Delays in breast cancer care can result in patient dissatisfaction as well as increased risks of local recurrence and death.1–3 However, no studies have examined the full continuum of care, from presentation to imaging, to diagnosis, to surgery, to chemotherapy, to radiation therapy (RT). Some studies have examined the time to diagnosis of breast cancer, whereas others have focused on time from diagnosis to surgical treatment.2,4–8 Yet others have examined the interval from surgery to chemotherapy,9–13 or surgery to RT,1,14–16 and a few have examined combinations of these intervals.17–19 Our study examines the full continuum of care from presentation through adjuvant RT, as well as the smaller intervals in between.
Most studies of timeliness in breast cancer treatment have been conducted using large cancer registries in the United States,4–6,20–22 Canada,2,12,18 and Europe.23 A few timeliness studies have been performed at institutions with white majority populations.10,19,24 Two institutional studies have examined time to treatment in low-income populations.7,17 However, no studies have examined the full continuum of breast cancer care in an underserved setting. Given racial and ethnic disparities in breast cancer outcomes, it is important to understand processes of care for underserved and minority populations.17
This study examines the time intervals from presentation to imaging, diagnosis, to surgery, to chemotherapy, and to RT in a safety-net population with breast cancer. We examined the association between time intervals and socioeconomic factors such as language, ethnicity, and insurance. We also assessed the relationship between time intervals and patient medical factors such as disease stage, symptoms at presentation, and surgical management with lumpectomy or mastectomy.
Methods
Study Design and Setting
We conducted a retrospective cohort analysis of patients receiving breast cancer care at Denver Health and Hospital Authority (DH), which is an integrated, safety-net hospital system that serves Denver and the surrounding counties.
Study Sample
Our initial cohort consisted of all patients who received any care for breast cancer (N=120) from July 1, 2010, through June 30, 2012. Patients were identified by the hospital-based cancer registry. We excluded patients with primary stage IV disease or missing staging data (n=11) because they have a different treatment trajectory than those with stage 0–III disease. We also excluded patients with recurrent breast cancer within 5 years of primary diagnosis (n=2) because of the possibility that they were already under the care of an oncologist, and therefore their timeliness of care was not comparable to those who were newly diagnosed. An additional 2 patients who had both stage IV disease and recurrent cancer were excluded. The remaining 105 patients comprised our analytic study sample.
Data Collection
Data were abstracted from electronic health records and entered into a REDCap database. Date of diagnosis was considered the date of the diagnostic biopsy. Data elements included intervals between presentation to diagnosis, diagnosis to first treatment, last surgery to chemotherapy start, and last surgery to RT start. We also stratified specific steps within these larger intervals. In the interval from presentation to diagnosis, we measured the time from presentation to first imaging, first imaging to last imaging before diagnostic biopsy, and last imaging to diagnostic biopsy. In the interval from diagnosis to first treatment, we measured the time from diagnostic biopsy to the time when the patient was notified of their diagnosis, their first visit with an oncology clinic (either surgical or medical), and the time to first treatment. Date of first treatment was defined as either the date of the first surgery or the first date of neoadjuvant chemotherapy.
Data Analysis
We defined presentation as either symptomatic (ie, patient had a primary care or urgent care visit with specific breast complaints, such as mass, discharge, pain) or asymptomatic (ie, patient had an abnormal screening mammogram). If screening mammography was the method of presentation, the first image was defined as the date of presentation. Underinsured patients were defined as those with coverage through CICP (Colorado Indigent Care Program; a state-funded program) or DFAP (Denver Health Financial Assistance Program; a hospital-based charity program), or were self-pay. Timely treatment occurred at less than the median time, whereas delayed treatment occurred at or later than the median time. The limited number of patients in our study did not allow a more nuanced comparison of the fastest versus slowest quartile.
All calculated intervals were limited to events occurring at DH or at contracted neighboring hospitals for RT. As a safety-net hospital, patients may enter and exit the hospital system at all points, resulting in interrupted care. For example, a patient may come to DH after completion of diagnostic workup or may have the diagnostic biopsy performed at DH but then choose to go elsewhere for treatment.
We determined the median time for all intervals. We used logistic regression to calculate unadjusted odds of receiving timely treatment as a function of age, language, ethnicity, insurance, Charlson comorbidity index, disease stage, context of first presentation (screening mammography vs care provider), symptoms at presentation, and type of surgical treatment.
Results
A total of 62 patients (59.0%) were aged ≥55 years. Most patients were of Hispanic origin (43.8%), 80 (76.2%) spoke English, and 31 (29.5%) were underinsured. Of the 74 people who were insured, 32 (43.2%) were on Medicaid (Table 1).
Among patients who presented with breast cancer, underwent imaging, and were diagnosed at DH (n=97), the median time from presentation to diagnosis was 23 days (Figure 1). For most patients, screening mammography was the method of presentation
Patient Demographics
Among patients who were diagnosed and treated at DH (n=91), the median time from diagnosis to first treatment was 37 days (Figure 2). Once the patient underwent a diagnostic biopsy, it took a median of 8 days to notify them of the result and an additional 8 days to be seen in the surgical or medical oncology clinic. Once evaluated in the clinic, a median of 16 days was needed for the patient to undergo initial treatment. Most patients (n=88; 96.7%) received surgery as their first treatment, whereas 3 (3.3%) had chemotherapy.
Patients experienced different intervals between treatments depending on their treatment path. The average transition time from surgery to the medical oncology clinic was 13 days. Of the 84 patients who went on to visit the medical oncology clinic, 33 (39.3%) received chemotherapy. Median time from last surgery to chemotherapy initiation was 48 days. For patients needing surgery and RT only, without intervening chemotherapy (n=29), median time
from last surgery to first radiation treatment was 69 days (Table 2). For patients with an available date of radiation oncology referral (n=45), median time from referral to evaluation in the radiation oncology clinic was 22 days. For patients electing RT (n=53), median time from radiation oncology evaluation to first radiation treatment was 16 days.A number of patient characteristics were found to significantly impact a patient's odds of timely care. As Table 3 illustrates, patients with stage II or III breast cancer (odds ratio [OR], 2.32; 95% CI, 1.04–5.15) or who presented to a care provider (OR, 3.03; 95% CI, 1.33–6.89) were more likely to experience longer intervals between presentation and diagnosis. Patients who spoke English as their primary language (OR, 0.20; 95% CI, 0.07–0.61) experienced a
Intervals of Care
Discussion
In 2001, the Institute of Medicine identified timeliness of care as 1 of 6 measures of quality.25 Time to diagnosis and to treatment of breast cancer has become the subject of accreditation and quality control agencies, such the National Quality Measures for Breast Centers (NQMBC),26 ASCO, and NCCN.27 However there is no consensus on what time frame constitutes a delay.
Causes of longer intervals between diagnosis and treatment are clearly multifactorial; patient factors, symptomatology, treatment factors, and hospital system factors may all play a role. Our study found that patient factors such as being underinsured, Hispanic, and non–English-speaking all were associated with delays greater than the median time. This is similar to findings in the SEER population and the National Cancer Database, which showed that Hispanic and African American patients experienced diagnostic and treatment delays.4,6,9 Although our study found an unadjusted OR of 4.4 for underinsured patients experiencing delay to first treatment, a study from another safety-net hospital found that only African American race (OR, 2.7) was associated with treatment delay; however, this study did not specifically examine insurance status.28 A US comprehensive cancer center also found that women with ≥5 risk factors, including non-White or Hispanic race, breast symptoms, and far distance from cancer center, had a 12-fold risk of diagnostic delay.29
In our study, patients' disease stage, method of presentation, and symptomatology are likely related. Patients with later stage of disease (stage II or III) were more likely to experience delay in diagnosis. This is likely due to the fact that patients with later-stage disease often present to a provider with symptoms, who must then order imaging, rather than
Unadjusted Odds Ratio of Taking Longer Than the Median Time
This study highlights the need for hospital system process improvements. Part of the diagnostic delay may be the process of ordering and scheduling mammography after being seen by a provider. Arranging imaging may not occur while the patient is physically still in clinic, which could explain the delay. This initial delay also affects the time to first treatment. Patients who presented to a care provider had approximately 3 times the odds of taking longer than the median to start treatment. Development of standard care pathways through the emergency room, urgent care, and primary care could impact these delays. Additionally, nurse navigation programs, which have been shown to improve adherence to guideline-concordant breast cancer care in safety-net hospital systems,31 may also improve timeliness.
Process improvements in radiology may also be required. Approximately half of the patients needed additional imaging beyond initial studies, and these patients experienced delays between first and last imaging, with a median of 27 days for the complete radiologic evaluation prior to biopsy. The reasons for this could be multifactorial, and may include patient preference or limitations in radiologic scheduling. Further examination of imaging availability is warranted.
In the time from diagnostic biopsy to first treatment, the median of 8 days for the patient to be notified of the results plus an additional 8 days to be seen in an oncology clinic contributed significantly to the overall median 37 days to starting treatment. Process improvements in the radiology department and improved access to the oncology clinics could significantly reduce this delay.
Treatment factors can also affect timeliness. In our study, patients who underwent lumpectomy took longer to start their first treatment, potentially because of additional workup required to evaluate disease extent and to ensure that they were adequate candidates for lumpectomy. Although many would expect that patients undergoing mastectomy would have a longer time to first treatment, potentially due to more advanced disease that requires imaging for staging prior to surgery or due to patient preference for reconstruction, our study did not demonstrate this to be the case. Patients who underwent neoadjuvant therapy (n=3) did so to facilitate mastectomy rather than breast-conserving surgery. Treatment delays >12 weeks have been shown to have adverse survival outcomes compared with treatment within <4 weeks of diagnosis.32 Median time to first treatment in our cohort was 5.2 weeks.
The most apparent treatment delay attributed to our hospital system is the delay to RT treatment. With radiation oncology services contracted with neighboring hospitals, our patients have a median time of 69 days to starting RT after their last surgery when no other adjuvant chemotherapy was indicated. The process of external referral to radiation oncology adds significantly to the delay (median of 22 days from referral to being seen in radiation clinic), but does not explain all of the delay. Another potential source of delay is the fact that during the study time frame, radiation referral was not issued by surgeons in the postoperative period. Instead, patients were sent from surgeons to the medical oncology clinic, who would then issue radiation referral. This is particularly concerning because delays beyond 6 to 8 weeks have been associated with an increase in local recurrence rates, particularly for patients undergoing breast-conserving therapy.14,16,33 Other studies have shown that when radiation services are located farther away, patients are more likely to undergo mastectomy, suggesting that the distance to the radiation treatment facility could be a barrier to successful breast-conserving therapy.34 This finding clearly highlights the need for more timely referrals to radiation services and/or locating radiation services closer to the main campus of our hospital.
Our study has several limitations. It is a single-institution, retrospective study with a relatively small sample size, with data from 2010 to 2012. This initial study is the baseline for our current studies, which are continuing to examine the timeliness of more recent populations of patients. Additionally, as a quantitative study, we lack the informative details that a qualitative analysis can bring. Our future studies will need to incorporate key informant interviews to better understand why some populations experience delays. An additional limitation of our database is that we are unable to capture a physician's recommended treatment relative to whether the patient received it. For future studies, we would like to capture the provider recommendation as well as whether the patient was able to follow through with that recommendation. Lack of adherence to recommendations may also provide an important insight into delays experienced by our patients.
The strengths of our study include the safety-net hospital setting in which it was conducted. Funding at safety-net hospitals for breast cancer quality improvement efforts is limited, and therefore there are few published studies from safety-net systems. This study brings attention to vulnerable populations and sought to understand delays in their care so they are not further disadvantaged. This study also examined the entire continuum of breast cancer from presentation to RT as well as many smaller intervals within the continuum.
Conclusions
Our study has elucidated patient and system factors affecting the timeliness of care at a safety-net hospital. Programmatic changes that could enhance efficiency of obtaining imaging among symptomatic patients and accessibility to subsequent diagnostic imaging could improve time to diagnosis. Concentrating efforts on non–English-speaking, Hispanic patients and those who need RT could improve time to treatment.
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