Family Practice Advance Access published online on December 7, 2006
Family Practice, doi:10.1093/fampra/cml063
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Minimizing delays in ovarian cancer diagnosis: an expansion of Andersen's model of ‘total patient delay’
DIPEx, Department of Primary Health Care, University of Oxford, Old Road Campus, Oxford OX3 7LF, UK
Correspondence to Julie Evans. Email: julie.evans{at}dphpc.ox.ac.uk
Received 16 December 2005; Revised 27 June 2006; Accepted 25 October 2006.
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Abstract |
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Background. Ovarian cancer symptoms are vague and commonly occur in benign conditions; it often presents late and is diagnosed at an advanced stage when survival rates are poor. Studies of diagnostic delay in conditions with non-specific symptoms are rare.
Objectives. To study accounts of diagnostic delays in a sample of British women with ovarian cancer using Andersen's five-stage model of ‘total patient delay’ as an analytic framework.
Methods. Semi-structured interviews were conducted with 43 women. Maximum variation sample was recruited via GPs, clinicians, support organizations and personal contacts.
Results. Most women reported pre-diagnostic symptoms and diagnostic delays. Patient delays conformed to Andersen's first four types: ‘appraisal, illness, behavioural and scheduling' delays. ‘Treatment delays', attributable at least in part to a doctor or the health care system, were common and we have broken them down into five categories: non-investigation of symptoms, treatment for non-cancer causes, lack of follow-up, referral delays and system delays.
Conclusions. Our data illuminate the reasons why some British women experience delays in obtaining an ovarian cancer diagnosis. Delays attributable to the women were often compounded by doctor or health service delays, enabling us to expand the fifth stage of Andersen's model. Diagnostic delays in general practice could be minimized by better history taking, explaining the rationale for ruling out non-cancer causes, adopting an ‘open-door’ policy for patients whose symptoms persist, considering abdominal ultrasound scans and introducing educational sessions for GPs about ovarian cancer symptomatology.
Keywords. Early diagnosis, ovarian neoplasms, provider delay, qualitative research, signs and symptoms.
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Introduction |
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Ovarian cancer is the fourth commonest women's cancer in the UK, with 6800 new cases each year, mainly in post-menopausal women. It is difficult to diagnose, particularly in primary care—the symptoms are vague and less serious conditions also commonly cause them. Presentation and diagnosis are therefore often delayed until the cancer is advanced. Screening asymptomatic women by ultrasound and testing for the tumour marker CA125 can sometimes detect ovarian cancer earlier,1 but it is still uncertain whether these methods can detect the disease early enough to save lives.2 It is important to diagnose ovarian cancer as early as possible from symptom presentation because 5-year survival from early disease is much higher (73%) than that from metastatic disease (16%).3
Numerous surveys have identified pre-diagnostic symptoms of ovarian cancer, even in early disease.4 The symptoms are rarely gynaecological and include abdominal swelling, abdominal pain, digestive difficulties, altered bowel habits and urinary frequency or urgency. Compared with controls, women with ovarian cancer have been shown to experience a wider range of symptoms,5,6 of greater severity and frequency,7 although this knowledge may be of little practical help in making a differential diagnosis.
Qualitative research into pre-diagnostic symptom experiences has described diagnostic delays due to a lack of suspicion of malignancy.8,9 Studies of diagnostic delay in conditions with non-specific symptoms are rare. Andersen's model of ‘total patient delay’10 includes four stages of delay attributable to the patient and a fifth stage attributable to health care providers. Published studies using this model with diagnoses other than ovarian cancer have found that delays attributable to patients account for most of the total delay.11 However, a review of the literature on delay in diagnosing breast cancer concluded that provider delay is significant, underestimated and under-researched and needs documenting.12 A more recent study of six cancers, including breast and ovarian, found that patient and primary care delays were the most important contributors to total delay, although these components were not calculated separately.13
We have used accounts of provider delay from a sample of British women with ovarian cancer to enhance Andersen's model of total patient delay.10 We also suggest what GPs might do to minimize delays. We focus on the delays attributed at least in part to a doctor or the health care system because they have had less attention and were relatively common in our study.
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Methods |
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With multi-centre research ethics committee approval, we invited women throughout the UK to be interviewed about their experiences of ovarian cancer. An information pack was given to potential participants by GPs, clinicians, support organizations and personal contacts. The packs included a reply slip that interested parties could return direct to the researcher in a reply-paid envelope. The researcher telephoned the interested women and arranged the interview. Consent to be interviewed was sought at the time of the interview and further copyright was sought after participants had checked the transcript of their interview.
We chose a maximum variation sample14 to include women from various social backgrounds at different stages of treatment and short- and long-term follow-up, diagnosed at different ages and experiencing different outcomes. Interviewing was conducted throughout 2003 and continued until no new themes emerged from the data.15 Further analyses, clips from the interviews and more details about our research methods can be seen on the DIPEx website (www.dipex.org), a resource based on narrative interviews about people's experiences of health and illness.
We asked women to describe what had happened to them since they first suspected a problem. Supplementary questions were about their pre-diagnostic symptoms, including those that, with hindsight, might have been associated with their cancer. Two researchers (JE, SZ) read, reread and discussed interpretation of the data. With the help of N6 (qualitative data-indexing software), data from each interview were allocated to codes that reflected emergent themes, using the method of constant comparison.16 Each woman's account of her pre-diagnostic experience was also coded according to the types of delays in Andersen's model.10
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Findings |
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Characteristics of the sample are shown in Table 1. Most women reported pre-diagnostic symptoms (Table 2) and one or more delays in obtaining a diagnosis. Some delays were attributable to the women (Box 1) and these are consistent with Andersen's ‘appraisal, illness, behavioural and scheduling' delays and are not discussed further here. Instead, we focus on what Andersen calls ‘treatment delays', referring to the time between a patient first receiving medical attention and obtaining treatment. We have categorized these as follows: non-investigation of symptoms, treatment for non-cancer causes, lack of follow-up and referral and system delays. For most women in our study, treatment began before the definitive diagnosis was made since this was based upon pathology results from debulking surgery. Where the pathology was from biopsies, treatment began within days, so no delays occurred between diagnosis and treatment.
| BOX 1 Patient-attributable delays Misattribution of symptoms to stress or menopause. Misattribution of symptoms to previous benign conditions, e.g. bowel problems, IBS, pelvic inflammatory disease. Did not recognize symptoms as particularly serious, so self-treated or delayed seeing a doctor or proceeding with surgery.
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Non-investigation of symptoms
In accounts of their pre-diagnostic experiences, women described a range of symptoms, some not necessarily associated with their ovarian cancer. GPs therefore did not always investigate malignancy as a possible cause of all the reported symptoms. Any particular symptom could have been due to the subsequent diagnosis or to some other condition, especially if months or years had passed between symptom presentation and diagnosis. Nevertheless, some women reported symptoms which in retrospect they found significant but that their GP had not investigated. For example, a post-menopausal woman experienced period-type pains. Her GP examined her but found nothing wrong and advised her to return if the pains persisted. Another woman told her GP that something had popped inside her abdomen. The GP said it was probably a cyst that had burst, but did not investigate. A woman in her early 30s experienced night sweats for more than 3 years, which her GP attributed to hormonal problems but did not think of as possible malignancy. One woman had a suspected deep vein thrombosis and breathlessness.
I was on holiday in the Greek Islands on a cruise ship and I had a pain in my leg and my leg started swelling up. Being a nurse, I thought I'd had a DVT. I went to see the ship's doctor and he didn't speak any English, or hardly any English, asked me what I thought was wrong with me, I told him I thought I'd had a DVT and he agreed with me. I then left the ship, because I had to, and I was admitted to a private clinic in Corfu. They decided that they weren't sure if I'd had a DVT or not, so eventually flew me home, after a few days. And I got home and I was rather breathless, went to see my GP who said "no, you're not breathless, you're fine." (OV25: aged 61 at interview, diagnosed 2000)
Treatment for non-cancer causes
Women often said that GPs attributed their symptoms to a non-cancer cause and treated accordingly (Table 3). Not all of the symptoms may have been related to the ovarian cancer, some being due to a coexisting condition. Women were treated with antibiotics, painkillers, antacids, inhalers, laxatives, mebeverine, thyroxine and surgery (for varicose veins) and advised to do pelvic floor exercises. A woman who said she first felt ill 4 years ago described the following symptoms: persistent constipation, for which she eventually consulted her GP; tiredness, which led to blood tests and prescription of thyroxine; and urinary incontinence, for which pelvic floor exercises were recommended.
So I went away and managed these symptoms, although they were very unpleasant and the tiredness was getting worse. I resigned from my part-time job because I just couldn't be active for a whole day any longer, but I didn't think that there was anything seriously wrong with me until summer last year, when the constipation suddenly changed to uncontrollable diarrhoea and I became very bloated. I had an umbilical hernia, problems with breathing. I was just so tired that after the first few hours in the morning I could really do very little at all. And I went to my GP and I think she suspected irritable bowel syndrome so she gave me a medication called mebeverine which I was to take before meals which would slow down the diarrhoea. It didn't get any better and I was really feeling extremely unwell, I was absolutely enormous, I looked about seven months pregnant. I couldn't lay down in bed at night, and I went back to the GP again and she decided to refer me to the gastrointestinal unit, but she said I would have to wait some time because she didn't consider it was an urgent need, she thought it was just IBS. (OV43: aged 62 at interview, diagnosed 2002)
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A woman who was convinced there was something seriously wrong with her said she struggled to get that message across to her GP.
Well I was first diagnosed with ovarian cancer in June 2000. I'd known for a long time before there was something seriously wrong to the point that I was even drawing up a list of women and good friends who'd keep an eye on my daughter, but to get the doctor to understand how ill I was, was very, very difficult. There'd been a lot of things happening in my life at the time, obviously I'd had my daughter and my parents had died not long before, so what I knew I was very ill, I think they perceived as depression really.
So the Tuesday before I was finally diagnosed I'd been to the doctors, and all the doctor could do was turn round and say "Well you have put on a lot of weight, you have put on a lot of weight." And by this time I was swimming three kilometres a week, doing everything to try and lose weight, you know, I was running after a three year old, you know, I have a very supportive husband thank goodness, and I just could not make them understand how ill I felt. I mean it was silly things like I was bleeding after intercourse but because I was so ill I was forgetting the symptoms that I had. ... Anyway so, you know, I'd been to the doctors on the Tuesday and she put it down to oesophagitis, and I could not get her to understand that it was much more than that. I was so exhausted all the time, I was in so much pain. I remember I used to push my daughter's pram and suddenly would think I'm going to keel over with such an awful pain in my side. But this was all ignored or put to one side. (OV20: aged 41 at interview, diagnosed 2000)
She says that her illness affected her ability to recall all her symptoms, so she might not have given her GP the full story, and the GP might have acted reasonably given the information presented.
Lack of follow-up
Women whose symptoms persisted after being tested or treated for non-cancer causes did not always return to see their doctor, and doctors did not always establish whether the problem had resolved. For instance, a woman with a history of constipation was sent by her GP for a scan, with negative results. A year later, she consulted again with abdominal distension and weight gain, and a locum GP requested a second scan, revealing an ovarian cyst. Another woman who was sent for a scan with negative results delayed returning to her GP because she feared that her continuing symptoms might be blamed on the menopause.
Well I started to feel unwell in the middle of the year, last year. I had a pain just under my ribs on the left hand side and it gradually got worse and I went to the doctor's with this pain and the doctor was very sympathetic and [um] very good but he was totally convinced that I'd got gall stones. And so he was oh full of beans, "Oh well don't worry about it, just what my wife had", he said, "It's exactly the same symptoms, exactly the same everything and we'll get this sorted out, no problem". So that was fine. I then went for a scan and had the scan, that took a few weeks obviously to come through, so that was a little bit more time wasted, which I feel now, you know, I suppose a bit cross about I suppose. I had the scan and the scan was clear when it came back, which was I suppose quite a surprise really because he was so convinced that that was what was wrong with me. [pause] I then [er] left it I suppose 3 or 4 weeks I suppose because I thought, "Well if the scan's clear I obviously haven't got that", you know, and, "Am I, am I imagining all this?" And of course at my age, everything that's the matter with you, everybody always thinks it's about the menopause and it's, so you know, you know that every time you go to the doctor they're going to think that's what's the matter with you, if you say there's anything wrong with your stomach or your head or your, what you feel like. (OV42: aged 57 at interview, diagnosed 2003)
Other examples of missing follow-up included a woman in whom an antenatal scan found a cyst, which the obstetrician said would be investigated after the birth, but it was not; a woman had a small fibroid detected on an ultrasound scan while having a variety of diagnostic tests—it was apparently ignored; two women who presented at emergency departments, one because of severe abdominal pain and distension, the other abdominal pain and vomiting, were discharged after having tests; a woman who complained of breathlessness was referred to hospital, had fluid removed from her lungs and then sent home; a woman with indigestion, ‘bloating’ and appetite loss was referred for a barium enema that suggested diverticulitis, was put on a 6-week exclusion diet that had no effect on her symptoms, and she was not followed up.
Referral delays
Women presenting with gastrointestinal symptoms were often referred by their GPs to gastroenterology. Sometimes that led to ultrasound scans which revealed ovarian masses, and referral to gynaecology. However, a gastroenterologist diagnosed one woman as having diverticulitis and discharged her back to her GP. A second referral to gastroenterology resulted in an ultrasound scan and referral to gynaecology.
In the UK, people who are suspected of having cancer can now expect to see a specialist within 2 weeks.17 Many women in our study were diagnosed before 2000 when this policy was introduced, and had long waits for hospital appointments. Nevertheless, some women diagnosed more recently were not sent urgently to hospital for tests or a consultation, presumably because the GP did not suspect cancer or other serious condition. For instance, the woman whose GP gave her thyroxine, pelvic floor exercises and mebeverine before referring her to gastroenterology with suspected irritable bowel syndrome (IBS) (see OV43 quoted earlier) waited 6 weeks to see a gastroenterologist. Another woman waited over 6 months to see a gynaecologist after ovarian cysts were diagnosed on ultrasound scans that her GP requested. We do not know whether she told her GP about the long wait or whether the GP could have referred her earlier elsewhere.
So [um] I went, had a scan of my ovaries and when the lady was scanning it, she actually said to me, "Oh, your ovaries are enlarged [um] they're still [um] over stimulating and there's something there. I can see something" [um] because each time I did IVF, I did have a cyst on my ovaries and I had to try and get rid of the cyst each time. So I went back to my doctor and he said [um] "Oh we'll send you to a gynaecologist and find out". So I thought [um] he gave me an option of about three people to go and see. So I thought well I'd go and see the person who [um] first [um] did everything regarding my IVF. [um] Unfortunately [um] on the NHS, this was September, I had to wait three months but the doctor went away to India for three months, so it was [um] April before I got an appointment. So being busy at work I thought ‘well I'm, I'm very busy at work, [um] that's fine’. (OV07: aged 50 at interview, diagnosed 2000)
System delays
When GPs did refer women urgently to hospital, the specialist sometimes had a long waiting list for surgery. Women with cysts could wait several weeks but some were told that if their blood test showed elevated levels of the tumour marker CA125 their appointment would be brought forward.
Delays or concerns that their symptoms were not being taken seriously sometimes prompted women to use private health insurance. A woman with painful urination, abdominal pain and distension with weight gain was initially sent for a cervical smear test. This was followed by a urine test and prescription (at the woman's request) of antibiotics. When this did not improve her symptoms, she consulted a private gynaecologist who immediately did an ultrasound scan and diagnosed her cancer.
When I came back [from holiday] I thought "I've got to do something about this. This is really bad." At work I had knocked into the side of a desk and nearly, you know, it, the pain was so bad I thought, you know, something's very bad going on there and it doesn't matter how long you can spend on the Atkins Diet, I was losing no weight at all, in fact I was gaining. [um] So I [um] realised that I'd been paying a private medical insurance for quite a long time and I'd done nothing about it, so I investigated. Phoned up [um] a place in Harley Street who, described my symptoms over the phone and they told me to come in immediately. So I went in, I saw a, a female gynaecologist. She did a sort of ultrasound thing and, obviously, saw something straight away. (OV44: aged 48 at interview, diagnosed 2003)
Sometimes emergency treatment becomes necessary when symptoms worsen while a woman is waiting for a hospital appointment. A woman with tiredness and a palpable abdominal mass woke up one night in acute pain, 2 months into her wait to see a gynaecologist and was sent to the hospital as an emergency and had surgery to remove her ovaries and womb. Another, whose symptoms were constipation, abdominal distension, bloating and weight gain and who had a cyst detected on ultrasound, also experienced acute pain, leading to emergency surgery.
So eventually, she sent me for a scan in the February, and they discovered a cyst the size of about a pineapple on my right ovary, and the reason it hadn't shown up in examinations was, it was obviously behind the bowel, which was causing so many of the problems I was suffering. And ... erm ... that was on March 22nd, and I was due to go into hospital to have that removed, but before I could do that, which would have been about April, I think they said ... erm ... 25th March last year, I got terrible pains in my stomach at about half past seven in the evening, that lasted all through the night, I couldn't sit, stand or lie, I just didn't know what to do, and my husband kept wanting to ... [um] ... take me to hospital, and I said, "No, wait and see in the morning". But we went, as an emergency, in the end. He took me to Casualty. They checked me over, they sent me for another scan, and this time it had got as big as a football, so that was in the space of a month. So they said they had to operate that afternoon, and ... [um] ... which they did. (OV16: aged 52 at interview, diagnosed 2002)
A woman who reported period-type pains (post-menopausally) to her GP had emergency surgery to clear a blocked bowel after her pain worsened. A woman who was admitted as an emergency but discharged after various tests gave negative results continued to have abdominal pain and vomiting; her GP attended daily until she finally saw a consultant a month later.
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Discussion |
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TopAbstractIntroductionMethodsFindingsDiscussionDeclarationReferences |
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Principal findings
Our data illuminate the reasons why some British women experience delays in obtaining an ovarian cancer diagnosis. In addition to the types of delays attributable solely to patients (reported elsewhere with other patient groups),18 we have expanded Andersen's model to include further factors attributable at least in part to health care providers. Delays attributable to the women are often compounded by doctor or health service delays because ovarian cancer is so difficult to diagnose. Some women perceived that their GPs were not taking their symptoms seriously and felt frustrated by being treated for non-cancer causes. Follow-up after non-cancer treatments or negative diagnostic tests did not always happen especially if women felt reluctant to return to their GP too soon with the same symptoms. It often took a long time to reach the point where a doctor suspected cancer, so referrals to hospital or for surgery were rarely urgent.
Strengths and weaknesses of the study
Our data are drawn only from women who were diagnosed with ovarian cancer and we could not interview their GPs. More research is needed into GPs’ perspectives of women's symptom experiences, particularly where diagnostic delays were minimal or non-existent. In-depth interviews to explore women's experiences of ovarian cancer did not include the exhaustive detail about symptom experiences possible in more focused surveys. The data rely on women's recall of events and their accounts of the pre-diagnostic phase benefit from hindsight. What respondents say in such retrospective narrative interviews should be treated as accounts that serve several functions, including to present oneself as a competent member of the community, and may or may not accurately reflect what really happened.19,20 This qualitative study aimed for a maximum variation sample, not numerical representation. As such, we included women with a wide range of backgrounds and experiences, not just those who had particular concerns about diagnostic delays. We believe we have identified a wider range of diagnostic delays attributable at least in part to doctors or the health care system than have previous studies. These new insights suggest possible ways to minimize delays in diagnosing ovarian cancer in the absence of screening.
Meaning and implications
The vagueness and non-specificity of ovarian cancer symptoms challenge British GPs, who may see only one ovarian cancer patient in 5 years. Women may present with a variety of symptoms all of which could be caused by common benign conditions. Some may be related to non-malignant illnesses coexisting with the undiagnosed ovarian cancer, further confusing the situation. Furthermore, symptoms of illness may easily be misattributed in women of menopausal age because menopausal symptoms and those caused by illness can be difficult for doctors and women themselves to distinguish.
GPs’ ability to make a differential diagnosis also depends upon the quality of communication with the patient. Studies that compare patients’ accounts with GP data show that patients sometimes try to self-diagnose and may ‘select’ a subset of their symptoms to report to the GP (Bankhead C, personal communication). GPs may only note those symptoms they believe are salient at the time,4 thus further reducing the information available. GPs are also likely to re-label patients with pre-existing benign diagnoses rather than consider new explanations for persistent symptoms.12 Several women in our study who experienced gastric symptoms also reported a history of gastric problems or IBS . Their earlier gastric problems might actually have been symptoms of early ovarian cancer.
Where the symptoms do not immediately suggest a serious condition, it is reasonable to try to rule out non-cancer causes. Women whose GPs think the symptoms do not sound serious may welcome this reassurance and hesitate to return when symptoms persist because they fear learning that something is seriously wrong. Nevertheless, follow-up of patients treated for non-cancer conditions is vital to establish whether the treatment given has relieved the symptoms. Similarly, women whose symptoms persist despite negative diagnostic tests for other conditions need follow-up. UK government referral guidelines recommend that primary health care professionals should be ready to review their initial diagnosis in patients in whom common symptoms do not resolve as expected, and be alert to the possibility of cancer when patients thought not to have cancer fail to recover as expected.21 Active follow-up by GPs of all patients with uncertain diagnoses is unrealistic when National Health Service resources are stretched, but GPs can promote a more ‘open-door’ policy that encourages women to return if their symptoms persist. Women with persistent symptoms may be more likely to re-consult if the GP has explained their rationale for trying certain treatments or tests and encouraged them to make another appointment if symptoms persist or tests prove negative. Furthermore, setting a time limit should leave women in no doubt about how long they should leave their symptoms unchecked.
For many of the women we interviewed, an abdominal ultrasound scan revealed ovarian pathology. If GPs could arrange these scans as easily and quickly as blood tests they might be used more to investigate vague abdominal symptoms. However, UK government referral guidelines do not mention ultrasound scans.21 GPs have to act as gatekeepers to such diagnostic services, but may sometimes do so to the detriment of patients. Whether CA125 tests may be useful in primary health care is not clear. The results of a pilot study are awaited.22
Some authors have suggested that increasing knowledge of ovarian cancer symptoms among women might help to reduce delays in presentation,11,23 but this can also cause unnecessary anxiety. Others advocate better educating health professionals.5,8,9,24–27 UK government referral guidelines recommend educational interventions to improve primary health care professionals’ ability to detect cancer. They suggest training in consulting skills, workshops on features of cancer, educational outreach and computerized decision support.21
Conclusion and recommendations
The vagueness of the symptoms experienced by women with ovarian cancer in our study caused doctor delay as well as patient delay in diagnosis. Women's perspectives of provider delays in diagnosing ovarian cancer have enabled us to expand the fifth stage of Andersen's model of total patient delay into five categories: non-investigation of symptoms, treatment for non-cancer causes, lack of follow-up, referral delays and system delays. Further expansion of the model to elucidate treatment delays would require exploration of conditions where delays occur between diagnosis and treatment. Other authors have defined ‘patient and primary care’, ‘referral’ and ‘secondary care’ delays for the purposes of calculating their length.13 While our categories overlap with these, our qualitative approach provides greater insights into these delays, allowing us to further break down their separate components. Based on our findings, we recommend ways in which diagnostic delays in general practice could be reduced (see Box 2).
| BOX 2 Recommendations for reducing diagnostic delays in general practice.
More detailed history taking. Explain the rationale for trying to rule out non-cancer causes. Adopt an open-door policy for patients whose symptoms persist. Consider an abdominal ultrasound scan. Educational sessions for GPs about ovarian cancer symptoms.
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Declaration |
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Funding: This work was supported by Cancer Research UK (CUK) grant number C7663/A2903. The authors' work was independent of the funders.
Ethical approval: This study was approved by Eastern Multicentre Research Ethics Committee.
Conflicts of interest: None.
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Acknowledgments |
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We thank the women we interviewed and those who helped to find volunteers, particularly Ovacome; we also thank Clare Bankhead, Dr Peter Rose, Dr Andrea Pithers and Professor David Mant for their comments on an earlier draft of this paper. Contributors: JE interviewed the patients and analysed the data together with SZ. The ovarian cancer study is part of the DIPEx project. JE drafted the paper; all authors contributed to subsequent drafts and the final version.
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Notes |
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Evans J, Ziebland S and McPherson A. Minimizing delays in ovarian cancer diagnosis: an expansion of Andersen's model of ‘total patient delay’. Family Practice 2006; Pages 1–8 of 8.
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References |
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1 Jacobs I, Prys Davies A, Bridges J, et al. (1993) Prevalence screening for ovarian cancer in postmenopausal women by CA125 measurement and ultrasonography. Br Med J 306:1030–1034.
2 UKCTOCS Group. (2006) UK Collaborative Trial of Ovarian Cancer Screening. http://www.ukctocs.org.uk.
3 Bankhead C and Kehoe S. CancerStats: Ovarian Cancer—UK(Cancer Research UK, London).
4 Bankhead C, Kehoe S, Austoker J. (2005) Symptoms associated with diagnosis of ovarian cancer: a systematic review. BJOG 112:857–865.[CrossRef][Web of Science][Medline]
5 Vine MF, Calingaert B, Berchuck A, Schildkraut JM. (2003) Characterization of prediagnostic symptoms among primary epithelial ovarian cancer cases and controls. Gynecol Oncol 90:75–82.[CrossRef][Web of Science][Medline]
6 Olson SH, Mignone L, Nakraseive C, Caputo TA, Barakat RR, Harlap S. (2001) Symptoms of ovarian cancer. Obstet Gynecol 98:212–217.[CrossRef][Web of Science][Medline]
7 Goff BA, Mandel LS, Melancon CH, Muntz HG. (2004) Frequency of symptoms of ovarian cancer in women presenting to primary care clinics. JAMA 291:2705–2712.
8 Ferrell B, Smith S, Cullinane C, Melancon C. (2003) Symptom concerns of women with ovarian cancer. J Pain Symptom Manage 25:528–538.[CrossRef][Web of Science][Medline]
9 Fitch MI, Deane K, Howell D, Gray RE. (2002) Women's experiences with ovarian cancer: reflections on being diagnosed. Can Oncol Nurs J 12:152–168.[Medline]
10 Andersen BL, Cacioppo JT, Roberts DC. (1995) Delay in seeking a cancer diagnosis: delay stages and psychophysiological comparison processes. Br J Soc Psychol 34:33–52.
11 De Nooijer J, Lechner L, de Vries H. (2001) A qualitative study on detecting cancer symptoms and seeking medical help; an application of Andersen's model of total patient delay. Patient Educ Couns 42:145–157.[CrossRef][Web of Science][Medline]
12 Facione NC. (1993) Delay versus help seeking for breast cancer symptoms: a critical review of the literature on patient and provider delay. Soc Sci Med 36:1521–1534.[CrossRef][Web of Science][Medline]
13 Allgar VL and Neal RD. (2005) Delays in the diagnosis of six cancers: analysis of data from the National Survey of NHS Patients: Cancer. Br J Cancer 92:1959–1970.[CrossRef][Web of Science][Medline]
14 Coyne IT. (1997) Sampling in qualitative research. Purposeful and theoretical sampling; merging or clear boundaries? J Adv Nurs 26:623–630.[CrossRef][Web of Science][Medline]
15 Marshall MN. (1996) Sampling for qualitative research. Fam Pract 13:522–525.
16 Glaser BG and Strauss AL. (1967) The Discovery of Grounded Theory(Aldine, Chicago).
17 Department of Health. (1997) The New NHS—Modern, Dependable(The Stationery Office, London).
18 Smith LK, Pope C, Botha JL. (2005) Patients’ help-seeking experiences and delay in cancer presentation: a qualitative synthesis. Lancet 366:825–831.[CrossRef][Web of Science][Medline]
19 Murphy E, Dingwall R, Greatbatch D, Parker S, Watson P. (1998) Qualitative research methods in health technology assessment: a review of the literature. Health Technol Assess 2:1–274.[Medline]
20 Dixon-Woods M, Findlay M, Young B, Cox H, Heney D. (2001) Parents' accounts of obtaining a diagnosis of childhood cancer. Lancet 357:670–674.[CrossRef][Web of Science][Medline]
21 National Collaborating Centre for Primary Care. (2005) Referral Guidelines for Suspected Cancer. (National Institute for Clinical Excellence, London).
22 Menon U. Targeted Screening for Ovarian Cancer in Women over 50 Years of Age with Vague Presenting Symptoms, http://www.controlled-trials.com/isrctn/04011070/04011070.
23 Smith EM and Anderson B. (1985) The effects of symptoms and delay in seeking diagnosis on stage of disease at diagnosis among women with cancers of the ovary. Cancer 56:2727–2732.[CrossRef][Web of Science][Medline]
24 Flam F, Einhorn N, Sjovall K. (1988) Symptomatology of ovarian cancer. Eur J Obstet Gynecol Reprod Biol 27:53–57.[CrossRef][Web of Science][Medline]
25 Igoe BA. (1997) Symptoms attributed to ovarian cancer by women with the disease. Nurse Pract 22:122–144.[Medline]
26 Goff BA, Mandel L, Muntz HG, Melancon CH. (2000) Ovarian carcinoma diagnosis: results of a national ovarian cancer survey. Cancer 89:2068–2075.[CrossRef][Web of Science][Medline]
27 Koldjeski D, Kirkpatrick MK, Swanson M, Everett L, Brown S. (2003) Ovarian cancer: early symptoms patterns. Oncol Nursg Forum 30:927–933.
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