Clinician’s use of automated reports of estimated glomerular filtration rate: A qualitative study

Background There is a growing awareness in primary care of the importance of identifying patients with chronic kidney disease (CKD) so that they can receive appropriate clinical care; one method that has been widely embraced is the use of automated reporting of estimated glomerular filtration rate (eGFR) by clinical laboratories. We undertook a qualitative study to examine how clinicians use eGFR in clinical decision making, patient communication issues, barriers to use of eGFR, and suggestions to improve the clinical usefulness of eGFR reports. Methods Our study used qualitative methods with structured interviews among primary care clinicians including both physicians and allied health providers, recruited from Kaiser Permanente Northwest, a non-profit health maintenance organization. Results We found that clinicians generally held favorable views toward eGFR reporting but did not use eGFR to replace serum creatinine in their clinical decision-making. Clinicians used eGFR as a tool to help identify CKD, educate patients about their kidney function and make treatment decisions. Barriers noted by several clinicians included a desire for greater education regarding care for patients with CKD and tools to facilitate discussion of eGFR findings with patients. Conclusions The manner in which clinicians use eGFRs appears to be more complex than previously understood, and our study illustrates some of the efforts that might be usefully undertaken (e.g. specific clinician education) when encouraging further promulgation of eGFR reporting and usage.


Background
Pre-dialysis chronic kidney disease (CKD) is a common condition with an estimated prevalence of more than 13% of the US population [1]. But less than half of patients with CKD are unaware they have it [2] or don't carry a diagnosis in their medical record [3], suggesting low patient and provider awareness. Historically, serum creatinine has been the principal way of assessing kidney function. But serum creatinine is an imperfect method of identifying diminished kidney function. The use of a formula that includes serum creatinine age, sex, and race produces an estimate of the kidney's glomerular filtration rate (eGFR) which improves the diagnostic accuracy over serum creatinine alone. Recently, automated reporting of patients' eGFR by clinical laboratories has been promulgated as a method for increasing CKD awareness and, therefore, also improving appropriate treatment and follow-up. For example, automated reporting of eGFR by clinical laboratories has been encouraged to by the National Kidney Foundation [4] and National Kidney Disease Education Program [5] and is required by at least six states [6].
Using eGFR has its own disadvantages, such as underestimating renal function in healthy individuals, leading to increased false positive diagnoses [7]. Even so, a recent systematic review found that automated eGFR reporting was associated with changed care patterns, including increased nephrology referrals and consultations [8]. But as noted in that review it is unclear how eGFR reporting may have caused those changes.
Many factors likely influence how health care providers use laboratory tests. For example, a provider's knowledge of the patient's clinical situation, their reimbursement, and understanding of the sensitivity and specificity probably all influence how often a test is ordered and how it is interpreted and used clinically [9]. As a result, efforts to influence the laboratory ordering patterns of physicians have met with varying success [10,11]. Little is known about how clinicians (i.e. both physicians and allied health care providers) understand and respond to laboratory reports of renal function, or whether they respond to and interpret eGFR differently than serum creatinine. To help fill that gap we undertook a qualitative study using structured interviews to enhance our understanding of how primary care clinicians use eGFR in clinical decision making, patient communication issues, barriers to use of eGFR, and suggestions to improve the clinical usefulness of eGFR.

Study site and systems
The study was conducted in 2010 (April through June) at a nonprofit group-model health-maintenance organization (HMO), Kaiser Permanente Northwest (KPNW), in Washington and Oregon. The site has 15 medical centers and approximately 485,000 members. Electronic databases provided administrative and clinical data and a full electronic medical record (EMR) has been in place since 1996. The study was approved by the institutional review board at KPNW and clinician participants provided written informed consent.
The EMR and related systems used at KPNW contain several tools that clinicians can use to automate functions. Several of these automated tools were referred to by our participants so we give a brief description of them here. The Panel Support Tool (PST) is a 'dashboard' indicator of potential care gaps that are reported at the patient level. For example, it reports on the current status of testing and follow-up for patients with diabetes, cardiovascular disease, asthma and CKD, among other co-morbid conditions, and recommends treatment and testing strategies to close the care gaps. The EMR also allows the creation of 'dot phrases' that can be used, for example, to automatically populate text in clinical notes and in patient letters.

Estimated GFR (eGFR) reporting by laboratory
Our study was designed to take advantage of a systematic change at KPNW where all laboratory locations began automatically reporting eGFR routinely with serum creatinine in its laboratory results to clinicians. This reporting began on February 1, 2004. Prior to this, only the serum creatinine value was reported to clinicians on laboratory reports. The laboratory used the 4 variable version of the Modification in Diet and Renal Disease (MDRD) Study [12], which includes a binary variable for whether the patient is black. Because race data were not available, the laboratory reported eGFR values for both black and non-black routinely with each serum creatinine result. eGFR values above 60 ml/min/1.73 m 2 were reported at ">60". No further comments or information was provided.

Qualitative methods
Qualitative methods are effective strategies for documenting and analyzing unique, complex social phenomena, such as clinician experiences with a "newly" reported lab value [13][14][15]. Qualitative data, such as interviews, can reveal information unanticipated by researchers [16][17][18], and may be key to helping us understand how clinicians' are interacting with automatic reporting of the eGFR. Additionally, individual interviews are designed to elicit the participant's perspective and experience on a topic, and are therefore particularly useful in defining the range and variability of beliefs, behaviors, and experiences of study populations, as well as the natural language people use to discuss these issues [13,14,19]. To this end, primary care clinicians' experiences of the automatic laboratory reporting of the eGFR were captured and analyzed through a series of 30 minute, structured, open-ended face to face interviews.

Recruitment and study participants
We identified a list of 139 Family Practice (FP) or Internal Medicine (IM) based primary care providers (PCPs) who had been employed with KPNW from at least January 2002 to the present. This time frame was chosen so that clinicians could speak about their experiences of eGFR both before and after automatic reporting began in 2004. We included clinicians who were either physicians (MD) or allied health practitioners (NP or PA). We aimed to interview a minimum of 16 PCPs, a number we determined as sufficient for reaching redundancy of information and themes based on prior experience with qualitative methods and interviewing clinicians. Of these 16 clinicians, our goal was to interview 8 allied health practitioners (distributed equally between IM and FP), and 8 MDs (distributed equally between IM and FP). We also attempted to balance the participants geographically across the 13 clinics. Clinicians were recruited by email, sent by the Chief of Nephrology (coauthor MLT), inviting them to participate in a 30 minute structured interview. Lunch was provided to the participants. We completed 19 in-depth individual interviews with PCPs. Of these, 13 were MDs (8 IM, 5 FP) and 6 were allied health practitioners (2 IM, 4 FP). We sent 89 individual recruitment emails to reach this total, with 64 participants providing no response to the email and 6 participants indicating scheduling conflicts or lack of time as their reason for not participating.

Data collection and analysis
The research team developed a structured guide (based upon prior experience [16][17][18]20] and a literature review) which was refined following the first few interviews. With each participant we followed the interview guide, which consisted of 15 key questions and approximately 45 follow up prompts. The guide elicited information about clinicians' overall reaction to the automatic reporting of the eGFR, barriers and facilitators to the use of the eGFR, work practices related to the use of the eGFR, and overall advice on how to improve it. Interviews were conducted by a trained, third-party qualitative methodologist not known to the participants [co-author JS], audio-recorded, and professionally transcribed for analysis. Analysis was led by co-author JS with guidance and input from the research team. Analyses focused on representing, describing, and interpreting data, using standard techniques [15,19,21,22] and a qualitative research software package, ATLAS.ti 5.0 (Scientific Software Development, 1997) to code data and generate reports of coded text for analysis. We developed a coding dictionary based on the interview guide and review of the transcribed interviews. Transcribed interviews were coded by marking passages of text with phrases indicating content of the discussions. Using the report and query functions of Atlas.ti, coded text was further reviewed through an iterative process, resulting in refined themes [22,23].

Results
We interviewed 19 clinicians, 10 in the department of IM, 9 in the department of FP ( Table 1). Thirteen of the 19 were physicians, 2 nurse practitioners and 4 physician assistants. The average number of years that the clinician participants worked at KPNW was 16.3 years for physicians and 18.5 years for allied health practitioners. The average panel sizes (i.e. number of patients assigned to the clinician for health care management) were 1251 for the physicians and 1176 for the allied health practitioners. Eight clinicians worked full time and 11 part time. While our interviews occurred approximately 6 years after the 2004 initiation of automatic reporting of eGFR, participants had no trouble recalling when the shift to automatic reporting began, nor any hesitation describing their reaction, feelings, or impact on workload both at the onset of the reporting and over time.
Clinician use of eGFR: before and after automated reporting We asked clinicians about their use of eGFR prior to, and after, automated eGFR reporting was instituted. About half of the physicians said they had, at least sometimes, calculated eGFR before the implementation of automated reporting, while none of the allied health professionals did so. In fact, all the clinicians said they had primarily used serum creatinine as their gauge of kidney health before automated reporting ( Table 2).
When asked about whether their overall approach to CKD management had changed since automated eGFR reporting, more than half of the clinicians said that it had. However, a minority said their overall approach had not changed, and by clinician type, there seemed to be little difference in whether management of CKD had changed. We found that the majority of clinicians reported currently using both eGFR and serum creatinine in clinical decision-making. Only one clinician reported currently using serum creatinine more often than eGFR.

Benefits and challenges of automated eGFR
Clinicians' perceived benefits of automated eGFR included time savings, increased disease awareness and improved patient care. Clinicians mentioned that having the eGFR calculated saved them valuable clinic time because it streamlined their work and removed the need for calculating it themselves. For example an internal medicine clinician commented (Table 3): [Previously] I would very frequently have to look up their kidney function and actually calculate the GFR. . .So, definitely in an older population you encounter that often with certain medications. When automatic reporting came on, it was really helpful. I've never calculated it since then, and I said to myself, 'Oh, that's so going to save me time!'.
Clinicians also discussed being appreciative of the information, and wished they'd had the information earlier because there were patients in whom opportunities for clinical intervention were previously missed. They said eGFR, and the subsequent staging of CKD, gives them a better picture of renal health than they could get with serum creatinine alone. Clinicians mentioned that their awareness of CKD was greater with eGFR being   • now know about and can manage all the patients provider did not know about before automatic reporting began that have a "normal or slightly abnormal" creatinine and an abnormal eGFR Well, it' s made more awareness of chronic kidney disease. It' s sort of opened up a whole new [population] of chronic kidney disease patients. And it' s probably a more sensitive number to follow, rather than the creatinines. . .I can have a creatinine of 1.4 in one person, with a normal GFR, and a creatinine of .9 with an abnormal GFR -the GFR is simpler to pull. So ultimately I like it better. -FM PCP • identified a pool of patients on providers' panel with CKD status much worse than the creatinine value alone was indicatingwould not have "known" about these patients or referred on to Nephrology without automatic reporting Some of the patients who had a mildly abnormal creatinine I'm now finding have a much more reduced GFR, and that puts them in a higher stage of chronic kidney disease. And I am picking up a few of those that I wouldn't have known before and then referring them on. . .It' s just that it alerts me to the fact that their kidney disease is worse than I might have suspected just from the level of creatinine. • having the more sensitive value of the eGFR, along with creatinine, helps give gradation and refinement to patients' renal healthhelps provider determine "just how bad" a patient may or may not be • helps provider manage the Medicare refresh diagnosis process related to CKD status

Patient Confusion / Fear
Some patients were shockedthey were dismayed. They wanted to talk to me. I had some people who just couldn't understand, asking 'What' s wrong with my kidneys?'. . . FM NP • initially caused some otherwise healthy patients concern and upset regarding "suddenly" having a CKD diagnosis So, I think it caused distress and some fear because I never told them anything was wrong before, or I was waiting until their creatinine got high before I figured it out. -FM PCP • initially caused some otherwise healthy patients undue fear and stress regarding their kidney health and future possibility of dialysis It' s still a bit of an issue where there is that disconnect between some of the older patients who have a normal creatinine but their GFR is in the chronic kidney disease range. So it generated for some patients' questions, concern, alarm that I think wasn't really necessary. • generated more follow up and tracking work for providersanother condition to now follow and manage • extra time and workload for provider to create their own systems and processes for tracking, monitoring, and following up on patients eGFR values and renal health Initially I felt there was a little confusion to patients around giving the limits of normal GFR, so that the patient who was older could have a normal creatinine but an abnormal GFR, and the lab result would indicate chronic kidney disease. And it just added a little extra problem of something you either had to explain to the patient, or that they would ask questions about. . .I would usually then end up having to generate some sort of a letter explaining it, rather than just sending out a copy of the lab report, which made more work for me. -IM PCP • extra time and workload for provider to address patient fears and concerns regarding meaning of eGFR value and CKD stage/status (phone calls, creating patient letters) automatically reported. For example, before automated reporting some patients with a normal serum creatinine were missed as having CKD. They said like the reporting allowed them to identify those patients and take appropriate action like referral to nephrology. While it is recommended at KPNW that patients be referred to a nephrologist when their eGFR falls below 30, there are no barriers to referral at any level of kidney function. Clinicians reported improved patient management because it allowed them to assess and act on patient's renal health at earlier stages than with serum creatinine alone. Additionally they noted that the appropriateness of medication and medication dosing was improved. They also discussed organizational financial improvements related to more accurate diagnosis, specifically Medicare. Several concerns of eGFR reporting were also noted, including patient confusion and increased clinician workload. At KPNW it is common for patients to be sent a record of their laboratory values, including automated eGFR reporting. Especially in the initial phase of automated reporting, some patients 'suddenly' had kidney dysfunction, causing patient confusion and some anxiety over their health. For example, patients were confused about the new information including seeing two values of eGFR (one for black, and one for nonblack), and were also concerned about their risk of renal dialysis. Addressing these patient concerns translated into added workload for clinicians by necessitating phone calls and explanatory letters to be sent. The dual reporting of two values by race also caused a 'thinking' burden for clinicians since they were not able to simply examine the eGFR value without also determining the patient's race. Perhaps the most important burden perceived to clinician workload was that of adding another disease to manage, because eGFR reporting revealed a new and potentially quite large group of patients to manage. Allied Health providers reported being less likely to incorporate a diagnosis of CKD into the patient's health record, and some clinicians reported creating systems to monitor and track eGFR values for their patients. Table 4 illustrates work practices findings influenced by eGFR automated reporting, stratified by MD and allied health clinicians. Approximately half (53%) of the clinicians reported they increased the amount of patient education they provided following eGFR automated reporting. Allied health practitioners and family practice MDs were more likely to report this increase in patient counseling and education than internal medicine MDs. Additionally, 68% of the clinicians noted the onset of eGFR automated reporting created a need for designing and implementing additional follow-up communication strategies in the form of specialized letters and telephone 'talking points' for explaining eGFR results to their patients.

Changes in work practices related to CKD management
Most clinicians (74%) said that they had increased their overall referrals to Nephrology, but only very slightly. Four of the 13 physicians did not believe eGFR automated reporting had any impact on their referrals, as they still tended to manage and treat their patients up to a later CKD stage of 4 prior to referring. However, all the allied health practitioners reported a perceived increase in referrals, and allied health practitioners were more likely to refer at higher eGFRs (i.e. for less sick patients) than physicians. Physicians divided evenly between referring at late CKD stage 3b and 4, while most allied health reported referring to nephrology at earlier CKD stage 3a. Slightly less than half the clinicians (47%) reported ever referring to the HMO's 'kidney class' , a dietician-led class aimed at helping patients take a greater role in their kidney health; most clinicians said their referral pattern to this class did not change with eGFR reporting.

Suggestions to improve utilization of automated eGFR reporting in clinical practice
The clinicians we interviewed had several suggestions for improving the utilization of automated eGFR reporting, and for improving their overall CKD management. Ongoing clinician education, using a case-study approach, was noted as something they desired and suggested these trainings could be made available both in-person and online. They reported being especially interested in 1) why it is better to use eGFR (versus serum creatinine), 2) how eGFR should be used clinically at different CKD stages, and 3) best ways to communicate to patients about their eGFR at different CKD stages (Table 5).
Clinicians were also interested in hearing feedback, on an on-going basis, from nephrology on their actions related to CKD care. They particularly mentioned desiring feedback on timing of nephrology referrals, ordering of follow-up laboratory tests and the timing if these tests, and clinical care they should be providing both before and after nephrology referral.
Other specific types of needs identified were related to clinician tools and reminders. In the past, the HMO's department of nephrology supplied laminated 4″ × 6″ cards that summarized CKD guidelines and best practices. Several clinicians, particularly allied health practitioners, mentioned that they had found these helpful and would like them updated and made available. Clinicians also desired help with patient communication templates for both letters and telephone scripts that could be used by them and their medical assistants. They also mentioned it would be helpful to have reminders of where to access CKD guidelines and reminders of options for patient education such as the aforementioned kidney class.  When they get down to the twenties or especially below, then I usually will refer. Or if they may be Stage 3, but for some reason they seem to be dropping rapidly. • refer infrequently to occasionally 4 3 7 When people are anxious, I will refer to the class for reassurance purposes and education. But I don't send a high percentage of patients to that class, and I don't take advantage of that resource as often as I could.   Clinicians had several suggestions for the integration of the eGFR reporting into the EMR. Some of these suggestions had to do with reminders to obtain follow-up laboratory measures, perhaps incorporated into patients' diagnosis list, in the laboratory values reports, and in the section of the EMR that reports trended laboratory values. They also discussed the need to address the confusion over the eGFR report containing two values that depend on race. Clinicians also expressed a desire to see improvements in the ability of the EMR to facilitate appropriate laboratory orders and follow-up, for example through 'smart sets' that automatically allow a pended order for future laboratory kidney-related tests.
The clinicians we interviewed were also keen to see more patient related education tools, including handouts that explain kidney function, the meaning of eGFR and CKD staging. They said exam room posters of kidney function could facilitate communication with patients, and that the HMO's external website could be used to improve communication about kidney health.

Discussion
We found that clinicians were aware of eGFR reporting and generally held favorable views toward it, but also noted some barriers to its use. Perhaps the most interesting theme that emerged from our interviews was that eGFRs were not used to replace serum creatinines, but were used as an added source of information. Clinicians used eGFR as a tool to help: 1) identify CKD; 2) educate patients about their kidney function and; 3) make treatment decisions. The clinicians we interviewed suggested that the added gradation provided by eGFR allowed them to identify CKD at earlier stages than serum creatinine alone, but for most of the clinicians we interviewed the eGFR did not replace serum creatinine as an indication of later staged kidney disease.
It appears from clinician responses that serum creatinine is used as a means of validating eGFR measures. While this may seem redundant, it may be entirely appropriate. Though serum creatinine overestimates renal function when it is poor, eGFR underestimates renal function when it is normal [7,24]. A number of comments by the clinicians we interviewed highlight that concern. Undue stress and fear expressed by patients and the increased burden of tracking patients who may have normal kidney function seem likely to be the result of GFR underestimation. This finding may help confirm prior efforts to measure the cost/effectiveness ratio of eGFR reporting which have found that while eGFR may be beneficial to patients with CKD the benefit was offset by false positive diagnoses of CKD [25], At KPNW we have subsequently switched to the CKD-EPI formula which reduces the effect of underestimation of GFR at normal and near normal levels.
Reporting of eGFR has seemingly created a greater awareness of kidney dysfunction among the clinicians we interviewed. This is a significant finding because that enhanced awareness highlights shortcomings in clinician education; in fact, suggestions made by the clinicians we interviewed to improve utilization of eGFR value revolved primarily around clinician education. Interaction between nephrologists and primary care physicians would appear to play an important role in how eGFRs are utilized. KPNW has made efforts to educate primary care clinicians (CME conferences, written literature, guidelines embedded in the EMR), and the message from our study illustrate that ongoing educational efforts are important. It may also suggest that, because busy primary care clinicians can't always avail themselves of these opportunities, it is incumbent on the system to advertise the educational opportunities widely, on an ongoing basis, and offer several venues to accommodate varied learning and practice styles. The need for clinician education is likely to be greater in other medical systems that have not undertaken similar efforts.
Our study was qualitative, meaning it lacks the empiric information necessary to discern whether the responses represented the feelings of clinicians across the Kaiser Permanente system, or whether they can be extrapolated to other clinicians and medical systems. For example, our findings are specific to a health system with an extant, fully functioning EMR. Such a system may allow clinicians more immediate access to ancillary information (e.g. guidelines) about eGFR interpretation, perhaps easing the transition. The opinions expressed may have been different if the interviews were conducted by a different interviewer or if solicited by another means (i.e. a survey). Additionally, our modest number of interviews may yield less stable frequency estimates than if we had access to a larger sample. But strengths of our approach include the use of a pre-specified interview guide, use of trained interviewers, and interviewing to "saturation".

Conclusion
The manner in which clinicians use eGFRs appears to be more complex than previously understood, and our study illustrates some of the efforts that might be usefully undertaken (e.g. specific clinician education) when encouraging further promulgation of eGFR reporting and usage.