Impact of socioeconomic status on incidence, mortality, and survival of colorectal cancer patients: a systematic review.

REVIEW ARTICLE

Impact of socioeconomic status on incidence, mortality, and survival of colorectal cancer patients: a systematic review Christine N. Manser, MD, Peter Bauerfeind, MD Zurich, Switzerland

Colorectal cancer (CRC) is one of the most commonly diagnosed cancers in the world.1 CRC-associated mortality rates are high, with approximately 610,000 deaths recorded in 2008.1 Besides genetic predisposition, several risk factors are suggested to play a role in the development and progression of CRC, such as obesity,2-6 smoking, and diet.6 At the same time, factors that protect people from CRC are also well established. Several studies during the past years have demonstrated that endoscopic screening is the most important factor, not only in reducing the incidence of CRC, but also in decreasing CRC-related mortality.7-14 The term socioeconomic status (SES) designates the position of an individual within a given social structure. Social inequalities result from a skewed distribution of material and nonmaterial goods among the members of the society. Most commonly, SES is measured by the meritocratic triad of profession, income, and education. However, there are several other SES indices available, comprising mainly aggregated data, such as the Townsend, Jarman, and Carstairs indices,15 and many studies use newly set up indices. The lack of a uniform set of indices for measuring SES impedes comparability of studies investigating the impact of SES on morbidity and mortality in specific population groups. The impact of socioeconomic inequalities has been studied in the context of several malignant diseases.16-20 Data on the impact of SES on CRC, however, are sparse. CRC screening programs are available in many countries, but indiscriminate inclusion of a population into such a program is expensive and, in the context of exploding health care costs, might not be economically feasible in the long term. To make a CRC screening program cost-effective and efficient, potential risk factors as well as high-risk populations should be evaluated. This review analyzes the impact of SES on CRC incidence, mortality, and survival, enabling identification of high-risk groups. Abbreviations: CI, confidence interval; CRC, colorectal cancer; HR, hazard ratio; OR, odds ratio; RR, relative risk; SES, socioeconomic status. DISCLOSURE: All authors disclosed no financial relationships relevant to this article. Copyright ª 2014 by the American Society for Gastrointestinal Endoscopy 0016-5107/$36.00 http://dx.doi.org/10.1016/j.gie.2014.03.011

42 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

METHODS For a systematic analysis, the electronic database of PubMed was searched by using the following combination of search terms (date of search: June 4, 2013): (social[All Fields] or socioeconomic[All Fields]) AND (status[All Fields] or class[All Fields] or position[All Fields]) AND (“colorectal neoplasms”[MeSH Terms] or (“colorectal”[All Fields] AND “neoplasms”[All Fields]) or “colorectal neoplasms”[All Fields] or (“colorectal”[All Fields] AND “cancer”[All Fields]) or “colorectal cancer”[All Fields]) or (“colonic neoplasms”[MeSH Terms] or (“colonic”[All Fields] AND “neoplasms”[All Fields]) or “colonic neoplasms”[All Fields] or (“colon”[All Fields] AND “cancer”[All Fields]) or “colon cancer”[All Fields]) or (“rectal neoplasms”[MeSH Terms] or (“rectal”[All Fields] AND “neoplasms”[All Fields]) or “rectal neoplasms”[All Fields] or (“rectal”[All Fields] AND “cancer”[All Fields]) or “rectal cancer”[All Fields]) or CRC[All Fields]) AND (“English” [Language] or “German”[Language]). Publications without an abstract were excluded. Moreover, only those articles published since January 1995 were included. Article abstracts were read and were considered for further analysis if they focused on the impact of SES on incidence, mortality, or survival of colon, rectal, or CRC. SES had to be defined by socioeconomic index or data on profession, income, or education. As shown in Figure 1, 97 articles were found to be suitable for further analysis, and the full texts of the publications were read. Of these, 51 had to be excluded for the following reasons: focus only on late-stage CRC (exclusion was made because in most studies, it was not easy to differentiate between the impact of SES on CRC and the impact of SES on access to therapy. This was further complicated by a lack of multivariate regression in most studies, which failed to clearly differentiate between the impact of SES on CRC and its impact on therapy), focus on reasons for social inequalities and not their impact on CRC incidence, mortality or survival and focus only on special ethnic or therapeutic subgroups (such as focus only on Asians or Hispanics in the United States or focus only on patients with special surgical or chemotherapeutic treatment). To ensure completeness of data, included articles were compared with reference lists of review articles www.giejournal.org

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Impact of socioeconomic status on incidence, mortality, and survival of CRC patients

Figure 1. Flow chart of the search process. CRC, colorectal cancer.

on this issue published within the past 5 years,21,22 which yielded 19 more articles of potential interest, of which 16 were included in the review. Thus, a total of 62 articles were included in this systematic review. Data extracted were authors, journal, year of publication, country where the study was conducted, time interval of analysis as well as follow-up time, type of SES measure (distinguishing individual and neighborhood data) and source of data on SES, cancer (sub)site and source of data on CRC, number of patients included, primary endpoints (incidence, mortality, survival) as well as results.

RESULTS Association between CRC incidence and SES Results are differentiated by study endpoints (incidence, mortality, and survival). Tables 1 through 8 show the results of 21 studies reporting on the impact of SES on the incidence of colon, rectal, or CRC. Ten studies are from Europe, 6 from the United States, 2 from Asia, 2 from Australia, and 1 from South America. Eighteen studies provide data on the incidence of colon cancer, 15 on the incidence of rectal cancer, and 3 on the incidence of CRC without site-specific information. Eleven studies present individual data, 8 provide aggregated data, and 2 provide both types of data. Indices of SES were used in 8 studies. In 4 studies, each incidence rate ratio or odds ratio (OR) was reported. In 4 studies, the standardized incidence or rate ratio was reported; in 1 study, the relative index of inequality, and in 1 study, the Pearson correlations were reported. Most frequently, in 6 of the studies, the relative risk (RR) was reported. There was a large variance in the results of the studies analyzed in this review. Although some studies reported that the risk of the development of CRC among people www.giejournal.org

with a low SES was reduced, others reported exactly the opposite, namely, an increased CRC risk in this population. The lowest risk for the development of colon cancer was reported in a study by Pisa et al,23 who investigated the impact of migration and SES on CRC; this study included a total of 1953 patients with CRC, of whom 1225 patients had colon cancer: the OR for the development of colon cancer was 0.33 (95% confidence interval [CI], 0.18-0.63) for women and 0.26 (95% CI, 0.15-0.43) for men. In their study examining the association between education and the risk of the development of cancer, Mouw et al24 reported that women had the highest risk of colon cancer (multivariate adjusted: RR 1.37; 95% CI, 1.06-1.77). For men, the results were nonsignificant (RR 1.10; 95% CI, 0.94-1.29). In this study, data for 2791 patients with colon cancer were analyzed. Notably, studies from the United States reported an association between increased risk of colon cancer and low SES, whereas according to most European studies, the risk was reduced or nonsignificantly altered. Five of the 10 European studies reported a significantly reduced incidence of colon cancer among people with a low SES.20,23,25-28 There are only 3 European studies reporting significant results on rectal cancer. According to 1 study, men with a low SES had an increased risk of rectal cancer (RR 1.27; 95% CI, 1.07-1.50 to RR 1.57; 95% CI, 1.15-2.14),27 whereas the results of another study showed this risk to be lower (HR 0.41; 95% CI, 0.31-0.53).28 Interestingly, both studies are from Italy and included comparable numbers of individuals investigated over almost the same length of time. In both studies, SES was assessed by using education as the index measure. In the third study, the risk of the development of rectal cancer in men was found to be either increased or decreased, depending on the SES variable used. Low SES as measured by income was associated with an increased risk of the development of rectal Volume 80, No. 1 : 2014 GASTROINTESTINAL ENDOSCOPY 43


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TABLE 1. Association between the incidence of colon, rectal, or colorectal cancer and socioeconomic status in North America Country and inclusion period

No. of patients included

I vs A data

Steinbrecher et al,29 2012

U.S., 1998-2002

52,608

A

Kim et al,63 2010

U.S., 1986-2000

1223

I and A

Mouw et al,24 2008

U.S., 1995-1996

2791

I

Education

Mackillop et al,64 2000

U.S., 1988-1992 Canada, 1989-1993

Not stated

A

Income

Krieger et al,65 1999

U.S., 1988-1992

4559

A

Block group socioeconomic measures

Steinbrecher et al,29 2012

U.S., 1998-2002

52,608

A

SES index (based on education, median household income, percentage living 200% below poverty level, percentage of blue-collar workers, percentage older than 15 years in work force, without job, median rent, and median house value

Kim et al,63 2010

U.S., 1986-2000

305

I and A

Mouw et al,24 2008

U.S., 1995-1996

1135

I

Education


U.S., 1988-1992 Canada, 1989-1993

Not stated

A

Income

Ref.

SES indicator

Colon SES index (based on education, median household income, percentage living 200% below poverty level, percentage of blue-collar workers, percentage older than 15 y in work force, without job, median rent, and median house value Education SES summary score (based on income, education, and occupation)

Rectum

Education SES Summary Score (based on income, education, and occupation)

Colorectal (without differentiation of colon and rectum) Doubeni et al,49 2012

U.S., 1995-2006

7676

I and A

Education SES index (based on percentage of persons in the census tract who had less than a high school education or were unemployed, non-Hispanic blacks, or in managerial jobs (separately for men and women), and percentage of households below 1999 federal poverty levels, on public assistance, or with annual income of !$30,000, no car, or headed by a female with dependent children

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; IRR, incidence rate ratio; RR, relative risk.

cancer, whereas decreased risk was associated with a low SES measured by social class.25 Most North American studies reported almost exclusively an increased risk of the development of both colon and rectal cancer in individuals of low SES. Only the study by Steinbrecher et al29 showed a decreased risk of right-sided colon cancer in patients with a low SES (incidence rate ratio 0.91; 95% CI, 0.88-0.96).

Association between CRC mortality and SES Data on the association between CRC mortality and SES are shown in Supplementary Tables 1 through 3 (available 44 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

online at www.giejournal.org). Of 29 studies that were included in the analysis, 12 are from Europe, 9 from the United States, 4 from Australia, 3 from Asia, and 1 from South America. Data on colon cancer mortality are reported in 9 studies, data on rectal cancer mortality in 6, and CRC mortality in 20 studies. Individual data are presented in 13 studies and aggregated data in 14 studies; in 2 of the studies, there were individual as well as aggregated data. In 12 studies, indices of SES were used and in others only indicators of SES. The mortality risk was expressed by standardized mortality rate ratio or the www.giejournal.org

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TABLE 1.


Continued Risk (low vs high SES)

Measured value

Female

Male

Colon IRR

Colon: IRR 1.03 (95% CI, 1-1.06) Right colon: IRR 0.91 (95% CI, 0.88-0.96) Left colon: IRR 1.08 (95% CI, 1.02-1.14)

RR

RR 1.10 (95% CI, 0.91-1.35) In women with less than college education: RR 0.94 (95% CI, 0.75-1.20) In women with more than college education: RR 1.92 (95% CI, 1.25-3.03)

RR

RR 1.37 (95% CI, 1.06-1.77)

RR 1.10 (95% CI, 0.94-1.29)

RR

U.S.: RR 1.10 (95% CI, 1.03-1.16) Canada: RR 1.15 (95% CI, 1.05-1.28)


RR

IRR 1.3 (95% CI, 1.1-1.6)

IRR 1.3 (95% CI, 1.1-1.6)

Rectum IRR

IRR 1.14 (95% CI, 1.08-1.20)

RR

RR 1.56 (95% CI, 1.08-2.27)

RR

RR 1.05 (95% CI, 0.68-1.62)

RR 1.50 (95% CI, 1.17-1.92)

RR



Colorectal (without differentiation of colon and rectum) IRR

IRR 1.42 (95% CI, 1.29-1.56) IRR 1.31 (95% CI, 1.19-1.45)

mortality rate in each of 4 studies, by the relative index of inequality or the RR in each of 3 studies, by the OR in 2 studies, or by the hazard coefficient or the case fatality rate in 1 study each. Mortality risk was most frequently given in terms of the hazard ratio (HR), which was used in 11 studies. In all the included studies (1996–2010), an increased CRC mortality rate in the group with a low SES was reported regardless of the geographic region in which the study was conducted. According to Menvielle et al,30 women with a low SES had the highest risk of dying of www.giejournal.org

rectal cancer (RR 2.9; 95% CI, 1.3-6.4 to RR 3.1; 95% CI, 1.4-6.8), whereas Yim et al31 reported the risk of colon cancer mortality for women and men as being the same (HR 2.37; 95% CI, 1.17-4.80). In particular, studies that included a large number of patients reported an increased risk of CRC mortality in association with low SES.32,33 Niu et al33 (N Z 62,038) reported a risk of an HR of 1.37 (95% CI, 1.23-1.53) in women and an HR of 1.20 (95% CI, 1.081.34) in men, whereas Le et al32 (N Z 127,805) reported an HR of 1.26 (95% CI, 1.20-1.32) for colon cancer and an HR of 1.33 (95% CI, 1.24-1.42) for rectal cancer. Volume 80, No. 1 : 2014 GASTROINTESTINAL ENDOSCOPY 45


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TABLE 2. Association between incidence of colon, rectal, or colorectal cancer and socioeconomic status in Europe

Ref.

Country and inclusion period


I vs A data

Europe, 1991-2000

2447

I

Italy, 1985-1999

3839

I

Denmark, 1994-2003

9958

I

Weiderpass et al,20 2006*

Finland, 1971-1995

6331

A

Braaten et al,67 2005

Norway, 1991-2001

205

I

Sweden, 1961-1998

19,657

I

Italy, 1992-1996

1225

I

Italy, 1985- 1996

2180

I

The Netherlands, 1980-1989

351

I

Europe, 1991-2000

2447

I

Italy, 1985-1999

1966

I

Denmark, 1994-2003

7411

I

Weiderpass et al,20 2006*

Finland, 1971-1995

5274

A

Braaten et al,67 2005

Norway, 1991-2001

112

I

Sweden, 1961-1998

11,778

I

Italy, 1992-1996

728

I

Italy, 1985- 1996

1353

I

21,905

A

Colon Leufkens et al,66 2012 27

Spadea et al,

2009

Egeberg et al,25 2008

26

Hemminki and Li, 23

Pisa et al,

2003

2000

Tavani et al,28 1999 Van Loon et al,68 1995* Rectum Leufkens et al,66 2012 27

Spadea et al,

2009


Hemminki et al, 23

Pisa et al,

26

2003

2000

Tavani et al,28 1999

Colorectal (without differentiation of colon and rectum) Pollock and Vickers,69 1997*

Great Britain, 1987-1992

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; HR, hazard ratio; RR, relative risk; IRR, incidence rate ratio; SIR, standardized incidence rate; OR, odds ratio. *Relative risk was calculated from data in the publication.


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TABLE 2.


Continued

SES indicator

Risk (low vs high SES)

Measured value

Female

Male

Colon Education

HR

HR 0.90 (95% CI, 0.76-1.07)

Education

RR

1985-1999: RR 0.93 (95% CI, 0.80-1.07) 1985-1989 RR 0.79 (95% CI, 0.61-1.03) 1990-1994: RR 1.00 (95% CI, 0.77-1.30) 1995-1999: RR 1.04 (95% CI, 0.82-1.30)

1985-1999: RR 0.93 (95% CI, 0.83-1.04) 1985-1989 RR 0.73 (95% CI, 0.60-0.90) 1990-1994: RR 1.12 (95% CI, 0.90-1.38) 1995-1999: RR 1.00 (95% CI, 0.82-1.21)

Education Disposable income Social class

IRR

IRR 1.02 (95% CI, 0.93-1.12) IRR 0.94 (95% CI, 0.88-1.01) IRR 0.87 (95% CI, 0.67-1.14)


Social classes (based on education, work, industrial status, industry Grouping)

SIR

SIR 0.92 vs 1.13 (RR 0.8)

SIR 0.78 vs 1.37 (RR 0.6)

Education

Education

RR 1.23 (95% CI, 0.70-2.20)

Education

SIR

SIR 0.90 (95% CI, 0.81-0.99)

Education Occupation

OR

OR 0.33 (95% CI, 0.18-0.63) OR 0.77 (95% CI, 0.43-1.43)

OR 0.26 (95% CI, 0.15-0.43) OR 0.42 (95% CI, 0.26-0.67)

Education Social class

OR

OR 0.78 (95% CI, 0.53-1.14) OR 0.75 (95% CI, 0.58-0.97)

OR 0.41 (95% CI, 0.31-0.53) OR 0.43 (95% CI, 0.34-0.55)

Education Profession

RR

RR 1.14 (95% CI, 0.50-2.56) RR 1.59 (95% CI, 0.78-3.34)

RR 1.00 (95% CI, 0.54-1.85) RR 0.92 (95% CI, 0.55-1.54)

Rectum Education

HR

HR 0.92 (95% CI, 0.74-1.15)

Education

RR

1985-1999: RR 1.16 (95% CI, 0.94-1.43) 1985-1999: RR 1.27 (95% CI, 1.07-1.50) 1985-1989: RR 1.09 (95% CI, 0.73-1.63) 1985-1989: RR 0.94 (95% CI, 0.71-1.25) 1990-1994 1990-1994 RR 1.57 (95% CI, 1.15-2.14) RR 1.27 (95% CI, 0.88-1.84) 1995-1999 1995-1999 RR 1.44 (95% CI, 1.09-1.91) RR 1.08 (95% CI, 0.76-1.55)

Education Disposable income Social class

IRR



Social classes (based on education, work, industrial status, industry grouping)

SIR

SIR 0.92 vs 1.10 (RR 0.8)

SIR 0.92 vs 0.98 (RR 0.9)

Education

RR

RR 0.63 (95% CI, 0.33-1.20)

Education

SIR

SIR 0.92 (95% CI, 0.80-1.06)


OR

OR 0.31 (95% CI, 0.14-0.67) OR 0.83 (95% CI, 0.38-2.00)

OR 0.77 (95% CI, 0.42-1.43) OR 1.11 (95% CI, 0.67-2.00)

Education Social class

OR

OR 0.99 (95% CI, 0.60-1.64) OR 0.85 (95% CI, 0.61-1.19)

OR 0.41 (95% CI, 0.31-0.53) OR 0.85 (95% CI, 0.63-1.16)

Colorectal (without differentiation of colon and rectum) Townsend Deprivation Index

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SIR

98 (95% CI, 87-111) vs 100 (95% CI, 90-111) (RR 0.98)

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European data were very homogeneous and almost invariably reported increased mortality risk in low SES individuals, although the risk is not the same in men and women (Supplementary Table 3). Although in Turin in northern Italy and in Switzerland, France, Belgium, and Sweden, the relative index of inequality was statistically significantly increased for women; in Barcelona, Slovenia, Belgium, Denmark, Norway, and Sweden, this was the case for men.

Association between CRC survival and SES Studies on CRC survival can be divided into 2 types with regard to their primary endpoints, ie, 5-year survival or rates of mortality. Based on this difference, this review has 2 major sections addressing these endpoints separately. Supplementary Tables 4 and 5 (available online at www. giejournal.org) show the results of 11 studies on survival; Supplementary Tables 6 through 8 (available online at www.giejournal.org) show the results on mortality rates. Among the studies on survival, 7 are from Europe, and the rest are from the United States and Canada. Data on survival of colon cancer are provided by 6 studies, on survival of rectal cancer by 7 studies, and CRC survival by 2 studies. In 3 studies, individual data were used, and in 11 studies, aggregated data were used. SES was measured in 4 studies by using an index. Whereas most of the studies used 5-year survival rates as the endpoint (Supplementary Tables 4 and 5), 1-year survival rates were reported in some studies. All studies included in this review found the chance of survival for more than 5 years to be low in patients from a low SES background (RR 0.5-0.94). Only Gorey et al34 found increased survival in Canadian females with lower SES. This was true for both 1- and 5-year survival rates. Of the 11 studies on survival focusing on risk of death from specific forms of CRC, 5 are from the United States or Canada, 4 from Europe, and 1 each from Australia and Asia (Supplementary Tables 6-8). Eight studies report on the association with rectal cancer, 6 on the association with colon cancer, and 2 on CRC. Three studies are based on individual data and 9 on aggregated data. All the studies report an increased risk of dying of colon, rectal, or CRC among patients with low SES, with the highest risk reported by Nitzkorski et al35 with an HR of 2.01 (95% CI, 1.66-2.43). This was also observed in the study by Møller et al36 that included 181,359 patients with an increased risk of death up to 1.12/SES quintile.

DISCUSSION In this review, selected publications were analyzed that addressed the issue of an association between SES and CRC incidence, mortality, and survival. As far as the impact of SES on CRC incidence is concerned, analysis revealed clear geographic differences. Although in the United States, lower SES is associated with an increased incidence of CRC, an inverse association is observed among Europeans. This 48 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

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discrepancy is puzzling, and several hypotheses are available that attempt to explain these starkly contrasting observations. One major difference is in the health behavior of the populations of the 2 continents. An increase in the body mass index is associated with an increased risk of the development of CRC. This effect is reported to be more marked in men.2 Obesity is an increasing global problem, which is especially pronounced among the American population. According to the report of the Centers of Disease Control and Prevention, 34.4% of the American population is obese (data for 2007-2008). In the 20- to 74-year-old age group, this represents a 12% increase compared with 1988 to 1994.37 In the low-SES group, obesity rates are even higher. Increased psychosocial stressors, on the one hand, and less effective coping strategies, on the other, have been suggested as possible explanations for this high obesity rate in the lowSES group. Elevated blood cortisol levels resulting from increased psychosocial stressors induce an increase in appetite and a concomitant increase in visceral fat.38,39 These can lead not only to increased use of addictive substances, but also to increased intake of food.38,40,41 In their study of an association between poverty and obesity among U.S. adolescents, Miech et al42 observed an increased prevalence of obese teenagers 15 to 17 years of age in families living below the poverty line. In contrast to increased obesity in the lowSES population, a healthier lifestyle was observed among individuals with higher SES43-48 who consumed more fruit and vegetables44,48 and lower amounts of fatty foods44,46 and snacks.44 In addition, they were less frequently on a diet,47 indicating fewer obesity problems. Doubeni et al49 reported an increased risk of CRC among persons with low SES. In another study investigating the impact of health behavior and obesity on socioeconomic differences regarding CRC incidence,50 the authors showed that, after adjustments for several risk factors, the proportion of people adopting a healthy Mediterranean diet and engaging in physical activity was lower among people with low SES compared with those in the high SES population (highest Mediterranean diet score of 4.1% vs 2.0% [highest vs lowest SES quintile] and highest physical activity [20.7% vs 16.5%]). When adjusted for healthy behavior (smoking history, Mediterranean diet, physical activity) and body mass index, the impact of SES on CRC incidence declined but at 43.9% (range 35.1%-57.9%), it still remained statistically significant, and for right-sided colon cancer, it was 95.0% (range 50.1%-100%). Thus, the authors conclude that “a substantial proportion of the socioeconomic disparity in risk of new-onset CRC, and particularly of right colon cancers, may be attributable to the higher prevalence of adverse health behaviors on low-SES populations.”50 However, there are other risky health behaviors beside consumption of less healthy foods that can have an impact on the development of CRC. A higher proportion of smokers has been reported among unemployed people,51 single mothers on financial support,52,53 and residents of poor neighborhoods.54 According to a 2009 publication of the CDC, the www.giejournal.org

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TABLE 3. Association between incidence of colon, rectal, or colorectal cancer and socioeconomic status in South America, Asia, and Australia



I vs A data

Kim et al,70 2012

South Korea, 2009

7555

I

Monthly premium of insurance as proxy indicator of income class

Kim et al,71 2008

South Korea, 2001

Not stated

I

Burnley,72 1997

Australia, 1985-1993

757

Smith et al,73 1996


Kim et al,70 2012

Ref.

Risk (low v. high SES) SES indicator

Measured value

Female

Male

OR

OR 1.12 (95% CI, 0.97-1.30)

OR 0.92 (95% CI, 0.81-1.05)

Income

RII/100.000

RII 0.69 (95% CI, 0.59-0.80)

RII 0.98 (95% CI, 0.61-1.57)

A

Income Jarman index

Pearson correlation

6993

A

SES index (based on income, education, and occupation)

OR

OR 0.85 (95% CI, 0.76-0-94)

OR 1.37 (95% CI, 1.18-1.59)

South Korea, 2009

7555

I

Monthly premium of insurance as proxy indicator of income class

OR

OR 1.29 (95% CI, 1.08-1.53)

OR 1.37 (95% CI, 1.18-1.59)

Kim et al,71 2008

South Korea, 2001

Not stated

I

Income

RII/100.000

RII 1.29 (95% CI, 0.84-1.98)

RII 0.97 (95% CI, 0.66-1.43)

Smith et al,73 1996


3676

A

SES index (based on income, education, and occupation)

OR

OR 0.86 (95% CI, 0.75-10.3)

OR 1.17 (95% CI, 1.03-1.33)

SIR

1995-1999: SRR 0.83 (95% CI, 0.71-0.98) 2000-2004: SRR 0.81 (95% CI, 0.70-0.94)

1995-1999: SRR 0.74 (95% CI, 0.64-0.85) 2000-2004: SRR 0.76 (95% CI, 0.66-0.87)

Colon

0.27 0.21

Rectum

Colorectal (without differentiation of colon and rectum) TorresCintron et al,74 2012

Puerto Rico, 1995-2004

Not stated

A

SES index (based on unemployment rate; medium annual household income; percentage of the population living below the poverty level; percentage of the population 25 y of age or older with !12 y of education; percentage of occupied housing units without a car; percentage of the employed civilian population 16 y of age or older in a management, professional, and related occupation (used to define white-collar occupation); percentage of occupied housing units without telephone; and percentage of the population fluent in both English and Spanish

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; OR, odds ratio; RII, relative index of inequality; SIR, standardized incidence rate.

highest prevalence of smokers was observed among Americans older than 25 years of age and with a lower level of education. Among persons with a GED (General Educational Development) certificate, 41.3% were smokers compared with 27.5% among individuals with less than a high school education and 5.5% among those with a graduate degree.55 Therefore, increased nicotine consumption might be www.giejournal.org

another contributing factor to the increased incidence of colon cancer in the United States. Screening colonoscopy is 1 major protective factor with regard to CRC incidence and mortality. Participation rates as high as 80% have been reported by U.S.-American screening campaigns.56,57 The CDC also analyzed screening participation in relation to SES measured by Volume 80, No. 1 : 2014 GASTROINTESTINAL ENDOSCOPY 49


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TABLE 4. Association between mortality of colon, rectal, or colorectal cancer and socioeconomic status in North America

Ref.



I vs A data

Le et al,32 2008

U.S., 1994-2003

127,805

A

Du et al,75 2007

U.S., 1992-1999

18,492

A

U.S., 1994-2003

127,805

A

Colon

Rectum Le et al,32 2008

Colorectal (without differentiation of colon and rectum) Steinbrecher et al,29 2012

U.S., 1999-2001

14,515

A

Lian et al,76 2011

U.S., 1995-2006

7024 CRC, 2468 deaths

I and A

Niu et al,33 2010

U.S., 1986-1999

62,038

A

U.S., 1997

4422

A

Albano et al,78 2007

U.S., 2001

Not stated

I

79

U.S., 1990-2000

Not stated

A

U.S., 1959-1972 and 1982-1996

Not stated

I

77

Byers et al,

Chu et al,

2008

2007

Steenland et al,80 2002

Values in bold indicate statistical significance. I, Individual; A, Aggregated; SES, socioeconomic status; HR, hazard ratio; CRC, colorectal cancer; MRR, mortality rate ratio; RR, relative risk.

education and household income.56 Participation rates among people with a graduate degree were approximately 72.1% (range 71.5%-72.6%), whereas it was 48.6% (range 47.1%-50-0%) in those without a high school degree. Nonparticipation in screening programs might therefore be 1 factor with a major impact on the increased risk of 50 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

the development of CRC in low-SES populations. Despite the importance of screening participation in rates of survival and mortality in CRC, none of the cited publications adjusted for screening participation, which must be considered a major factor that might possibly skew study conclusions. www.giejournal.org

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TABLE 4.


Continued Risk (low vs high SES) SES indicator

Measured value

Female

Male

SES index (based on education level, median household income, proportion below 200% poverty level, median house value, median rent, percentage employed, percentage with blue-collar employment)

HR

HR 1.26 (95% CI, 1.20-1.32)

Education

HR

Overall mortality: HR 1.20 (95% CI, 1.14-1.27) CRC-specific mortality: HR 1.29 (95% CI, 1.17-1.42) Overall mortality: HR 1.17 (95% CI, 1.10-1.23) CRC-specific mortality: HR 1.14 (95% CI, 1.03-1.27) Overall mortality: HR 1.20 (95% CI, 1.13-1.27) CRC-specific mortality: HR 1.24 (95% CI, 1.12-1.38) Overall mortality: HR 1.21 (95% CI, 1.14-1.27) CRC-specific mortality: HR 1.26 (95% CI, 1.14-1.39)

HR

HR 1.33 (95% CI, 1.24-1.42)

Colon

Poverty Income Combined SES Rectum SES index (based on education level, median household income, proportion below 200% poverty level, median house value, median rent, percentage employed, percentage with blue-collar employment)

Colorectal (without differentiation of colon and rectum) SES index (based on education, median household income, percentage living 200% below poverty level, percentage of bluecollar workers, percentage older than 15 y of age in work force, without job, median rent, and median house value

MRR

MRR 1.12 (95% CI, 1.06-1.19)

Education Deprivation index (based on education, employment, occupation, housing conditions, income and poverty, racial composition, residential stability)

HR

Overall mortality: HR 0.83 (95% CI, 0.71-0.91) CRC-specific mortality: HR 0.83 (95% CI, 0.67-0.91)

Poverty

HR

Education and household income in the region

HR

Education

RR

RR 1.7 (95% CI, 1.63-1.82)

RR 1.81 (95% CI, 1.73-1.89)

Mortality/100,000

1990-1994: 18.8 vs 20.1 (RR 0.9) 1995-2000: 17.5 vs 17.9 (RR 1.0)

1990-1994: 27.8 vs 29.7 (RR 0.9) 1995-2000: 25.8 vs 25.6 (RR 1.0)

MRR

1959-1972: MRR 1.27 (95% CI, 1.12-1.44) 1982-1996: MRR 1.21 (95% CI, 1.01-1.40)

1959-1972: MRR 0.96 (95% CI, 0.86-1.08) 1982-1996: MRR 1.10 (95% CI, 0.97-1.25)

Poverty level Education

In Europe, the incidence of CRC is reduced in low-SES individuals. The study by Leufkens et al66 reports that this is particularly true of people from Southern Europe despite the fact the rural population in Southern Europe www.giejournal.org

HR 1.20 (95% CI, 1.08-1.34)

HR 1.37 (95% CI, 1.23-1.53)

HR 1.09 (95% CI, 0.97-1.23)

has a lower SES and a low level of education. A possible explanation for this apparent discrepancy is that these people are known for their healthy dietary habits with adherence to a Mediterranean diet, which, as was described Volume 80, No. 1 : 2014 GASTROINTESTINAL ENDOSCOPY 51


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TABLE 5. Association between mortality of colon, rectal, or colorectal cancer and socioeconomic status in Europe

Ref.



I vs A data

Puigpinòs et al,81 2009

Spain, 1992-2003

7085

I

Menvielle and Luce,30 2005

France, 1975-1990

350

I

Fernandez and Burrell,82 1999

Spain, 1992-1995

1658

I

Puigpinòs et al,81 2009

Spain, 1992-2003

7085

I

Menvielle et al,30 2005

France, 1975-1990

149

I

Fernandez et al,82 1999

Spain, 1992-1995

476

I

Norway, 1971-2002

19,687

I

Denmark, 2001-2004

8763

I


2481

A

12 European populations (region of Madrid, Basque region, region of Barcelona, Slovenia, region of Turin, Switzerland, France, Denmark, Norway, Sweden, Finland)

Not stated

I

Rosengren and Wilhelmsen,87 2004

Sweden, 1970-1990

145

I

Lyratzopoulos et al,88 2004

England, 1991-1997

608

A

Wrigley et al,89 2003

England, 1991-1995

5176

A

Pollock et al,69 1997


21,905

A

Italy, 1985-1992

1290

I

Colon

Rectum

Colorectal (without differentiation of colon and rectum) Elstad et al,83 2011

Frederiksen et al,84 2009

Nur et al,85 2008 86

Menvielle et al,

90

Rosso et al,

2008

1997

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; RII, relative index of inequality; RR, relative risk; OR, odds ratio; HR, hazard ratio; EHR, excess hazard ratio; CRC, colorectal cancer; SMR, standardized mortality index; CFR, case fatality rate. Relative risk was calculated from data in the publication.


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TABLE 5.


Continued

SES indicator


Measured value

Female

Male

Colon Education

RII

1992-1994: RII 1.44 (95% 1995-1997: RII 1.57 (95% 1998-2000: RII 2.85 (95% 2001-2003: RII 1.66 (95%

CI, 0.87-2.40) CI, 0.96-2.57) CI, 1.76-4.60) CI, 1.05-2.63)


RII

RII 1.0 (95% CI, 0.3-1.4) RII 0.6 (95% CI, 0.3-1.4)

RII 0.9 (95% CI, 0.6-1.6) RII 1.6 (95% CI, 1.0-2.7)

Education

RR

RR 0.76 (95% CI, 0.56-1.03)

RR 1.05 (95% CI, 0.85-1.30)

Rectum Education

RII

1992-1994: RII 1.44 (95% 1995-1997: RII 1.57 (95% 1998-2000: RII 2.85 (95% 2001-2003: RII 1.66 (95%

CI, 0.87-2.40) CI, 0.96-2.57) CI, 1.76-4.60) CI, 1.05-2.63)


RII

RII 1.0 (95% CI, 0.4-2.6)

RII 2.9 (95% CI, 1.3-6.4) RII 3.1 (95% CI, 1.4-6.8)

Education

RR

RR 1.27 (95% CI, 0.64-2.52)

RR 1.29 (95% CI, 0.85-1.96)

Colorectal (without differentiation of colon and rectum) Education

OR

Income (per 100,000 Danish kroner reduction) Education Rental vs owner occupied

HR

HR 1.08 (95% CI, 1.04-1.11) HR 1.28 (95% CI, 1.16-1.41) HR 1.18 (95% CI, 1.10-1.25)

Deprivation index (not specified)

EHR

EHR 1.20 (95% CI, 0.92-1.57)

Education

Occupation

RII

1971-1979: OR 1.13 (95% CI, 0.92-1.39) 1980-1989: OR 1.03 (95% CI, 0.88-1.20) 1990-2002: OR 1.17 (95% CI, 1.05-1.31)

Madrid: RII 1.19 (95% CI, 0.67-2.10) Basque region: RII 0.77 (95% CI, 0.44-1.33) Barcelona: RII 1.36 (95% CI, 1.00-1.84) Slovenia: RII 1.28 (95% CI, 1.03-1.59) Turin: RII 0.97 (95% CI, 0.67-1.41) Switzerland: RII 1.02 (95% CI, 0.90-1.16) France: RII 1.24 (95% CI, 0.70-2.17) Belgium: RII 1.24 (95% CI, 1.05-1.45) Denmark: RII 1.18 (95% CI, 1.01-1.39) Norway: RII 1.25 (95% CI, 1.11-1.41) Sweden: RII 1.31 (95% CI, 1.18-1.45) Finland: RII 1.03 (95% CI, 0.88-1.21)

1971-1979: OR 0.92 (95% CI, 0.80-1.05) 1980-1989: OR 1.00 (95% CI, 0.89-1.12) 1990-2002: OR 1.07 (95% CI, 0.99-1.16)

Madrid: RII 1.08 (95% CI, 0.75-1.56) Basque region: RII 0.92 (95% CI, 0.69-1.24) Barcelona: RII 1.15 (95% CI, 0.95-1.40) Slovenia: RII 0.97 (95% CI, 0.83-1.14) Turin: RII 1.46 (95% CI, 1.09-1.95) Switzerland: RII 1.27 (95% CI, 1.14-1.40) France: RII 1.58 (95% CI, 1.06-2.36) Belgium: RII 1.18 (95% CI, 1.04-1.34) Denmark: RII 1.03 (95% CI, 0.90-1.18) Norway: RII 1.08 (95% CI, 0.97-1.1.9) Sweden: RII 1.11 (95% CI, 1.01-1.21) Finland: RII 0.94 (95% CI, 0.81-1.09)

Mortality/ 100,000

51 vs 29 (RR 1.8)

Townsend index

RR

Overall mortality: RR 1.04 (95% CI, 0.75-1.46) CRC-specific mortality: RR 1.15 (95% CI, 0.77-1.71)

Townsend index

HR

Overall mortality: HR 1.15 (95% CI, 1.04-1.27) CRC-specific mortality: HR 1.11 (95% CI, 0.99-1.25)

Townsend Deprivation Index

SMR

SMR: 104 (95% CI, 91-120) vs 97 (95% CI, 85-111) (RR 1.07)

Education

CFR

CFR 1.49 (95% CI, 1.05-1.92)

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TABLE 6. Association between mortality of colon, rectal, or colorectal cancer and socioeconomic status in South America, Asia, and Australia Country and inclusion period


I vs A data

Yim et al,31 2012

South Korea, 2000

270

I

Health insurance premium (income dependent)

Kim et al,71 2008

South Korea, 2001

Not stated

I

Income

Burnley et al,72 1997


757

A

Socioeconomic group

Ref.

Risk (low vs high SES) SES indicator

Measured value

Female

Male

Colon

Income

Modified Jarman index

Smith et al,73 1996


3380

A

SES index (based on the economic resources of households, education, and occupation)

Kim et al,71 2008

South Korea, 2001

Not stated

I

Income

Smith et al,73 1996


1768

A

SES index (based on the economic resources of households, education and occupation)

HR

HR 2.37 (95% CI, 1.17-4.80)

MRR

MRR 1.30

Death/100,000

1986-1989: 20.6 vs 32.1 (RR 0.6) 1990-1993: 29.1 vs 41.8 (RR 0.7) 1985-1991: 0.91 vs 1.04 0.17

SMR

Correlation with mortality rate

MRR 1.54

OR

OR 0.87 (95% CI, 0.75-1.01)

OR 0.95 (95% CI, 0.82-1.09)

MRR

MRR 1.66

MRR 1.61

OR

OR 1.06 (95% CI, 0.84-1.33)

OR 1.28 (95% CI, 1.06-1.54)

SRR

1995-1999: SRR 0.86 (95% CI, 0.67-1.10) 2000-2004: SRR 1.01 (95% CI, 0.81-1.26)

1995-1999: SRR 0.68 (95% CI, 0.53-0.86) 2000-2004: SRR 0.72 (95% CI, 0.58-0.89)

Rectum

Colorectal (without differentiation of colon and rectum) TorresCintron et al,74 2012

Puerto Rico, 1995-2004

Not stated

A

SES index (based on unemployment rate, medium annual household income, percentage of the population living below the poverty level, percentage of the population 25 y of age or older with !12 y of education, percentage of occupied housing units without a car, percentage of the employed civilian population 16 y of age or older in management, professional, and related occupation (used to define whitecollar occupation), percentage of occupied housing units without a telephone, and percentage of the population fluent in both English and Spanish


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TABLE 6. Continued Country and inclusion period


I vs A data

Kelsall et al,91 2009

Australia 1990-1994

520

I and A

Haynes et al,92 2008

New Zealand, 1994-2004

24,187

A

New Zealand Deprivation index (based on car access, tenure, benefit receipt, unemployment, low income, telephone access, single-parent families, qualifications, and living space)

Nishi et al,93 2008

Japan 1980/19812001

348

I

Education

Ref.

Risk (low vs high SES) Measured value

SES indicator Education Deprivation index (based on low income, low educational attainment, high unemployment, relatively unskilled jobs, and other variables that reflect disadvantage)

Female

Male

HR

Overall mortality: HR 1.35 (95% CI, 0.88-2.08) CRC-specific mortality: HR 1.27 (95% CI, 0.81-2.00) Overall mortality: HR 1.40 (95% CI, 1.00-1.89) CRC-specific mortality: HR 1.25 (95% CI, 0.89-1.75)

Hazard coefficient

Hazard coefficient 0.88

HR

HR 0.71 (95% CI, 0.31-1.67)

HR 1.14 (95% CI, 0.72-1.79)

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; HR, hazard ratio; MRR, mortality rate ratio; RR, relative risk; SMR, standardized mortality index; OR, odds ratio; SRR, standard rate ratio; CRC, colorectal cancer.

TABLE 7. Association between survival (relative survival) of colon, rectal, or colorectal cancer and socioeconomic status in North America

Ref.

Country and No. of inclusion patients I vs A period included data


Measured value

5-y survival

Female

Male

Colon Gorey et al,94 2011

U.S., 1996-2000

1944

A

Income and poverty level


Canada, 1982-1991

Not stated

A

Area income 5-y survival

Gorey et al,34 1997

U.S. and Canada, 1986-1992

Not stated

I

Income

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1-y survival 5-y survival

Toronto: RR 0.93 (95% CI, 0.79-1.10) San Francisco: RR 0.84 (95% CI, 0.72-0.98) Colon: 42% vs 48% (RR 0.88) U.S.: 0.94 (95% CI, 0.89-0.99) Canada: 1.06 (95% CI, 1.01-1.12) U.S.: 0.82 (95% CI, 0.69-0.98) Canada: 1.33 (95% CI, 1.14-1.55)

U.S.: 0.90 (95% CI, 0.86-0.94) Canada: 0.97 (95% CI, 0.92-1.02) U.S.: 0.78 (95% CI, 0.65-0.94) Canada: 0.97 (95% CI, 0.84-1.11)



Manser & Bauerfeind

TABLE 7. Continued

Ref.

Country and No. of inclusion patients I vs A period included data


Measured value

5-y survival

Female

Male

Rectum Kim et al,96 2011

U.S., 1988-2006

9504

I

Household income


Canada, 1982-1991

Not stated

A

Area income 5-y survival

Gorey et al,34 1997

U.S. and Canada, 1986-1992

Not stated

I

Income

Median survival low SES: 3.8 y Median survival high SES: 8.4 y 5-y survival: 45% vs 61% (RR 0.74) Rectum: 36% vs 45% (RR 0.8)

U.S.: 0.88 (95% CI, U.S.: 0.89 (95% CI, 0.83-0.93) 0.80-0.99) Canada: 0.96 (95% CI, 5-y survival Canada: 1.02 (95% CI, 0.89-1.03) 0.89-1.17) U.S.: 0.80 (95% CI, 0.61-1.05) U.S.: 0.87 (95% CI, 0.69-1.09) Canada: 0.90 (95% CI, Canada: 1.05 (95% CI, 0.72-1.12) 0.81-1.37)

1-y survival

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; RR, relative risk.

TABLE 8. Association between survival (relative survival) of colon, rectal, or colorectal cancer and socioeconomic status in Europe

Ref.



I vs A data


Denmark, 1994-2003

9958

I

SES indicator

Measured value

Female

Male

46% vs 49% (RR 0.9) 45% vs 55% (RR 0.8) 42% vs 45% (RR 0.9)

42% vs 46% (RR 0.9) 40% vs 46% (RR 0.9) 49% vs 48% (RR 1.0)

L1.4 (95% CI, L2.5 to L0.2) L2.2 (95% CI, L3.6 to L0.8)

L2.2 (95% CI, L3.5 to L1.0) L1.9 (95% CI, L3.4 to L0.3)

Colon Egeberg et al,25 2008

Education

5-y survival

Disposable income Social class Mitry et al,97 2008

Dejardin et al,98 2006

England and Wales, 1986-1999

206,879

A

1986-1995: Carstairs deprivation index (based on car ownership, overcrowding, unemployment, social class IV or V of the head of household) 1996-1999: index of multiple deprivation (based on income, employment, health and disability, education, skills and training, houses and services, living environment, crime)

France, 1980-1997

28,010

A

Education Income


486

A

Deprivation index (based on income deprivation, employment deprivation, health deprivation and disability, education, skills and training deprivation, barriers to housing and services, living environment deprivation and crime)

Average change every 5 y in deprivation gap 1-y survival 5-y survival

Survival

RR 0.93 (95% CI, 0.88-0.93) RR 0.92 (95% CI, 0.88-0.97)

5-y survival

33% vs 64% (RR 0.5)

Rectum Harris et al,99 2009


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TABLE 8. Continued

Ref. Egeberg et al,25 2008



I vs A data


Denmark, 1994-2003

7411

I

SES indicator Education

Measured value 5-y survival

Disposable income Social class Mitry et al,100 2008



France, 1980-1997

156,000

18,080

A

A

1986-1995: Carstairs Deprivation index (based on car ownership, overcrowding, unemployment, social class IV or V of the head of household) 1996-1999: index of multiple deprivation (based on income, employment, health and disability, education, skills and training, houses and services, living environment, crime) Education Income

Average change every 5 y in deprivation gap 1-y survival 5-y survival

Female

Male

51% vs 57% (RR 0.9) 49% vs 58% (RR 0.8) 68% vs 72% (RR 0.9)

44 vs 50% (RR 0.9) 41% vs 51% (RR 0.8 46% vs 56% (RR 0.8)

L1.2 (95% CI, L2.8 to 0.3) L2.5 (95% CI, L4.5 to L0.5)

L1.4 (95% CI, L2.7 to L0.1) L2.4 (95% CI, L4.1 to L0.6)

Survival

RR 0.92 (95% CI, 0.87-0.97) RR 0.96 (95% CI, 0.90-1.01)

Colorectal (without differentiation of colon and rectum) Pollock et al,69 1997


17,516

A

Townsend deprivation index

5-y survival

32% (29%-36%) vs 40% (37%-44%) (RR 0.8)

Schrijvers et al,101 1995


3558

A

Education

5-y survival

49% (95% CI, 45%-53%) vs 55% (95% CI, 50%-60%) (RR 0.9)

Values in bold indicate statistical significance. I, Individual; A, aggregated; SES, socioeconomic status; RR, relative risk. Relative risk was calculated from data in the publication.

earlier, seems to be protective with respect to CRC. This aspect has been considered in detail by studies from Italy.23,27,28 Data from Northern European countries such as Denmark25 and Finland20 also show a reduced risk of CRC in rural populations, although the reduction is much less than that reported by Italian studies. The reasons for the differences between the United States and Europe are difficult to define. On the one hand, screening participation in Europe lags behind participation rates in the United States. This protective factor for members of higher social classes therefore is of little significance among Europeans. However, with increasing screening participation rates among Europeans, the gap between high and low SES in the CRC incidence might be narrowed over the next few years. Furthermore, differences in access to health-care systems have to be mentioned. Although in most European countries, regardless of whether a Bismarck or a Beveridge model health-care system is available, everyone has access to health care; in the United States, access to health care is, on the whole, more difficult. However, this, as well as participation rates in screening, might change in the www.giejournal.org

coming decades as the health-care reforms in the United States get more rigorously implemented. Results on rectal cancer were much less significant, with no clear geographic pattern, suggesting that the impact of the previously mentioned factors on rectal cancer is much less than on colon cancer. With respect to the association between SES and mortality and survival of CRC, respectively, the data are much more distinct and homogeneous with regard to geographic pattern. Most of the U.S. and European studies report an increased CRC-specific and overall mortality among people with a low SES. This is in agreement with reports of reduced survival in people with a low SES. Again, 1 possible explanation for the increased mortality and decreased survival rates might be the fact that a low-SES population less frequently participates in cancer screening programs, with the result that CRC is not diagnosed at an early stage but at an advanced stage when CRC-related symptoms have already developed in the patients. Furthermore, access to health services is worse for people with a low SES. A recent large study by Crawford et al58 analyzed data for 39,619 CRC patients registered in the Northern Volume 80, No. 1 : 2014 GASTROINTESTINAL ENDOSCOPY 57


and Yorkshire Cancer Registry and Information Service between 1994 and 2002. The authors showed that individuals belonging to the lowest SES quartile had a significantly increased risk of receiving a diagnosis of end-stage CRC compared with individuals with a higher SES (OR 1.516; 95% CI, 1.053-2.182). A comparable risk was reported by Morgan et al59 analyzing 66,806 cases of CRC (OR 1.22). This effect was also observed when aggregated data were used or when neighborhoods were compared.60-62 One last important factor, which also is an indicator of access to health care, is the therapy of the disease. Aarts et al21 also focused on the association of SES and therapy for CRC in their review. Surgical and adjuvant radio- or chemotherapy were less likely to be accessed by individuals with a low SES (OR 0.4-0.99), indicating a continuing trend in inequalities between low and high SES groups in treatment and the associated outcome of survival and therefore of mortality. This review gives an overview of published data on the impact of SES on the incidence, mortality, and survival of CRC. However, it must be kept in mind that none of the studies included in this review made adjustments for participation in screening for CRC. Because participation in screening might be one of the most relevant confounders in this area of research, the study results may not correctly reflect the relationship between the variables investigated. Therefore, an adjustment for screening needs to be made in future studies. In addition, it should be mentioned that at least some of the studies cited only investigated potential risk or protective factors in a univariate fashion. This does not take interactions between variables as well as major potential of confounding into account. Therefore, multivariate analysis should be done in future studies. The heterogeneity in the methods used makes comparison of results not only difficult but almost impossible. On the one hand, SES has been measured by using individual as well as aggregated data, and, on the other, single variables as well as indices of SES have been used. If a criterion standard to be used in studies focusing on the impact of SES on incidence, mortality, or survival of different diseases were available, this would improve comparability of study results. The problem regarding individual data is that they most often have to be collected in interviews with every individual with the disease on which the study is focusing. This would yield high-quality data; however, in large populations, this method would not be feasible. In addition, the use of the meritocratic triad of profession, income, and education is getting more and more difficult and inconsistent as higher education and profession are no longer consistently associated with high income. Focusing only on 1 variable, irrespective of whether it derives from individual or aggregated data, often does not reflect the complexity of the SES. However, indices that involve several indicators of the SES will more accurately do so. Therefore, the authors of this review are of the opinion that an index should be used in future 58 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

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studies for this issue to improve comparability. Furthermore, it is equally important to use the same index across studies because diversity of indices would also make comparison of study results difficult. In our opinion, a neighborhood index that takes the neighborhood in which one lives into account should be used to illustrate one’s SES.

ACKNOWLEDGMENT The authors thank Rajam Csordas-Iyer for a critical reading of the manuscript and helpful suggestions.

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Received November 26, 2013. Accepted March 5, 2014. Current affiliations: Division of Gastroenterology and Hepatology, Department of Internal Medicine, Zurich University Hospital, Zurich, Switzerland. Reprint requests: Christine Manser, MD, Division of Gastroenterology and Hepatology, Department of Internal Medicine, Rämistrasse 100, CH-8091 Zurich, Switzerland.

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SUPPLEMENTARY TABLE 1. Association between survival (risk of dying) of colon, rectal, or colorectal cancer and socioeconomic status in North America Country and inclusion period


I vs A data

Booth et al,102 2010

U.S., 2003-2007

7976

A

Median household income

ZhangSalomons et al,103 2006

U.S., 1988-1992 Canada, 1989-1993

13,449

A

Income


Canada, 1982-1991

Not stated

A

Area income

Nitzkorski et al,35 2013

U.S., 2000-2009

748

A


U.S., 2003-2007

3713


U.S., 1988-1992 Canada, 1989-1993

5635


Canada, 1982-1991

Not stated

Ref.


Measured value

Female

Male

Colon Overall survival

Overall survival of colon cancer: HR 1.36 (95% CI, 1.20-1.55)

RR

U.S.: RR 1.36 Canada: RR 1.07 U.S.: RR 1.46 Canada: RR 1.05

RR

RR 1.05 (95% CI, 0.95-1.16)

Household income Education

Overall survival

HR 1.95 (95% CI, 1.62-2.36) HR 2.01 (95% CI, 1.66-2.43)

A


Overall survival

Overall survival of colon cancer: HR 1.36 (95% CI, 1.20-1.55)

A

Income

RR

U.S.: RR 1.61 Canada: RR 1.20 U.S.: RR 1.57 Canada: RR 1.00

RR

RR 1.23 (95% CI, 1.05-1.44)

RR

RR 1.47 (95% CI, 1.05-2.04)

Percentage of residents living below the US poverty threshold

Rectum

Percentage of residents living below the U.S. poverty threshold A

Area income

Colorectal (without differentiation of colon and rectum) Polednak,104 2001

U.S., 1992

1219

A

Percentage of residents living below the U.S. poverty threshold

I, Individual; A, aggregated; SES, socioeconomic status; HR, hazard ratio; RR, relative risk. Values in bold indicate statistical significance.

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SUPPLEMENTARY TABLE 2. Association between survival (risk of dying) of colon, rectal, or colorectal cancer and socioeconomic status in Europe Country and inclusion period


I vs A data

Sweden, 1990-2004

6605

I

Education

HR

HR 1.23 (95% CI, 1.08-1.41)

Hussain et al,36 2008

Sweden, 1990-2004

3445

I

Education

HR

HR 1.15 (95% CI, 0.96-1.37)

Dickman et al,105 1998

Finland, 1977-1985

5619

I

Occupation

Excess mortality

38% (95% CI, 28%-47%)

Change in death rates after 1 mo, 1 y, 2 y, 5 y

Increase in the rate/SES quintile for colon cancer 0-1 mo: 1.11 1 mo-1 y: 1.07 1-2 y: 1.01 2-5 y: 1.02 Increase in the rate/SES quintile for rectal cancer 0-1 mo: 1.12 1 mo-1 y: 1.11 1-2 y: 1.09 2-5 y: 1.06

HR

HR 1.14 (95% CI, 0.97-1.34)

Ref.


Measured value

Female

Male

Colon Hussain et al,36 2008 Rectum

Colorectal (without differentiation of colon and rectum) Møller et al,36 2012

England, 1996-2004

181,359

A

Deprivation index (based on income and lower super output areas)



3558

A

Education

I, Individual; A, aggregated; SES, socioeconomic status; HR, hazard ratio. Values in bold indicate statistical significance.

60.e2 GASTROINTESTINAL ENDOSCOPY Volume 80, No. 1 : 2014

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SUPPLEMENTARY TABLE 3. Association between survival (risk of dying) of colon, rectal or colorectal cancer and socioeconomic status in Australia and Asia

Ref.



I vs A data



18,053

A

Education and occupation

Relative excess risk of death

RR 1.14


10,412

A



RR 1.11

SES indicator

Measured value

Female

Male

Colon Yu et al,106 2008 Rectum Yu et al,106 2008

Colorectal (without differentiation of colon and rectum) Chang et al,107 2012

Taiwan, 2002-2007

5135

I and A

Income-related insurance payment amount

5-y survival

Per-capita personal income

High NH SES, age !65 y: HR 1.40 (95% CI, 1.11-1.77) High NH SES, age R65 y: HR 0.96 (95% CI, 0.68-1.37) Low NH SES, age !65 y: HR 1.45 (95% CI, 1.14-1.83) Low NH SES, age R65 y: HR 1.07 (95% CI, 0.75-1.53)

I, Individual; A, aggregated; SES, socioeconomic status; RR, relative risk; NH, neighborhood; HR, hazard ratio. Values in bold indicate statistical significance.

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SUPPLEMENTARY TABLE 4. Association between survival (relative survival) of colon, rectal, or colorectal cancer and socioeconomic status in North America


Number of patients included

Individual (1) vs. aggregated (2) data

Gorey et al,94 2011

USA, 1996-2000

1944


Canada, 1982-1991

Gorey et al,34 1997

USA and Canada, 1986-1992

Author, year of publication

risk (low vs. high SES)

SES indicator

Measured value

2

Income and poverty level

5 year survival

Toronto RR 0.93 (95% CI, 0.79-1.10) San Francisco RR 0.84 (95% CI, 0.72-0.98)a

Not stated

2

Area Income

5 year survival

Colon 42% vs. 48% (RR[0.88)

Not stated

1

Income

1 year survival

USA 0.94 (95% CI, 0.89.0.99) Canada 1.06 (95% CI, 1.01-1.12) USA 0.82 (95% CI, 0.69-0.98) Canada 1.33 (95% CI, 1.14-1.55)

female

male

Colon

5 year survival

USA 0.90 (95% CI, 0.86-0.94) Canada 0.97 (95% CI, 0.92-1.02) USA 0.78 (95% CI, 0.65-0.94) Canada 0.97 (95% CI, 0.84-1.11)

Rectum Kim et al,96 2011

USA, 1988-2006

9504

1

Household income

5 year survival

Median survival low SES: 3.8 years Median survival high SES: 8.4 years 5-years survival: 45% vs. 61% (RR[0.74)


Canada, 1982-1991

Not stated

2

Area Income

5 year survival

Rectum 36% vs. 45% (RR[0.8)

Gorey et al,34 1997

USA and Canada, 1986-1992

Not stated

1

Income

1 year survival


5 year survival


a

Bold marked values with statistical significance.


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SUPPLEMENTARY TABLE 5. Association between survival (relative survival) of colon, rectal, or colorectal cancer and socioeconomic status in Europe





Denmark, 1994-2003

9958

1


206879

2

France, 1980-1997

28010

2

Great Britain 2000-2007

486

2

Denmark, 1994-2003

7411

1


156000

2

France, 1980-1997

18080

2

Colon Egeberg et al,25 2008

Mitry et al,97 2008

Dejardin et al,97 2006 Rectum Harris et al,99 2009


Mitry et al,100 2008


Colorectal (without differentiation of colon and rectum) Pollock et al,69 1997


17516

2


Netherlands, 1980-1989

3558

2

a

Bold marked values with statistical significance. Relative risk (RR) shown in parentheses were calculated from data in the publication.

b

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SUPPLEMENTARY TABLE 5.

Manser & Bauerfeind

Continued

Measured value

SES indicator

risk (low vs. high SES) female

male

46% vs. 49% (RRZ0.9) 45% vs. 55% (RR[0.8) 42% vs. 45% (RRZ0.9)

42% vs. 46 % (RRZ0.9) 40% vs. 46% (RRZ0.9) 49% vs. 48% (RRZ1.0)

-1.4 (95% CI, -2.5 – -0.2) -2.2 (95% CI, -3.6 – -0.8)

-2.2 (95% CI, -3.5 – -1.0) -1.9 (95% CI, -3.4 – -0.3)

Colon Education Disposable income Social Class

5 year survival

1986-1995 Carstairs deprivation index (based on car ownership, overcrowding, unemployment, social class IV or V of the head of household)) 1996-1999 Index of multiple deprivation (based on income, employment, health and disability, education, skills and training, houses and services, living environment, crime)

Average change every 5 years in deprivation gap 1 year survival 5 year survival

Education Income

Survival

RR 0.93 (95% CI, 0.88-0.93) RR 0.92 (95% CI, 0.88-0.97)

Rectum Deprivation index (based on income deprivation, employment deprivation, health deprivation and disability, education, skills and training deprivation, barriers to housing and services, living environment deprivation and crime)

5 year survival

Education

5 year survival

33 % vs. 64% (RR[0.5)b

51% vs. 57% (RRZ0.9)

Disposable income

49% vs. 58% (RRZ0.8)

Social Class

68% vs. 72% (RRZ0.9)

1986-1995 Carstairs Deprivation index (based on car ownership, overcrowding, unemployment, social class IV or V of the head of household)) 1996-1999 Index of multiple deprivation (based on income, employment, health and disability, education, skills and training, houses and services, living environment, crime)

Average change every 5 years in deprivation gap 1 year survival 5 year survival

Education Income

Survival

-1.2 (95% CI, -2.8 – 0.3) -2.5 (95% CI, -4.5 – -0.5)

44% vs. 50% (RRZ0.9) 41% vs. 51% (RR[0.8)a 46% vs. 56% (RRZ0.8)

-1.4 (95% CI, -2.7 – -0.1) -2.4 (95% CI, -4.1 – -0.6)

RR 0.92 (95% CI, 0.87-0.97) RR 0.96 (95% CI, 0.90-1.01)

Colorectal (without differentiation of colon and rectum) Townsend Deprivation Index

5 year survival

32% (29-36) vs. 40% (37-44) (RRZ0.8)

Education

5 year survival

49% (95% CI, 45-53) vs. 55% (95% CI, 50-60) (RRZ0.9)


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SUPPLEMENTARY TABLE 6. Association between survival (risk of dying) of colon, rectal, or colorectal cancer and socioeconomic status in North America






SES indicator

Measured value

female

male

Colon Booth et al,102 2010

USA, 2003-2007

7976

2


Overall Survival


USA, 1988-1992 and Canada, 1989-1993

13449

2

Income

Relative risk

USA RR 1.36 Canada RR 1.07 USA RR 1.46 Canada RR 1.05


Canada, 1982-1991

Not stated

2

Area Income

Relative risk

RR 1.05 (95% CI, 0.95-1.16)

Nitzkorski et al,35 2013

USA, 2000-2009

748

2

Household income Education

OverallSurvival

HR 1.95 (95% CI, 1.62-2.36) HR 2.01 (95% CI, 1.66-2.43)


USA, 2003-2007

3713

2


Overall Survival

Overall Survival colon cancer HR 1.36 (95% CI, 1.20-1.55)

USA, 1988-1992 and Canada, 1989-1993

5635

2

Income

Relative risk

USA RR 1.61 Canada RR 1.20 USA RR 1.57 Canada RR 1.00

Canada, 1982-1991

Not stated

Area Income

Relative risk

RR 1.23 (95% CI, 1.05-1.44)

percentage of residents living below the US poverty threshold

Risk ratio

RR 1.47 (95% CI, 1.05-2.04)a

percentage of residents living below the US poverty threshold

Overall Survival colon cancer HR 1.36 (95% CI, 1.20-1.55)a

Rectum

ZhangSalomons et al.,103 2006


percentage of residents living below the US poverty threshold 2

Colorectal (without differentiation of colon and rectum) Polednak et al,104 2001

USA, 1992

1219

2

a


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SUPPLEMENTARY TABLE 7. Association between survival (risk of dying) of colon, rectal or colorectal cancer and socioeconomic status in Europe



Sweden, 1990-2004

6605

1

Education

Hazard Ratio

HR 1.23 (95% CI, 1.08-1.41)a

Hussain et al,36 2008

Sweden, 1990-2004

3445

1

Education

Hazard Ratio

HR 1.15 (95% CI, 0.96-1.37)

Dickman et al,105 1998

Finland, 1977-1985

5619

1

Occupation

Excess mortality

38% (95% CI, 28-47%)

Increase of the rate/SES-Quintile for colon cancer -In months 0-1: 1.11 -1 month-1 year: 1.07 -1-2 years: 1.01 -2-5 years: 1.02 Increase of the rate/SES-Quintile for rectal cancer -In months 0-1: 1.12 -1 month-1 year: 1.11 -1-2 years: 1.09 -2-5 years: 1.06




SES indicator

Measured value

female

male

Colon Hussain et al,36 2008 Rectum

Colorectal (without differentiation of colon and rectum) Møller et al,36 2012

England, 1996-2004

181359

2

Deprivation index (based on Income and Lower Super Output Areas (LSOAs)

Change in death rates after 1 months, 1 year, 2 years, 5 years


Netherlands, 1980-1989

3558

2

Education

Hazard Ratio

HR 1.14 (95% CI, 0.97-1.34)

a



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Manser & Bauerfeind


SUPPLEMENTARY TABLE 8. Association between survival (risk of dying) of colon, rectal, or colorectal cancer and socioeconomic status in Australia and Asia







18053

2



RR 1.14a


10412

2



RR 1.11

income-related insurance payment amount

5 year survival

High NHb SES, Age !65J HR 1.40 (95% CI, 1.11-1.77) High NH SES, Age R65J HR 0.96 (95% CI, 0.68-1.37) Low NH SES, Age !65J HR 1.45 (95% CI, 1.14-1.83) Low NH SES, Age R65J HR 1.07 (95% CI, 0.75-1.53)

SES indicator

Measured value

female

male

Colon Yu et al,106 2008 Rectum Yu et al,106 2008

Colorectal (without differentiation of colon and rectum) Chang et al,107 2012

Taiwan, 2002-2007

5135

1 and 2

Per capita personal income

a

Bold marked values with statistical significance. NH Z Neighborhood.

b

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Socioeconomic status and cancer mortality and incidence in Melbourne.

Socioeconomic inequalities in breast cancer incidence and mortality in Europe-a systematic review and meta-analysis.

Socioeconomic status and cancer survival.

Low socioeconomic status is associated with worse survival in children with cancer: a systematic review.

The impact of socioeconomic status on foodborne illness in high-income countries: a systematic review.

Association between socioeconomic status, surgical treatment and mortality in patients with colorectal cancer.

The Impact of Adjustment for Socioeconomic Status on Comparisons of Cancer Incidence between Two European Countries.

Disparities in cancer incidence and mortality by area-level socioeconomic status: a multilevel analysis.

Racial disparities and socioeconomic status in the incidence of colorectal cancer in Arizona.

Survival benefits of metformin for colorectal cancer patients with diabetes: a systematic review and meta-analysis.

Socioeconomic position and incidence of gastric cancer: a systematic review and meta-analysis.

Systematic review of the impact of registration and screening on colorectal cancer incidence and mortality in familial adenomatous polyposis and Lynch syndrome.

[Sleep in adolescents of different socioeconomic status: a systematic review].

Impact of age and mismatch repair status on survival in colorectal cancer.

The impact of socioeconomic status and multimorbidity on mortality: a population-based cohort study.

Excess adiposity and survival in patients with colorectal cancer: a systematic review.

Smoking and survival of colorectal cancer patients: systematic review and meta-analysis.

Impact of Resection Margin Distance on Survival of Pancreatic Cancer: A Systematic Review and Meta-Analysis.

Colorectal cancer mortality among Hispanics in California: differences by neighborhood socioeconomic status and nativity.

Impact of physical activity on cancer-specific and overall survival of patients with colorectal cancer.

The impact of osteopontin on prognosis and clinicopathology of colorectal cancer patients: a systematic meta-analysis.

Impact of age and comorbidity on survival in colorectal cancer.

The impact of primary tumor location on efficacy of cetuximab in metastatic colorectal cancer patients with different Kras status: a systematic review and meta-analysis.

Incidence and mortality of colorectal cancer in individuals with a family history of colorectal cancer.