Abstract
Background/Purpose: Delay in diagnosis may affect the survival of breast cancer patients. The purpose of this study was to investigate delayed diagnosis in breast cancer under the National Health Insurance system in Taiwan.
Methods: This study was conducted via one-to-one interviews with structured questionnaires in hospital outpatient visit. Subjects of this study were 600 breast cancer patients seeking medical care in two medical centers in central Taiwan.
Results: Average delay in breast cancer diagnosis is 27.8 days. Service level of the patients’ first visit and number of hospitals patients visited before obtaining a correct diagnosis are significantly associated with delay in diagnosis. Logistic regression analysis found that patients who had visited two, and three or more hospitals before getting a correct diagnosis had longer delays in diagnosis than patients who had visited one hospital [odds ratio (OR) = 2.23, 95% confidence interval (CI):1.37-3.63; OR = 9.26, 95% CI:3.87-22.15, respectively]. Conclusion: Results of this study are anticipated to serve as a reference for the government and medical institutions to develop policies to reduce the number of hospitals visited before diagnosis for breast cancer patients, and ultimately to achieve the goal of early detection and treatment.
Key words: breast cancer; delayed diagnosis; hospital level; number of hospitals visited
Word Count: 3,485 (excluding abstract, references, acknowledgment, Conflict on interest statement)
Introduction
Breast cancer is the most prevalent cancer in women around the world, and it has had the leading incidence of cancer in Taiwanese females for 25 years.1 In 2008, breast cancer
was ranked among the four leading causes of cancer-attributable deaths. Incidence rate of breast cancer among women in Taiwan is approximately 56.07 per 100,000 females and mortality rate is 11.33 per 100,000 females.2 Breast cancer is also the leading cause of cancer
mortality for women in the United States and Canada.3 Previous studies showed that its
incidence rate in US was 124.3 per 100,000 and mortality rate was 23.0 per 100,000 females.4
The age at onset of Taiwan female breast cancer is between 45 and 59 years old,5 which is
almost 10 years younger than that in Western countries. This indicates an early-onset trend in Taiwanese women.6,7
Survival rate of breast cancer patients depends greatly on the cancer stage; the earlier the cancer is detected and treated, the better the prognosis and the higher the survival rate.8-10
Since 2004, the Department of Health has provided free breast mammograms once every two years for women aged between 50 and 69 years old, but only 12 % of all eligible women take advantage of this screening service.6 In comparison with other developed countries,
Taiwanese women have lower awareness of the danger of breast cancer;6 approximately 85 to
96 % of patients discovered the symptoms for breast cancer by themselves, not via breast screening.11-14 Furthermore, if the patients do not seek medical treatment promptly after the
symptoms are discovered, the clinical stage of breast cancer advances and their survival rate drops as the delay is prolonged.12,14,15
Presently, the international definition of “delay” is not consistent; Unger-Saldana (2009) divides total delay into two categories16: (1) delay by patients, which indicates the time from
the patients first discovery of the symptoms to the time the patients pay their first visit to the doctor; (2) delay by providers, which can be further divided into delay in diagnosis and delay
in treatment. Smith et al (2008) defined diagnosis delay as the time between the first examination and the abnormality being found by CBE (clinical breast exam) or a mammogram and the diagnosis of breast cancer.17 Delay in diagnosis signifies the time
between the first doctor visit and the time breast cancer is confirmed by the doctor.16,18-21
Caplan et al. (1996) found that there is a delay of approximately 81 days from the patients’ first visit to the doctor, to the time of correct diagnosis;19 Norsati et al (2000) defined system
delay as the time between first medical consultation and first clinic visit, with a mean of 44.8 days and a median of 18 days,22 while Allgar and Neal (2005) found that from the breast
cancer patients’ first visit to the general practice to the time of correct diagnosis, the delay is approximately 27 days.23
Lin (2001) from Taiwan discovered that the delay in diagnosis of breast cancer is approximately 92 days on average, and for 35.0% of breast cancer patients the delay is greater than 60 days.13 Wang and Hou (1993) found that although 32.4% of women seek
medical attention within one week of discovering an abnormality in the breasts, 45% of women delay seeking medical attention for more than three months.14 Chen (2009) have
studied changes of the social and psychological well-being of breast cancer patients with and without delay in medical seeking and diagnosis, and found that the average delay from presenting symptoms to the diagnosis is 187 days24 from the discovery of suspicious
symptoms in patients, to the time of confirmed diagnosis. Literature indicates that age, socioeconomic status, and marital status are potential factors associated with delay in diagnosis in women diagnosed with breast cancer.18,19,25-27
Taiwan has adopted a single-payer, universal health care system, the National Health Insurance (NHI), of which the coverage rate currently exceeds 99%.28 Using this healthcare
system, people can freely access any level of health care institutions, from primary clinics, district hospitals, and regional hospitals to medical centers. No restriction is placed on the
frequency or level of care a patient wishes to receive. Treatments for severe diseases, such as breast cancer, and services used in the pre-diagnosis stage are mostly covered by the NHI, but only medical institutions and regional hospital of sufficient magnitude can provide such advanced technology such as tumor imaging. A literature review on diagnosis delay found that most studies are concerned with the delays caused by the referral system between general practices and hospitals.23,26 But contrarily, due to the implementation of the NHI system, the
medical environment allows patients in Taiwan high accessibility to medical care, and people have the freedom to choose their preferred hospitals. Thus, long delays caused by general practices or referral processes are not expected in Taiwan.
Although previous research has examined various aspects of delay in diagnosis, most have focused on the influence of the primary physician and health care system referral systems.23 The system in Taiwan, however, differs from those of other countries in that
insurance beneficiaries have the freedom of choice in seeking medical assistance. This difference in procedure among insurance providers is worth investigating to understand the particular delays in diagnosing breast cancer under the NHI system in Taiwan, to identify the factors associated with such delays, and to predict the crucial factors influencing the delay in diagnosis of breast cancer.
Methods Subjects
Research subjects were breast cancer patients cared at two medical centers in central Taiwan. Face-to-face interviews were conducted in clinics during July 26th 2007 and July 31st
2008 with structured questionnaires; 615 questionnaires were completed and returned, 600 of which were effective.
Data collection
This study was carried out using a structured questionnaire survey. The survey contents included basic personal information (age, educational level, marital status, occupation, and economic status), factors delaying the diagnosis (level of the hospital first visited, number of hospitals the patients visited before breast cancer diagnosis, items inspected on the first visit), and number of days of delayed diagnosis (defined as time elapsed between the first visit for breast cancer-related symptoms and the time of diagnosis).9,12-16 At the time of survey, these
patients had either completed or were undergoing cancer treatments. The number of days of delay in diagnosis was reported by the patients from memory. Consent was obtained from all participants included in the study.
The questionnaire was designed and developed cooperatively, and its validity was evaluated by five medical experts specializing in breast cancer. This study plan was validated by the Institute Review of Board of China Medical University Hospital (DMR96-IRB-78)
The four hospital levels were categorized according to the NHI’s classification of medical institutions by their accreditation criteria. We believe that this parameter reflects patients’ preference and their healthcare seeking behavior under universal coverage. The type of examination at the initial visit of patients would indicate if relative advancement in medical technology on the provider side effectively reduces delay in diagnosis.
Data analyses first used descriptive statistics to measure frequency distributions of the participants by socio-demographic status and diagnosis delay factors (hospital level the patient first visited, number of hospitals visited before diagnosis, and items examined in the first visit). Mean days taken to have the breast cancer diagnosed were also measure by the same variables. We used t-test and one-way analysis of variance (ANOVA) to examine differences in mean days taken to have the final diagnosis between groups. The distribution of days required to have breast cancer diagnosed in this group of patients shows that approximately half of study subjects had their breast cancer diagnosed no more than 7 days. We further divided days taken for the final diagnosis into two groups (≤ 7 days vs. > 7days). Logistic regression analysis was used to investigate factors that may have association with the earlier diagnosis of the disease. All statistical analyses were performed using SAS software, version 9.2 (SAS Institute Inc., Cary, NC, U.S.A.).
Results
Of the 600 breast cancer patients recruited for this study, their average age when the symptoms were discovered was 48.1 years old, with 36.4% patients under 44 years old. Most 76.5% of the patients were married, 42.2% had only secondary education, and 27.9% had an average monthly household income between 25,001 and 45,000 Taiwan Dollars (TWD) (Table 1). More than half (55.2%) of breast cancer patients made their first hospitals visits at medical centers, followed by regional hospitals (20.8%). Most of the subjects (61.0%) visited only one hospital and 30.4% visited two hospitals before diagnoses were given. In the first clinical visit, 63.9% subjects received a mammogram and 73.1% subjects received a breast ultrasound. Diagnoses also used the magnetic resonance imaging (MRI) scan for 21 women, and both breast ultrasound and mammogram for 316 women in the first visit. The average delay in diagnosis was approximately 27.8 days: 302 (67.3%) subjects had the disease diagnosed in less than 7 days, and 43 (9.6%) subjects experienced a delay of more than one month (Table 1).
Table 2 shows mean days it took for women had breast cancer diagnosed by socio-demographic status and health care characteristics. Mean diagnoses days were not significantly different measured by the socio-demographic status. However, it took more days for younger patients to have the disease diagnosed, 37.7 days for those in the age of less than 44 years of age. Women divorced or separated were at higher risk of delay (66.7 days). Average income was less likely associated with delayed diagnosis.
Table 2 also shows that women cared at medical centers had the breast cancer diagnosed in a shortest mean period of 19.2 days, 57.2 days shorter than days required at community clinics (p< 0.001). Number of hospitals visited was also associated with the delay of disease diagnosis. It took 10-fold more days to have the breast cancer diagnosed for women visiting 3 hospitals compared with women visiting only 1 hospital (147.4 vs. 14.3 days in average)
(p<0.001). Women received the MRI examination also had the disease diagnosed much earlier compared with those without the test (8.4 vs. 28.9 days in average).
Table 3 shows that approximately half of the patients had the breast cancer diagnosed as early as 7 days or earlier. Diagnosis taking longer than 7 days was not significantly associated with the socio-demographic status. Among the diagnosis-related health care factors, only number of hospital patient visited was significantly associated with the earlier diagnosis of the cancer. Compared with women cared by one hospital, those who visited 2 hospitals had an odds ratio (OR) of 2.23 (95% CI: 1.37-3.63) to have the disease diagnosed longer than 7 days. The OR increased to 9.26 (95% CI: 3.87-22.15) for patients had visited 3 hospital.
Discussion
Breast cancer occurs in Taiwanese women mostly between 45 and 59 years of age, approximately 10 years younger than European and American women.5,13,14,24,29 This study
finds that approximately 60.0 % of breast cancer patients in Taiwan are under 49 years old, suggesting that the age of Taiwanese women afflicted with breast cancer is declining.5
Moreover, while approximately 85 to 96 % of Taiwanese breast cancer patients discover the symptoms by themselves, most breast cancer patients do not have the habit of performing breast self-examination or any other breast cancer screening before being diagnosed with breast cancer.11,13,14 It can be seen from the outcomes of our study that women in Taiwan have
insufficient knowledge and awareness in breast cancer prevention.6,30 Therefore, the
importance of practicing regular breast self-examinations and screening should be emphasized in young women when implementing preventive medical policies, both at service or government level.
This study finds that of the patient characteristics, age, educational level, marital status, and average monthly household income do not have a significant statistical correlation with delay in diagnosis. However, similar to the studies of Neal and Allgar (2005), Barber et al. (2004), and Ramirez et al. (1990), this study observes that delay in diagnosis is longest (38 days) in breast cancer patients less than 44 years old and 60% of the breast cancer patients are less than 49 years old.18,26,27 For those that are not yet married and assume multiple roles, Chie
and Chang (1994) also indicate in their study that the general opinion holds that younger population is less likely to have cancer and does not have regular breast self-examination.11 In
addition, patients in Taiwan prefer to seek treatment from well-known doctors and would rather be put on waiting list just to be examined or treated by these physicians. As a result, it is likely that patients are too late to start process of diagnosis and treatment. Caplan et al. (1996), on the other hand, find that patients experience longer delays because most tend to
believe their conditions are not serious.19
In comparison with single women, divorced or separated women have a longer delay in diagnosis of approximately 36 days. The divorce rate increases gradually year after year in modern Taiwanese society, with an increase of 10.0 % since 2000 - the divorce rate was 11.45% in 2010 (58,037 couples in total).31 Neal and Allgar (2005) point out that single,
separated or divorced women are more likely to experience delays in diagnosis as compared to married women.26 It has been argued that divorced and separated women have extensive
socio-economic burden and family responsibilities which consequently leads to a delay in diagnosis after acknowledging symptoms of breast cancer. One other potential factor is that women who have spouses are likely to discover abnormalities on the breast through their spouses. In addition, their spouses can support them in seeking medical help promptly, and thus shorten the delay in diagnosis. Thus, divorced women should be a group to which government related organizations must pay more attention, particularly in regards to their health condition.
Low socioeconomic status is one of the factors for delay in diagnosis.25,26 However,
results of this study show that the average monthly household income has no significant correlation with delay in diagnosis. This discrepancy from other studies may be due to the different health systems between Taiwan, Europe, and the United States. Caplan et al. (1995) finds no significant correlation between income and delay in diagnosis in breast cancer patients, but Caucasian women who participate in Medicaid are more likely to experience a delay in diagnosis, as compared to those having both Medicaid and private insurance.25
Despite the free services at point of use, the referral system in the United Kingdom is stringent. Patients must consult general practitioners first, and are only referred to hospitals for further examination and treatment when necessary. Therefore, waiting in line for medical attention, and delays in diagnosis and treatment may occur. However, people with better
economic status would purchase private insurance to avoid having to wait in line to get further treatment. Since the implementation of Taiwan’s NHI in 1995, the coverage rate in 2010 reached 99.43% (approximately 23.03 million people), the accessibility of medical care for the Taiwanese is high; and people are free to choose preferred hospitals for treatment.6
Thus, we believe that socioeconomic status is unlikely to be the factor for delay in diagnosis for patients.
Results of this study indicate a significant difference between the level of the hospital first visited and days delayed in diagnosis (p= 0.005): the lower the hospital level of the first visit, the longer the delay in diagnosis. If patients visit a local clinic first, they may be transferred to larger hospitals for further examination, diagnosis, and treatment. This transfer from small to large hospitals would prolong the diagnosis process. Average delay in diagnosis for breast cancer is approximately 28 days in this study, but the study of Lin (2001) finds that the delay in diagnosis is 92 days on average.13 Length of delay in diagnosis has
been reduced significantly since Lin’s study; which might be a result of the launch of the policy of “free mammogram once every two years for women aged between 50 and 69” by the government in 2004, and the corresponding emphasis of breast cancer diagnosis quality by hospitals. It could also be the outcome of the government’s active promotion of preventive medical policy. But generally, in Taiwan, it takes about 2 to 10 days from organizing a breast cancer examination to obtain a confirmed diagnosis by a pathology report, and this can be a key factor for generating a delay in diagnosis. Because of the health insurance system in Taiwan, patients have high accessibility to medical care, and is free of the referral processes as seen in the European and American countries. The length of delay in diagnosis (28 days) in breast cancer patients, however, is still similar to the 27-day delay reported in Allgar and Neal’s (2005) study in regards to breast cancer patients in England’s health system with referral system.23 Therefore, medical institutes should carefully review and improve the
internal procedures in regards to examination arrangements, and report waiting time to shorten the diagnosis time for breast cancer patients.
Caplan et al. (1996) take American women as their study subjects, and find that the average delay in diagnosis is 81 days.19 Because the U.S. strictly implements the referral
system, the diagnoses are often delayed for many patients during the referral process. In contrast, Taiwanese have high accessibility to medical care, and thus experience shorter delays in diagnosis. Also, Taiwanese patients tend to seek medical attention in large hospitals if an abnormality is suspected;32 more than half of the patients in this study chose medical
centers as their first hospitals. In addition, the results of this study indicate that delays in diagnosis for patients who visit more than 3 hospitals before confirmed diagnosis are approximately 133 days longer than for patients who visit only one hospital, and patients who had three or more hospitals before getting a correct diagnosis had longer delays in diagnosis than patients who had visited one hospital (OR = 9.63, 95% CI: 3.99-23.27). This result verifies the assumption that the fewer the hospitals visited before a correct diagnosis, the shorter the delay.
For the examination items received in the first visit to the hospital, only MRI has a significant association with delay in diagnosis (p< 0.001). Patients who received MRI had shorter delays in diagnosis. But the cost for MRI is higher, therefore, a breast ultrasound is often performed as an initial screening at the initial stage of detecting abnormalities in the breasts, and a mammogram would be performed later if necessary.13
Overall, the NHI system reduces the economic barriers to seeing doctors, and increases access to medical services across populations in Taiwan. Therefore, the length of delay in diagnosis for breast cancer is shorter in comparison to European countries and to the United States. Positive outcomes in some of the preventive health care of NHI are also illustrated. This study also finds that the higher the level of the hospital first visited, the shorter the delay
in diagnosis, and the more hospitals visited before a breast cancer diagnosis, the longer the delay in diagnosis. Therefore, this study suggests that when a clinic or small hospital discovers that a patient is suspicious of having the symptoms of breast cancer, the hospital should take the initiative of transferring the patient to a larger hospital for further examination. This would prevent the repetitive use of medical services and subsequently shorten the delay in diagnosis.
Although the subjects of this study were confirmed breast cancer patients in two medical centers in central Taiwan, because of convenient transportation, it takes only one hour from central Taiwan to reach northern or southern Taiwan. As a consequence, these two medical centers also include patients from northern and southern Taiwan, and therefore, the sample selection bias is minimal. Finally, for the administering of questionnaire for this study, patients were asked to fill out the length of delay of their diagnosis from memory that may pose recall bias on the collected data despite precautions adopted by conducting the interviews with breast cancer patients during or right after treatment. However, the four interviewers of this study have more than three years of clinical experience and have received interview training, and should be able to ensure consistency in the data collected.
Findings of this study would help the Bureau of National Health Insurance to better understand the conditions of delay in the diagnosis of breast cancer in Taiwan, to serve as a reference for developing breast cancer prevention policies, to educate and remind the population of the importance of earlier detection and earlier treatment, to encourage medical systems to pay attention to the timeliness of breast cancer diagnosis, and to improve the quality of Taiwan’s breast cancer medical treatment. Besides investigating the causes of the low breast cancer screening ratio among the public, the government should also clarify whether conducting breast cancer screenings has any effect on diagnosis delays. This study can also provide information related to delays in the diagnosis of breast cancer in Taiwan for
international comparison and reference.
Conflict on interest statement
There are no potential conflicts of interest for any of the authors. All authors have no reportable conflicts.
Acknowledgement
This study is supported by grants of commissioned research projects “101 Building cancer research excellence system project” (DOH101-TD-C-111-005) of the Department of Health, Executive Yuan.
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