Identification and Referral of Patients With Progressive CKD: A National Study

Identification and Referral of Patients With Progressive CKD: A National Study

Identification and Referral of Patients With Progressive CKD: A National Study L. Ebony Boulware, MD, MPH, Misty U. Troll, MPH, Bernard G. Jaar, MD, M...

209KB Sizes 0 Downloads 36 Views

Identification and Referral of Patients With Progressive CKD: A National Study L. Ebony Boulware, MD, MPH, Misty U. Troll, MPH, Bernard G. Jaar, MD, MPH, Donna I. Myers, MD, and Neil R. Powe, MD, MPH, MBA ● Background: It is unclear whether primary care physicians (PCPs) and nephrologists differ in their recognition of progressive chronic kidney disease (CKD), agree on diagnostic and referral strategies, and identify similar barriers to caring for patients. Methods: We conducted a national study of PCPs and nephrologists in the United States through a questionnaire describing a PCP caring for a patient with progressing CKD and questions to assess recognition of kidney dysfunction and approaches to diagnostic evaluation and referral. We identified participant and patient characteristics independently associated with CKD recognition and referral. Results: We randomly identified a national sample of 304 physicians (126 nephrologists [39% response rate], 89 family physicians [28% response rate], and 89 general internists [28% response rate]). PCPs recognized CKD less (adjusted percentage, 59%; 95% confidence interval [CI], 47 to 69, family physicians; adjusted percentage, 78%; 95% CI, 67 to 86, general internists; adjusted percentage, 97%; 95% CI, 93 to 99, nephrologists; P < 0.01), differed from nephrologists in their recommendations for diagnostic testing, and recommended referral less (adjusted percentage, 76%; 95% CI, 65 to 84, family physicians; adjusted percentage, 81%; 95% CI, 70 to 89, general internists; adjusted percentage, 99%; 95% CI, 95 to 100, nephrologists; P < 0.01). PCPs differed from nephrologists in their expected intensity of specialists’ involvement in care (16%, family physicians; 20%, general internists; 6%, nephrologists recommending nephrologist input monthly to every 6 months; P ⴝ 0.01). Lack of awareness of clinical practice guidelines and lack of clinical and administrative resources were identified as important barriers to care. Conclusion: PCPs recognize and recommend specialist care for progressive CKD less than nephrologists and differ in their clinical evaluations and expectations for referral. Improved dissemination of existing guidelines and targeted education in conjunction with efforts to build consensus among PCPs and nephrologists regarding their roles in the care of patients with CKD, including the collaborative development of clinical practice guidelines, could enhance patient care. Am J Kidney Dis 48:192-204. © 2006 by the National Kidney Foundation, Inc. INDEX WORDS: Chronic kidney disease (CKD); guidelines; barriers.

C

HRONIC KIDNEY DISEASE (CKD) is a growing epidemic, with at least 10 million persons with kidney damage.1 Persons with modFrom the Department of Medicine, Division of General Internal Medicine, and Department of Medicine, Division of Nephrology, Johns Hopkins School of Medicine; Department of Epidemiology, Johns Hopkins Bloomberg School of Public Health; Nephrology Center of Maryland; and Welch Center for Prevention, Epidemiology and Clinical Research, Johns Hopkins Medical Institutions, Baltimore, MD. Received March 10, 2006; accepted in revised form April 20, 2006. Originally published online as doi:10.1053/j.ajkd.2006.04.073 on June 14, 2006. Support: Funding sources are National Kidney Foundation of Maryland Mini-Grant (L.E.B.); Robert Wood Johnson Harold Amos Faculty Development Program (L.E.B.); Grant no. K240502643 from National Institute of Diabetes and Digestive and Kidney Diseases (N.R.P.). Potential conflicts of interest: None. Address reprint requests to L. Ebony Boulware, MD, MPH, Assistant Professor of Medicine and Epidemiology, Welch Center for Prevention, Epidemiology and Clinical Research, Division of General Internal Medicine, Johns Hopkins Medical Institutions, 2024 E Monument St, Ste 2-600, Baltimore, MD 21205. E-mail: [email protected] © 2006 by the National Kidney Foundation, Inc. 0272-6386/06/4802-0002$32.00/0 doi:10.1053/j.ajkd.2006.04.073 192

erately advanced CKD (glomerular filtration rate [GFR] ⬍ 60 mL/min/1.73 m2 [⬍1.0 mL/s]), particularly those with hypertension or diabetes and persistent proteinuria, have substantially increased risks for progression toward end-stage renal disease, hospitalization, cardiovascular disease events, heart failure, and death.2-9 Institution of appropriate therapies for patients with progressive CKD and early referral of patients to nephrologists for evaluation and kidney disease management are associated with improved quality of care and outcomes.5,6,10-14 Although early referral of patients is optimal, it is widely recognized that given the relatively small number of practicing nephrologists nationwide, nephrologists cannot manage exclusively all patients with CKD, and a majority of these patients will be cared for by primary care physicians (PCPs) or multispecialty teams that include both PCPs and nephrologists.15,16 Efforts are underway to increase physicians’ awareness of CKD as an important health problem and clinical practice guidelines put forth in the National Kidney Foundation (NKF)–Kidney Disease Outcomes Quality Initiative (KDOQI). Recognition

American Journal of Kidney Diseases, Vol 48, No 2 (August), 2006: pp 192-204

PHYSICIAN CARE OF PATIENTS WITH CKD

and evaluation of CKD, as well as referral of persons at high risk for progression to stage 4 CKD (GFR ⬍ 30 mL/min/1.73 m2 [⬍0.50 mL/s]) to specialist care, are central components of these guidelines.17,18 However, it is unclear whether these efforts have produced consistency in the care of patients with progressive CKD. We performed a national study to assess and compare the state of US PCP and nephrologist identification, evaluation, and recommendation for referral of patients with progressive CKD. METHODS

Study Design We conducted a national cross-sectional study of PCPs and nephrologists in the United States between August 2004 and August 2005 by using a self-administered mailed questionnaire designed to ascertain physicians’ approaches to the identification, evaluation, and referral of patients with NKFKDOQI stages 3 (GFR, 30 to 59 mL/min/1.73 m2 [0.50 to 0.98 mL/s]) and 4 (GFR, 15 to 29 mL/min/1.73 m2 [0.25 to 0.48 mL/s]) CKD, a group at high risk for progression of CKD and associated morbidity. We identified a national random stratified sample of 400 nephrologists and 800 PCPs (400 family physicians and 400 general internists) by using the American Medical Association Physician Masterfile. Physicians who were no longer participating in active clinical practice, had moved and were not contactable through follow-up mailings or telephone calls, and were not practicing nephrology, general internal medicine, or family practice were considered ineligible. We repeatedly contacted physicians by mail (7 total mailings) and telephone (4 reminder telephone calls), with an offer of a $20 incentive for their participation. The questionnaire could be completed on paper or on the Internet. The Johns Hopkins Medicine Institutional Review Board approved the study protocol and questionnaire.

Questionnaire Content All physicians received a questionnaire consisting of a hypothetical scenario (describing a PCP evaluating a new patient with stage 3 CKD progressing to stage 4 CKD) followed by questions designed to assess physicians’ abilities to recognize the patient’s severity of kidney disease, recommendations to the PCP for further diagnostic evaluation of the patient, and recommendations for referral of the patient to a nephrologist. Scenarios were identical for all physicians (featuring a 50-year-old woman who had been seen by another physician 4 months earlier than the current time), with the exception of 2 patient characteristics (race [African American or Caucasian] and comorbid illness profile [hypertension only or hypertension with diabetes]), which varied at random within each scenario. We varied race and comorbid illness profiles of patients to assess our a priori hypothesis that physicians’ recommendations might change based on these patient characteristics. For patients with hypertension only, the patient was described as taking a

193

daily diuretic with appropriate blood pressure control and normal physical examination findings. For patients with both hypertension and diabetes, the patient was described as taking an oral hypoglycemic agent and an angiotensin 2 receptor blocking agent with appropriate blood pressure control and normal physical examination findings. In each scenario, the patient was described to have persistent proteinuria (ascertained by using gross colorimetric dipstick) during a 4-month period and laboratory findings (ie, serum creatinine) consistent with, but not explicitly stated as, KDOQI stage 3 CKD (GFR, 30 to 59 mL/min/1.73 m2 [0.50 to 0.98 mL/s]) progressing to stage 4 (GFR, 15 to 29 mL/min/1.73 m2 [0.25 to 0.48 mL/s]) CKD within a 4-month period. The patient also was described to have height of 5= 2⬙ (157.5 cm) and weight of 154 lb (69.9 kg). Physicians were provided with enough clinical information in the scenario to use either the Cockcroft-Gault or the modified Modification of Diet in Renal Disease19 equations to calculate the patient’s estimated GFR themselves, but they were not provided with actual estimated GFR using either calculation. Physicians also were provided with information regarding the patient’s laboratory values from 4 months before the first visit to the general internist and repeated laboratory values obtained as a result of the patient’s current visit to the PCP (Table 1). Before conducting the study, the questionnaire was pilot tested among 30 practicing internists, family practice physicians, and nephrologists in Baltimore, MD, who provided feedback regarding hypothetical scenarios and study questions. Modifications to scenarios and study questions were made in response to comments provided during pilot testing.

Estimation of Kidney Function After physicians read the patient scenario, we asked them, “What is your estimate of the patient’s kidney function?” Answers for this question corresponded to NKF-KDOQI stages and could be: (1) GFR of 90 to 120 mL/min/1.73 m2 (1.5 to 2.0 mL/s), (2) GFR of 60 to 89 mL/min/1.73 m2 (1.0 to 1.48 mL/s), (3) GFR of 30 to 59 mL/min/1.73 m2 (0.50 to 0.98 mL/s), (4) GFR of 15 to 29 mL/min/1.73 m2 (0.25 to 0.48 mL/s), (5) GFR less than 15 mL/min/1.73 m2 (⬍0.25 mL/s), and (6) “I am unsure.” Answers of GFR of 30 to 59 mL/min/1.73 m2 or 15 to 29 mL/min/1.73 m2 correctly identified the patient’s level of kidney function. To confirm physicians’ abilities to identify the patient’s severity of kidney function, we independently reassessed their judgments of patients’ kidney function at a later point in the survey, asking them, “How would you describe the patient’s kidney disease?” Answers for this question corresponded to NKF-KDOQI description of stages of CKD and could be: (1) “normal or no kidney disease,” (2) “mild kidney disease,” (3) “moderate kidney disease,” (4) “severe kidney disease,” or (5) “end-stage kidney disease.” Answers of “moderate” or “severe” were considered to be concordant with correct identification of the patient’s level of kidney function.

Diagnostic Evaluation We also asked physicians to report which diagnostic studies they thought the PCP should order for further evaluation and whether they thought the PCP should refer the patient to a nephrologist. We asked, “Should the PCP order

194

BOULWARE ET AL Table 1. Example of Information Provided to Study Physicians in Hypothetical Patient Scenario Clinical History and Physical Examination

History of present illness

Past medical history Social history

Review of systems Medications

Physical examination

50-year-old African-American (Caucasian*) woman who recently moved to the area and is seeing a PCP for the first time. She takes her previously prescribed medications regularly. Remainder of history of present illness is unremarkable. Hypertension (10-y duration) only (or with diabetes [5-y duration]),* obesity Married, has 3 children, works as administrative assistant, nonsmoker, indemnity (fee-for-service) health insurance plan that does not restrict receipt of referral to specialist if needed Negative Daily diuretic and acetaminophen (for patient with hypertension only) or angiotensin 2 receptor blocking agent and oral hypoglycemic agent (for patient with hypertension and diabetes) Blood pressure, 125/80 mm Hg; weight, 154 lb; height, 5= 2⬙; otherwise unremarkable (including eye, cardiovascular, and neurological examinations) Laboratory Studies

Complete blood count Electrolytes and liver function studies Urinalysis (gross dipstick) Serum creatinine (mg/dL)

4 Months Before Visit

1 Week After Visit

Normal Normal 1⫹ protein 2.1†

Normal Normal 1⫹ protein 2.3‡

NOTE. To convert serum creatinine in mg/dL to ␮mol/L, multiply by 88.4; GFR in mL/min to mL/s, multiply by 0.01667. *Hypothetical patient scenarios randomly varied patient race and patient comorbid disease status. †Estimated GFR, 32.1 mL/min/1.73 m2 (using modified Modification of Diet in Renal Disease equation) and 35.4 mL/min/1.73 m2 (using Cockcroft-Gault equation) for African-American patient. ‡Estimated GFR, 28.9 mL/min/1.73 m2 (using modified Modification of Diet in Renal Disease equation) and 32.3 mL/min/1.73 m2 (using Cockcroft-Gault equation) for African-American patient.

any of the following laboratory tests within the next few weeks?” and we provided a list of serology, hematology, immunology, virology, urine, and radiological studies on which they could indicate “yes,” “no,” or “maybe” for each test. We considered answers of yes or no to indicate physicians’ definitive preferences and answers of maybe to indicate their uncertainty regarding ordering certain diagnostic testing for the patient.

Guideline Awareness

Recommendations for Referral

To assess perceptions regarding potential barriers in the care of their patients with CKD, we assessed physicians’ agreement with the statements, “The medical care I implement for patients such as this helps slow the progression of CKD and improve outcomes over time,” and “I believe I have enough clinical and administrative resources available to provide all the appropriate care that my patients with CKD need based on their current conditions.” We also assessed reasons why participants did not completely agree with these statements. We asked PCPs, “How much of the time do you experience difficulties referring patients like this [referring to the patient scenario] to a nephrologist?” and their reasons for difficulties.

We also asked, “Based on the information you know about this patient, do you recommend that the PCP refer [the patient] to a nephrologist at this time?” with possible answers of “yes” or “no.” For participants recommending referral, we also asked them their preferences regarding: (1) the optimal time frame for referral, (2) whether the nephrologist should take over the patient’s care or the PCP should maintain primary supervision, (3) the desired frequency of nephrologist input, and (4) types of guidance the PCP should seek from a nephrologist. To further assess physicians’ thresholds for referral of patients, we asked them to identify the estimated GFR at which they believed the PCP should refer a patient such as the patient featured in the scenario to a nephrologist by using a visual analogue scale in which physicians could circle the GFR level (ranging from 0 to 12 mL/min/1.73 m2 [0 to 0.20 mL/s]) they believed was appropriate for referring the patient.

We assessed physicians’ awareness of existing clinical practice guidelines for CKD by providing them with a list of several professional medical organizations and asking them if they were aware of clinical guidelines published by any of the organizations. Answers could be “yes” or “no.”

Barriers to Care

Statistical Analysis We used bivariate (chi-square) statistics to identify differences (according to physician specialty) in physicians’ characteristics, their identification of stages 3 to 4 CKD, and

PHYSICIAN CARE OF PATIENTS WITH CKD

their recommendations regarding the diagnostic evaluation and referral of the patient, including their preferences regarding the optimal time frame for referral of the patient to a nephrologist, primary supervision of the patient’s care, frequency of nephrologist input regarding the patient’s care, and types of guidance physicians believed nephrologists should provide the PCP. To address test-retest reliability, we included questions in different sections of the questionnaire that allowed us to test the consistency of scenario responses with regard to recognition of CKD and recommendations for referral. We assessed consistency in individual physicians’ assessments of patients’ kidney function by comparing responses to separate questions requiring a response of a range of GFR versus a qualitative descriptive response (eg, “severe kidney dysfunction”). We also assessed the median GFR at which physicians of different specialties recommended the patient be referred for nephrologist care. We used logistic regression to estimate the proportion of physicians recommending specific diagnostic testing after adjustment for patient race and comorbid conditions. We performed multivariable logistic regression to identify physician (years in practice, physician specialty, practice setting, and proportion of time spent in clinical settings) or patient scenario (patient race and comorbid disease status [hypertension only versus hypertension and diabetes]) characteristics independently associated with recognition of CKD and referral of hypothetical patients. We also performed multivariable logistic regression to determine whether potential differences in physicians’ recommendations for referral of the patient remained after adjustment for physicians’ recognition of stages 3 to 4 CKD. In separate multivariable logistic regression models, we assessed whether PCPs’ awareness of CKD or perceived barriers to the care of patients with CKD was associated with their recommendations for referral.

RESULTS

Response Rate, Scenario Randomization, and Physician Characteristics Of 1,200 physicians initially targeted, 131 had moved, were no longer contactable, or had incorrect addresses; 52 were not PCPs or nephrologists; and 58 were dead or no longer practicing medicine (total, 241 ineligible physicians). Of the remaining 959 eligible physicians, 304 physicians responded (comprising 178 PCPs [89 family physicians and 89 general internists] and 126 nephrologists; 28% response rate for family physicians, 28% for general internists, 39% for nephrologists). There were no differences between responding and nonresponding physicians with regard to age (mean, 46 ⫾ 11 [SD] versus 47 ⫾ 11 years, respectively; P ⬎ 0.05), sex (29% men versus 27% women, respectively; P ⬎ 0.05), years in clinical practice (mean, 14 ⫾ 12 versus 14 ⫾ 11 years, respectively; P ⬎ 0.05), or geographic census region of residence (North-

195

east, 23% versus 26%; North Central, 24% versus 23%; South, 32% versus 34%; and West, 20% versus 19%, respectively; P ⬎ 0.05). Hypothetical patient characteristics (hypertension alone versus hypertension plus diabetes and African-American versus white race) were distributed equally among study physicians. PCPs and nephrologists were similar with respect to their self-reported ethnicity, race, and years in practice. PCPs were more likely than nephrologists to be women, practice in solo or group private practice settings, spend more time in clinical settings, and spend the majority of their time caring for patients with diseases other than kidney disease. PCPs also were more likely than nephrologists to turn to non–kidney disease– specific professional organizations for clinical practice guidelines (Table 2). Successful Identification of CKD and Recommendations for Evaluation In bivariate analyses, PCPs were statistically significantly less likely to recognize the hypothetical patient as having CKD compared with nephrologists, with nearly 30% of family physicians and 15% of general internists reporting they were “unsure” of the patient’s GFR (versus 2% of nephrologists unsure; P ⬍ 0.01; Table 3). Differences in recognition persisted after adjustment for practice setting, years in practice, percentage of clinical time, patient scenario, and census region (Fig 1). There was a strong correlation between physicians’ separate assessments of patients’ kidney dysfunction: 98% of nephrologists who recognized the patient as having CKD assessed the patient as having “moderate” or “severe” kidney dysfunction, 85% of generalists who recognized the patient as having CKD assessed the patient as having “moderate” or “severe” kidney dysfunction, and 59% of family medicine physicians who recognized the patient as having CKD assessed the patient as having “moderate” or “severe” kidney dysfunction, all P ⬍ 0.01. There was a graded relation between degree of adult and kidney disease specialization and physicians’ recommendations for many diagnostic studies, with family physicians and general internists less likely than nephrologists to recommend many diagnostic tests with certainty (Fig 2). PCPs were more likely than nephrologists to

196

BOULWARE ET AL Table 2. Characteristics of Responding Physicians Selected Randomly Across the United States

Characteristic

Family Practice Physicians (n ⫽ 89)

General Internists (n ⫽ 89)

34 (38) 54 (61)

50 (56) 39 (44)

56 (44) 64 (51)

54 (61) 34 (38)

62 (70) 27 (30)

95 (75) 26 (21)

4 (4) 84 (94)

4 (4) 82 (92)

7 (6) 117 (93)

6 (7) 6 (7) 72 (81) 1 (1) 2 (2)

27 (30) 2 (2) 54 (61) 1 (1) 3 (3)

31 (25) 5 (4) 78 (62) 2 (2) 8 (6)

17 (19) 23 (26) 27 (30) 22 (25)

28 (31) 19 (21) 25 (28) 17 (19)

30 (24) 27 (21) 50 (40) 19 (15)

22 (25) 39 (44) 0 10 (11) 17 (19) 13 (15)

14 (16) 36 (40) 7 (8) 21 (24) 22 (25) 8 (9)

11 (9) 68 (54) 5 (4) 40 (32) 32 (25) 7 (6)

0.03 NS NS ⬍0.01 NS NS

89 ⫾ 17 1⫾4 12 ⫾ 16

89 ⫾ 20 9 ⫾ 20 11 ⫾ 17

76 ⫾ 26 15 ⫾ 22 15 ⫾ 18

⬍0.01 ⬍0.01 NS

9⫾9 91 ⫾ 10

17 ⫾ 13 81 ⫾ 18

86 ⫾ 20 15 ⫾ 18

⬍0.01 ⬍0.01

Years in practice 0-10 ⬎10 Sex Male Female Ethnicity Hispanic Non-Hispanic Race Asian African American White ⱖ2 races Other Region Northeast North central South West Practice setting* Solo private Group private Health maintenance organization, staff model University Community hospital Government health care facility Percentage of time spent in Clinical activities Research activities Administrative activities Percentage of time spent seeing Patients with kidney disease Patients with other diseases

Nephrologists (n ⫽ 126)

P

NS

0.03

NS

⬍0.01

NS

NOTE. Values expressed as number (percent) or mean ⫾ SD. Percentages may not equal 100% because of missing values. Abbreviation: NS, not significant. *Options were not mutually exclusive; physicians may have selected more than 1 option.

express uncertainty regarding recommendations of urine microscopic examination (11% of family physicians versus 1% of general internists and 3% of nephrologists; P ⬍ 0.01), magnetic resonance angiography of the renal arteries (23% of family physicians, 19% of general internists, 8% of nephrologists; P ⬍ 0.01), and renal ultrasound (18% of family physicians, 14% of general internists, and 5% of nephrologists; P ⬍ 0.01). Physicians’ Preferences for Referral PCPs were statistically significantly less likely than nephrologists to recommend referral to a nephrologist (Table 3). This finding remained

robust after adjustment for physicians’ recognition of the patient’s CKD (Fig 1). Among physicians recommending referral, most preferred that referral occur within 2 to 3 months of the patient’s evaluation by the PCP. Among physicians believing the PCP should continue to assume primary supervision of the patient’s care with guidance from the nephrologist, PCPs were more likely than nephrologists to recommend less frequent input from referring nephrologists (16% of family physicians and 20% of general internists versus 6% of nephrologists recommending referring nephrologist input monthly to every 6 months; P ⫽ 0.01; Table 3). In a separate general

PHYSICIAN CARE OF PATIENTS WITH CKD

197

Table 3. Physician Identification of CKD, Recommendation for Referral, and Preferences Regarding Referral for Hypothetical Patient With Progressive CKD

Estimation of GFR (mL/min/1.73 m2) 90-120 60-89 30-59 15-29 ⬍15 I am unsure Correct recognition of CKD Recommendation for referral Yes No Optimal time frame* Next 1-4 wk Next 2-3 mo Next 4-6 mo Next 7-9 mo Next 10-11 mo Within 1 y Primary supervision of care* Let PCP continue care with nephrologist’s guidance Let nephrologist take over care Frequency of input† Once and then later if needed Every mo Every 2-3 mo Every 4-6 mo Every 7-9 mo Every 10-12 mo Every 1-2 y Every 2⫹ y Types of guidance desired from nephrologist (v not desired)† Confirmation of appropriate evaluation Additional evaluation and testing Nutritional advice Advice about medication regimen Predialysis/renal replacement therapy preparation Electrolyte management Assessment/management of anemia Assessment/management of metabolic bone disease Assessment/management of cardiovascular disease risk factors Management and assessment of kidney disease severity Patient education

Family Practice Physicians (n ⫽ 89)

General Internists (n ⫽ 89)

Nephrologists (n ⫽ 126)

1 (1) 8 (9) 44 (49) 6 (7) 2 (2) 27 (30) 50 (56)

0 7 (8) 47 (53) 16 (18) 1 (1) 13 (15) 63 (71)

0 2 (2) 107 (85) 14 (11) 0 2 (2) 121 (96)

63 (71) 23 (26)

66 (74) 21 (24)

121 (96) 3 (2)

32 (51) 26 (41) 1 (2) 0 0 1 (2)

33 (50) 26 (39) 3 (5) 0 0 1 (2)

63 (52) 52 (43) 4 (3) 0 0 0

51 (81) 9 (14)

54 (82) 10 (15)

113 (93) 7 (6)

8 (16) 2 (4) 8 (16) 24 (47) 2 (4) 6 (12) 1 (2) 0

11 (20) 0 15 (28) 22 (41) 2 (4) 2 (4) 1 (2) 0

7 (6) 4 (4) 34 (30) 60 (53) 0 2 (2) 1 (1) 0

48 (94) 50 (98) 41 (80) 50 (98) 25 (49) 25 (49) 0 (0) 0 (0)

51 (94) 49 (91) 41 (76) 46 (85) 30 (56) 23 (43) 0 (0) 0 (0)

107 (95) 105 (93) 101 (89) 109 (96) 83 (73) 91 (81) 14 (12) 14 (12)

NS NS NS NS ⬍0.01 ⬍0.01 ⬍0.01 ⬍0.01

0 (0)

1 (2)

8 (7)

NS

0 (0) 0 (0)

3 (6) 0 (0)

5 (4) 4 (4)

NS NS

P

⬍0.01

⬍0.01 ⬍0.01

NS

NS

0.01

NOTE. Values expressed as number (percent). Percentages may not equal 100% because of missing values. To convert GFR in mL/min to mL/s, multiply by 0.01667. Abbreviation: NS, not significant. *Applies to only 250 physicians (129 PCPs and 121 nephrologists) who recommended referral of patient. †Applies to only 218 physicians (105 PCPs and 113 nephrologists) who believed PCPs should continue to care for the patient with nephrologist’s guidance.

198

BOULWARE ET AL

Fig 1. Correct identification of CKD and recommendations for referral by physician specialty. *Adjusted for years in practice, practice setting, percentage of clinical time, census region, and patient race and comorbid conditions. **Adjusted for correct identification of stages 3 to 4 CKD, years in practice, practice setting, percentage of clinical time, census region, and patient race and comorbid conditions.

question about referral to assess physicians’ consistency, nephrologists recommended that patients similar to the patient in the scenario be referred earlier than general internists and family medicine physicians (median estimated GFR for referral, 39 mL/min/1.73 m2 (interquartile range, 34 to 44 mL/min/1.73 m2 [0.65 mL/s; interquartile range, 0.57 to 0.73 mL/s] versus 32 mL/min/ 1.73 m2; interquartile range, 26 to 36 mL/min/ 1.73 m2 [0.53 mL/s; interquartile range, 0.43 to 0.60 mL/s] and 32 mL/min/1.73 m2; interquartile range, 26 to 36 mL/min/1.73 m2 [0.53 mL/s; interquartile range, 0.43 to 0.60 mL/s], respectively; P ⬍ 0.001). Physicians recommending referral most frequently believed the following types of guidance should be sought from nephrologists: confirmation of appropriate evaluation of the patient by the PCP (95%), additional evaluation and testing (94%), advice about the patient’s medication regimen (94%), nutritional advice (84%), advice regarding electrolyte management (64%), and predialysis/renal replacement therapy preparation (63%). Family physicians and general internists were less likely than nephrologists to believe advice should be sought from consulting nephrologists on predialysis/renal replacement therapy preparation, advice on electrolyte man-

agement, assessment/management of anemia, and assessment/management of metabolic bone disease (Table 3). Characteristics Associated With Correct Identification of CKD Severity and Recommendation of Referral After adjustment, family physicians with more than 10 years in clinical practice were least likely to recognize CKD (Table 4). Family physicians and general internists with more than 10 years in clinical practice were least likely to recommend patient referral (Table 4). Perceived Barriers to Patient Referral and Relation of Perceived Barriers to Referral PCPs were less likely than nephrologists to: (1) be aware of existing clinical practice guidelines, (2) believe the medical care they implement for patients with CKD slows CKD progression and improves clinical outcomes, and (3) believe they have enough clinical and administrative resources to provide appropriate care for patients with CKD. Family physicians were more likely than general internists to report that they experience difficulties referring patients with CKD to nephrologists at least a little of the time (Table 5).

PHYSICIAN CARE OF PATIENTS WITH CKD

199

Fig 2. Diagnostic studies recommended* by physicians for the evaluation of a hypothetical patient with progressive CKD. (A) Serological and hematologic studies, (B) immunologic and virological studies, and (C) urine and radiological studies. *Adjusted for patient race and comorbid conditions. †Complete blood count. ‡Magnetic resonance angiography. □ ⴝ Family practice physicians; p ⴝ general internists;  ⴝ nephrologists.

Among family physicians, those agreeing that their care improves the health of patients had 6-fold greater odds (odds ratio, 6.1; 95% confi-

dence interval [CI], 1.2 to 31.6) of recommending referral of patients with CKD compared with their counterparts not agreeing that their care

200

BOULWARE ET AL Table 4. Physician and Patient Characteristics Associated With Correct Identification of GFR and Recommendation of Referral

Physician Characteristic

Specialty and years in practice Family practice physician, 0-10 y Family practice physician, ⬎ 10 y General internist, 0-10 y General internist, ⬎10 y Nephrologist, 0-10 y Nephrologist, ⬎10 y Practice setting‡ Community hospital All other settings Time spent in clinical setting (%) ⱖ50 ⬍50 Patient scenario characteristic§ Patient race African American Caucasian Patient comorbid conditions Hypertension only Diabetes and hypertension

Correct Identification of Stage 3-4 CKD Adjusted* % (95% CI)

P Trend

Recommendation for Patient Referral Adjusted† % (95% CI)

⬍0.01 64 (46-79) 55 (42-69) 77 (62-87) 78 (61-89) 96 (87-99) 99 (92-100)

⬍0.01 85 (68-93) 69 (54-81) 88 (75-95) 66 (48-81) 98 (90-99) 99 (92-100)

NS 90 (80-95) 88 (80-93)

NS 91 (81-96) 92 (86-96)

NS 87 (79-92) 98 (87-100)

NS 90 (84-94) 99 (89-100)

NS 90 (83-95) 86 (77-92)

NS 92 (85-96) 90 (82-95)

NS 91 (83-95) 86 (77-92)

P Trend

NS 92 (85-96) 90 (83-95)

Abbreviation: NS, not significant. *Adjusted for years in practice, physician specialty, practice setting, percentage of clinical time, census region, and version of questionnaire (patient race and comorbid conditions). †Adjusted for correct identification of stage 3 to 4 CKD, years in practice, physician specialty, practice setting, percentage of clinical time, census region, and version of questionnaire (patient race and comorbid conditions). ‡No significant differences in other practice settings. §For patient scenario characteristics: adjusted for years in practice, physician specialty, practice setting, percentage of clinical time, census region, patient comorbid conditions (hypertension only or diabetes and hypertension), and patient race (African American or Caucasian).

improves clinical outcomes. Among general internists, those aware of existing clinical guidelines had 14-fold greater odds (odds ratio, 14.5; 95% CI, 1.1 to 186.3) of recommending referral compared with their counterparts who were not aware of guidelines, whereas those stating that they have enough clinical and administrative support to care for patients with CKD were 90% less likely (odds ratio, 0.10; 95% CI, 0.02 to 0.68) to recommend referral compared with their counterparts reporting that they do not have enough support. DISCUSSION

In this study of physicians sampled randomly from across the United States, our findings suggest that efforts to raise physicians’ awareness of progressive CKD and disseminate recently developed

clinical practice guidelines have not been as effective as hoped.17,18 Our findings highlight that PCPs and nephrologists have different perceptions of how the evaluation of patients with progressive CKD should be undertaken and the intensity with which specialists should be involved in their care. This national study is consistent with results of earlier regional studies showing that patients with CKD who receive care in primary care settings frequently do not receive care in accordance with NKF-KDOQI guideline recommendations released in 2000.12,20 Our study also extends previous research by assessing physicians’ care for a standardized patient, thereby eliminating potential confounding caused by practice setting or unmeasured patient characteristics. Most importantly, it identifies physician-related mechanisms through which suboptimal care might occur.

PHYSICIAN CARE OF PATIENTS WITH CKD

201

Table 5. Potential Barriers to Referral of Patients With CKD: Physicians’ Awareness of Guidelines and Attitudes Regarding Care

Characteristic

To your knowledge, have any [organizations] issued guidelines regarding referral of patients with CKD? Yes No I am unsure The medical care I implement for patients such as this helps to slow progression of CKD and improve outcomes over time Completely agree Less than completely agree Reasons for incomplete agreement with the above question† Many patients are nonadherent (Agree [v not agree]) See little evidence that treatments slow disease (Agree [v not agree]) Although improvement is shown in studies, I do not see improvement in my patients (Agree [v not agree]) My patients have so many important clinical issues to address that I have little time to address their kidney disease (Agree [v not agree]) I believe I have enough clinical and administrative resources available to provide all the appropriate care that my patients with CKD need based on their current conditions Completely agree Less than completely agree Reasons for incomplete agreement with the above question‡ No electronic patient records (Agree [v not agree]) No electronic laboratory studies (Agree [v not agree]) Need ancillary support (Agree [v not agree]) Not enough secretarial support (Agree [v not agree]) Many patients cannot afford appropriate medications (Agree [v not agree]) How much of the time do you experience difficulties referring patients like this to a nephrologist? Not at all At least a little of the time Agreement with statements among those facing difficulty§ Nephrologists are not interested in seeing these patients (Agree [v not agree]) There are no (few) nephrologists in my geographic area (Agree [v not agree]) Nephrologists are overbooked and often cannot accommodate patients like this in their practice (Agree [v not agree]) Nephrologists may want to completely take over the patient’s care (Agree [v not agree]) Insurance companies restrict my abilities to refer patients to nephrologists (Agree [v not agree])

Family Practice Physicians (n ⫽ 89)

General Internists (n ⫽ 89)

Nephrologists (n ⫽ 126)

30 (34)* 8 (9) 48 (54)

29 (33)* 11 (12) 49 (55)

100 (79) 3 (2) 22 (17)

22 (25)* 64 (72)

41 (46) 47 (53)

66 (52) 59 (47)

48 (72) 6 (9)*

33 (69) 4 (8)

46 (77) 1 (2)

NS NS

13 (19)

5 (10)

7 (12)

NS

11 (16)*

7 (15)*

2 (3)

⬍0.01

20 (22)* 67 (75)

22 (25)* 67 (75)

50 (40) 74 (59)

17 (25) 11 (16) 18 (26)* 14 (27)

14 (21) 10 (15) 22 (33) 14 (21)

28 (37) 14 (18) 38 (50) 24 (32)

NS NS NS NS

40 (58)

42 (63)

57 (75)

NS

45 (51) 42 (47)

61 (69) 28 (31)

NA NA

6 (14)

6 (21)

NA

NS

23 (52)

8 (29)

NA

NS

18 (41)

16 (57)

NA

NS

6 (14)

5 (18)

NA

NS

15 (34)

4 (14)

NA

NS

P

⬍0.01

⬍0.01

⬍0.01

0.02

NOTE. Values expressed as number (percent). Percentages may not equal 100% because of missing values. Abbreviations: NS, not significant; NA, not applicable. *P ⬍ 0.05 in comparison between family physicians or general internists and nephrologists. †Applies to only 175 physicians (115 PCPs and 60 nephrologists) who did not completely agree with the statement: “The medical care I implement for patients such as this helps to slow progression of CKD and improve outcomes over time.” ‡Applies to only 212 physicians (136 PCPs and 76 nephrologists) who believed that PCPs should continue to care for the hypothetical patient with nephrologist’s guidance. §Applies to only 72 PCPs who answered “A little of the time, much of the time, or most/all of the time” to the statement “How much of the time do you experience difficulties referring patients like this to a nephrologist?”

202

Suboptimal recognition of progressive CKD could be attributed to a variety of potential reasons, including lack of knowledge regarding methods to calculate estimated GFR, lack of time, and inadequate knowledge of CKD risk factors. A recent regional study showed that PCPs were not aware of significant risk factors for CKD, suggesting that targeted education of PCPs is needed.21 Provider differences in recommendations for referral of patients with more rapid progression of CKD (as presented in our hypothetical scenarios) may represent an even more clinically relevant problem than lack of recognition of CKD on the part of generalists because referral to nephrologist care and institution of appropriate therapies for such persons has been shown to improve clinical outcomes.5,14,22-25 Possible explanations for differences in recommendations for referral include lack of knowledge of or uncertainty regarding clinical recommendations regarding specialty referral, lack of knowledge of risk factors for CKD progression,21,26 or lack of agreement with clinical recommendations (shown in other diseases to affect physician practice adherence to clinical practice guidelines).27 Our findings that general internists aware of recent clinical guidelines and family practice physicians who believe their care could enhance patients’ clinical outcomes were more likely to recommend referral support this hypothesis. Although this study did not directly measure the effectiveness of efforts by the National Institutes of Health’s National Kidney Disease Education Program (which began in 2003) and others to implement uniform laboratory reporting of GFR and expose physicians to educational materials and clinical decision aids for CKD care that could help PCPs estimate the severity of CKD more accurately, provide support for decisions to refer patients, and enhance some physicians’ confidence in the likelihood of improving clinical outcomes by instituting recommended care, it provides evidence that physicians may not have had adequate exposure to these or similar efforts at the time of this study.28 Our results also suggest mechanisms for variation in recommendations for referral. General internists who reported that they had enough clinical and administrative support were less likely to recommend referral. Some general internists may have confidence in their abilities to

BOULWARE ET AL

provide appropriate care for these patients and may not perceive added benefit to referring patients for specialty care. Prior work indicates that physicians may not seek referrals if they believe they have informal access to clinical specialists who can provide answers to needed questions regarding management of patients with chronic illnesses.29,30 General internists may have more ready access to medical specialists than family physicians. Family physicians more often reported a lack of nephrologists in their geographic area. Whereas evidence suggests early referral for appropriate care of patients with CKD can improve clinical outcomes,13,14 it remains unclear whether appropriate care delivered by PCPs with limited nephrologist input leads to worse clinical outcomes. Disagreement regarding when and why patients with CKD should be referred for specialist care may reflect not only a lack of uniformity regarding information disseminated to physicians, but also differences in how physicians perceive their roles in the care of such patients. PCPs may desire to maintain continuity of care for their patients with chronic illnesses while minimizing unnecessary testing. In addition, they may be faced with balancing competing priorities among other chronic illnesses. However, disagreement between PCPs and specialists could contribute to confusion regarding care and potentially lead to omissions or redundancies in care, ultimately decreasing overall quality of care or increasing costs. Recent research indicates that implementation of models with shared clinical care by PCPs and nephrologists may enhance outcomes without overburdening nephrologists.31 Thus, efforts to achieve consensus with regard to optimal management strategies could improve clinical outcomes. Although existing CKD clinical practice guidelines in the United States were generated from within the nephrology community, the development of additional guidelines simultaneously endorsed by family medicine, general internal medicine, and nephrologist groups could move efforts to reach consensus forward. Physicians in other countries have sought to develop guidelines incorporating generalist and specialist input into care of patients with CKD, but similar efforts have not yet occurred within the United States.32 Collaborative efforts in guideline development for other

PHYSICIAN CARE OF PATIENTS WITH CKD

illnesses may have helped achieve broader dissemination of clinical practice guidelines for these illnesses among specialists and generalists in the United States.33-36 It is noteworthy that PCPs with more than 10 years of clinical practice experience were least likely to recognize CKD and also least likely to recommend referral. These findings strongly confirm other studies indicating that more recently trained physicians are more aware of current treatment guidelines and potentially deliver better quality care.37,38 Physicians with more years in practice should be targeted for dissemination of information regarding the identification and appropriate referral of patients with CKD. Limitations of this study deserve mention. Although we studied a national sample of US physicians and made many follow-up contacts, our response rate was suboptimal, potentially limiting generalizability. However, our analyses comparing participating with nonparticipating physicians indicate that the only difference was physician specialty. The lower primary care response may indicate lack of awareness or interest in CKD as an important clinical problem. Second, we asked physicians to provide advice regarding a hypothetical patient. Clinicians seeing patients in real life might act differently, although scenarios have been shown to have validity in quality or care assessment.39 Although we were interested in assessing physicians’ responses when evaluating patients with progressive kidney disease, one of our scenarios featured a patient with hypertension. It is possible that some physicians believed this patient was not likely to experience a further rapid decrease in kidney function because such rapid decrease is not observed as frequently in patients with hypertension. Third, our questionnaire asked physicians about a brief episode of care with a single patient. Practice patterns might vary for patients seen over longer periods. Fourth, we did not provide physicians with tools to estimate GFR or information on where to find tools.40 Comparing physicians with no information on tools for calculating estimated GFR with physicians with prompting to use tools would help ascertain the effect of ongoing efforts to enhance both calculation of estimated GFR by clinicians and reporting of GFR among clinical laboratories.28

203

Notwithstanding these limitations, we found that PCPs were less likely to recognize CKD or recommend referral of patients and differed from specialists with regard to their recommended evaluation of patients and preferences regarding the degree of specialist involvement in patients’ care. Awareness of clinical guidelines, confidence in the effectiveness of care, and perceptions regarding the amount of available clinical and administrative support were related strongly to primary care referral recommendations. Greater dissemination of existing clinical guidelines, targeted education of PCPs, and work to involve both PCPs and nephrologists in consensusbuilding efforts that more clearly delineate strategies for diagnosing and managing patients with progressive CKD, including collaboration to develop joint clinical practice guidelines, could enhance the care of these high-risk patients. REFERENCES 1. Coresh J, Astor BC, Greene T, Eknoyan G, Levey AS: Prevalence of chronic kidney disease and decreased kidney function in the adult US population: Third National Health and Nutrition Examination Survey. Am J Kidney Dis 41:112, 2003 2. Shlipak MG, Sarnak MJ, Katz R, et al: Cystatin C and the risk of death and cardiovascular events among elderly persons. N Engl J Med 352:2049-2060, 2005 3. Sarnak MJ, Katz R, Stehman-Breen CO, et al: Cystatin C concentration as a risk factor for heart failure in older adults. Ann Intern Med 142:497-505, 2005 4. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY: Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351:12961305, 2004 5. Agodoa LY, Appel L, Bakris GL, et al: Effect of ramipril vs amlodipine on renal outcomes in hypertensive nephrosclerosis: A randomized controlled trial. JAMA 285: 2719-2728, 2001 6. Jafar TH, Stark PC, Schmid CH, et al: Proteinuria as a modifiable risk factor for the progression of non-diabetic renal disease. Kidney Int 60:1131-1140, 2001 7. Agewall S, Wikstrand J, Ljungman S, Fagerberg B: Usefulness of microalbuminuria in predicting cardiovascular mortality in treated hypertensive men with and without diabetes mellitus. Risk Factor Intervention Study Group. Am J Cardiol 80:164-169, 1997 8. Brancati FL, Whelton PK, Randall BL, Neaton JD, Stamler J, Klag MJ: Risk of end-stage renal disease in diabetes mellitus: A prospective cohort study of men screened for MRFIT. Multiple Risk Factor Intervention Trial. JAMA 278:2069-2074, 1997 9. Garg AX, Clark WF, Haynes RB, House AA: Moderate renal insufficiency and the risk of cardiovascular mortality: Results from the NHANES I. Kidney Int 61:1486-1494, 2002

204

10. Ruggenenti P, Perna A, Remuzzi G: ACE inhibitors to prevent end-stage renal disease: When to start and why possibly never to stop: A post hoc analysis of the REIN trial results. Ramipril Efficacy in Nephropathy. J Am Soc Nephrol 12:2832-2837, 2001 11. Hansson L, Lindholm LH, Niskanen L, et al: Effect of angiotensin-converting-enzyme inhibition compared with conventional therapy on cardiovascular morbidity and mortality in hypertension: The Captopril Prevention Project (CAPPP) randomised trial. Lancet 353:611-616, 1999 12. Cleveland DR, Jindal KK, Hirsch DJ, Kiberd BA: Quality of prereferral care in patients with chronic renal insufficiency. Am J Kidney Dis 40:30-36, 2002 13. Kinchen KS, Sadler J, Fink N, et al: The timing of specialist evaluation in chronic kidney disease and mortality. Ann Intern Med 137:479-486, 2002 14. Cass A, Cunningham J, Snelling P, Ayanian JZ: Late referral to a nephrologist reduces access to renal transplantation. Am J Kidney Dis 42:1043-1049, 2003 15. Levin A, Stevens LA: Executing change in the management of chronic kidney disease: Perspectives on guidelines and practice. Med Clin North Am 89:701-709, 2005 16. Nissenson AR, Collins AJ, Hurley J, Petersen H, Pereira BJ, Steinberg EP: Opportunities for improving the care of patients with chronic renal insufficiency: Current practice patterns. J Am Soc Nephrol 12:1713-1720, 2001 17. National Kidney Foundation: K/DOQI Clinical Practice Guidelines 2000. Available at: http://www.kidney.org/ professionals/doqi/kdoqi/p4_class_g1.htm. Accessed January 18, 2002 18. Hostetter TH, Lising M: National kidney disease education program. J Am Soc Nephrol 14(7 Suppl 2):S114S116, 2003 19. Levey AS, Bosch JP, Lewis JB, Greene T, Rogers N, Roth D: A more accurate method to estimate glomerular filtration rate from serum creatinine: A new prediction equation. Modification of Diet in Renal Disease Study Group. Ann Intern Med 130:461-470, 1999 20. Martinez-Ramirez HR, Jalomo-Martinez B, CortesSanabria L, et al: Renal function preservation in type 2 diabetes mellitus patients with early nephropathy: A comparative prospective cohort study between primary health care doctors and a nephrologist. Am J Kidney Dis 47:78-87, 2006 21. Lea JP, McClellan WM, Melcher C, Gladstone E, Hostetter T: CKD risk factors reported by primary care physicians: Do guidelines make a difference? Am J Kidney Dis 47:72-77, 2006 22. The GISEN Group (Gruppo Italiano di Studi Epidemiologici in Nefrologia): Randomised placebo-controlled trial of effect of ramipril on decline in glomerular filtration rate and risk of terminal renal failure in proteinuric, nondiabetic nephropathy. Lancet 349:1857-1863, 1997 23. Brenner BM, Cooper ME, de Zeeuw D, et al: Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med 345:861869, 2001 24. Lewis EJ, Hunsicker LG, Clarke WR, et al: Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. N Engl J Med 345:851-860, 2001

BOULWARE ET AL

25. Kinchen KS, Sadler J, Fink N, et al: The timing of specialist evaluation in chronic kidney disease and mortality. Ann Intern Med 137:479-486, 2002 26. Fox CH, Brooks A, Zayas LE, McClellan W, Murray B: Primary care physicians’ knowledge and practice patterns in the treatment of chronic kidney disease: An Upstate New York Practice-based Research Network (UNYNET) study. J Am Board Fam Med 19:54-61, 2006 27. Cabana MD, Rand CS, Powe NR, et al: Why don’t physicians follow clinical practice guidelines? A framework for improvement. JAMA 282:1458-1465, 1999 28. National Kidney Disease Education Program: Health professionals: rationale for use and reporting of estimated GFR. 2006. Available at: http://nkdep.nih.gov/professionals/ estimated_gfr.htm. Accessed January 11, 2006 29. Kuo D, Gifford DR, Stein MD: Curbside consultation practices and attitudes among primary care physicians and medical subspecialists. JAMA 280:905-909, 1998 30. Keating NL, Zaslavsky AM, Ayanian JZ: Physicians’ experiences and beliefs regarding informal consultation. JAMA 280:900-904, 1998 31. Jones C, Roderick P, Harris S, Rogerson M: An evaluation of a shared primary and secondary care nephrology service for managing patients with moderate to advanced CKD. Am J Kidney Dis 47:103-114, 2006 32. Mendelssohn DC, Barrett BJ, Brownscombe LM, et al: Elevated levels of serum creatinine: Recommendations for management and referral. CMAJ 161:413-417, 1999 33. Snow V, Weiss KB, LeFevre M, et al: Management of newly detected atrial fibrillation: A clinical practice guideline from the American Academy of Family Physicians and the American College of Physicians. Ann Intern Med 139: 1009-1017, 2003 34. Gonzales R, Bartlett JG, Besser RE, et al: Principles of appropriate antibiotic use for treatment of uncomplicated acute bronchitis: Background. Ann Emerg Med 37:720-727, 2001 35. Gonzales R, Bartlett JG, Besser RE, et al: Principles of appropriate antibiotic use for treatment of uncomplicated acute bronchitis: Background. Ann Intern Med 134:521-529, 2001 36. Snow V, Mottur-Pilson C, Gonzales R: Principles of appropriate antibiotic use for treatment of nonspecific upper respiratory tract infections in adults. Ann Intern Med 134:487489, 2001 37. Chamany S, Schulkin J, Rose CE Jr, Riley LE, Besser RE: Knowledge, attitudes, and reported practices among obstetrician-gynecologists in the USA regarding antibiotic prescribing for upper respiratory tract infections. Infect Dis Obstet Gynecol 13:17-24, 2005 38. Choudhry NK, Fletcher RH, Soumerai SB: Systematic review: The relationship between clinical experience and quality of health care. Ann Intern Med 142:260-273, 2005 39. Peabody JW, Luck J, Glassman P, Dresselhaus TR, Lee M: Comparison of vignettes, standardized patients, and chart abstraction: A prospective validation study of 3 methods for measuring quality. JAMA 283:1715-1722, 2000 40. National Kidney Disease Education Program: Tools and Resources for Health Professionals: GFR Calculators.Available at: http://www.nkdep.nih.gov/. Accessed April 10, 2006