data, that is, the segments that minimize the sum of the square of the differences between the estimated and observed data. APC was estimated with JoinPoint regression models available in the software distributed by the NCI (https://surveillance.cancer.gov/joinpoint/download).

Five-year net survival was estimated with the Pohar-Perme method (7). Survival changes were measured in terms of absolute percentage difference (APD) between the 5-year age-adjusted net survival estimates in 2008-2010 and 1999-2001. We combined statistically significant changes of the 3 indicators to identify patterns discriminating optimal/inadequate progress in cancer control. Incidence and mortality rates were standardized by age with the direct method using the old (1960) European standard population.

Analysis by tumor histology was performed considering among adenocarcinoma the ICDO-3 codes 8050, 8140-8149, 8160-8162, 8190-8221, 8250-8263, 8270-8280, 8290-8337, 8350-8390, 8400-8560, 8570-8576 and 8940-8941 and among squamous cell carcinomas the ICD-O3 codes 8051-8052, 8070-8084 and 8120-8131 (8).

For the joint analyses of incidence and mortality trends and projection to 2016 (6), 10 CRs covering the period 1999-2011 were included (Varese, Parma, Reggio Emilia, Modena, Romagna, Umbria, Naples, Turin, Ragusa and Siracusa).

Results and discussion

Figures 1 and 2 present changes in incidence, mortality and 5-year net survival between 1999-2001 and 2008-2010 for lung cancer in males and females, respectively.

POOL AIRTUM 1990-2010, males. Age-standardized incidence (A) and mortality (B) rates (direct method, standard population: European population) by triennia and geographic area. Five-year net survival (C). Reproduced with permission from Coviello et al. AIRTUM Working Group. La sopravvivenza dei pazienti oncologici in Italia. Epidemiol Prev. 2017;41(2 Suppl 1):1-244.

APC = Annual Percent Change; APD = Absolute Percent Difference; *Statistically Significant Change.

POOL AIRTUM 1990-2010, females. Age-standardized incidence (A) and mortality (B) rates (direct method, standard population: European population) by triennia and geographic area. Five-year net survival (C). Reproduced with permission from Coviello et al. AIRTUM Working Group. La sopravvivenza dei pazienti oncologici in Italia. Epidemiol Prev. 2017;41(2 Suppl 1):1-244.

APC = Annual Percent Change; APD = Absolute Percent Difference; *Statistically Significant Change.

Incidence

In the period 2008-2010 the lung cancer incidence in Italy was 67.8/100,000 in men and 21.8/100,000 in women (Figs. 1A and 2A). This translated into more than 41,000 new lung cancer cases, 28,000 in men and 13,500 in women (6). The number of new lung cancer cases must be interpreted with caution because it reflects both the distribution of risk factors (including smoking prevalence over time in the 2 sexes) and population aging.

A big difference between the incidence rates for men and women was still observed in 2008-2010 (68 and 22, respectively), even though the rates were gradually converging over time (Figs. 1A and 2A). This was due to the downward trend among men and the sustained increase in incidence in women. These trends may be largely attributable to previous smoking rates. Cigarette smoking or tobacco use is the most important causal risk factor for lung cancer development, with a long latency of 30 years between exposure to tobacco smoke and lung cancer development. Thus, the incidence trends and figures reported in this paper reflect the smoking prevalence of the late 1970s and 80s. In Italy, the smoking prevalence steadily declined until 2008 overall (from 35.4% to 21.7%) and in men (from 65.0% to 23.9%), while in women it increased from 6.2% in 1957 to 25.9% in 1990, and declined thereafter to 17.9% in 2008 (9). According to the recent survey on smoking habits in Italy (10), the smoking prevalence reached 24% in men and 21% in women in 2017. The latter percentage needs to be interpreted with caution since the variability for this estimate in a subgroup could be very large. Decreasing male tobacco use was most likely responsible for the decreasing incidence trends observed in men in this paper. By contrast, the increasing incidence trend in women was most likely due to the increasing smoking rates in women until the 1990s. A point of concern is that in just 1 year (from 2016 to 2017) the number of smoking women increased from 4.6 million to 5.7 million whereas the number of smoking men decreased from 6.9 to 6 million. This trend in women is extremely worrying because, if no changes occur, it will most likely lead to an increase in lung cancer incidence in women in the future.

Considering the carcinogenic role of secondhand smoke, also the data on the exposure to secondhand smoke in homes and cars are of note. Out of 688 smokers, 34% reported they could smoke everywhere in the home while 29% reported they could smoke only in selected rooms such as the bathroom or kitchen (10). In cars, 10% of nonsmokers reported having traveled with people who smoked and 61% of smokers reported they smoked in the car (10).

Figures 3 and 4 report the incidence trends (POOL AIRTUM CRs, period 2003-2012) for adenocarcinoma and squamous cell carcinoma in men and women, respectively. Data for other histological types are not available. The incidence of squamous cell carcinomas decreased in men while no major changes were observed in women; the incidence of adenocarcinomas increased in both men and women. A factor that may have contributed to the decreased incidence of squamous cell carcinomas of the central airways and the increased incidence of peripheral adenocarcinomas is the changed composition of cigarettes, which has resulted in deeper inhalation (11). Furthermore, with smoking cessation the risk declines more rapidly for squamous cell carcinoma than adenocarcinoma, which partly explains the increasing incidence trends of adenocarcinoma observed in men and women (11, 12). However, in this context it is important to take into account the recent findings of Gharibvand et al (13), who assessed the association between ambient fine particulate matter (PM2.5) and lung cancer among never smokers. Most of the lung cancers in this study (66.4%) were adenocarcinomas and an increase of 22% in the lung cancer risk was observed for each 10-μg/m3 increase in ambient PM2.5 concentration. In another study the increase in risk was found to be 55% for adenocarcinomas (14). Future studies that evaluate trends in adenocarcinomas and other histological subtypes should consider specific airborne environmental exposures in addition to socioeconomic factors and tobacco exposure (11). Finally, studies in Southeast Asia, where the prevalence of smoking among women is low, have suggested that the rise of adenocarcinomas in women can be attributed to secondhand smoke and cooking fumes (15).

AIRTUM estimates of incidence time trends for 1999-2016 by histology in males. Age-standardized incidence (direct method, standard population: European population). APC = annual percent change. Reproduced with permission from AIOM & AIRTUM. I numeri del cancro in Italia 2016. Rome: Il Pensiero Scientifico Editore 2016.

AIRTUM estimates of incidence time trends for 1999-2016 by histology in females. Age-standardized incidence (direct method, standard population: European population). APC = annual percent change. Reproduced with permission from AIOM & AIRTUM. I numeri del cancro in Italia 2016. Rome: Il Pensiero Scientifico Editore 2016.

The Italian incidence rates were high but comparable to those reported internationally in similar countries in 2012. The highest incidence rates for men were reported in Central and Eastern Europe (53.5/100,000) and East Asia (50.4/100,000) and for women in the United States (33.8/100,000) and Northern Europe (23.7/100,000) (15). For these estimates the world standard population was used whereas for the Italian data the European standard population was chosen. The European population was used for Italy because it was closer to the distribution of the resident population. The world population is slightly younger than the European population and the rates therefore tend to be lower.

Interestingly, the incidence pattern reported in Italy was observed in many countries with a high or very high human development index (HDI), namely Australia, Canada, Russia, the United States and Europe (Denmark, Germany, Netherlands, Sweden and United Kingdom), although in the United States the incidence has begun to show signs of a decreasing trend among females since 2010 (16). Also in these countries, the epidemic of lung cancer aligns with historical patterns of tobacco use. From 1980 to 2012, for men, annualized rates of decline of 2% or more occurred in 17 countries: Canada, Mexico, United States, Australia, South Africa, Venezuela, Nigeria, Antigua and Barbuda, New Zealand and Japan, and in Europe in Iceland, Norway, Sweden, Denmark, Italy, United Kingdom and Poland (16). For women, annualized rates of decline greater than 2% were achieved in 22 countries, while 12 countries exhibited statistically significant increases in prevalence since 1980. Bolivia, Canada, Denmark, Iceland, Israel, Norway, Sweden and the United States all had prevalence rates higher than 20% in 1980 but achieved annualized rates of decline of greater than 2%, whereas Austria, Bulgaria and Greece, which also had prevalence rates greater than 20% in 1980, showed statistically significant increases since then (16).

Mortality

In Italy, in the period 2008-2010 the mortality rate of lung cancer was 58 in 100,000 men and 16 in 100,000 women (Figs. 1B and 2B). The lung cancer mortality rates have changed substantially over time (Figs. 1 and 2), mirroring the incidence rates, with reductions in mortality among men and increasing trends among women, and with male-to-female mortality rates converging over time.

If we look at the geographic regions of the world, the highest mortality rates for men were observed in Central and Eastern Europe (47.6 in 100,000) and East Asia (44.8 in 100,000) (14). The highest mortality rates among women were in North America (23.5 in 100,000) and Northern Europe (19.1 in 100,000) (15). For many EU and non-EU countries (e.g., Australia, Denmark, France, Germany, Sweden and the United States), the trends in lung cancer mortality closely mirrored those for incidence (15). Parallel and increasing sex-specific mortality trends were observed in Romania; mortality rates were stable for both sexes in Japan; and parallel decreasing trends by sex were reported in Hong Kong and the Russian Federation. Also the mortality trends align with the historical patterns of tobacco use previously reported (16). These results are not surprising considering that, because of the high fatality associated with lung cancer, the geographical patterns in mortality closely follow those of incidence. As noted for the incidence comparison, also for the mortality rates these international data should be compared with the Italian ones considering the different standardization used.

Survival

In Italy, the 5-year lung cancer survival was 14.3% (12.6% for men and 16.6% for women) (Figs. 1C and 2C), which was higher than the EU average (13%) and that of the Northern European countries (12.2%) (17).

The low survival rate of patients with lung cancer is related to the stage of lung cancer at diagnosis. This determines the treatment options and has a strong influence on the length of survival. The earlier lung cancer is caught, the better chance a person has of surviving 5 years after being diagnosed. A population-based study performed in Northern Italy showed that, overall, 10% of new lung cancer cases were stage I, 50% stage IV, and 12% stage unknown. Three-year survival was 14% overall: 69% for stage I and 3% for stage IV (18). In the United States, in the period 2007-2013, 16% of lung and bronchus cancers were diagnosed at localized stage, 22% at regional stage, and 57% with distant metastases. The 5-year survival was 55.6%, 28.9% and 4.5% for localized, regional and distant lung cancer, respectively (19).

In addition to stage at diagnosis, variation in the treatment of lung cancer (e.g., time to curative treatment and adherence to guidelines) is likely an important determinant of survival and of the differences in survival between countries (20, 21).

Women tended to have higher survival rates than men (5-year net survival 20.5% in women and 14.5% in men) (5). This is a well-known phenomenon attributed to a mix of biological factors and tumor characteristics: hormonal status, comorbidities, histolological case mix (more adenocarcinomas in women than men), and the different natural history of lung cancer for men and women (22).

Despite the poor prognosis, a slight increase in survival was observed for men and women with an absolute percentage difference of 1.9 and 3.9, respectively (Figs. 1 and 2).

Any progress in lung cancer control?

Figures 1 and 2 present the changes in incidence and mortality rates and in 5-year net survival between 1999-2001 and 2008-2010 for lung cancer in men and women. We identified different patterns for men and women according to the progress in lung cancer control.

Men showed progress in lung cancer control, as characterized by a decrease in incidence and mortality and a slight increase in survival. Between 1999-2001 and 2008-2010, the incidence and mortality rates declined significantly by 2.5% and 2.7% per year, respectively. Survival increased significantly from 12.6% to 14.5%.

By contrast, women had no progress because the cancer burden worsened, i.e., the incidence and mortality were both on the rise, even though survival improved slightly. For lung cancer in women, the incidence rates increased annually by 2.4% in 1999-2010 (from 17.7 to 21.8 per 100,000); the mortality increase (APC +1.5%) was possibly mitigated by a small but statistically significant 5-year net survival improvement (from 17% to 20%).

As discussed earlier, the key driver of trends in lung cancer incidence is smoking. Because of the limited efficacy of high-cost screening and treatment measures, smoking is also a key driver of lung cancer mortality (23, 24). Thus, smoking cessation and changes in other risk factors mainly contribute to explaining the decline in incidence and therefore in mortality. The slight increase observed in survival might be due to changes in stage distribution at diagnosis, changes in the histological subtype case mix (more adenocarcinomas, which have higher survival than large cell and small cell lung cancer (15)), a high proportion of EGFR mutation-positive lung cancers for targeted therapies (15), as well as to a real improvement in diagnostic and treatment strategies (17). Further studies focused on histological, clinical and molecular features of lung cancer are needed to properly interpret the survival changes and disentangle the role of the diagnostic pathway and treatment progress.

In Italy, men have benefited from a decreasing smoking prevalence and are likely to experience continued reductions of the lung cancer incidence over the coming years. Conversely, the rates of lung cancer in women are expected to rise, given the new signs of increasing smoking prevalence.

Currently, effective tobacco control programs seem critically important in the battle to reduce the burden of lung cancer. This will be of particular importance for young women. In the young population (25-44 years), female lung cancer mortality is predicted to reach similar rates to those of men if not to surpass those of men by 2017 (1.38 in women vs. 1.21 in men) in the EU (25), and the same pattern was seen in Italy (25).

Italy was the first large country in 2005 to adopt comprehensive tobacco legislation, banning smoking in all indoor workplaces and public places (26). However, from 2006 to 2013 a decrease in the implementation rate of tobacco control measures was observed in Italy compared with other European countries (27, 28). This could explain the trends in smoking prevalence reported in Italy in the recent survey (28). In 2016, new legislation on tobacco, transposing the Directive 2014/40/EU, was introduced in Italy to further decrease the social acceptability of smoking, reduce smoking by the younger generations, and limit secondhand smoking exposure among children.

Conclusion

The availability of population-based cancer data to assess the lung cancer burden and monitor emerging trends is of crucial importance together with the availability of surveys on the prevalence of tobacco smoking. Primary prevention is the most effective way to control the lung cancer epidemic. Tobacco legislation and tax policies still offer a great opportunity to control lung cancer; however, a comprehensive lung cancer control policy including coordinated strategies to reduce exposure to all recognized risk factors including secondhand smoke, air pollution, radon, asbestos, and occupational carcinogens will be essential to tackle the lung cancer epidemic in future.

In Italy, the incidence and mortality trends in males clearly demonstrate that primary prevention is the most effective way to reduce the lung cancer mortality. By contrast, a 24% increase in the prevalence of smoking in women in just 1 year is extremely worrying, and calls for immediate action and targeted strategies to reduce tobacco consumption by women and avert the dreadful prospect of a lung cancer epidemic in Italy.

Appendix

AIRTUM working group

Coviello V1, Buzzoni C2, Fusco M3, Barchielli A2, Cuccaro F4, De Angelis R5, Giacomin A6, Luminari S7, Randi G8, Mangone L7, Mazzoleni G9, Bulatko A9, Devigili E9, Tschugguel B9, De Valiere E9, Facchinelli G9, Falk M9, Vittadello F9, Coviello V10, Cuccaro F10, Calabrese A10, Pinto A10, Cannone G10, Vitali ME10, Galasso R11, Del Riccio L11, Napolitano D11, Sampietro G12, Ghisleni S12, Giavazzi L12, Zanchi A12, Zucchi A12, Giacomin A13, Vercellino PC13, Andreone S13, Fedele M13, Barale A13, Germinetti F13, Magoni M14, Salvi O14, Puleio M14, Gerevini C14, Chiesa R14, Lonati F14, Cavalieri d’Oro L15, Rognoni M15, Le Rose L15, Merlo E15, Bracchi A15, Negrino L15, Pezzuto L15, Ardizzone A16, Spagnolo G16, Cozzi E16, De Lorenzis L16, Lotti F16, Pagliara MC16, D’Argenzio A17, D’Abronzo M17, De Francesco D17, Pereira da Silva MCM17, Menditto V17, Perrotta E17, Pesce MT17, Sessa A17, Sciacca S18, Sciacchitano S18, Fidelbo M18, Benedetto G18, Benedetto A18, Calabretta LMR18, Caruso AM18, Castaing M18, Di Prima AA18, Dinaro YM18, Fidelbo P18, Grosso G18, Ippolito A18, Irato E18, Leone A18, Paderni F18, Pesce PNR18, Pollina Addario S18, Savasta A18, Sciacchitano CG18, Torrisi AAM18, Torrisi A18, Varvarà M18, Viscosi C18, Sutera Sardo A19, Sia A19, Scalzi S19, Lavecchia AM19, Mancuso P19, Nocera V19, Mancusi F19, Del Duca S19, Gola G20, Corti M20, Caparelli M20, Ferretti S21, Marzola L21, Migliari E21, Carletti N21, Biavati P21, Petrucci C21, Serraino D22, Angelin T22, Bidoli E22, Birri S22, Dal Maso L22, De Dottori M22, De Santis E22, Forgiarini O22, Zucchetto A22, Zanier L22, Pannozzo F23, Busco S23, Rossi M23, Curatella S23, Bugliarello E23, Macci L23, Bernazza E23, Calabretta F23, Tamburrino S23, Sperduti I23, Tamburo L23, Serafini G23, Quarta F24, Melcarne A24, Golizia MG24, Arciprete C24, De Maria V24, Filiberti RA25, Casella C25, Marani E25, Puppo A25, Celesia MV25, Cogno R25, Vitarelli S26, Ricci P27, Autelitano M28, Ghilardi S28, Leone R28, Filipazzi L28, Bonini A28, Giubelli C28, Russo AG29, Quattrocchi M29, Distefano R29, Panciroli E29, Bellini A29, Pinon M29, Spinosa S29, Spagnoli G30, Carrozzi G30, Cirilli C30, Valla K30, Amendola V30, Fusco M31, Bellatalla C31, Ciullo V31, Di Buono M31, Fusco M31, Panico M31, Perrotta C31, Vitale MF31, Usala M32, Pala F32, Sini GM32, Pintori N32, Canu L32, Demurtas G32, Doa N32, Vitale F33, Cusimano R33, Traina A33, Guttadauro A33, Cascio MA33, Mannino R33, Ravazzolo B33, Brucculeri MA33, Rudisi G33, Adamo MS33, Amodio R33, Costa A33, Zarcone M33, Sunseri R33, Bucalo G33, Trapani C33, Staiti R33, Michiara M34, Bozzani F34, Sgargi P34, Boschetti L35, Migliazza S35, Reggiani E35, Incardona N35, Borciani E36, Seghini P36, Prazzoli R36, Zanetti R37, Rosso S37, Patriarca S37, Prandi R37, Sobrato I37, Gilardi F37, Busso P37, Sacchetto L37, Tumino R38, Cascone G38, Frasca G38, Giurdanella MC38, Martorana C38, Morana G38, Nicita C38, Rollo PC38, Ruggeri MG38, Spata E38, Vacirca S38, Mangone L39, Vicentini M39, Di Felice E39, Pezzarossi A39, Ferrari F39, Roncaglia F39, Sacchettini C39, Caroli S39, Falcini F40, Colamartini A40, Bucchi L40, Balducci C40, Ravegnani M40, Vitali B40, Cordaro C40, Caprara L40, Giuliani O40, Giorgetti S40, Palumbo M40, Vattiato R40, Ravaioli A40, Mancini S40, Caiazzo AL41, Cavallo R41, Colavolpe AFG41, D’Alessandro A41, Iannelli A41, Lombardo C41, Senatore G41, Sensi F42, Cesaraccio R42, Pirino D42, Mura F42, Contrino ML43, Madeddu A43, Tisano F43, Dinaro Y43, Muni A43, Mizzi M43, Bella F43, Rossitto L43, Sacco G43, Aletta P43, Colanino Ziino A43, Maspero S44, Fanetti AC44, Cometti I44, Cecconami L44, Minerba S45, Mincuzzi A45, Carone S45, Tanzarella M45, Galluzzo C45, Barchielli A46, Buzzoni C46, Caldarella A46, Corbinelli A46, Intrieri T46, Di Dia PP46, Manneschi G46, Nemcova L46, Visioli C46, Zappa M46, Candela G47, Scuderi T47, Crapanzano G47, Taranto V47, Piffer S48, Gentilini M48, Rizzello R48, Bombarda L48, Pedron M48, Clivati E48, Stracci F49, D’Alò D49, Scheibel M49, Costarelli D49, Spano F49, Rossini S49, Santucci C49, Petrinelli AM49, Solimene C49, Bianconi F49, Brunori V49, Tagliabue G50, Contiero P50, Tittarelli A50, Fabiano S50, Maghini A50, Codazzi T50, Barigelletti G50, D’Agostino A50, Modonesi C50, Rugge M51, Baracco M51, Baracco S51, Bovo E51, Dal Cin A51, Fiore AR51, Greco A51, Guzzinati S51, Martin G51, Memo L51, Monetti D51, Rizzato S51, Rosano A51, Stocco C51, Tognazzo S51, Zorzi M51, Brustolin A52, Beggiato S52, Aniceti S52, Fiocchetti L52, Schirra G52, Galeotti P52, Capati A52, Nami A52, Montanaro M52, Verrico G52, Poleggi F52, Rashid I52, Grappasonni I53, Pascucci C53, Merletti F54, Magnani C54, Pastore G54, Terracini B54, Alessi D54, Cena T54, Lazzarato F54, Macerata V54, Maule M54, Mosso ML54, Sacerdote C54, Romanelli A55, Mangone L55, Storchi C55, Sala O55, Gabbi C55, Gennaro V56, Benfatto L56, Malacarne D56, Lando C56, Campi MG56, Mazzucco G56, Ponz de Leon M57, Domati F57, Rossi G57, Goldoni CA57, Kaleci S57, Rossi F57, Benatti P57, Roncucci L57, Di Gregorio C57, Magnani G57, Pedroni M57, Maffei S57, Mariani F57, Reggiani-Bonetti L57, Sassatelli R58, Cassetti T58, Giorgi Rossi P58, Vicentini M58

Disclosures

Registro Tumori ASL BT (Barletta-Andria-Trani)
Registro Tumori Toscano, Istituto per lo studio e la prevenzione oncologica (ISPO), Firenze
Registro Tumori di Popolazione della Regione Campania, ASL Napoli 3 Sud, Napoli
Registro Tumori ASL BT (Barletta-Andria-Trani)
Centro Nazionale di Epidemiologia, Sorveglianza e Promozione della Salute (CNESPS), Istituto Superiore di Sanità, Roma
Registro Tumori Piemonte: province di Biella e Vercelli, Biella
Registro Tumori Reggiano, USL di Reggio Emilia, Reggio Emilia
European Commission, DG Joint Research Center (JRC), Ispra, Varese
Registro Tumori dell’Alto Adige - Tumorregister Südtirol, Servizio di Anatomia e Istologia Patologica, Ospedale di Bolzano
Registro Tumori ASL BT (Barletta-Andria-Trani), Sezione Registro Tumori Puglia, Unità di Epidemiologia e Statistica
Registro Tumori di Basilicata, SC Registro Tumori Regionale, Epidemiologia Clinica e Biostatistica, IRCCS CROB
Registro Tumori della ATS di Bergamo, Servizio Epidemiologico Aziendale, Agenzia di Tutela della Salute di Bergamo
Registro Tumori Piemonte, Province di Biella e Vercelli, Centro di Riferimento Regionale per l’Epidemiologia e la Prevenzione Oncologica (CPO) c/o SOS di Epidemiologia, SC Programmazione e Qualità ASL BI
Registro Tumori della ATS di Brescia, UO Osservatorio Epidemiologico, Dip. Programmazione, Accreditamento, Acquisto Prestazioni, ATS Brescia
Registri Tumori Regione Lombardia - Registro Tumori dell’ATS della Brianza, Servizio di Epidemiologia
Registro Tumori della Provincia di Brindisi, Sezione Registro Tumori Puglia, Unità di Statistica ed Epidemiologia ASL Brindisi
Registro Tumori di Popolazione ASL Caserta
Registro Tumori Integrato di Catania, Messina e Enna
Registro Tumori dell’Azienda Sanitaria Provinciale (ASP) di Catanzaro, ASP di Catanzaro, Servizio di Epidemiologia e Statistica Sanitaria
Registro Tumori Provincia di Como, ATS Insubria Area Territoriale di Como, UOS Registro Tumori e Screening
Registri Tumori Regione Lombardia - Registro Tumori di Cremona, ATS della Val Padana. Paolo Ricci (staff in fase di riorganizzazione) Registro Tumori dell’Area Vasta Emilia Centrale, Azienda USL di Ferrara, Dipartimento di Sanità Pubblica
Registro Tumori del Friuli Venezia Giulia, Direzione Centrale Salute, Integrazione Sociosanitaria e Politiche Sociali, Udine c/o SOC Epidemiologia e Biostatistica, IRCCS CRO, Aviano
Registro Tumori di Latina, Dipartimento di Prevenzione AUSL Latina c/o Centro Commerciale Le Corbusier snc
Registro Tumori di Popolazione della Provincia di Lecce, UOC Epidemiologia e Statistica, Azienda ASL Lecce. UO Registro Tumori, Polo Oncologico Vito Fazzi
Registro Tumori Regione Liguria, Epidemiologia Clinica IRCCS AOU San Martino-IST
Registro Tumori della Provincia di Macerata, Scuola di Bioscienze e Medicina Veterinaria, Università di Camerino
Registri Tumori Regione Lombardia - Registro Tumori di Mantova, ATS della Val Padana
Registro Tumori di Milano, ASL di Milano, SS di Epidemiologia
Registri Tumori Regione Lombardia - Registro delle ASL della Provincia di Milano, Osservatorio Epidemiologico e Registri Specializzati
Registro Tumori della Provincia di Modena, Dipartimento di Sanità Pubblica c/o Centro Servizi AUSL di Modena
Registro Tumori di Popolazione ASL Napoli 3 Sud
Registro Tumori di Nuoro, UO Registro Tumori di Nuoro, ASL di Nuoro e ASL di Lanusei
Registro Tumori di Palermo e Provincia e Registro Tumori della Mammella di Palermo, UOC di Epidemiologia Clinica con Registro Tumori di Palermo e Provincia, Dipartimento di Scienze per la Promozione della Salute Materno-Infantile “G. D’Alessandro”
Registro Tumori della Provincia di Parma, UOC di Oncologia Medica c/o Azienda Ospedaliera Universitaria di Parma
Registro Tumori della Provincia di Pavia c/o Osservatorio Epidemiologico ATS Pavia
Registro Tumori della Provincia di Piacenza, Dipartimento di Sanità Pubblica, UO di Epidemiologia e Comunicazione del Rischio, ASL di Piacenza
Registro Tumori Piemonte, Centro di Riferimento per l’Epidemiologia e la Prevenzione Oncologica (CPO) Piemonte, AOU Città della Salute e Scienza di Torino
Registro Tumori ASP Ragusa esteso alla Provincia di Caltanissetta, Dipartimento di Prevenzione Medica, Azienda Sanitaria Provinciale (ASP7) Ragusa
Registro Tumori Reggiano, AUSL, ASMN-IRCCS, Unità di Epidemiologia, Azienda USL di Reggio Emilia
Registro Tumori della Romagna, IRCCS - Istituto Tumori della Romagna (IRST)
Registro Tumori della Provincia di Salerno
Registro Tumori Nord Sardegna e Coordinamento Regionale dei Registri della Sardegna - ATS Sardegna, Azienda Regionale per la Tutela della Salute-Direzione Generale - SC Pianificazione Strategica, Organizzazione Aziendale, Governance, Marketing Istituzionale
Registro Tumori della Provincia di Siracusa, ASP Siracusa
Registro Tumori della Provincia di Sondrio, ATS della Montagna, Osservatorio Epidemiologico
Registro Tumori ASL di Taranto, SC di Statistica Epidemiologia, Settore Registro Tumori, ASL Taranto
Registro Tumori Toscano, Istituto per lo Studio e la Prevenzione Oncologica (ISPO), SS Infrastruttura Registri, SC di Epidemiologia Clinica
Registro Tumori della Provincia di Trapani, Servizio Sanitario Regione Sicilia, Dipartimento di Prevenzione, Area Igiene e Sanità Pubblica, ASP Trapani
Registro Tumori della Provincia di Trento, Servizio Epidemiologia Clinica e Valutativa, Azienda Provinciale per i Servizi Sanitari, Centro per i Servizi Sanitari
Registro Tumori Umbro di Popolazione, Dipartimento di Specialità Medico-Chirurgiche e Sanità Pubblica, Sezione di Sanità Pubblica, Università degli Studi di Perugia
Registro Tumori della Lombardia, Provincia di Varese, Fondazione IRCCS Istituto Nazionale dei Tumori
Registro Tumori del Veneto, Sistema Epidemiologico Regionale (SER) - Regione del Veneto
Registro Tumori della Provincia di Viterbo c/o UOC PreSAL - Dipartimento di Prevenzione, ASL Viterbo, Cittadella della Salute
Registro Tumori Infantili e negli Adolescenti Regione Marche, Scuola in Scienze del Farmaco e dei Prodotti della Salute, Centro Ricerche Igienistiche e Sanitarie, Ambientali, Università di Camerino
Registro dei Tumori Infantili del Piemonte, SCDU Unità di Epidemiologia dei Tumori, Università di Torino, Centro di Riferimento per l’Epidemiologia e la Prevenzione Oncologica (CPO) Piemonte
Registro Mesoteliomi della Regione Emilia-Romagna, COR Emilia-Romagna del Registro Nazionale Mesoteliomi (ReNaM) presso AUSL di Reggio Emilia
Registro Mesoteliomi Liguria, COR Liguria del Registro Nazionale dei Mesoteliomi (ReNaM), Dip. Terapie Oncologiche, UO Epidemiologia, IRCCS AOU San Martino, Istituto Nazionale Ricerca sul Cancro (IST)
Registro dei Tumori Colorettali di Modena c/o Dipartimento di Medicine e Specialità Mediche, Medicina 1, Policlinico Universitario di Modena
Registro Tumori Specialistico del Pancreas della Provincia di Reggio Emilia, SC di Gastroenterologia ed Endoscopia Digestiva, Arcispedale Santa Maria Nuova-IRCCS, Servizio Interaziendale di Epidemiologia, AUSL Reggio Emilia
Financial support: None.
Conflict of interest: The authors declare no conflicts of interest.
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Authors

Affiliations

  • Evaluative Epidemiology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan - Italy
  • Tobacco Control Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan - Italy
  • Environmental Epidemiology Unit, Fondazione IRCCS Istituto Nazionale dei Tumori, Milan - Italy
  • Cancer Prevention and Research Institute, Istituto per lo Studio e la Prevenzione Oncologica, Florence - Italy
  • Osservatorio Fumo Alcol e Droga, Istituto Superiore di Sanità, Rome - Italy
  • Interinstitutional Epidemiology Unit, AUSL Reggio Emilia, Reggio Emilia - Italy
  • The full list of members of AIRTUM Working Group is available in the Appendix

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