Annals of Oncology Advance Access originally published online on September 2, 2005
Annals of Oncology 2006 17(1):5-19; doi:10.1093/annonc/mdj007
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
© 2005 European Society for Medical Oncology
review |
Origins of socio-economic inequalities in cancer survival: a review
Non-Communicable Disease Epidemiology Unit, London School of Hygiene and Tropical Medicine, London, UK
* Correspondence to: L. M. Woods, Non-Communicable Disease Epidemiology Unit, London School of Hygiene and Tropical Medicine, Keppel Street, London WC1E 7HT, UK. Tel: +44-20-7927-2245; Fax: +44-20-7436-4230; E-mail: laura.woods{at}lshtm.ac.uk
 |
Abstract |
|---|
 Top Abstract introductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
Background: Cancer survival is known to vary by socio-economic group. A review of studies published by 1995 showed this association to be universal and resilient to the many different ways in which socio-economic status was determined. Differences were most commonly attributed to differences in stage of disease at diagnosis.
Materials and methods: A review of research published since 1995 examining the association of cancer survival with socio-economic variables.
Results: An association between socio-economic status and cancer survival has continued to be demonstrated in the last decade of research. Stage at diagnosis and differences in treatment have been cited as the most important explanatory factors. Some research has evaluated the psychosocial elements of this association.
Conclusions: Socio-economic differences in cancer survival are now well documented. The explanatory power of stage at diagnosis, although great, should not detract from the evidence of differential treatment between social groups. Neither factor can completely explain the observed socio-economic differences in survival, however, and the importance of differences in tumour and patient factors should now be quantified.
Key words: cancer, deprivation, poverty, social class, socio-economic status, survival analysis
|
introduction |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
Strong evidence for socio-economic differences in cancer survival and mortality was revealed by a comprehensive review in the late 1990s, for many cancers and in many populations [1
]. These variations were resilient to the variety of ways in which socio-economic status had been determined. Differences were greatest for malignancies of the breast, large bowel, bladder and body of the uterus, which have relatively good prognoses, and for which stage at diagnosis is a key prognostic factor.
Possible reasons for survival differences between social groups were also reviewed [2]. Stage at diagnosis was the factor most often cited, but its influence varied by anatomic site and between populations, and it was not the sole explanatory factor for socio-economic differences in survival in much of the research. The reasons for differences in stage at diagnosis between social groups were also unclear: neither delay in diagnosis nor differences in tumour aggressiveness appeared to explain the variation. Differences in treatment were also identified as contributory factors, but the patterns observed were difficult to interpret because of the absence of data on (or adjustment for) stage of disease in most studies. The authors concluded [2] that further study into the causes of socio-economic differences in survival was required, particularly in relation to treatment differentials and psychosocial factors.
In this review, we summarise research published in the last decade on the association between socio-economic status and cancer survival, and discuss current evidence for the possible explanations of these differences.
|
methods |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
Reproducible database searches of PubMed, EMBASE, Web of Knowledge and, for grey literature, NML Gateway, HMIC and SIGLE, were conducted [3
–7]. The search terms used were designed to identify references that indexed or mentioned (i) cancer, (ii) survival analysis and (iii) socio-economic status, or their synonyms. Suitable papers were identified on the basis of the title and abstract. All studies that had cited the previous review [1] were also included. Details of these were obtained using the Web of Knowledge ‘cited reference’ facility [5]. Further applicable references cited by each selected paper were then identified by hand-searching the bibliographies. Papers that had been included in the previous review [1] or that were published before 1995 were excluded. |
results |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
A large number of studies have examined socio-economic variation in cancer survival during the last decade [8
–46] (Table 1). A large body of literature also exists on the joint effect of socio-economic status and ethnicity. Some authors describe independent effects of ethnicity and poverty, whilst others have argued that ethnic differences in survival are simply socio-economic differences under a different guise. For this review, research examining both ethnic and socio-economic differences in survival has only been included where the findings contribute to understanding the causes of socio-economic patterns.
|
Studies of the association between socio-economic variables and cancer survival since 1995 have examined a number of different malignancies in a range of different settings including bladder [9
, 28], breast [21, 22, 25, 32, 40–42, 46], cervix [38], large bowel [11, 44, 45], digestive tract [16, 17, 29], head and neck [30], prostate [21, 23], childhood malignancies [35], selected groups of frequent cancers [14, 18–20, 24, 26, 27, 31, 36, 39, 43], and all malignancies [8, 10, 12, 13, 33, 34, 37]. Almost all have used an ecologic measure of social deprivation to categorise patients by social status. In a minority of studies, socio-economic status has been defined instead by health insurance status [27], health care delivery system [32] or by one of several direct measures of individual wealth [11, 17, 23, 24, 33, 34, 39]. Most studies have used population-based cancer registry data to investigate these associations, but differences have also been shown to exist in other types of data including randomised controlled trials [44], cohort studies [23, 33], case–control studies [17], hospital-based data series [11, 39] and audit data [41, 42, 45]. A few studies [15, 17, 21, 22, 33, 42, 44] examined crude survival (survival from cancer and all causes of death combined) rather than disease-specific (either net or relative) survival, which can be interpreted as survival from cancer in the absence of other causes of death.
evidence for socio-economic differences
Nearly all the studies document a relationship between cancer survival and measures of social class, socio-economic status or deprivation. The impact of deprivation on cancer survival is generally moderate. Most estimates of the relative risk of death within 5 years of diagnosis in the most deprived group, compared with the most affluent group, are in the range 1.3- to 1.5-fold.
null associations
A few studies have reported no association between socio-economic status and cancer survival [8, 9, 11, 12, 15, 18–20, 22, 25, 28, 29, 35, 40]. These studies suggest that social class differences are not evident for childhood malignancies [12, 35]. Socio-economic differences are also smaller in some ecological studies. In such studies, individuals are assigned to a deprivation category derived from characteristics of the geographic area in which they live. If these geographic units are large, with heterogeneous populations, socio-economic differences in survival are less readily identifiable [8, 40, 47]. In some studies, the sample size was small [11, 15, 28]. A handful of findings are less easily explained. For example, in one group of studies, a persistent association between survival and tertiles of relative income has been demonstrated for patients residing in the USA, with the poor surviving less time than the rich, but not for Canadian patients [18–20, 22]. These findings are in contrast to a weak deprivation gap between poor and rich cancer patients demonstrated in similar Canadian data by a different group of authors [10]. Two studies from the UK dealing with survival from cancers of the bladder [9] and digestive tract [29] showed no association with deprivation, despite the fact that sufficient numbers of cases were analysed and previous work on similar data showed small but significant differences [12].
|
discussion |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
These papers leave little doubt that socio-economic status remains an important prognostic factor for most common cancers in adults, but not in children, and in many populations.
The explanations for socio-economic differences in survival are not so well documented. The possible underlying causes can be separated into three groups: factors relating to the tumour, the patient and the health care system [2]. We discuss each of these in turn.
tumour characteristics
stage at diagnosis.
Many of the attempts at explaining social differences in cancer survival in the past have focused upon differences in the stage of disease at diagnosis [2]. Stage, however it is defined, certainly varies substantially between populations for which survival differences have been observed, and it has been shown to be a key explanation for international differences in survival [48], at least for breast cancer [49] and colorectal cancer [50]. Similarly, in other studies, racial differences in survival have been largely explained by stage at diagnosis [51–56].
Amongst the most recent studies focused on socio-economic differences in survival, Brewster et al. [57] report no differences between socio-economic groups in stage at diagnosis for breast, colorectal, ovarian and lung cancers, although a re-analysis of their breast cancer data by Kaffashian et al. [25] shows a significant trend of increasing tumour size with increasing deprivation. In the USA, health insurance status has been taken as a surrogate for socio-economic status. Lee-Feldstein et al. [58] showed that uninsured or publicly insured patients with breast cancer were less likely to have early-stage disease at diagnosis, and had lower survival than privately insured patients. A population-based study in Kentucky, USA, showed a similar effect of health insurance on survival from cancers of the breast, lung, bowel and prostate; the effect was reduced by adjustment for stage at diagnosis [27]. Similar results have been obtained for several other malignancies, with both ecologic and individual measures of socio-economic status [11, 16, 59–63]. Two small studies found no relationship between socio-economic status and stage [41, 45].
Variations in the stage of disease at diagnosis offer an attractive explanation for socio-economic patterns in survival, because stage is the most strongly predictive of all clinical prognostic factors [64]. For breast cancer, it is inversely related to patient delay in seeking health care [65], which is also associated with lower survival [66]. This implies that patient or health care provider delay is longer amongst individuals of lower socio-economic status. There is some suggestive evidence for the patient element of this hypothesis, such as a greater number of emergency and in-patient admissions amongst deprived individuals for lung, colorectal and breast cancer [67], and longer reported duration of symptoms prior to diagnosis for cervical cancer [68]. In contrast, a recent systematic review did not find convincing evidence for increased patient delay among more deprived women diagnosed with breast cancer [69], nor was there any evidence of differential delay from either the patient or the provider in a small sample of bladder cancer patients [9]. One hospital-based study offers some evidence that both patient and provider delays in access to care for colorectal cancer are associated with fewer years of education. Neither stage nor education were significant predictors of crude survival in a multi-variable model, but the sample was small [11]. Overall, the idea that socio-economic differences in the stage of disease at diagnosis are the result of differential delays in diagnosis, whether by the patient or by the provider, is not supported by strong research evidence.
Other work has implied a more complex relationship between stage, socio-economic status and survival. In one population-based study, stage at diagnosis explained 28% of the differences in breast cancer survival between social class categories defined by individual occupation, but none of the difference between deprivation categories defined ecologically [25]. The authors suggest this indicates that some non-occupational aspects of poverty lead to lower survival, independently of the stage of disease at diagnosis. In population-based data for 10 common cancers in south-east England, stage explained little of the differences in survival between deprivation categories based upon area-based scores [36]. More detailed analysis of the breast cancer data showed that differences in stage at diagnosis explained part of the socio-economic gradient in survival for older women (65–99 years) but not for younger women (30–64 years) [70]. In the south-eastern Netherlands, the absence of metastasis at diagnosis explained most of the differences in survival by social class for cancers of the breast and stomach, but stage at diagnosis did not explain the observed survival differentials for cancers of the lung, large bowel or prostate [71]. Indications of the independent prognostic value of deprivation over and above differences in stage of disease are also evident from other studies [16, 17, 24].
To the extent that socio-economic differentials in cancer survival are not explained by differences in the stage of disease recorded at diagnosis, it is conceivable that they result from residual confounding by stage. Under this scenario, socio-economic differences in the quality or intensity of diagnostic investigation would lead to deprived patients having their tumours misclassified as localised—when in fact they were more advanced—more frequently than affluent patients [70]. This results in stage migration bias, also known as the ‘Will Rogers’ phenomenon [72]. This bias would lead to poorer stage-specific and stage-adjusted survival in deprived patients. The impact on survival differentials is likely to be small, at least for colorectal and breast cancers, since socio-economic differences in stage-specific and stage-adjusted survival are still evident in studies where stage has been independently re-classified by researchers blinded to the patient's deprivation status [11, 28, 41, 45]. However, it remains possible that stage migration may explain part of the socio-economic variation in population-based estimates of cancer survival that cannot be quantitatively attributed to stage.
In summary, although stage of disease at diagnosis explains much of the socio-economic differentials in survival in some studies, it cannot explain all the differences, and the postulated relationship between health-seeking behaviour and stage is not supported by strong evidence of differential delay in diagnosis between socio-economic groups. Most of the recent research summarised here highlights the role of other factors in socio-economic survival gradients, suggesting that an emphasis on stage of disease alone is likely to be too simplistic if we are fully to understand these inequalities.
biological characteristics.
Biological characteristics of the tumour itself have also been considered as explanatory factors for socio-economic differentials in survival. The morphologic type of breast cancer in women is a prognostic factor [73] that has been shown to vary by socio-economic group [74], but it has not been found to have a large impact upon socio-economic survival differences [25, 70]. Anatomic site, morphology and grade are unlikely to explain socio-economic survival differences for colon cancer [75]. Although tumour grade has been shown to influence breast cancer survival [64], only a non-significant association between socio-economic status and grade has been observed in the UK [76]. For breast cancer, estrogen receptor (ER) status has been shown to explain at least some of the socio-economic and racial differences in survival [41, 42, 77], although an association between deprivation and ER status has not always been observed [74, 78–80]. The underlying reasons for variability in ER status by socio-economic group have not been fully investigated. Variations in systemic inflammatory response, thought to be related both to smoking and to alcohol consumption, were considered as a potential explanation for socio-economic differences in survival in patients with colon cancer undergoing curative resection, but found to be non-significant [81]. There is limited evidence from a small population-based study in Scotland that later stage at diagnosis of cervical cancer is associated more strongly with faster tumour cell proliferation than with delay in diagnosis, and that cell proliferation may be faster in deprived patients. The authors speculate that lifestyle factors could influence tumour biology; this question needs further research [68].
|
patient characteristics |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
host factors and the effect of treatment.
Use of relative survival as an outcome measure in population-based studies of cancer patient survival compensates for overall background mortality in the cancer patient group [82
]. Co-morbidity (the presence of other chronic conditions) may reduce survival from cancer over and above the impact that such conditions have on overall mortality, however, by interacting with the treatment given for cancer [83]. In studies that make no correction for background mortality, co-morbidity has been found to predict survival [54, 84]. In a population-based study in The Netherlands, co-morbid conditions were more common in deprived patients with cancers of the breast and lung, but not in patients with stomach or prostate cancer [85]. In the only study we could find that examined the presence of other diseases in relation to cancer-specific survival, co-morbidity increased the risk of death from bowel cancer, but did not vary by socio-economic status [86]. This study of 483 consecutive patients in a large regional centre was not population-based. There is evidence that smoking amongst cancer patients varies with deprivation status [9]. Such differentials in high-risk behaviours may also lead to poorer health status amongst deprived patients that are not evident in quantifiable co-morbidity scores but which nevertheless have an impact upon patient survival. However, in the one study that controlled for smoking and alcohol consumption prior to cancer diagnosis, the impact of these health behaviours upon crude survival was small, both for respiratory-related malignancies and all cancers combined [33]. Further research is needed on the extent to which socio-economic gradients in cancer survival may be confounded by co-morbidity and health behaviours.
Similarly, it has been postulated that better nutrition amongst the affluent may also influence a person's ability to withstand treatment, above and beyond the differentials in background mortality accounted for with disease-specific or relative survival [2]. Little work has been done in this area. It has been shown that obesity, more prevalent amongst deprived women [87], is inversely associated with survival for localised breast cancer [88, 89]. However, nutritional measures appear to have little impact upon survival from laryngeal cancer [90]. Possible confounding of socio-economic differences in survival by nutrition or body composition has not yet been explicitly examined.
psychosocial factors.
Some evidence suggests that social support leads to better overall survival. Married individuals have been found to have significantly better survival in some studies [23, 24, 56, 61], possibly because increased social support leads to appropriate diagnosis and treatment being sought in a more timely fashion [69]. Social support in the 3 months after surgery for non-metastatic breast cancer was non-significantly associated with improved survival in one small study [91]. Such factors are probably most influential in the earliest stages of the disease and for young patients [92]. Social support is less frequent amongst low-income or disadvantaged groups, and if such factors have any impact on survival, they could contribute to socio-economic differentials [93].
A recent study highlighted the importance of other socially influenced factors, including poor or unclear access to medical services, the social stigma attached to cancer and the associated delay in seeking health care, individual perceptions of personal risk, inappropriate health promotion strategies and poor communication with health care professionals [94]. Other research has shown that women from lower socio-economic groups are able to identify significantly fewer symptoms of breast cancer [95] and that breast cancer patients living in affluent areas are more likely to have received information on their disease from a hospital specialist, and less likely to have concerns about money, other health problems and family issues [93]. In a hospital-based study of 578 women with early breast cancer, high scores on depression, ‘helplessness’ or ‘hopelessness’, derived from survey instruments that reflect the psychological health of cancer patients, were found to have a negative impact on relapse and crude 5-year survival [96].
|
health care factors |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
treatment received.
There is increasing evidence of different treatment being given to cancer patients in different socio-economic groups. For example, linkage of hospital discharge records with population-based cancer registry data in Washington State, USA, showed that adjuvant chemo- or radiotherapy following surgery for stage II or III colon cancer, recommended by national guidelines, was significantly less likely to be given to patients aged over 65 years, to those in the poorest quartile of zip (postal) code areas and to those insured by Medicare compared with those with private insurance, none of which are specified by the guidelines as criteria for treatment [97
]. Affluent patients in south-east England have been shown to be more likely to receive surgery for lung, colorectal and breast cancer [67]. Differences between socio-economic groups in follow-up after an abnormal mammogram for breast cancer and in post-treatment care for colorectal cancer have also been suggested as explanations for differences in survival where treatment with curative intent is available [46, 98]. Despite universal, comprehensive health insurance coverage and a centrally organised radiotherapy service in Ontario, Canada, elderly or poor women with breast cancer were significantly less likely to receive radiotherapy within a year of diagnosis. This suggests a degree of ‘implicit’ rationing with respect to age and income [99]. Women with breast cancer living in deprived areas have been found to be more likely to receive a mastectomy than breast-conserving therapy in comparison with those living in affluent places in both the UK [41, 74, 100] and the USA [101]. Variation in mastectomy rates between screening centres in one region of England was not accounted for by differences in tumour size, site, grade, patient age or year of presentation [102]. However, since survival after mastectomy and breast conserving surgery is similar [103], such differences seem unlikely to explain socio-economic inequalities in survival unless there is also differential access to radiotherapy or systemic treatment between socio-economic groups.
It has been suggested that differences in treatment largely explain socio-economic differences in cancer survival in the USA [104], and either most [105] or all [106–108] of the observable racial differences. These studies examined both data from clinical trials, in which treatment was equalised within each trial arm, and information from population-based settings in which all patients received an equal level of care. The explanatory power of unequal treatment for racial differences in survival is particularly striking, since the alternative explanation is that differences in survival between ethnic groups are attributable to genetic factors; this cannot apply to socio-economic variability in survival within ethnically homogeneous populations. It has been suggested that breast carcinoma is more aggressive in African-American than Caucasian women, since onset is substantially younger and more aggressive in the former group [60, 109, 110]. If the conclusion from these studies, that ‘equal treatment yields equal outcome, ... regardless of race’ [108], is valid despite possible differences in the biological spectrum of tumours, it follows that ensuring equal access to treatment could be at least as important in eliminating differences in survival between groups that are defined solely by social characteristics.
Research in other countries has not identified such clear distinctions in survival with respect to treatment. For women with breast cancer in Glasgow, Scotland, patterns of treatment and care were similar for affluent and deprived groups, as defined by their area of residence, although deprived women consulted more frequently for other conditions, suggesting much higher co-morbidity [59]. In a population-based study in California, USA, the likelihood of younger women with breast cancer receiving breast-conserving therapy did not differ by health insurance category, but varied by type of hospital [58]. However, in South Australia, survival after breast cancer was not associated with the hospital attended [111].
medical expertise.
The expertise or experience of the treating physicians could also differ between socio-economic groups. In one population-based study in Calvados, France, unemployed colorectal patients were half as likely as more affluent patients to be seen by a gastroenterologist or to be treated in a specialised centre, although these patterns did not explain all the survival differences [112]. In a population-based study of over 75 000 patients with cancer of the breast, bowel or lung in the UK, linkage to hospital admission data showed that patients living in deprived areas were admitted more often as emergencies. Deprived patients with breast or lung cancer were also less likely to be recorded as having had surgery, and bowel cancer patients were less likely to be treated in a centre with a large caseload, although the opposite was true for women with breast cancer [67].
Women with breast cancer treated by specialist surgeons in Scotland had higher survival than other women, regardless of the level of deprivation [113]. However, specialised surgeons have been shown to treat higher proportions of both affluent and deprived women than non-specialists [114, 115], a finding supported by data on colorectal cancer [45]. Consequently, local variations in the extent to which patients are managed by specialists may account for some differentials in survival, but there is little evidence to suggest that this can account for deprivation gradients in survival.
The availability of doctors in the USA, used as a crude measure of health care quality, appears to improve the early detection of tumours [116], but not survival [61]. Initial treatment at hospitals with a high caseload [45] or at a teaching hospital [117] has been shown to have a positive impact on survival in the UK and Canada. It is not clear, however, that individuals with low socio-economic status are less likely to be attended in teaching or high-volume hospitals [118]. Consequently, these patterns appear unlikely to explain socio-economic differences in survival.
screening.
Low uptake of mammography among groups of lower socio-economic status may lead to socio-economic differentials in the stage of disease at diagnosis and in survival, even though screening is similarly effective in all socio-economic groups [119, 120]. In a clinical trial of screening for colorectal cancer in the UK, compliance was shown to be associated with earlier diagnosis and longer post-operative survival. Deprived subjects were less likely to accept the invitation to be screened [44], but after adjustment for age and participation in screening, the impact of deprivation on survival was only evident for women. Further work on the confounding of socio-economic differentials in survival by participation in screening will be required in order to confirm this finding and, in particular, to quantify the impact on survival of differential participation in screening between socio-economic groups.
|
conclusions |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
An association between cancer survival and measures of socio-economic status has been observed for many different cancers, in several different clinical and geographic settings, and with various definitions of social position. This pattern is not confined to cancer survival. Similar differences have been observed in mortality from stroke in Canada [121
] and from cardio-vascular disease in the UK [122], despite evidence that socio-economic status was not associated with differences in appropriate treatment [123]. Differences between socio-economic groups in the stage of disease at diagnosis and in access to optimal treatment clearly explain at least part of the association between social deprivation and cancer survival. It seems unlikely, however, that differences in the expertise of medical personnel involved in treating patients in different social groups explains much of the survival differentials. The impact on disease stage, and on survival, of delay in seeking health care (patient delay) and delay in referral for diagnosis and specialist care (system delay) is also unclear. This requires further research. Characteristics of the patient, such as nutrition, co-morbidity and health-seeking behaviours, may also interact with treatment decisions and, ultimately, with the outcome. These characteristics have received little attention. It is important to find out whether socio-economic differences in how patients seek and obtain access to health services, or participate in screening, are associated with socio-economic differences in cancer survival.
Received for publication July 15, 2005. Accepted for publication July 18, 2005.
|
References |
|---|
|
TopAbstractintroductionmethodsresultsdiscussionpatient characteristicshealth care factorsconclusionsReferences |
|---|
1. Kogevinas M, Porta M. Socioeconomic differences in cancer survival: a review of the evidence. In Kogevinas M, Pearce M, Susser M, Boffetta M (eds): Social Inequalities and Cancer. IARC Scientific Publications No. 138. Lyon: International Agency for Research on Cancer 1997; 177–206.
2. Auvinen A, Karjalainen S. Possible explanations for social class differences in cancer patient survival. In Kogevinas M, Pearce N, Susser M, Boffetta P (eds): Social Inequalities and Cancer. IARC Scientific Publications No. 138. Lyon: IARC 1997; 377–397.
3. PubMed. United States National Library of Medicine (NLM). [on-line] http://www.ncbi.nlm.nih.gov/PubMed/ (October 2004, date last accessed).
4. EMBASE. Ovid Technologies, Inc. [on-line] http://gateway1.uk.ovid.com/ovidweb.cgi (October 2004, date last accessed).
5. ISI Web of Knowledge service for UK education. JISC, MIMAS, Thompson ISI. http://wok.mimas.ac.uk/ (October 2004, date last accessed).
6. NLM Gateway. United States National Library of Medicine (NLM). [on-line] http://gateway.nlm.nih.gov/gw/Cmd (October 2004, date last accessed).
7. WebSPIRS 5.0. SilverPlatter's Information Retrieval System for the World Wide Web. Ovid Technologies, Inc. [on-line] http://web5s.silverplatter.com/webspirs/start.ws (October 2004, date last accessed).
8. Australian Institute of Health and Welfare (AIHW), Australasian Association of Cancer Registries (AACR). Cancer survival in Australia 1992–1997: geographic categories and socioeconomic status. Report No. 22. Cancer Series. Vol. Canberra: Australian Institute of Health and Welfare, 2003.
9. Begum G, Dunn JA, Bryan RT et al. Socio-economic deprivation and survival in bladder cancer. BJU Int 2004; 94: 539–543.[CrossRef][ISI][Medline]
10. Boyd C, Zhang-Salomons JY, Groome PA, Mackillop WJ. Associations between community income and cancer survival in Ontario, Canada, and the United States. J Clin Oncol 1999; 17: 2244–2255.
11. Ciccone G, Prastaro C, Ivaldi C et al. Access to hospital care, clinical stage and survival from colorectal cancer according to socio-economic status. Ann Oncol 2000; 11: 1201–1204.
12. Coleman MP, Babb P, Damiecki P et al. Cancer survival trends in England and Wales 1971–1995: deprivation and NHS Region. Series SMPS No. 61. London: The Stationery Office 1999.
13. Coleman MP, Babb P, Sloggett A et al. Socioeconomic inequalities in cancer survival in England and Wales. Cancer 2001; 91 (1 Suppl): 208–216.[CrossRef][Medline]
14. Coleman MP, Rachet B, Woods LM et al. Trends and socioeconomic inequalities in cancer survival in England and Wales up to 2001. Br J Cancer 2004; 90: 1367–1373.[CrossRef][ISI][Medline]
15. Dawkins FW, Laing AE, Smoot DT et al. The impact of health insurance on an African-American population with colorectal cancer. J Natl Med Assoc 1995; 87: 301–303.[Medline]
16. Edwards DM, Jones J. Incidence of and survival from upper aerodigestive tract cancers in the UK: the influence of deprivation. Eur J Cancer 1999; 35: 968–972.[CrossRef][ISI][Medline]
17. Fontana V, Decensi A, Orengo MA et al. Socioeconomic status and survival of gastric cancer patients. Eur J Cancer 1998; 34: 537–542.[CrossRef][ISI][Medline]
18. Gorey KM, Holowaty EJ, Fehringer G et al. An international comparison of cancer survival: Toronto, Ontario, and Detroit, Michigan, metropolitan areas. Am J Public Health 1997; 87: 1156–1163.
19. Gorey KM, Holowaty EJ, Laukkanen E et al. An international comparison of cancer survival: advantage of Toronto's poor over the near-poor of Detroit. Can J Public Health 1998; 89: 102–104.[ISI][Medline]
20. Gorey KM, Holowaty EJ, Fehringer G et al. An international comparison of cancer survival: relatively poor areas of Toronto, Ontario and three US metropolitan areas. J Public Health Med 2000; 22: 343–348.
21. Gorey KM, Holowaty EJ, Fehringer G et al. An international comparison of cancer survival: metropolitan Toronto, Ontario, and Honolulu, Hawaii. Am J Public Health 2000; 90: 1866–1872.
22. Gorey KM, Kliewer E, Holowaty EJ et al. An international comparison of breast cancer survival: Winnipeg, Manitoba and Des Moines, Iowa, metropolitan areas. Ann Epidemiol 2003; 13: 32–41.[CrossRef][ISI][Medline]
23. Harvei S, Kravdal O. The importance of marital and socioeconomic status in incidence and survival of prostate cancer. An analysis of complete Norwegian birth cohorts. Prev Med 1997; 26: 623–632.[CrossRef][ISI][Medline]
24. Kravdal Ø. Social inequalities in cancer survival. Pop Stud 2000; 54: 1–18.
25. Kaffashian F, Godward S, Davies T et al. Socioeconomic effects on breast cancer survival: proportion attributable to stage and morphology. Br J Cancer 2003; 89: 1693–1696.[CrossRef][ISI][Medline]
26. Mackillop WJ, Zhang-Salomons J, Groome PA et al. Socioeconomic status and cancer survival in Ontario. J Clin Oncol 1997; 15: 1680–1689.[Abstract]
27. McDavid K, Tucker TC, Sloggett A, Coleman MP. Cancer survival in Kentucky and health insurance coverage. Arch Intern Med 2003; 163: 2135–2144.
28. Moran A, Sowerbutts AM, Collins S et al. Bladder cancer: worse survival in women from deprived areas. Br J Cancer 2004; 90: 2142–2144.[ISI][Medline]
29. Newnham A, Quinn MJ, Babb P et al. Trends in oesophageal and gastric cancer incidence, mortality and survival in England and Wales 1971–1998/1999. Aliment Pharmacol Ther 2003; 17: 655–664.[CrossRef][ISI][Medline]
30. Paterson IC, John G, Adams JD. Effect of deprivation on survival of patients with head and neck cancer: a study of 20,131 cases. Clin Oncol (R Coll Radiol) 2002; 14: 455–458.[Medline]
31. Pollock AM, Vickers N. Breast, lung and colorectal cancer incidence and survival in South Thames Region, 1987–1992: the effect of social deprivation. J Public Health Med 1997; 19: 288–294.
32. Potosky AL, Merrill RM, Riley GF et al. Breast cancer survival and treatment in health maintenance organization and fee-for-service settings. J Natl Cancer Inst 1997; 89: 1683–1691.
33. Rosengren A, Wilhelmsen L. Cancer incidence, mortality from cancer and survival in men of different occupational classes. Eur J Epidemiol 2004; 19: 533–540.[CrossRef][ISI][Medline]
34. Rosso S, Faggiano F, Zanetti R, Costa G. Social class and cancer survival in Turin, Italy. J Epidemiol Community Health 1997; 51: 30–34.[Abstract]
35. Schillinger JA, Grosclaude PC, Honjo S et al. Survival after acute lymphocytic leukaemia: effects of socioeconomic status and geographic region. Arch Dis Child 1999; 80: 311–317.
36. Schrijvers CT, Mackenbach JP, Lutz JM et al. Deprivation, stage at diagnosis and cancer survival. Int J Cancer 1995; 63: 324–329.[ISI][Medline]
37. Singh GK, Miller BA, Hankey BF, Edwards BK. Area socio-economic variations in US cancer incidence, mortality, stage, treatment, and survival, 1975–1999. NCI Cancer Surveillance Monograph Series. Report No. 4. NIH Publication No. 03-5417. Bethesda, MD: National Cancer Institute, 2004.
38. Singh GK, Miller BA, Hankey BF, Edwards BK. Persistent area socioeconomic disparities in US incidence of cervical cancer, mortality, stage, and survival, 1975–2000. Cancer 2004; 101: 1051–1057.[CrossRef][ISI][Medline]
39. Stavraky KM, Skillings JR, Stitt LW, Gwadry-Sridhar F. The effect of socioeconomic status on the long-term outcome of cancer. J Clin Epidemiol 1996; 49: 1155–1160.[CrossRef][ISI][Medline]
40. Supramaniam R, Smith D, Coates M et al. Breast cancer survival in NSW in 1973 to 1995. Cancer Epidemiology Research Unit and NSW Central Cancer Registry Cancer Control Information Centre, NSW Cancer Council, Sydney, 1998.
41. Thomson CS, Hole DJ, Twelves CJ et al. Prognostic factors in women with breast cancer: distribution by socioeconomic status and effect on differences in survival. J Epidemiol Community Health 2001; 55: 308–315.
42. Twelves CJ, Thomson CS, Gould A, Dewar JA. Variation in the survival of women with breast cancer in Scotland. The Scottish Breast Cancer Focus Group and The Scottish Cancer Therapy Network. Br J Cancer 1998; 78: 566–571.[ISI][Medline]
43. West Midlands Cancer Intelligence Unit. Cancer and deprivation 2002. Report No. R002. West Midlands Public Health Observatory, Birmingham, 2002.
44. Whynes DK, Frew EJ, Manghan CM et al. Colorectal cancer, screening and survival: the influence of socio-economic deprivation. Public Health 2003; 117: 389–395.[CrossRef][ISI][Medline]
45. Wrigley H, Roderick P, George S et al. Inequalities in survival from colorectal cancer: a comparison of the impact of deprivation, treatment, and host factors on observed and cause specific survival. J Epidemiol Community Health 2003; 57: 301–309.
46. Yabroff KR, Gordis L. Does stage at diagnosis influence the observed relationship between socioeconomic status and breast cancer incidence, case-fatality, and mortality? Soc Sci Med 2003; 57: 2265–2279.[CrossRef][ISI][Medline]
47. Woods LM, Rachet B, Coleman MP. Choice of geographic unit influences socioeconomic inequalities in breast cancer survival. Br J Cancer 2005; 92: 1279–1282.[CrossRef][ISI][Medline]
48. Berrino F, Capocaccia R, Coleman MP et al. Survival of cancer patients in Europe: the EUROCARE-3 study. Ann Oncol 2003; 14 (Suppl 5): v1–v155.[CrossRef]
49. Sant M, Allemani C, Capocaccia R et al. Stage at diagnosis is a key explanation of differences in breast cancer survival across Europe. Int J Cancer 2003; 106: 416–422.[CrossRef][ISI][Medline]
50. Ciccolallo L, Capocaccia R, Coleman MP et al. Survival differences between European and US patients with colorectal cancer: role of stage at diagnosis and surgery. Gut 2005; 54: 268–273.
51. O'Malley CD, Le GM, Glaser SL et al. Socioeconomic status and breast carcinoma survival in four racial/ethnic groups: a population-based study. Cancer 2003; 97: 1303–1311.[CrossRef][ISI][Medline]
52. Roetzheim RG, Pal N, Gonzalez EC et al. Effects of health insurance and race on colorectal cancer treatments and outcomes. Am J Public Health 2000; 90: 1746–1754.
53. Baquet CR, Commiskey P. Socioeconomic factors and breast carcinoma in multicultural women. Cancer 2000; 88 (5 Suppl): 1256–1264.[CrossRef][ISI][Medline]
54. Prout GR Jr, Wesley MN, McCarron PG et al. Survival experience of black patients and white patients with bladder carcinoma. Cancer 2004; 100: 621–630.[CrossRef][ISI][Medline]
55. Velikova G, Booth L, Johnston C et al. Breast cancer outcomes in South Asian population of West Yorkshire. Br J Cancer 2004; 90: 1926–1932.[CrossRef][ISI][Medline]
56. Meng L, Maskarinec G, Wilkens L. Ethnic differences and factors related to breast cancer survival in Hawaii. Int J Epidemiol 1997; 26: 1151–1158.
57. Brewster DH, Thomson CS, Hole DJ et al. Relation between socioeconomic status and tumour stage in patients with breast, colorectal, ovarian, and lung cancer: results from four national, population based studies. BMJ 2001; 322: 830–831.
58. Lee-Feldstein A, Feldstein PJ, Buchmueller T, Katterhagen G. The relationship of HMOs, health insurance, and delivery systems to breast cancer outcomes. Med Care 2000; 38: 705–718.[CrossRef][ISI][Medline]
59. Macleod U, Ross S, Twelves C et al. Primary and secondary care management of women with early breast cancer from affluent and deprived areas: retrospective review of hospital and general practice records. BMJ 2000; 320: 1442–1445.
60. Bradley CJ, Given CW, Roberts C. Disparities in cancer diagnosis and survival. Cancer 2001; 91: 178–188.[CrossRef][Medline]
61. Polednak AP. Survival of breast cancer patients in Connecticut in relation to socioeconomic and health care access indicators. J Urban Health 2002; 79: 211–218.[ISI][Medline]
62. Karjalainen S, Pukkala E. Social class as a prognostic factor in breast cancer survival. Cancer 1990; 66: 819–826.[CrossRef][ISI][Medline]
63. Ayanian JZ, Kohler BA, Abe T, Epstein AM. The relation between health insurance coverage and clinical outcomes among women with breast cancer. N Engl J Med 1993; 329: 326–331.
64. Ugnat AM, Xie L, Morriss J et al. Survival of women with breast cancer in Ottawa, Canada: variation with age, stage, histology, grade and treatment. Br J Cancer 2004; 90: 1138–1143.[CrossRef][ISI][Medline]
65. Richards MA, Westcombe AM, Love SB et al. Influence of delay on survival in patients with breast cancer: a systematic review. Lancet 1999; 353: 1119–1126.[CrossRef][ISI][Medline]
66. Richards MA, Smith P, Ramirez AJ et al. The influence on survival of delay in the presentation and treatment of symptomatic breast cancer. Br J Cancer 1999; 79: 858–864.[CrossRef][ISI][Medline]
67. Pollock AM, Vickers N. Deprivation and emergency admissions for cancers of colorectum, lung, and breast in south east England: ecological study. BMJ 1998; 317: 245–252.
68. Symonds P, Bolger B, Hole D et al. Advanced-stage cervix cancer: rapid tumour growth rather than late diagnosis. Br J Cancer 2000; 83: 566–568.[CrossRef][ISI][Medline]
69. Ramirez AJ, Westcombe AM, Burgess CC et al. Factors predicting delayed presentation of symptomatic breast cancer: a systematic review. Lancet 1999; 353: 1127–1131.[CrossRef][ISI][Medline]
70. Schrijvers CT, Mackenbach JP, Lutz JM et al. Deprivation and survival from breast cancer. Br J Cancer 1995; 72: 738–743.[ISI][Medline]
71. Schrijvers CT, Coebergh JW, van der Heijden LH, Mackenbach JP. Socioeconomic variation in cancer survival in the southeastern Netherlands, 1980–1989. Cancer 1995; 75: 2946–2953.[CrossRef][ISI][Medline]
72. Feinstein AR, Sosin DM, Wells CK. The Will Rogers phenomenon: stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. N Engl J Med 1985; 312: 1604–1608.[Abstract]
73. Allemani C, Sant M, Berrino F et al. Prognostic value of morphology and hormone receptor status in breast cancer – a population-based study. Br J Cancer 2004; 91: 1263–1268.[CrossRef][ISI][Medline]
74. Taylor A, Cheng KK. Social deprivation and breast cancer. J Public Health Med 2002; 25: 228–233.[Medline]
75. Lyratzopoulos G, West CR, Williams EM. Socioeconomic variation in colon cancer tumour factors associated with poorer prognosis. Br J Cancer 2003; 89: 828–830.[CrossRef][ISI][Medline]
76. Adams J, White M, Forman D. Are there socioeconomic gradients in stage and grade of breast cancer at diagnosis? Cross sectional analysis of UK cancer registry data. BMJ 2004; 329: 142.
77. Miller BA, Hankey BF, Thomas TL. Impact of sociodemographic factors, hormone receptor status, and tumor grade on ethnic differences in tumor stage and size for breast cancer in US women. Am J Epidemiol 2002; 155: 534–545.
78. Macleod U, Ross S, Gillis C et al. Socio-economic deprivation and stage of disease at presentation in women with breast cancer. Ann Oncol 2000; 11: 105–107.
79. Carnon AG, Ssemwogerere A, Lamont DW et al. Relation between socioeconomic deprivation and pathological prognostic factors in women with breast cancer. BMJ 1994; 309: 1054–1057.
80. Gordon NH. Association of education and income with estrogen receptor status in primary breast cancer. Am J Epidemiol 1995; 142: 796–803.
81. McMillan DC, Canna K, McArdle CS. The effect of deprivation and the systemic inflammatory response on outcome following curative resection for colorectal cancer. Br J Cancer 2003; 89: 612–614.[CrossRef]