Abstract
Background:
The comparison of cancer mortality rates and risk factors among foreign-born populations in a host country with those in the country of origin provides insights into differences in access to care, timely diagnosis, and disease management between the two countries.
Methods:
Using 2008-2018 cancer mortality data for the Italian population and for Italy-born Americans, we calculated age-standardized mortality rates (ASMRs) and standardized mortality ratios (SMRs).
Results:
ASMRs were lower in Italy-born Americans (201.5 per 100,000) compared to Italians (255.1 per 100,000). For all neoplasms combined, SMRs for Italy-born American men and women were 0.75 (95%CI: 0.73-0.77) and 0.78 (95%CI: 0.76-0.80), respectively. Among men, the SMRs were significantly below 1 for oral cavity, stomach, colorectal, liver, lung, prostate, bladder, and kidney cancer. Among women, the SMRs were 0.69 for oral, 0.40 for stomach, 0.61 for colorectal, 0.72 for liver, 0.73 for breast, and 0.53 for kidney cancers. Mortality was not reduced for lung (1.02, 95%CI: 0.94-1.10) cancer in women.
Conclusion:
Generational differences in smoking prevalence patterns between the US and Italy may explain the advantages for Italy-born Americans for lung and other tobacco-related cancers compared to their Italian male counterparts. Lower prevalence of Helicobacter pylori, alcohol consumption, hepatitis B and C virus in the US may justify the lower mortality for stomach and liver cancer, among Italy-born Americans. Earlier and more widespread adoption of cancer screening and effective treatments in the US is likely to be influential in breast, colorectal, and prostate cancer mortality.
Keywords: Immigrants, European, Italians, Americans, Cancer, Mortality, Italy, US Italian-Americans, Diaspora
Introduction
Among specific immigrant populations, cancer mortality rates tend to deviate from those in the countries of origin and approach rates of the majority population in the host country at different times, sometimes taking generations. A side from changes in lifestyle habits, diets, and risk factor exposures, this transition/trajectory may be influenced by host country healthcare-related dependent factors such as access to cancer care and screening, timely diagnosis, and adequate treatment (McCredie, 1998,Arnold et al., 2010).
Previous studies have examined the differences and similarities in cancer patterns between either Italy and the US, or between Italy-born Americans and non-Italian US Whites using group data from the 1970s and 1980s (La Vecchia et al., 1988,Geddes et al., 1991,Bernstein et al., 1993). However, an analysis between Italian populations only, directly comparing the diaspora (Italy-born Americans)-using individual-level data rather than areas with a high density of Italians-and those in the country of origin, Italy, has never been carried out. The rationale for the current study is that there is genetic similarity between these two populations but differences in lifestyle habits as well remarkable differences in health care systems (a universal health system in Italy, while one linked to employment and social programs in the US) also impact cancer patterns.
In this study, we assess site-specific differences in cancer mortality between two Italian ancestry populations (Italy-born Americans and Italians in Italy), using individual-level mortality data available from Italy and four American states: California, Florida, New York, and Massachusetts, which combined represent over 25% of the US population. The population of Italy-born Americans (approximately 440,000) predominantly consists of elderly individuals in age-groups for which cancer is a common cause of death, reflecting the Italian migration to the US up until the late 1960s.
Methods
Individual-level mortality data by sex and age for all cancers combined and for 20 select cancer sites for Italy-born Americans were obtained from the California, Florida, Massachusetts, and New York Departments of Vital Statistics from 2008-2018. These states were common destinations for the Italian diaspora in the US during the twentieth century. State mortality datasets have close to 99% completeness in terms of country of birth for all deceased subjects (Pinheiro et al., 2020). The combined population totals (rate denominators) stratified by five-year age-group and sex for the same years were obtained based on the “non-Hispanic White Race” and “country of birth Italy” categories from the single-year American Community Survey data for the four states combined and pooled for years 2008-2018 (Ruggles et al., 2019). For Italians in Italy (hereafter referred to as Italians), we retrieved corresponding official Italian death certificate data and resident population estimates, based on official census, from the World Health Organization (WHO) database (World Health Organization, 2020) for 2008-2016. The list of corresponding International Classification of Diseases (ICD) codes used is available in Supplementary Table 1.
Using the matrices of certified deaths and resident populations, we computed sex-specific death rates for each five-year age-group (from 0-4 to 85+ years); we then derived age-standardized death rates for all ages combined, ages 0-74, and 75 and over, using the European and the World Standard Populations (Supplementary Table 2) (European Commission, 2013,Esteve et al., 1994). The very small Italy-born American population in younger age-groups (0-19 years of age) and corresponding low number of deaths, may contribute to unstable age-adjusted rates that occur in cancers sites with recorded deaths among children. As such, for these cancer sites, rates were computed for all ages combined as well as for those older than 20 only. To compare mortality among Italy-born Americans and Italians, we calculated the standardized mortality ratios (SMRs) and corresponding 95% confidence intervals (CIs) using the Vandenbroucke Method (Vandenbroucke, 1982). For the data corresponding to Italians, ethics committee approval was not required given the use of anonymous public data only. However, institutional review board authorizations were obtained in order to use data from the four US states. For all statistical analyses, we used SAS software version 9.4 (SAS Institute Inc., Cary, North Carolina).
Results
Totals of 10,269 cancer deaths recorded among Italy-born Americans and 1,513,860 among Italians living in Italy were available for analysis. Table 1 shows the age-standardized death rates by sex, using the European Standard Population for the Italy-born American (2008-2018) and the Italian populations (2008-2016). The all-combined cancer death rate in Italy-born Americans was 260.3/100,000 and 154.6/100,000 for men and women, respectively, while for Italians it was 345.7/100,000 for men and 192.4/100,000 for women.
Table 1.
Age-adjusted (European standard population) mortality rates per 100,000 for various cancers for all ages and both sexes, 2008-2018.
Males | Females | |||||||
---|---|---|---|---|---|---|---|---|
Italy-born Americans | Italiansa | Italy-born Americans | Italiansa | |||||
ASMR | Deathsa | ASMR | Deaths | ASMR | Deathsa | ASMR | Deaths | |
Oral cavity and pharynx | 2.89 | 63 | 7.03 | 17,819 | 1.69 | 43 | 2.31 | 7912 |
Esophagus | 4.05 | 91 | 4.91 | 12,336 | 1.00 | 33 | 1.18 | 4126 |
Stomach | 10.24 | 253 | 20.86 | 51,431 | 4.61 | 124 | 10.36 | 36,903 |
Colorectal | 23.43 | 554 | 42.28 | 103,324 | 17.26 | 468 | 25.14 | 90,004 |
Liver | 14.06 | 328 | 22.93 | 57,465 | 6.32 | 183 | 8.61 | 30,416 |
Gallbladder | 1.25 | 31 | 1.29 | 3165 | 1.40 | 38 | 1.92 | 6631 |
Pancreas | 16.96 | 395 | 18.95 | 47,431 | 13.82 | 410 | 14.49 | 50,402 |
Lung | 73.26 | 1756 | 89.52 | 223,537 | 23.23 | 611 | 23.74 | 78,739 |
Skin melanoma | 3.40 | 74 | 3.89 | 9864 | 1.66 | 34 | 2.09 | 6902 |
Breast | ‡ | ‡ | ‡ | ‡ | 25.66 | 593 | 32.73 | 109,576 |
Cervix | ‡ | ‡ | ‡ | ‡ | 1.23 | 23 | 1.23 | 3877 |
Corpus | ‡ | ‡ | ‡ | ‡ | 5.20 | 134 | 6.72 | 22,481 |
Ovary | ‡ | ‡ | ‡ | ‡ | 8.54 | 208 | 9.11 | 29,685 |
Prostate | 24.22 | 586 | 28.58 | 66,389 | ‡ | ‡ | ‡ | ‡ |
Bladder | 14.93 | 382 | 16.85 | 40,181 | 2.42 | 89 | 2.96 | 11,019 |
Kidney and other urinary sites | 7.55 | 125 | 10.14 | 25,082 | 1.89 | 56 | 3.64 | 12,766 |
Brain and CNS | 7.47 | 156 | 7.57 | 19,571 | 5.40 | 107 | 5.01 | 15,857 |
Non-Hodgkin’s lymphoma | 9.98 | 244 | 9.07 | 22,527 | 6.12 | 190 | 5.60 | 19,507 |
Multiple myeloma | 4.96 | 124 | 5.86 | 14,421 | 3.80 | 107 | 4.03 | 14,138 |
Leukemia | 12.79 | 310 | 12.28 | 30,141 | 7.73 | 180 | 6.93 | 24,144 |
All malignant cancers | 260.33 | 6168 | 345.69 | 851,923 | 154.55 | 4101 | 192.39 | 661,937 |
Abbreviations: ASMR, Age standardized mortality rate; CNS, Central Nervous System.
2008-2016 for Italy (WHO data).
Not reported; rate calculated from observations fewer than 10
Among Italy-born American males, the ranking in top causes of cancer death in decreasing order was lung, prostate, colorectal, pancreas, and bladder. For Italian males, it was lung, colorectal, prostate, liver, and stomach. Italian males showed higher cancer mortality rates compared to Italy-born Americans for all sites except non-Hodgkin’s lymphoma and leukemia. Among Italy-born American females, the top causes of cancer death were breast, lung, colorectal, pancreas and ovary. For Italian women, the rank order was breast, colorectal, lung, pancreas and stomach. Despite the different rank order, second and third among Italy-born Americans and Italians, respectively, mortality rates for lung cancer in the groups of interest are quite similar: 23.2 in Italy-born American females and 23.7 per 100,000 in Italians.
Table 2 reports the SMRs of select cancer sites for Italy-born Americans compared to the general population of Italy. Among Italy-born Americans, the SMR for all cancer deaths was 0.75 (95% CI 0.73-0.77) in men and 0.78 (95% CI 0.76-0.80) in women. For most cancers, the SMRs were below 1 and were particularly low for neoplasms of the digestive tract: 0.42 in men and 0.69 in women for oral and pharyngeal cancer; 0.51 for men and 0.40 for women for stomach; 0.54 for men and 0.61 for women for colorectal; 0.62 for men and 0.72 for women for liver cancer. Among Italy-born American males, lower mortality was observed for kidney (SMR: 0.52, 95% CI 0.43-0.62), prostate (SMR: 0.78, 95%CI 0.72-0.84), lung (SMR: 0.83, 95% CI 0.79-0.87), and bladder cancer (SMR: 0.89, 95% CI 0.80-0.98). Among females, the SMRs were lower than 1 for kidney (SMR: 0.53, 95% CI 0.40-0.68), skin melanoma (SMR: 0.70, 95% CI 0.49-0.96), breast (SMR: 0.73, 95% CI 0.67-0.79) and corpus uteri (SMR: 0.78, 95% CI 0.65-0.91). Non-Hodgkin’s lymphoma (NHL) was the only neoplasm with a SMR significantly above 1 for both sexes (SMR: 1.16, 95% CI 1.02-1.31 males and 1.21, 95% CI 1.04-1.39 females).
Table 2.
Standardized mortality ratios for select cancers in Italy-born Americans versus Italians for both sexes, 2008-2018.
Males | Females | |||
---|---|---|---|---|
Italy-born Americans | Italy-born Americans | |||
SMR | 95% CI | SMR | 95% CI | |
Oral cavity and pharynx | 0.42 | 0.32-0.53 | 0.69 | 0.50-0.91 |
Esophagus | 0.83 | 0.67-1.01 | 0.98 | 0.67-1.34 |
Stomach | 0.51 | 0.45-0.57 | 0.40 | 0.33-0.48 |
Colorectal | 0.54 | 0.50-0.59 | 0.61 | 0.56-0.67 |
Liver | 0.62 | 0.55-0.69 | 0.72 | 0.62-0.83 |
Gallbladder | 0.99 | 0.67-1.36 | 0.70 | 0.50-0.94 |
Pancreas | 0.90 | 0.82-1.00 | 0.99 | 0.90-1.09 |
Lung | 0.83 | 0.79-0.87 | 1.02 | 0.94-1.10 |
Skin melanoma | 0.90 | 0.70-1.11 | 0.70 | 0.49-0.96 |
Breast | ‡ | ‡ | 0.73 | 0.67-0.79 |
Cervix | ‡ | ‡ | 0.99 | 0.62-1.43 |
Corpus | ‡ | ‡ | 0.78 | 0.65-0.91 |
Ovary | ‡ | ‡ | 0.97 | 0.84-1.10 |
Prostate | 0.78 | 0.72-0.84 | ‡ | ‡ |
Bladder | 0.89 | 0.80-0.98 | 0.90 | 0.72-1.10 |
Kidney and other urinary sites | 0.52 | 0.43-0.62 | 0.53 | 0.40-0.68 |
Brain and CNS | 1.05 | 0.89-1.22 | 1.00 | 0.82-1.20 |
Non-Hodgkin’s lymphoma | 1.16 | 1.02-1.31 | 1.21 | 1.04-1.39 |
Multiple myeloma | 0.87 | 0.72-1.03 | 0.91 | 0.75-1.09 |
Leukemia | 1.08 | 0.96-1.20 | 0.93 | 0.80-1.07 |
All malignant cancers | 0.75 | 0.73-0.77 | 0.78 | 0.76-0.80 |
Abbreviations: SMR, Standardized mortality ratio; CI, Confidence Interval; CNS, Central Nervous System.
Not reported; calculated from observations fewer than 10
The number of deaths and SMRs for selected cancer sites among males younger than 75 years of age and those 75 years of age or older are given in Table 3. Table 4 gives the corresponding results for women. Among males, the SMR for all cancer sites combined was 0.68 (95% CI 0.65-0.71) for individuals younger than 75 years old and 0.79 (95% CI 0.77-0.81) for men 75 or older. There were no differences in the SMRs between those younger than 75 and those 75 or older, except for cancers of the stomach, lung, brain and CNS, and NHL whose SMRs were lower among men younger than 75. Among females, the SMR was 0.80 (95% CI 0.76-0.84) for those below 75 years of age and 0.77 (95% CI 0.74-0.80) for women ages 75 years old or more. No significant differences in SMRs were observed between age-groups for women.
Table 3.
Male standardized mortality ratios stratified for age for select cancers in Italy-born Americans versus Italians, 2008-2018.
Males <75 years | Males ≥75 years | |||||
---|---|---|---|---|---|---|
Italy-born Americans | Italy-born Americans | |||||
Observed deaths | SMR | 95% CI | Observed deaths | SMR | 95% CI | |
Stomach | 69 | 0.39 | 0.30-0.48 | 184 | 0.58 | 0.50-0.66 |
Colorectal | 176 | 0.52 | 0.45-0.60 | 378 | 0.55 | 0.50-0.61 |
Liver | 145 | 0.63 | 0.53-0.73 | 183 | 0.61 | 0.52-0.70 |
Pancreas | 166 | 0.84 | 0.72-0.98 | 229 | 0.95 | 0.83-1.08 |
Lung | 665 | 0.74 | 0.69-0.80 | 1091 | 0.90 | 0.85-0.95 |
Prostate | 99 | 0.78 | 0.64-0.94 | 487 | 0.78 | 0.71-0.85 |
Bladder | 82 | 0.79 | 0.63-0.97 | 300 | 0.92 | 0.82-1.03 |
Kidney and other urinary sites | 49 | 0.54 | 0.40-0.71 | 76 | 0.51 | 0.40-0.63 |
Brain and CNS | 80 | 0.88 | 0.69-1.08 | 76 | 1.33 | 1.05-1.65 |
Non-Hodgkin’s lymphoma | 66 | 0.84 | 0.65-1.06 | 178 | 1.35 | 1.16-1.56 |
Multiple myeloma | 44 | 0.91 | 0.66-1.19 | 80 | 0.85 | 0.67-1.05 |
Leukemia | 97 | 1.04 | 0.85-1.26 | 213 | 1.10 | 0.95-1.25 |
All malignant cancers | 2065 | 0.68 | 0.65-0.71 | 4103 | 0.79 | 0.77-0.81 |
Abbreviations: SMR, Standardized mortality ratio; CI, Confidence Interval; CNS, Central Nervous System.
Table 4.
Female standardized mortality ratios stratified for age for select cancers in Italy-born Americans versus Italians, 2008-2018.
Females <75 years | Females ≥75 years | |||||
---|---|---|---|---|---|---|
Italy-born Americans | Italy-born Americans | |||||
Observed deaths | SMR | 95% CI | Observed deaths | SMR | 95% CI | |
Stomach | 34 | 0.45 | 0.31-0.62 | 90 | 0.39 | 0.31-0.47 |
Colorectal | 128 | 0.70 | 0.59-0.83 | 340 | 0.58 | 0.52-0.65 |
Primary liver cancer | 57 | 0.87 | 0.66-1.10 | 126 | 0.67 | 0.56-0.79 |
Pancreas | 106 | 0.86 | 0.70-1.03 | 304 | 1.04 | 0.93-1.16 |
Lung | 213 | 0.88 | 0.77-1 | 398 | 1.11 | 1.01-1.23 |
Breast | 258 | 0.84 | 0.74-0.95 | 335 | 0.66 | 0.59-0.73 |
Corpus | 55 | 0.83 | 0.63-1.07 | 79 | 0.74 | 0.59-0.91 |
Brain and CNS | 50 | 0.93 | 0.69-1.21 | 57 | 1.06 | 0.80-1.36 |
Non-Hodgkin’s lymphoma | 40 | 0.92 | 0.65-1.22 | 150 | 1.32 | 1.12-1.54 |
Multiple myeloma | 38 | 1.14 | 0.81-1.54 | 69 | 0.82 | 0.64-1.03 |
Leukemia | 44 | 0.88 | 0.64-1.16 | 136 | 0.94 | 0.79-1.11 |
All malignant cancers | 1313 | 0.80 | 0.76-0.84 | 2788 | 0.77 | 0.74-0.80 |
Abbreviations: SMR, Standardized mortality ratio; CI, Confidence Interval; CNS, Central Nervous System.
Discussion
Mortality rates for all cancers combined and for most major sites were lower in Italy-born Americans compared to Italians. Overall, cancer mortality of the digestive tract (oral, stomach, colorectal, liver), tobacco-related cancers (lung and bladder) among males, as well as kidney and breast cancer were lower in Italy-born Americans compared to Italians. NHL was the only cancer for which Italy-born Americans showed higher mortality rates than Italians for both sexes.
In the two countries, mortality patterns for tobacco-related cancers, particularly lung cancer, follow the smoking prevalence patterns observed across generations. In US males, the smoking prevalence has been decreasing since 1964 (Thun et al., 2012), much earlier than in Italy, with subsequent declines in lung cancer death rates after three decades (i.e., around the early 1990s) (Carioli et al., 2020,Islami et al., 2020). In the US, women started smoking earlier and at higher rates than in Europe; however, smoking prevalence has stabilized and even declined slightly in recent years, also earlier than in Europe (GBD 2015 Tobacco Collaborators, 2017). As a consequence, female lung cancer trends started to decline around the 2000s in the US, while in most European countries the female lung cancer epidemic is still developing (Carioli et al., 2020,Islami et al., 2020,Santucci et al., 2020). In 2020, lung cancer rates in Italy approach 13/100,000 (world standard), having never reached the highest rates of about 26/100,000 observed among US females during the early 1990s (Ferlay et al., 2020). These differences in time and magnitude of smoking prevalence trends by sex explain the significant differences found here for tobacco-related cancers such as lung and bladder cancer in men (with higher rates in Italy), and the lack of difference between women of Italian ancestry in the US and Italy.
Italy-born Americans had particularly low rates for other tobacco-related cancers, such as kidney and oral cancer in comparison to Italians. For kidney cancer, obesity and hypertension are important risk factors aside from smoking (Pinheiro et al., 2021). The prevalence of obesity in Italy is lower than that in the US (Centers for Disease Control and Prevention, 2016,DiBonaventura et al., 2018). However, the most recent data available for 2014 has shown that 55% of adults suffer from hypertension in comparison to 42% of adults in the US for that year (Tocci et al., 2016,Zhang and Moran, 2017), and management of hypertension may be less effective in Italy. Along with the observed differences in smoking patterns amongst countries, this could partly account for the findings in our study. For oral cancer, it is known that tobacco and alcohol use increase the risk of developing this malignancy. Our findings parallel the smoking patterns observed for both countries, and they are in contrast to the greater alcohol per capita consumption and prevalence of heavy episodic drinking in the US compared to Italy (World Health Organization, 2018). However, specific data for alcohol consumption among Italy-born Americans is non-existent.
Colorectal cancer is the second or third most common cause of cancer deaths among Italy-born Americans and Italians for both sexes. Widespread screening for colorectal cancer started earlier in the US (Doubeni, 2014), reaching the participation of about 40% of the target population in 2012 (Barlow et al., 2020). Meanwhile, in Italy, organized screening was introduced in select regions around 2005 and less than 30% of the target population participated in 2014 (Giorgi Rossi et al., 2018). This can partly explain the lower mortality among Italy-born Americans. Moreover, there has been notable progress in the management and treatment of colorectal cancer in the US (Giorgi Rossi et al., 2018,Barlow et al., 2020) while variations in access to effective treatment between the US and Italy can explain some of these differences.
Breast cancer is the second major cause of cancer death among US women after lung cancer (IARC, 2021). However, it is the leading cause of cancer deaths in both Italy-born American and Italian women. Over the last three decades, rates for this cancer site have declined by about 40% in the US and 30% in Italy (Malvezzi et al., 2019,Smith et al., 2019). This decline has been mainly driven by improvements in treatments as well as uptake of mammographic screening over the past several decades (Giorgi Rossi et al., 2018,Islami et al., 2020), which has been earlier on and more widespread in the US and consequently among Italy-born Americans (Howard et al., 2009, Barlow et al., 2020). As is the case for colorectal cancer, data suggest that breast cancer screening prevalence is higher in the US, approaching nearly 73%, compared to 39% of women in Italy who participate in organized breast cancer screening programs (Ponti et al., 2017, Sabatino et al., 2015).
Italy-born Americans also had lower mortality compared to Italians for some infection-related cancers such as stomach and liver. Helicobacter pylori (H. pylori) is the key risk factor for gastric cancer. Differences in gastric mortality between Italy-born Americans and Italians are attributable to the variations in prevalence of infection. Indeed, H. pylori prevalence in the US general population is around 30% (IARC Working Group, 2012), while in Italy it is much higher, around 56% (Hooi et al., 2017), particularly in the elderly (Roberts et al., 2016). For liver cancer, the high rates in Italians are attributable to a higher prevalence of chronic infection with hepatitis B (HBV) and C (HCV) viruses (Baecker et al., 2018) and possibly higher regular alcohol consumption (Franceschi et al., 2006, La Vecchia et al., 2014) in Italy. Overall, HCV and HBV prevalence are 5.9% and 0.7% in Italy, which are higher when compared to the US population corresponding estimates of 1.0 % and 0.3% (European Centre for Disease Prevention and Control, 2016,Rosenberg et al., 2018,Lim et al., 2020). In the US, the mortality and incidence for liver cancer and hepatocellular carcinoma (HCC), specifically, is predominantly HCV-related (El-Serag, 2012) while in Western European countries, a high proportion of liver cancer cases are related to alcohol and/or metabolic conditions (Cancer Research UK, 2021,Borie et al., 2009,Pinheiro et al., 2019). There were no significant differences in mortality for cervical cancer amongst Italy-born American and Italian women. This parallels the similar prevalence in human papillomavirus (HPV) among women in the general population in Italy and the US, with 4.1% and 3.3%, respectively (Bruni et al., 2019,McQuillan et al.,2017). Unlike the US, in Italy, there is no organized screening program for cervical cancer, since a large portion of young and middle-aged women undergo voluntary screening. However, despite our findings, compared to the US, the proportion of women who participate in cervical cancer screening in Italy, remains low (Ponti et al., 2017,Sabatino et al., 2015).
Over the last two decades, favorable mortality rates for prostate cancer are attributed to improvements in treatments (surgery, radiotherapy, as well as the use of newer androgen deprivation therapies) and more widespread use of prostate-specific antigen (PSA) testing, particularly in the US. The combination of wider use of PSA testing and more aggressive treatment in the US may well justify this advantage for Italy-born Americans in comparison to Italians. Substantial advantages in mortality rates for prostate cancer among US immigrant populations in comparison to their countries of origin are also found for other nationalities in the US (Pinheiro et al., 2018). Lastly, the finding of excessive mortality for NHL in both sexes, especially in older ages among Italy-born Americans compared to Italians in both sexes lacks explanation and deserves further study.
Strengths of this study include its population-based design and the granular nature of its data, namely the availability of individual-level death data for Italy-born Americans and the availability of specific denominators for Italy-born populations in the US through the American Community Survey. Mortality certification in both the US and Italy is valid for most cancers, and changes in classification, coding, and registration are unlikely to affect our results. Moreover, death certificate criteria did not change over time and is similar between the US and Italy. Therefore, the observed differences in cancer mortality between Italy-born Americans and Italians are unlikely to be affected by major bias. However, our study is not without limitations. This includes the lack of specific data on socio-economic status and risk factors, particularly for the Italy-born American population; the only data available is for the non-Hispanic White US population. The healthy immigrant effect could account for a baseline inherent difference between the two populations, with an advantage for those who emigrate (i.e., Italy-born Americans). However, when considering cancer, a chronic disease for which the latency periods between risk factor exposures and actual diagnosis may take decades, this healthy immigrant advantage in relation to those in the country of origin has not been observed on a population basis (Pinheiro et al., 2018).
As a whole, the overall lower mortality rates in Italy-born Americans can be attributed to lower levels of smoking prevalence earlier on (especially among males), earlier and greater adoption of modern effective treatments, and a higher screening coverage for selected neoplasms (Giorgi Rossi et al., 2018,Barlow et al., 2020). This line of reasoning can be applied to several cancer sites (Smith et al., 2019) including tobacco-related cancers such as lung and bladder as well as screening-related cancers like breast, colorectal, and prostate. It is of interest that despite the worldwide accepted beneficial effects of the Mediterranean diet (albeit more so for heart disease), possibly more prevalent in Italy as a Mediterranean country, this “advantage” is not reflected in the cancer mortality rates shown here for digestive cancers as a whole. Italians showed higher rates for most digestive cancers in comparison to Italy-born Americans, a group that could have possibly adopted different dietary preferences over time given the assimilation to a new environment. Having said that, mortality rates capture both incidence and survival, and referred to factors such accessibility to treatment and screening may impact the current rates by means of improved survival; therefore, more detailed studies are necessary. In agreement with this, survival statistics for recent calendar periods show that the five-year relative survival for major cancer sites, except for stomach cancer, is higher in the US than in Italy (Santucci et al., 2020).
In conclusion, despite the absence of a national health service in the US, cancer mortality was lower for Italy-born Americans than Italians. Our mortality data suggests that, based on the comparison of patterns in populations of Italian descent, on a population-basis, cancer prevention, screening, and management seem more effective in the US as compared to Italy. More detailed studies focusing on comparisons of population-based indicators in more homogenous populations, in terms of ancestry, socio-economic status, and race-ethnicity are essential in order to more clearly ascertain the end results of different health systems.
Supplementary Material
Financial Disclosure:
Supplemental funding was provided by the Sylvester Comprehensive Cancer Center at University of Miami Miller School of Medicine. Research reported in this publication was also supported by the National Cancer Institute of the National Institutes of Health under Award Number P30CA240139. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.
Footnotes
Conflict of Interest Statement: The authors declare no conflicts of interest.
References
- Arnold M, Razum O, Coebergh JW (2010). Cancer risk diversity in non-western migrants to Europe: An overview of the literature. European journal of cancer 46(14):2647–2659. doi: 10.1016/j.ejca.2010.07.050. [DOI] [PubMed] [Google Scholar]
- Baecker A, Liu X, La Vecchia C, Zhang ZF (2018). Worldwide incidence of hepatocellular carcinoma cases attributable to major risk factors. Eur J Cancer Prev 27(3):205–212. doi: 10.1097/CEJ.0000000000000428. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Barlow WE, Beaber EF, Geller BM, Kamineni A, Zheng Y, Haas JS et al. (2020). Evaluating Screening Participation, Follow-up, and Outcomes for Breast, Cervical, and Colorectal Cancer in the PROSPR Consortium. Journal of the National Cancer Institute 112(3):238–246. doi: 10.1093/jnci/djz137. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bernstein L, Flannery J, Reynolds P (1993). Cancer in Italian migrant populations. The United States of America. IARC Sci Publ (123):67–94. [PubMed] [Google Scholar]
- Borie F, Trétarre B, Bouvier AM, Faivre J, Binder F, Launoy G et al. (2009). Primitive liver cancers: epidemiology and geographical study in France. Eur J Gastroenterol Hepatol 21(9):984–989. doi: 10.1097/MEG.0b013e3283293783. [DOI] [PubMed] [Google Scholar]
- Bruni L, Albero G, Serrano B, et al. Human Papillomavirus and Related Diseases in Italy. ICO/IARC Information Centre on HPV and Cancer. 2019. Accessed at https://hpvcentre.net/statistics/reports/ITA.pdf?t=1622577907063 on June 1, 2021.
- Cancer Research UK. Liver Cancer Statistics. Accessed at https://www.cancerresearchuk.org/health-professional/cancer-statistics/statistics-by-cancer-type/liver-cancer#heading-Three on June 1, 2021.
- Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C, Negri E et al. (2020). European cancer mortality predictions for the year 2020 with a focus on prostate cancer. Ann Oncol 31(5):650–658. doi: 10.1016/j.annonc.2020.02.009. [DOI] [PubMed] [Google Scholar]
- Centers for Disease Control and Prevention. Prevalence of overweight, obesity, and extreme obesity among adults aged 20 and over: United States, 1960–1962 Through 2013–2014. 2016. Accessed at https://www.cdc.gov/nchs/data/hestat/obesity_adult_13_14/obesity_adult_13_14.pdf on June 1, 2021.
- DiBonaventura M, Nicolucci A, Meincke H, Le Lay A, Fournier J (2018). Obesity in Germany and Italy: prevalence, comorbidities, and associations with patient outcomes. Clinicoecon Outcomes Res 10:457–475. doi: 10.2147/CEOR.S157673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Doubeni CA (2014). The impact of colorectal cancer screening on the US population: is it time to celebrate? Cancer 120(18):2810–2813. doi: 10.1002/cncr.28789. [DOI] [PMC free article] [PubMed] [Google Scholar]
- El-Serag HB (2012). Epidemiology of viral hepatitis and hepatocellular carcinoma. Gastroenterology 142(6):1264–1273.e1261. doi: 10.1053/j.gastro.2011.12.061. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Esteve J, Benhamou E, Raymond L (1994). Statistical methods in cancer research. Volume IV. Descriptive epidemiology. IARC Sci Publ (128):1–302. [PubMed] [Google Scholar]
- European Centre for Disease Prevention and Control. Systematic review on hepatitis B and C prevalence in the EU/EEA. Stockholm: ECDC; 2016. [Google Scholar]
- European Commission. Eurostat: European Population 2013. Accessed at https://ec.europa.eu/eurostat/en/web/products-manuals-and-guidelines/-/KS-RA-13-028 on July 20, 2021.
- Ferlay J, Ervik M, Lam F, Colombet M, Mery L, Piñeros M, et al. Global Cancer Observatory: Cancer Today. Lyon, France: International Agency for Research on Cancer. 2020:Accessed at https://gco.iarc.fr/today on May 15, 2021. [Google Scholar]
- Franceschi S, Montella M, Polesel J, La Vecchia C, Crispo A, Dal Maso L et al. (2006). Hepatitis viruses, alcohol, and tobacco in the etiology of hepatocellular carcinoma in Italy. Cancer Epidemiol Biomarkers Prev 15(4):683–689. doi: 10.1158/1055-9965.EPI-05-0702. [DOI] [PubMed] [Google Scholar]
- GBD 2015 Tobacco Collaborators (2017). Smoking prevalence and attributable disease burden in 195 countries and territories, 1990–2015: a systematic analysis from the Global Burden of Disease Study 2015. Lancet 389(10082):1885–1906. doi: 10.1016/S0140-6736(17)30819-X. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Geddes M, Balzi D, Buiatti E, Khlat M, Parkin D (1991). Cancer in Italian migrants. Cancer causes & control 2(2):133–140. doi: 10.1007/BF00053133. [DOI] [PubMed] [Google Scholar]
- Giorgi Rossi P, Carrozzi G, Federici A, Mancuso P, Sampaolo L, Zappa M (2018). Invitation coverage and participation in Italian cervical, breast and colorectal cancer screening programmes. Journal of medical screening 25(1):17–23. doi: 10.1177/0969141317704476. [DOI] [PubMed] [Google Scholar]
- Hooi JKY, Lai WY, Ng WK, Suen MMY, Underwood FE, Tanyingoh D et al. (2017). Global Prevalence of Helicobacter pylori Infection: Systematic Review and Meta-Analysis. Gastroenterology 153(2):420–429. doi: 10.1053/j.gastro.2017.04.022. [DOI] [PubMed] [Google Scholar]
- Howard DH, Richardson LC, Thorpe KE (2009). Cancer screening and age in the United States and Europe. Health Aff (Millwood) 28(6):1838–1847. doi: 10.1377/hlthaff.28.6.1838. [DOI] [PubMed] [Google Scholar]
- IARC. Cancer Today. Accessed at https://gcoiarcfr/today/home on January 15, 2021.
- IARC Working Group (2012). IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. IARC 100 B(Biological Agents). [Google Scholar]
- Islami F, Siegel RL, Jemal A (2020). The changing landscape of cancer in the USA-opportunities for advancing prevention and treatment. Nat Rev Clin Oncol 17(10):631–649. doi: 10.1038/s41571-020-0378-y. [DOI] [PubMed] [Google Scholar]
- La Vecchia C, Harris RE, Wynder EL (1988). Comparative Epidemiology of Cancer between the United States and Italy. Cancer Research 48(24 Part 1):7285–7293. [PubMed] [Google Scholar]
- La Vecchia C, Bosetti C, Bertuccio P, Castro C, Pelucchi C, Negri E (2014). Trends in alcohol consumption in Europe and their impact on major alcohol-related cancers. Eur J Cancer Prev 23(4):319–322. doi: 10.1097/CEJ.0b013e32836562f1. [DOI] [PubMed] [Google Scholar]
- Lim JK, Nguyen MH, Kim WR, Gish R, Perumalswami P, Jacobson IM (2020). Prevalence of Chronic Hepatitis B Virus Infection in the United States. Am J Gastroenterol 115(9):1429–1438. doi: 10.14309/ajg.0000000000000651. [DOI] [PubMed] [Google Scholar]
- Malvezzi M, Carioli G, Bertuccio P, Boffetta P, Levi F, La Vecchia C et al. (2019). European cancer mortality predictions for the year 2019 with focus on breast cancer. Ann Oncol 30(5):781–787. doi: 10.1093/annonc/mdz051. [DOI] [PubMed] [Google Scholar]
- McCredie M (1998). Cancer epidemiology in migrant populations. Recent results in cancer research 154:298–305. doi: 10.1007/978-3-642-46870-4_21. [DOI] [PubMed] [Google Scholar]
- McQuillan G, Kruszon-Moran D, Markowitz LE, Unger ER, Paulose-Ram R. Prevalence of HPV in adults aged 18–69: United States, 2011–2014. NCHS data brief, no 280. Hyattsville, MD: National Center for Health Statistics; 2017. [Google Scholar]
- Pinheiro P, Callahan K, Kobetz E Disaggregated Hispanic Groups and Cancer: Importance, Methodology, and Current Knowledge. In: Ramirez AG, Trapido EJ. Advancing the Science of Cancer in Latinos ed. Cham: Springer International Publishing, 2020:17–34. [PubMed] [Google Scholar]
- Pinheiro PS, Callahan KE, Stern MC, de Vries E (2018). Migration from Mexico to the United States: A high-speed cancer transition. International journal of cancer 142(3):477–488. doi: 10.1002/ijc.31068. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinheiro PS, Medina HN, Callahan KE, Koru-Sengul T, Sharma J, Kobetz EN et al. (2021). Kidney cancer mortality disparities among Hispanics in the US. Cancer Epidemiol 72:101938. doi: 10.1016/j.canep.2021.101938. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Pinheiro PS, Callahan KE, Jones PD, Morris C, Ransdell JM, Kwon D et al. (2019). Liver cancer: A leading cause of cancer death in the United States and the role of the 1945–1965 birth cohort by ethnicity. JHEP Rep 1(3):162–169. doi: 10.1016/j.jhepr.2019.05.008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ponti A, Anttila A, Ronco G, et al. Cancer Screening in the European Union. Report on the implementation of Council Recommendation on Cancer Screening. Brussels: European Commission; 2017. [Google Scholar]
- Roberts SE, Morrison-Rees S, Samuel DG, Thorne K, Akbari A, Williams JG (2016). Review article: the prevalence of Helicobacter pylori and the incidence of gastric cancer across Europe. Aliment Pharmacol Ther 43(3):334–345. doi: 10.1111/apt.13474. [DOI] [PubMed] [Google Scholar]
- Rosenberg ES, Rosenthal EM, Hall EW, Barker L, Hofmeister MG, Sullivan PS et al. (2018). Prevalence of Hepatitis C Virus Infection in US States and the District of Columbia, 2013 to 2016. JAMA Network Open 1(8):e186371–e186371. doi: 10.1001/jamanetworkopen.2018.6371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ruggles S, Flood S, Goeken R IPUMS USA: Version 9.0 [dataset]. In: IPUMS, ed. Minneapolis, MN, 2019. [Google Scholar]
- Sabatino SA, White MC, Thompson TD, Klabunde CN, Centers for Disease C, Prevention (2015). Cancer screening test use-United States, 2013. MMWR Morbidity and mortality weekly report 64(17):464–468. [PMC free article] [PubMed] [Google Scholar]
- Santucci C, Carioli G, Bertuccio P, Malvezzi M, Pastorino U, Boffetta P et al. (2020). Progress in cancer mortality, incidence, and survival: a global overview. Eur J Cancer Prev 29(5):367–381. doi: 10.1097/CEJ.0000000000000594. [DOI] [PubMed] [Google Scholar]
- Smith RA, Andrews KS, Brooks D, Fedewa SA, Manassaram-Baptiste D, Saslow D et al. (2019). Cancer screening in the United States, 2019: A review of current American Cancer Society guidelines and current issues in cancer screening. CA Cancer J Clin 69(3):184–210. doi: 10.3322/caac.21557. [DOI] [PubMed] [Google Scholar]
- Thun M, Peto R, Boreham J, Lopez AD (2012). Stages of the cigarette epidemic on entering its second century. Tob Control 21(2):96–101. doi: 10.1136/tobaccocontrol-2011-050294. [DOI] [PubMed] [Google Scholar]
- Tocci G, Muiesan ML, Parati G, Agabiti Rosei E, Ferri C, Virdis A et al. (2016). Trends in Prevalence, Awareness, Treatment, and Control of Blood Pressure Recorded From 2004 to 2014 During World Hypertension Day in Italy. J Clin Hypertens (Greenwich) 18(6):551–556. doi: 10.1111/jch.12711. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vandenbroucke JP (1982). A shortcut method for calculating the 95 percent confidence interval of the standardized mortality ratio. Am J Epidemiol (115):303–304. [Google Scholar]
- World Health Organization. Global status report on alcohol and health 2018. Geneva: World Health Organization; 2018. Accessed at https://apps.who.int/iris/bitstream/handle/10665/274603/9789241565639-eng.pdf?ua=1 on June 1, 2021. [Google Scholar]
- World Health Organization Statistical Information System. WHO mortality database: Estimated coverage of mortality data. Geneva: World Health Organization. Accessed at: https://www.whoint/healthinfo/statistics/mortality_rawdata/en/ on August 15, 2020. [Google Scholar]
- Zhang Y, Moran AE (2017). Trends in the Prevalence, Awareness, Treatment, and Control of Hypertension Among Young Adults in the United States, 1999 to 2014. Hypertension 70(4):736–742. doi: 10.1161/HYPERTENSIONAHA.117.09801. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.