Ethnic inequalities in time to diagnosis of cancer: a systematic review

The present study aimed to gather and critically appraise existing evidence on inequalities in cancer diagnosis by ethnic groups in the UK and in countries with a similar health care system - in terms of costs, availability and access [10], specifically examining literature reporting time to diagnosis of the cancer. We used the schema of intervals in cancer diagnosis described by Olesen and colleagues, and illustrated in Figure 1[11].

This used the Critical Appraisal Skills Programme (CASP) checklist for cohort studies, interpreted to fit our study topic (see rows 1 and 2 in Table 2 for details). Each retrieved article was independently appraised by two reviewers (TM and OU) and was classified as either “satisfactory”, “medium” or “high” quality paper depending on the extent to which the checklist items were met, and also on the level of concerns raised about their methodology in general. For instance, a concern was raised where authors classified ethnic groups differently to the contemporary ethnic classifications in their population.

In total, 8,520 articles were identified from the search strategy. After screening the titles and abstracts, and removing the duplicates, 8,489 irrelevant articles were excluded. The remaining 31 articles were then retrieved for full text review, and seven met the inclusion criteria and were included in the analysis (see flow chart in Figure 2).

Characteristics of the selected studies are shown in Table 3 with results of the quality assessment in Table 2. All seven studies were observational, with retrospective cohort designs, using hospital records, cancer registry records, survey questionnaires and in-depth interviews. Six were carried out in the UK, and one in New Zealand. Five studies [14‐18] investigated ethnic differences in breast cancer diagnosis while the remaining two focused on prostate [20] and oesophagogastric cancer [19] respectively. Neal and Allgar studied several other cancer sites in addition to breast: lung, prostate, colorectal non-Hodgkin’s lymphoma (NHL) and ovarian [18].

Five studies [14‐17, 20] investigated ethnic differences in patient delay, that is, delay occurring in the interval between first symptom and first GP presentation (see Figure 1). Two of these [16, 17] also examined ethnic differences in delay following the first GP presentation, but their definitions of these time periods differed. Nosarti et al. defined delay occurring in the interval between the first GP presentation and first specialist visit as system delay [17]. Velikova et al. defined the interval between first GP referral and the first hospital visit as provider’s delay [16]. Neither of these correspond with current definitions [13]. The remaining two studies took slightly different approaches in their definition of delay intervals. Sadler and colleagues used patients’ referral routes to the hospital as surrogate measures of primary care delay [19]. They considered two-week waits (2WW) or ‘Direct Access Oesophago-gastro-duodenoscopy’ (OGD) as optimal routes to diagnosis, while waiting for routine appointments and acute admission were both considered sub-optimal. In addition, they reported ethnic differences in total diagnostic interval, which is the interval from first symptom to diagnosis. Similarly, Neal and Allgar reported the same interval, naming it pre-hospital delay [18]. For the rest of this paper, we have renamed these ‘the diagnostic interval’. They also reported ethnic differences in referral delay, which they defined as the waiting time from first GP visit to first hospital appointment.

Our rigorous search strategy, and explicit inclusion/exclusion criteria, quality assessment of included studies and narrative synthesis followed best practice. Our search identified only a small number of studies, the bulk of which were (unsurprisingly) conducted in the UK, given that the UK is one of the most ethnically diverse countries in Europe. Our decision to omit American studies (other than Canada) was based on their very different health care system and ethnic groupings; it considerably reduced the number of selected studies, although this reflected our research question of whether there are ethnic inequalities in the time to diagnosis of cancer within a free health care system. A limitation was that most studies focused on breast cancer, reducing the scope of the review. Furthermore, any review is only as good as the studies it finds. Our selections differed considerably in methodology - especially in the definitions of intervals before diagnosis, which made quantitative synthesis inappropriate, and complicated the narrative synthesis. Participants’ ethnic groups were poorly defined in some studies; at times there was a mismatch between the ethnic groupings used for the study and contemporary ethnic groupings used in the whole population from which their sample was drawn [16, 20]. We interpreted the CASP quality instrument for this review - primarily to fit our study topic: it is unlikely these minor changes led to more studies ‘failing’ our quality assessment. Finally, publication bias is possible as studies showing no association between ethnicity and cancer diagnostic delays may have failed to be published, leaving us with disproportionately positive studies.

Two previous reviews [21, 22] have examined delays in cancer diagnosis, although neither examined ethnicity. In both (like in the present review), the intervals were defined in a nonstandard way. This is understandable, as terminology in this subject was ill-defined before the advent of the Aarhus statement [13]. This provides more precise description of milestones along the cancer diagnostic pathway, as well as describing preferred research methodologies. In an assessment of primary care use prior to cancer diagnosis, Lyratzopoulos and colleagues found that ethnic minority groups were more likely to have consulted their GPs three or more times before hospital referral (odds ratio for Asian vs. white 1 · 73, 1 · 45 to 2 · 08; p < 0 · 0001; odds ratio for black vs. white 1 · 83, 1 · 51 to 2 · 23; p < 0 · 0001. This study did not report durations or intervals to diagnosis, so would not have met our inclusion criteria, though its results are consistent with our findings.

We found limited, methodologically-weak evidence for ethnic inequalities in cancer diagnosis, though largely for breast cancer. Conversely, the review found no evidence to suggest that ethnic minority groups were doing better at any stage of cancer diagnostic pathway. For breast cancer, three (of five studies) found longer patient and pre-hospital delays in ethnic minority women compared to their white counterparts; while the remaining two reported no difference. The latter two studies sampled participants from a relatively small number of women referred to a specialist clinic for further investigation. It is well-recognised that cancer patients may take alternative routes to diagnosis, such as routine specialist clinics or emergency admission; these will have been omitted from the two studies based in specialist clinics [23, 24]. Furthermore, both studies were based on interviewing patients about their delay experiences whilst in the specialist waiting room. Therefore, their findings may have been influenced by selection and recall biases. In contrast, the three studies finding differences in diagnostic intervals across ethnic groups recruited participants with definite diagnosis of breast cancer, and then surveyed or examined their medical record for important dates of presentation and referral.