Population-based incidence trends of oropharyngeal and oral cavity cancers by sex among the poorest and underprivileged populations

Although health equity is a fundamental goal of many health care systems, it is well documented that inequalities in health outcomes exist both within and between countries. For example, adult mortality rates are twice as high in blacks as in whites in the United States [1] and almost three times as high in unskilled workers as in professionals in the United Kingdom [2]. An important reason for these differences relates to socioeconomic inequities because people residing in poorer neighbourhoods have higher prevalence of high risk behaviours such as smoking and alcohol and less access to health care services.

Disparities in incidence have been observed at multiple scales, varying between global regions [3–5], within countries [6, 7], and between neighbourhoods [8]. It is known that socioeconomic inequalities persist in cancer incidence [9] but little recognition has been given to the effects of socioeconomic status (SES) on the risk of developing oral cancers [10], a cancer showing significant change in trajectory worldwide [11–14]. A study from Scotland suggested that the risk for oral cancer is higher among people living in deprived neighbourhoods (OR = 4.66), a finding mainly attributed to higher rates of smoking (OR = 15.53) [6]. Another study from Canada suggested that SES status affects incidence of oral cancer, with higher rates reported among people with lower median income, less than 8^th grade education and visiting dentists less than once a year [15]. Although several studies have shown associations between SES and oral cancer risk, none have shown an independent effect of SES on risk for developing oral cancer. Conway et al. [16] conducted a systematic review and meta-analysis exploring the relationship between socioeconomic inequalities and oral cancer risk. Their research suggested that in comparison to populations with higher SES, the risk of developing oral cancer was 1.85 times higher with lower educational attainment, 1.84 times higher with low occupational social class and 2.41 times higher with lower income. Further, they suggested that lower SES was significantly associated with increased oral cancer risk in high and lower income countries, which remained after adjusting for potential behavioural confounders. However, after controlling for age, sex, smoking, and alcohol consumption, SES was no longer a significant variable [6, 7, 17]. Therefore, it is important to ascertain the risk of oral cancers according to SES status.

In our previous research in British Columbia (BC), we found that the incidence is increasing among both men and women for oropharyngeal cancers (OPC, in tonsil and oropharygeal areas), and decreasing among men for oral cavity cancer (OCC, other sites in the mouth) [18]. These observed differences were attributed to differences in the aetiology of oral cancers at these different sites [4, 12]; however, it is also important to determine how SES, which may influence the prevalence of risk behaviours (such as alcohol consumption, smoking, and oro-sexual practices) and access to health care [16, 19], is related to differences in incidence rates. Studies on SES disparities in oral cancer research are emerging from the European Union [20], Scotland [6, 7], California (US) [19], and Canada [15, 17, 21]; however, these studies have their own limitations, such as a lack of site-specific [6, 15, 20] and sex-specific [6, 15, 21] data and small sample sizes [6, 15]. A recent paper from California highlighted the importance of reporting population-based trends of oral cancers by site, SES and sex [19]. The objective of our paper is to analyse the relationship between neighbourhood SES status (using a composite index with multiple socioeconomic features including income, housing, education, family demographics and employment obtained from both census data and local health surveys) [22, 23] and incidence for both OPC and OCC stratified by sex, using the population-based cancer registry in BC.

Sample sizes for men with OPC in each socioeconomic deprivation quintile were: q1 (n = 266, 17.6%), q2 (n = 252, 16.6%), q3 (n = 237, 15.6%), q4 (n = 306, 20.2%), and q5 (n = 451, 29.8%); while for OCC they were q1 (n = 412, 15.3%), q2 (n = 437, 16.2%), q3 (n = 427, 15.8%), q4 (n = 509, 18.9%), and q5 (n = 907, 33.6%). Sample sizes for women with OPC in each quintile were: q1 (n = 49, 17.2%), q2 (n = 54, 18.9%), q3 (n = 43, 15.1%), q4 (n = 59, 20.7%), and q5 (n = 80, 28.1%); while for OCC they were q1 (n = 166, 16.1%), q2 (n = 170, 16.5%), q3 (n = 192, 18.6%), q4 (n = 240, 23.2%), and q5 (n = 265, 25.7%). Mean ages at diagnosis were calculated for OPC and OCC by sex and SES deprivation quintiles but no statistically significant differences were found (data not shown).

Men

Age-adjusted incidence rates (AAIR) for OPC and OCC by SES quintile

The AAIR for OPC and OCC are shown by SES deprivation quintiles and gender in Figure 1 for the total study period from 1981 to 2010. For OPC in men, AAIR for quintiles 1 (least deprived) to 5 (most deprived) were: 0.54 (95% CI, 0.28 – 0.80); 0.51 (95% CI, 0.26 – 0.75); 0.47 (95% CI, 0.24 – 0.70); 0.61 (95% CI, 0.34 – 0.87); and 0.89 (95% CI, 0.58 – 2.12), respectively. For OCC in men, AAIR for the deprivation quintiles 1 to 5 were: 0.82 (95% CI, 0.49 – 1.14); 0.87 (95% CI, 0.53 – 1.20); 0.73 (95% CI, 0.56 – 1.21); 1.01 (95% CI, 0.65 – 1.37); and 1.80 (95% CI, 1.33 – 2.26). The highest incidence rates in men for both OPC and OCC were observed in the most deprived quintile (q5), at 1.7 times and 2.2 times higher than men in the least deprived quintile (q1) for OPC and OCC, respectively. Of interest, AAIR for both OPC and OCC were similar in the less deprived quintiles (q1-3).

Temporal trends in AAIR for OPC and OCC by SES quintile

Figure 2A shows AAIR for men in all SES deprivation quintiles combined from 1981 to 2010, in which the AAIR for OPC significantly increased from 1.18 (95% CI, 0.81-1.55) to 4.92 (95% CI, 4.22-5.63), with an annual percent change (APC) of 0.97 (P <0.001). However, the AAIR for OCC decreased non-significantly from 4.95 (95% CI, 4.16-5.74) to 4.60 (95% CI, 3.83-5.37), with an APC of - 0.36 (P = 0.47). Of note, the AAIR for OPC surpassed OCC in 2006–2010. These AAIR trends were also observed in the different SES deprivation quintiles (Figure 2B and C). For OPC, the AAIR significantly increased in all quintiles with the highest increase observed in the most deprived quintile (q5). The APCs were 0.96 (P = 0.001), 0.95 (P = 0.001), 0.90 (P = 0.004), 0.87 (P = 0.006), and 0.98 (P < 0.001) for SES deprivation quintiles q1 to q5, respectively. For OCC, the APC initially increased and then levelled off in all quintiles, with a decline apparent in 2001–2005 and later; these results being non-significant. The APCs were 0.38 (P = 0.24), 0.53 (P = 0.10), 0.22 (P = 0.34), 0.37 (P =0.19) and 0.29 (P = 0.34) for SES deprivation quintiles 1 to 5, respectively. Of interest, the largest decline in OCC rates was seen in q5.

Figures 3A and C show change over time in inequalities in the AAIR for men in comparisons of the least (q1) and most deprived (q5) quintiles. For OPC, first the disparities widened and then narrowed in 2006–2010. The narrowing inequalities between 2001–05 and 2006–2010 were associated with a significant increase in incidence rates in q1 from 0.78 to 1.08 with only a marginal increase in q5 from 1.36 to 1.41. For OCC, there was a minimal disparity during 1981–85 but this widened considerably between 1986–2000. Thereafter, disparities narrowed because of lower incidence rates in both q1 and q5. Overall, disparities were highest for OCC among men.

Age-specific incidence rate (ASIR) in the most deprived quintile (q5)

We then calculated ASIRs for OPC and OCC in men in the most deprived quintile (q5), as these groups showed the highest incidence rates for both OPC and OCC (Figure 4A-C). As expected, OCC incidence rates increased with increasing age and the maximum burden of disease was observed among those age 75 years and older. The highest increase in OPC incidence was observed in the age group 55–64 years. For OPC, ASIRs in q5 were: 1.89 (95% CI, 1.41-2.83) for 45–54 years; 3.62 (95% CI, 2.43-4.19) for 55–64 years; 3.28 (95% CI, 1.52-4.23) for 65–74 years; and 1.97 (95% CI, 0.43-4.97) for 75 years and older (Figure 4A). For OCC, ASIRs in q5 were: 2.64 (95% CI, 2.12–3.84) for 45–54 years; 5.49 (95% CI, 3.91-6.20) for 55–64 years; 7.36 (95% CI, 4.12-9.61) for 65–74 years; and 9.73 (95% CI, 3.17-17.82) for 75 years and older (Figure 4A).

Temporal trends in ASIRs for OPC and OCC in men in the most deprived quintile (q5) are shown in Figure 4B and C. The highest ASIRs for both OPC and OCC were seen in recent years (2006–2010). The ages of highest ASIR differed for OPC and OCC, being ages 55–64 years and 75 years and older, respectively.

Our findings contribute to the growing body of global literature showing the increasing incidence of OPC [11–14, 29, 30] and provide sociodemographic information on those at high risk of both OPC and OCC in BC. To our knowledge, this is the first study in Canada examining temporal trends in incidence for OPC and OCC by sex and neighbourhood socioeconomic deprivation status using a population-based cancer registry. Our analysis revealed important findings that among men the incidence of OPC has now surpassed the incidence rates of OCC, and this increase in the incidence rates is seen across all neighbourhood SES quintiles. Although OPC incidence rates increased over time in all quintiles, the highest incidence was observed among men living in the most deprived neighbourhoods (q5); more specifically, among men ages 55–64 years. Among women, the incidence rates of both OCC and OPC are significantly increasing, with highest rates observed in the most deprived quintile (q5). Interestingly, the temporal trends in incidence rates for OPC and OCC differed in men and women, with widening of inequalities between the least (q1) and most deprived (q5) quintiles in 2006–10 as compared to 1981–85. These findings add to current research relating to associations between socioeconomic deprivation and health outcomes even in a country such as Canada with a universal health care system.

These observed gender differences in the temporal trends in the incidence rates for OPC and OCC can partially be explained by differences in smoking rates. In BC, smoking rates are declining in both sexes. Among men, smoking rates have decreased from 51% to 17.9% from 1965 to 2007. Decline in rates among women began later and was less dramatic; the rates have decreased from 38% to 11.1%, respectively [31]. More dramatic and earlier decreases in smoking rates of men may partially explain the differences in OCC incidence rates over time – the sharp decline in rates of OCC among men that has occurred concurrent to rates of OCC among women that are still increasing. For q5, this change means that incidence frequencies for women are approaching those seen in men in this quintile. The observed increase in incidence of OPC among both men and women is most likely related to the increased prevalence of human papilloma virus (HPV), which is associated with these tumours. Nicholas et al. [32] recently reported from Ontario that during 1993–99 to 2006–2011 the prevalence of HPV in oropharyngeal cancers increased from 25% to 62%; this is likely also the case in BC. Therefore, future research about the risk behaviours of OPC and OCC should target populations in the least deprived neighbourhoods, paying specific attention to patterns in the men and women.

Our findings are consistent with other Canadian studies from Ottawa [15] and from data of Canadian Cancer Registry [21] which showed that the highest head and neck cancer incidence was observed among populations with the lowest incomes. However, these studies did not provide sex-specific rates and their assessment of SES status was restricted to only material deprivation indices such as income. Many case–control and epidemiological studies suggest that prevalence of oral HPV infection is greater among men than women, which supports the observation that HPV-related OPC is predominantly seen in men [33–35]. In our study OPC rates have increased dramatically among men; women show similar but less dramatic trends. Our study shows the importance of reporting sex-specific rates when examining impact of factors such as SES status.

In contrast to the results of a recent study from Canada [21], which reported no significant change in rates of OCC over time, we found significant differences by gender, with a declining incidence of OCC in men but increasing in women. Hwang et al. [21] reported that lowest income quintiles had higher rates of OPC (66%) and OCC (48%) but that there was no significant narrowing of the gap between the highest and lowest quintiles. However, our study suggests a widening gap in incidence in BC in recent years as compared to 1981–5 for both OCC and OPC in both genders. Therefore, performing sex-based analysis and using VANDIX as a measure to determine SES status provided helpful insight and should be considered in future studies.

Living in wealthier neighbourhoods has been associated with better self-rated health resulting from better lifestyles and healthier choices [36]. People living in more deprived neighbourhoods have stresses associated with poverty and unemployment which can itself lead to cancer development [37] and studies have shown an increasing gradient of cancer with increasing socioeconomic deprivation [16, 38]. Further, people may be more inclined to smoke tobacco as a coping mechanism to deal with the stresses of poverty [39], which further increases their cancer risk. They may also have less access to social services. Increased burden of OPC and OCC among men in the most deprived neighbourhoods in our study may be explained in part by higher rates of smoking, less exercise, and poorer diets (e.g., eating less fruit) [38]. In BC, men have higher rates of smoking prevalence than women and these rates may be even higher in poorer neighbourhoods, which supports the observed higher rates of oral cancers [40]. Higher prevalence of risky behaviours and oral cancer burden was previously reported from Vancouver’s Downtown Eastside, one of the most socioeconomically deprived neighbourhoods in Canada [41]. Hence, new developing technologies such as optical screening devices for detection of OCC need to include the poor and underprivileged communities to obtain maximum benefit. Our findings also emphasize the need to continuously develop community outreach programmes and target the most deprived and vulnerable populations for oral cancer screening and prevention.

Although there is a need to develop targeted prevention approaches for the deprived neighbourhoods it’s important to also address the broader social determinants of health and address the underlying causes of inequitable distribution of wealth and resources which influences the lifestyle and risk behaviours increasing their risk for developing oral cancers [42]. Poor clients need to be empowered and encouraged to participate in health promotion and prevention services for reducing smoking and alcohol consumption, encouraged to adopt a healthy lifestyle and efforts should be made to improve their access to health care facilities [2, 43]. We need an integrated approach and political action for framing the social and health polices to tackle the root causes of disadvantage.

Our study provides evidence that the burden of oral cancers is highest in the most SES deprived populations in BC. Interestingly, this increase in the incidence rates of oral cancers is not linear or proportionate between different quintiles, but there is a sharp and dramatic increase in the incidence rates according to the deprivation status of the neighbourhood. Given a global increase in incidence of OPC and its association with HPV, this analysis of a population-based cancer registry and neighbourhood socioeconomic deprivation provides novel findings of increased disease burden of OPC in the most deprived neighbourhoods. This is an important evidence for informing targeted neighbourhood-based interventions (such as oral cancer screening, awareness, prevention and HPV vaccination) and facilitating a more focussed strategy on oral cancer prevention in BC. It also contributes to the growing body of global literature about epidemiological trends of oral cavity and oropharyngeal cancers, which is important for making policies and strategies for global oral cancer control and prevention.

As a next step, we will use geographic information systems (GIS) to identify clusters of cases in these high-risk neighbourhoods and relate these clusters to catchment areas for cancer clinics. This research is important because BC has a comprehensive oral cancer prevention programme, and the results of our research will help in the development of neighbourhood-based targeted approaches for health promotion, harm reduction, oral cancer screening, and prevention programmes for the most vulnerable and highest-risk population groups.