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/lp/ou_press/the-nature-and-frequency-of-abdominal-symptoms-in-cancer-patients-and-GRJNbgVqVU
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- Oxford University Press
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- Copyright © 2022 Faculty of Public Health
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- 1741-3842
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- 1741-3850
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- 10.1093/pubmed/fdx188
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Abstract
Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 Journal of Public Health | Vol. 40, No. 3, p. e388–e395 | doi:10.1093/pubmed/fdx188 | Advance Access Publication January 27, 2018 The nature and frequency of abdominal symptoms in cancer patients and their associations with time to help-seeking: evidence from a national audit of cancer diagnosis 1 1 2 3 Minjoung Monica Koo , Christian von Wagner , Gary A. Abel , Sean McPhail , 2 4 1 William Hamilton , Greg P. Rubin , Georgios Lyratzopoulos University College London, 1-19 Torrington Place, London WC1E 6BT, UK University of Exeter Medical School, St Luke’s Campus, Heavitree Road, Exeter EX1 2LU, UK National Cancer Registration and Analysis Service, Public Health England Zone A, 2nd Floor, Skipton House, 80 London Road, London SE1 6LH, UK Institute of Health and Society, Newcastle University, Sir James Spence Institute, Royal Victoria Infirmary, Newcastle upon Tyne NE1 4LP, UK Address correspondence to Minjoung Monica Koo, E-mail: Monica.koo.14@ucl.ac.uk ABSTRACT Background Raising awareness of possible cancer symptoms is important for timely help-seeking; recent campaigns have focused on symptom groups (such as abdominal symptoms) rather than individual alarm symptoms associated with particular cancer sites. The evidence base supporting such initiatives is still emerging however; understanding the frequency and nature of presenting abdominal symptoms among cancer patients could inform the design and evaluation of public health awareness campaigns. Methods We examined eight presenting abdominal symptoms (abdominal pain, change in bowel habit, bloating/distension, dyspepsia, rectal bleeding, dysphagia, reflux and nausea/vomiting) among 15 956 patients subsequently diagnosed with cancer in England. We investigated the cancer site case-mix and variation in the patient interval (symptom-onset-to-presentation) by abdominal symptom. Results Almost a quarter (23%) of cancer patients presented with abdominal symptoms before being diagnosed with one of 27 common and rarer cancers. The patient interval varied substantially by abdominal symptom: median (IQR) intervals ranged from 7 (0–28) days for abdominal pain to 30 (4–73) days for dysphagia. This variation persisted after adjusting for age, sex and ethnicity (P < 0.001). Conclusions Abdominal symptoms are common at presentation among cancer patients, while time to presentation varies by symptom. The need for awareness campaigns may be greater for symptoms associated with longer intervals to help-seeking. Keywords cancer, health promotion, public health Previous symptom awareness campaigns have tended to Introduction take a cancer-based approach, by targeting ‘red-flag’ or Diagnosing cancer early in symptomatic patients is a ‘alarm’ symptoms explicitly associated with specific cancers, prominent feature of contemporary cancer control strat- 10–12 such as ‘blood in poo’ and colorectal cancer. There is 1,2 egies. A range of pioneering studies during the last however growing interest in targeting symptoms relating to a decade have established associations between the knowl- body area or system, partly as this provides an opportunity edge (‘awareness’) of likely symptoms of cancer among the general public and timely presentation, diagnosis, Minjoung Monica Koo, PhD Student 3–6 and outcomes. Public health agencies have conse- Christian von Wagner, Reader in Behavioural Science and Health quently implemented educational interventions aimed at Gary A. Abel, Senior Lecturer raising awareness of cancer symptoms in order to pro- Sean McPhail, Senior Analyst 7–9 William Hamilton, Professor of Primary Care Diagnostics mote timely presentation. However, the evidence base Greg P. Rubin, Professor of General Practice and Primary Care supporting the design of such interventions is still Georgios Lyratzopoulos, Professor of Cancer Epidemiology emerging. © The Author(s) 2018. Published by Oxford University Press on behalf of Faculty of Public Health. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/), e388 which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 THE NATURE AND FREQUENCY OF ABDOMINAL SYMPTOMS IN CANCER PATIENTS e389 to promote the earlier presentation of rarer and less com- years or older), sex, presenting symptoms and cancer site mon cancers. In England, an abdominal symptoms cam- (see Supplementary Fig. S1 for flow chart of sample deriv- paign was recently piloted at regional level, focusing on a ation). Individuals diagnosed incidentally and those with can- range of symptoms (diarrhoea, bloating, abdominal discom- cer sites categorized as ‘No information’ and ‘Unknown fort, constipation, nausea, and blood in poo). Primary’ were excluded from the analysis. Among the 3661 Examining the length of the patient interval (time from cancer patients with one or more abdominal symptoms, symptom onset to presentation) associated with different 2936 (80%) had complete information on the patient inter- abdominal symptoms can contribute to the design of future val (see Supplementary Table S2 for the proportion of miss- campaigns. Awareness campaigns about possible cancer symp- ing values by individual symptom). Overall, the strongest toms aim to shorten the patient interval by encouraging timely predictor of missing interval or pre-referral consultation data symptom appraisal and help-seeking. Therefore, symptom- was first presentation to a healthcare facility other than the specific patient intervals may be interpreted as measures of patient’s own general practice, without evidence for substan- relative need for such interventions. Alongside considerations tive differences by socio-demographic characteristic (data of other important factors such as the predictive value of a not shown). symptom for cancer, and the prevalence of different symptoms in the general population, such evidence can support how the Variables of interest content of awareness campaigns could prioritize certain symp- General practitioners participating in the audit provided free toms over others. text answers to the question ‘what was the main presenting Further, estimating the impact of a symptom awareness symptom?’ for each patient, based on information in their pri- campaign has been shown to be challenging due to the diffuse mary care records. As described previously, we coded symp- and broad-reaching nature of campaigns; such difficulties are tom constructs following principles of natural language likely to be exacerbated by symptom-based approaches that processing (NLP), without prior definitions or restrictions 7,16 target more than one cancer site. Evidence regarding the regarding cancer-symptom associations. If multiple symp- anticipated cancer site case-mix of a particular symptom could toms were mentioned, they were assumed to be synchronous. help guide the direction of evaluation strategies, though such Symptoms were initially assigned by MMK, and cross-validated evidence is generally lacking. by GL and GPR, an approach also used previously. Based on We therefore examined the frequency of abdominal symp- the abdominal symptoms described by the 2015 National toms at presentation in a representative population of inci- Institute for Health and Care Excellence (NICE) guidelines for dent cancer patients; described the range of cancers suspected cancer, we selected a total of 18 symptom constructs associated with abdominal symptoms in an incident cohort; (see Supplementary Table S2) which were further aggregated and examined variation in the length of the patient interval into eight abdominal symptom groups: (non-acute) abdominal by presenting abdominal symptom. pain, bloating or distension, change in bowel habit, dysphagia, dyspepsia, nausea or vomiting, rectal bleeding and reflux. Methods The patient interval was defined as the number of days between symptom onset and the first presentation to pri- Data source mary care, in line with the Aarhus Statement. We used data from the first English cancer audit (National Audit of Cancer Diagnosis in Primary Care) 2009–10, details of which have been described previously. Briefly, partici- Statistical analysis pating clinicians collected information on the diagnostic pro- The frequency (and associated exact confidence intervals) of cess for incident cancer patients in ~14% of all general abdominal symptoms in the studied population of cancer practices in England, excluding screen-detected cases. The patients were estimated. We then described the cancer site audited cancer patient population was representative of inci- case-mix of abdominal symptoms, namely the range and dent cancer patients in England during the same period, relative frequencies (proportions) of different cancer sites while the characteristics of participating practices were found subsequently diagnosed among cancer patients presenting 18,19 to be comparable to non-participating practices. with abdominal symptoms. Subsequently, we examined variation in the patient interval Patient population by abdominal symptom. As public awareness campaigns target We analysed data from cancer patients with complete and individual symptoms rather than symptom combinations, valid information on age group (among patients aged 15 these analyses were restricted to the majority of cancer patients Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 e390 JOURNAL OF PUBLIC HEALTH Table 1 Frequency of abdominal symptoms among symptomatic cancer with a single recorded presenting abdominal symptom (n = patients (n = 15 956) 2253, 62% of all patients reporting an abdominal symptom)— though we examined common abdominal symptom combina- Symptom No. of patients Percentage of symptomatic tions in supplementary analyses. Firstly, the mean, median, cancer patients (95% CI) interquartile range and 90th centiles of the patient interval were estimated for each abdominal symptom along with 95% Abdominal pain 1268 7.9 (7.5–8.4) confidence intervals using a bootstrap approach with 1000 Change in bowel habit 1010 6.3 (6.0–6.7) replications. Kruskal–Wallis tests were used to test variation in Rectal bleeding 768 4.8 (4.5–5.2) median interval length by abdominal symptom. The propor- Dysphagia 418 2.6 (2.4–2.9) tion of patients with each symptom that experienced a patient Nausea or vomiting 261 1.6 (1.5–1.8) interval of 60 days or longer was also calculated to help to fur- Dyspepsia 256 1.6 (1.4–1.8) ther contextualize the findings. Bloating or distension 250 1.6 (1.4–1.8) Reflux 71 0.4 (0.4–0.6) We then used generalized linear models (GLM) to examine Any abdominal symptom 3661 22.9 (22.3–23.6) the association between abdominal symptoms and the patient interval adjusted for age group (parameterized as <50 years, NB the number of patients (percentages) sum to more than 3661 (23%) 50–69 years, 70+ years), ethnicity (white, non-white) and sex as patients could have more than one abdominal symptom. (men, women) given prior evidence supporting their associa- tions with diagnostic timeliness. To account for skewed out- (13%), ovarian (7%) and pancreatic (6%) cancers (Table 2 come data, a log link function was used (which allows the and Fig. 1). A further 14 cancer sites were represented covariates to be modelled on a linear additive scale, aiding among the remainder of patients, including solid tumours of interpretation), and significance testing was based on boot- non-abdominal (and non-adjacent) organs (8%) and haem- strapping (1000 replications). Variation in interval length was atological cancers (4%). examined using joint Wald tests, with statistical significance at We also considered the relative importance of abdominal the 5% level. All analyses were conducted using STATA SE v symptoms for each cancer site by calculating the proportion 13.1 (StataCorp, College Station, TX, USA). of patients with a given cancer who had presented with one or more abdominal symptoms. Unsurprisingly, over two- Supplementary analyses fifths (41%) of cancer patients diagnosed with an abdominal We conducted supplementary analyses examining the fre- cancer had presented with abdominal symptoms, although quency of 12 most common abdominal symptom combina- this ranged from 84% of patients later diagnosed with tions, and their associated distributions of the observed oesophageal cancer to 5% of patients later diagnosed with patient interval in the same way as described above. prostate cancer (see Table 2 for full breakdown). Patients with cancers arising outside the abdominal region were much less likely to report abdominal symptoms (4%, n = Results 279). In contrast, patients diagnosed with haematological Frequency of presenting abdominal symptoms in cancers were relatively more likely to report abdominal cancer patients symptoms at presentation (11%, n = 138), almost two-thirds Of a total of 15 956 patients with cancer, 3661 (23%) pre- of those being patients with lymphoma (Table 2). sented with one or more abdominal symptoms. Abdominal pain was the most common abdominal symptom across the entire cohort of cancer patients (8%), followed by change in Patient interval by presenting abdominal symptom bowel habit (6%), and rectal bleeding (5%) (Table 1). Among cancer patients with a single presenting abdominal symptom (n = 2253), there was strong evidence for variation Cancer site case-mix of abdominal symptoms in in the patient interval (symptom-onset-to-presentation) by cancer patients symptom (P < 0.001, Fig. 2 and Supplementary Table S3). Among the 3661 cancer patients who presented with Patients presenting with change in bowel habit or dysphagia abdominal symptoms, the majority (89%, 3244/3661) were had the longest patient intervals: one in two patients with either of these symptoms waited at least a month before diagnosed with solid cancers of abdominal or adjacent organs (Fig. 1). The most commonly diagnosed cancer site presentation, while a quarter waited 2 months or longer was colorectal cancer (47%), followed by oesophageal (median (IQR) patient interval: 30(4–73) days for change in Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 THE NATURE AND FREQUENCY OF ABDOMINAL SYMPTOMS IN CANCER PATIENTS e391 Fig. 1 Cancer site case-mix of patients who presented with one or more abdominal symptom (n = 3661). NB Proportions of the nine most frequent cancers across all abdominal symptoms shown only; other cancer diagnoses are represented as ‘Any other cancer site’ category. See Table 2 for exact proportions. bowel habit; and 30(10–61) days for dysphagia). A consider- stomach (65%), small intestinal (69%) and gallbladder cancers able proportion (25–30%) of patients with bloating or dis- (51%) presenting with abdominal symptoms. tension, reflux and rectal bleeding also waited for two Comparable evidence on the association between the months or longer before presentation. In contrast, cancer patient interval and abdominal symptoms is limited to two patients presenting with abdominal pain or nausea/vomiting English studies on colorectal and pancreatic cancers, respect- 26,27 went to the doctor sooner on average (7(0–28) days and 7- ively. Rectal bleeding and dyspepsia-like symptoms were (0–23) days, respectively). The variation in interval length by associated with shorter time to presentation compared with abdominal symptom persisted after adjusting for age group, other studied symptoms, in line with our findings regarding sex and ethnicity (Supplementary Table S4). these symptoms. In supplementary analyses, we considered the 12 most common categories of single or combinations of presenting What this study adds symptoms, including 3438 patients (94% of patients report- In order to improve the timeliness of diagnosis among can- ing one or more abdominal symptom). Results were largely cer patients who present with symptoms, we need a better comparable to the main analyses finding in respect of asso- appreciation of the nature and frequency of presenting ciations with the patient interval (see Supplementary Tables symptoms among these patients; currently, related epidemio- S5 and S6). logical evidence is limited in quantity and breadth . Consequently, our study adds substantially to the present evidence base, both regarding the burden of abdominal Discussion symptoms in incident cancer patients, and their associations Main findings of this study with time to help-seeking. Abdominal symptoms appear to be common among incident cases of cancer, suggesting that Almost one in four cancer patients presented with abdominal symptom awareness campaigns focusing on abdominal symptoms before diagnosis. The majority of cancer patients symptoms could potentially expedite the diagnosis of a large who presented with abdominal symptoms were subsequently range of both common and rarer cancers. diagnosed with a range of common and rarer cancers of Previous analyses have shown large variation in the abdominal or adjacent organs, but a proportion of patients 28,29 patient interval by cancer site. Our findings suggest that had tumours of other solid organ tumours, or haematological this chieflyreflects variation in interval length of the most malignancies. The median patient interval ranged from 7 days frequent symptoms of the different cancers. After consider- for abdominal pain to 30 days for dysphagia. The observed ing symptom prevalence and predictive values of each symp- differences in interval length by abdominal symptom remained tom, variation in the length of the patient interval associated when adjusted for age, sex and ethnicity. with different symptoms could help to identify particular symptoms for prioritization in campaigns. For example, we What is already known on this topic found that one in two cancer patients with dysphagia waited In our study, colorectal, oesophageal, ovarian and pancreatic almost a month before presenting. As dysphagia is also an cancers accounted for the majority of cancer patients that pre- established ‘alarm’ symptom for cancer, this finding argues sented with one or more abdominal symptoms, consistent for its further targeting by future campaigns. In contrast, 25,26 with previous evidence. However, we also found large cancer patients with abdominal pain presented after a proportions of patients diagnosed with rarer cancers such as median interval of 7 days, and given its high prevalence and Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 e392 JOURNAL OF PUBLIC HEALTH Table 2 Cancer site case-mix of patients with one or more abdominal symptoms (n=3661) and proportion of patients with a given cancer that had abdominal symptoms Cancer Number of patients Percentage of patients with one or more Percentage of patients with a given abdominal symptoms subsequently cancer who had one or more abdominal diagnosed with a given cancer (95% CI) symptoms Abdominal cancers Colorectal 1737 47.4 (45.8–49.1) 75 (73–77) Oesophageal 468 12.8 (11.7–13.9) 84 (80–87) Ovarian 267 7.3 (6.5–8.2) 70 (65–74) Pancreatic 214 5.8 (5.1–6.7) 59 (54–64) Stomach 189 5.2 (4.5–5.9) 65 (60–71) Prostate 110 3.0 (2.5–3.6) 5 (4–6) Renal 89 2.4 (2.0–3.0) 29 (24–34 Bladder 40 1.1 (0.8–1.5) 5 (4–7) Liver 38 1.0 (0.8–1.4) 44 (34–54) Small intestine 36 1.0 (0.7–1.4) 69 (56–80) Gallbladder 32 0.9 (0.6–1.2) 51 (39–63) Endometrial 24 0.7 (0.4–1.0) 6 (4–9) Sub-total 3244 88.6 (87.5–89.6) 41.0 (39.9–42.1) Other cancers Lung 91 2.5 (2.0–3.0) 5 (4–6) Oropharyngeal 20 0.5 (0.4–0.8) 10 (6–14) Breast 14 0.4 (0.2–0.6) 0.5 (0.3–0.9) Laryngeal 12 0.3 (0.2–0.6) 10 (6–17) Brain 10 0.3 (0.1–0.5) 5 (3–8) Cervical 10 0.3 (0.1–0.5) 8 (4–14) Sarcoma 10 0.3 (0.1–0.5) 10 (5–17) Testicular 5 0.1 (0.1–0.3) 3 (1–8) Melanoma 4 0.1 (0.04–0.3) 0.5 (0.2–1.3) Mesothelioma 4 0.1 (0.04–0.3) 6 (2–14) Thyroid 4 0.1 (0.04–0.3) 4 (2–10) c c c Sub-total 279 7.6 (6.8–8.5) 4.1 (3.6–4.6) Haematological cancers Lymphoma 97 2.6 (2.2–3.2) 15 (12–18) Leukaemia 25 0.7 (0.5–1.0) 7 (5–11) Myeloma 16 0.4 (0.3–0.7) 8 (5–13) Sub-total 138 3.8 (3.2–4.4) 11.5 (9.8–13.4) c c c Total 3661 100 23 Defined as cancers arising in the intra-abdominal organs, together with oesophageal and prostate cancer NB ordered by frequency among patients with abdominal symptoms. It is likely that a proportion of sarcomas and lymphomas were intra-abdominal but information regarding their exact location was not available. Includes 95 cases described as ‘Other’ cancers. low predictive value, there may be little to be gained by rais- anticipated range of affected cancer sites will be crucial for 31,32 ing its awareness amongst the general population. accurate assessment of the campaign’s impact. Previous evaluations have examined the increase in num- ber of ‘2-week wait’ referrals, the corresponding conversion Limitations of this study rates to cancer cases, and diagnostic activity. For cam- The study design enabled analysis of data on both the pre- paigns targeting groups of symptoms, understanding the senting symptoms and associated patient intervals among a Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 THE NATURE AND FREQUENCY OF ABDOMINAL SYMPTOMS IN CANCER PATIENTS e393 Our analysis focuses on the significance of abdominal symptoms among patients subsequently diagnosed with can- cer, and provides insight into how awareness campaigns may be evaluated. Nevertheless, it is clear that abdominal symp- toms in primary care may represent other important dis- 26,38 eases, such as inflammatory bowel disease. Coordinating our findings with evidence regarding the prevalence of abdominal symptoms among the general population, and the potential diagnostic experiences of patients that seek help for such symptoms beyond the cancer context may bring 39,40 further insight. We were unable to examine variation in patient interval by comorbidity status or deprivation: symp- tom appraisal and therefore the length of the patient inter- val, may be influenced by the presence of other conditions, and lower socioeconomic groups tend to experience lowest Fig. 2 The length of the patient interval by presenting abdominal symptom 41–43 symptom knowledge and longer time to presentation. (ordered by median interval; bar length = IQR, vertical line = median value). However, such associations, if present, are unlikely to sub- The dashed vertical line represents the median interval value across all stantially confound the observed variation by abdominal patients with abdominal symptoms (16 days). For corresponding values symptom, which is the main focus of our study. Finally, please see Supplementary Table S3 in the Supporting information. while our findings provide insight into the associations between symptoms and timeliness of help-seeking before large and representative cancer patient population in major population level campaigns were launched (in 2011), England. Our findings of symptom prevalence across a rep- further examination of these associations between symptoms resentative cohort of patients diagnosed with 1 of 28 cancer and timeliness of help-seeking in more recent cohorts will sites substantially augment previous evidence dominated by provide further insight. 25–27,30,34 cancer site-specific symptom studies. There are several limitations. Firstly, data on symptoms and Conclusions the patient interval used in our study is reliant on the infor- In conclusion, almost a quarter of all patients with cancer mation on presenting symptoms and their duration being initially present with an abdominal symptom, and their inter- accurately and completely declared or elicited during consult- val to presentation varies substantially by (abdominal) symp- ation, and recorded in the patient’s record. Nonetheless such tom type. The timeliness of presentation associated with approaches enable the profiling of large patient groups with- individual symptoms could inform the design of campaigns, 29,35 out potential concern about recall or survivorship bias. A while the cancer site case-mix of a particular symptomatic minority of patients with abdominal symptoms had missing presentation could be used to inform evaluation. outcome data regarding the patient interval, as noted in simi- 26,27,36,37 lar studies in this field. We restricted our analyses to eight abdominal symptoms Supplementary data based on those recommended for urgent referral in national Supplementary data are available at the Journal of Public clinical guidelines. This was a pragmatic decision that has Health online. face validity as symptom awareness campaigns are unlikely to include symptoms with a very low predictive value. We examined the patient interval among patients with a single Acknowledgements abdominal symptom for ease of interpretation, again because campaign messages have thus far focused on single We are grateful to all primary care professionals in partici- symptoms as opposed to synchronous symptom combina- pating practices for collecting, collating and submitting tions. Further, in sensitivity analyses considering the most anonymous data; and the respective former Cancer frequent symptom combination groups among nearly all Networks, the Royal College of General Practitioners, the cancer patients who presented with one or more abdominal former National Cancer Action Team and the National symptom, we found concordant findings (see Supplementary Cancer Registration and Analysis Service (formerly the Table S5 and S6). National Cancer Intelligence Network at the time of the Downloaded from https://academic.oup.com/jpubhealth/article/40/3/e388/4827055 by DeepDyve user on 20 July 2022 e394 JOURNAL OF PUBLIC HEALTH on sociodemographic inequalities in immediate key symptom aware- project) of Public Health England (PHE) for supporting the ness and GP attendances. Br J Cancer 2015;112:S14–21. National Audit of Cancer Diagnosis in Primary Care 2009-10. 8 Power E, Wardle J. Change in public awareness of symptoms and perceived barriers to seeing a doctor following Be Clear on Cancer Funding campaigns in England. Br J Cancer 2015;112(Suppl):S22–6. 9 Public Health England. Be Clear on Cancer. 2016. http://www.nhs. This work was supported by a grant from the UK uk/be-clear-on-cancer/. Department of Health [grant number no. 106/0001], as part 10 Public Health England. Be Clear on Cancer—Current Campaigns. 2016. of the programme of the Policy Research Unit in Cancer http://www.cancerresearchuk.org/health-professional/early-diagnosis- Awareness, Screening and Early Diagnosis. The Policy activities/be-clear-on-cancer. Research Unit in Cancer Awareness, Screening, and Early 11 NHS Scotland. Get Checked Early. 2012. http://www.getchecked Diagnosis is a collaboration between researchers from seven early.org/. institutions (Queen Mary University of London, University 12 Cancer Australia. Lung Cancer Awareness Month. Campaign. Events. College London, King’s College London, London School of 2013. https://canceraustralia.gov.au/healthy-living/campaigns-events/ lung-cancer-awareness-month. Hygiene and Tropical Medicine, Hull York Medical School, Durham University and Peninsula Medical School/ 13 Public Health England. Be Clear on Cancer—Abdominal Symptoms Campaign. 2016. http://www.cancerresearchuk.org/health-professional/ University of Exeter). G.L. is supported by a Cancer early-diagnosis-activities/be-clear-on-cancer/abdominal-symptoms- Research UK Advanced Clinician Scientist Fellowship [grant campaign. number: C18081/A18180]. The views expressed are those 14 Scott SE, Walter FM, Webster A et al. The model of pathways to of the authors and not necessarily those of the Department treatment: conceptualization and integration with existing theory. Br of Health or Cancer Research UK. 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Journal
Journal of Public Health – Oxford University Press
Published: Sep 1, 2018
Keywords: cancer; abdomen; help-seeking behavior; public health medicine