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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 ofrogressive chronic kidney disease (CKD), agree on diagnostic and referral strategies, and identify similar barrierso caring for patients. Methods: We conducted a national study of PCPs and nephrologists in the United Stateshrough a questionnaire describing a PCP caring for a patient with progressing CKD and questions to assessecognition of kidney dysfunction and approaches to diagnostic evaluation and referral. We identified participantnd patient characteristics independently associated with CKD recognition and referral. Results: We randomly

dentified a national sample of 304 physicians (126 nephrologists [39% response rate], 89 family physicians [28%esponse rate], and 89 general internists [28% response rate]). PCPs recognized CKD less (adjusted percentage, 59%;5% confidence interval [CI], 47 to 69, family physicians; adjusted percentage, 78%; 95% CI, 67 to 86, general internists;djusted percentage, 97%; 95% CI, 93 to 99, nephrologists; P < 0.01), differed from nephrologists in their recommenda-ions for diagnostic testing, and recommended referral less (adjusted percentage, 76%; 95% CI, 65 to 84, familyhysicians; adjusted percentage, 81%; 95% CI, 70 to 89, general internists; adjusted percentage, 99%; 95% CI, 95 to 100,ephrologists; P < 0.01). PCPs differed from nephrologists in their expected intensity of specialists’ involvement in care16%, family physicians; 20%, general internists; 6%, nephrologists recommending nephrologist input monthly to everymonths; P � 0.01). Lack of awareness of clinical practice guidelines and lack of clinical and administrative resourcesere identified as important barriers to care. Conclusion: PCPs recognize and recommend specialist care forrogressive CKD less than nephrologists and differ in their clinical evaluations and expectations for referral.

mproved dissemination of existing guidelines and targeted education in conjunction with efforts to build consen-us among PCPs and nephrologists regarding their roles in the care of patients with CKD, including theollaborative development of clinical practice guidelines, could enhance patient care. Am J Kidney Dis 48:192-204.2006 by the National Kidney Foundation, Inc.

NDEX WORDS: Chronic kidney disease (CKD); guidelines; barriers.

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HRONIC KIDNEY DISEASE (CKD) is agrowing epidemic, with at least 10 million

ersons with kidney damage.1 Persons with mod-

From the Department of Medicine, Division of Generalnternal Medicine, and Department of Medicine, Division ofephrology, Johns Hopkins School of Medicine; Depart-ent of Epidemiology, Johns Hopkins Bloomberg School ofublic Health; Nephrology Center of Maryland; and Welchenter for Prevention, Epidemiology and Clinical Research,ohns Hopkins Medical Institutions, Baltimore, MD.

Received March 10, 2006; accepted in revised form April0, 2006.Originally published online as doi:10.1053/j.ajkd.2006.04.073

n June 14, 2006.Support: Funding sources are National Kidney Foundation ofaryland Mini-Grant (L.E.B.); Robert Wood Johnson Haroldmos Faculty Development Program (L.E.B.); Grant no.240502643 from National Institute of Diabetes and Digestivend Kidney Diseases (N.R.P.). Potential conflicts of interest: None.

Address reprint requests to L. Ebony Boulware, MD,PH, Assistant Professor of Medicine and Epidemiology,elch Center for Prevention, Epidemiology and Clinicalesearch, Division of General Internal Medicine, Johnsopkins Medical Institutions, 2024 E Monument St, Ste-600, Baltimore, MD 21205. E-mail: lboulwa@jhmi.edu© 2006 by the National Kidney Foundation, Inc.0272-6386/06/4802-0002$32.00/0

cdoi:10.1053/j.ajkd.2006.04.073

American Journal of K92

rately advanced CKD (glomerular filtration rateGFR] � 60 mL/min/1.73 m2 [�1.0 mL/s]),articularly those with hypertension or diabetesnd persistent proteinuria, have substantially in-reased risks for progression toward end-stageenal disease, hospitalization, cardiovascular dis-ase events, heart failure, and death.2-9 Institu-ion of appropriate therapies for patients withrogressive CKD and early referral of patients toephrologists for evaluation and kidney diseaseanagement are associated with improved qual-

ty of care and outcomes.5,6,10-14

Although early referral of patients is optimal,t is widely recognized that given the relativelymall number of practicing nephrologists nation-ide, nephrologists cannot manage exclusively

ll patients with CKD, and a majority of theseatients will be cared for by primary care physi-ians (PCPs) or multispecialty teams that includeoth PCPs and nephrologists.15,16 Efforts arenderway to increase physicians’ awareness ofKD as an important health problem and clinicalractice guidelines put forth in the Nationalidney Foundation (NKF)–Kidney Disease Out-

omes Quality Initiative (KDOQI). Recognition

idney Diseases, Vol 48, No 2 (August), 2006: pp 192-204

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PHYSICIAN CARE OF PATIENTS WITH CKD 193

nd evaluation of CKD, as well as referral ofersons at high risk for progression to stage 4KD (GFR � 30 mL/min/1.73 m2 [�0.50 mL/s])

o specialist care, are central components ofhese guidelines.17,18 However, it is unclearhether these efforts have produced consistency

n the care of patients with progressive CKD.We performed a national study to assess and

ompare the state of US PCP and nephrologistdentification, evaluation, and recommendationor referral of patients with progressive CKD.

METHODS

tudy DesignWe conducted a national cross-sectional study of PCPs

nd nephrologists in the United States between August 2004nd August 2005 by using a self-administered mailed ques-ionnaire designed to ascertain physicians’ approaches to thedentification, evaluation, and referral of patients with NKF-DOQI stages 3 (GFR, 30 to 59 mL/min/1.73 m2 [0.50 to.98 mL/s]) and 4 (GFR, 15 to 29 mL/min/1.73 m2 [0.25 to.48 mL/s]) CKD, a group at high risk for progression ofKD and associated morbidity. We identified a national

andom stratified sample of 400 nephrologists and 800 PCPs400 family physicians and 400 general internists) by usinghe American Medical Association Physician Masterfile.hysicians who were no longer participating in active clini-al practice, had moved and were not contactable throughollow-up mailings or telephone calls, and were not practic-ng nephrology, general internal medicine, or family practiceere considered ineligible. We repeatedly contacted physi-

ians by mail (7 total mailings) and telephone (4 reminderelephone calls), with an offer of a $20 incentive for theirarticipation. The questionnaire could be completed onaper or on the Internet. The Johns Hopkins Medicinenstitutional Review Board approved the study protocol anduestionnaire.

uestionnaire ContentAll physicians received a questionnaire consisting of a

ypothetical scenario (describing a PCP evaluating a newatient with stage 3 CKD progressing to stage 4 CKD)ollowed by questions designed to assess physicians’ abili-ies to recognize the patient’s severity of kidney disease,ecommendations to the PCP for further diagnostic evalua-ion of the patient, and recommendations for referral of theatient to a nephrologist. Scenarios were identical for allhysicians (featuring a 50-year-old woman who had beeneen by another physician 4 months earlier than the currentime), with the exception of 2 patient characteristics (raceAfrican American or Caucasian] and comorbid illness pro-le [hypertension only or hypertension with diabetes]),hich varied at random within each scenario. We varied race

nd comorbid illness profiles of patients to assess our a prioriypothesis that physicians’ recommendations might changeased on these patient characteristics. For patients with

ypertension only, the patient was described as taking a p

aily diuretic with appropriate blood pressure control andormal physical examination findings. For patients withoth hypertension and diabetes, the patient was described asaking an oral hypoglycemic agent and an angiotensin 2eceptor blocking agent with appropriate blood pressureontrol and normal physical examination findings. In eachcenario, the patient was described to have persistent protein-ria (ascertained by using gross colorimetric dipstick) dur-ng a 4-month period and laboratory findings (ie, serumreatinine) consistent with, but not explicitly stated as,DOQI stage 3 CKD (GFR, 30 to 59 mL/min/1.73 m2 [0.50

o 0.98 mL/s]) progressing to stage 4 (GFR, 15 to 29L/min/1.73 m2 [0.25 to 0.48 mL/s]) CKD within a 4-month

eriod. The patient also was described to have height of 5= 2�157.5 cm) and weight of 154 lb (69.9 kg). Physicians wererovided with enough clinical information in the scenario tose either the Cockcroft-Gault or the modified Modificationf Diet in Renal Disease19 equations to calculate the pa-ient’s estimated GFR themselves, but they were not pro-ided with actual estimated GFR using either calculation.hysicians also were provided with information regarding

he patient’s laboratory values from 4 months before the firstisit to the general internist and repeated laboratory valuesbtained as a result of the patient’s current visit to the PCPTable 1) . Before conducting the study, the questionnaire wasilot tested among 30 practicing internists, family practicehysicians, and nephrologists in Baltimore, MD, who providedeedback regarding hypothetical scenarios and study questions.

odifications to scenarios and study questions were made inesponse to comments provided during pilot testing.

stimation of Kidney FunctionAfter physicians read the patient scenario, we asked them,

What is your estimate of the patient’s kidney function?”nswers for this question corresponded to NKF-KDOQI

tages 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 (1.0o 1.48 mL/s), (3) GFR of 30 to 59 mL/min/1.73 m2 (0.50 to.98 mL/s), (4) GFR of 15 to 29 mL/min/1.73 m2 (0.25 to.48 mL/s), (5) GFR less than 15 mL/min/1.73 m2 (�0.25L/s), and (6) “I am unsure.” Answers of GFR of 30 to

9 mL/min/1.73 m2 or 15 to 29 mL/min/1.73 m2 correctlydentified the patient’s level of kidney function. To confirmhysicians’ abilities to identify the patient’s severity ofidney function, we independently reassessed their judg-ents of patients’ kidney function at a later point in the

urvey, asking them, “How would you describe the patient’sidney disease?” Answers for this question corresponded toKF-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,” or5) “end-stage kidney disease.” Answers of “moderate” orsevere” were considered to be concordant with correctdentification of the patient’s level of kidney function.

iagnostic EvaluationWe also asked physicians to report which diagnostic

tudies they thought the PCP should order for further evalu-tion and whether they thought the PCP should refer the

atient to a nephrologist. We asked, “Should the PCP order

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BOULWARE ET AL194

ny of the following laboratory tests within the next feweeks?” and we provided a list of serology, hematology,

mmunology, virology, urine, and radiological studies onhich they could indicate “yes,” “no,” or “maybe” for each

est. We considered answers of yes or no to indicate physi-ians’ definitive preferences and answers of maybe to indi-ate their uncertainty regarding ordering certain diagnosticesting for the patient.

ecommendations for ReferralWe also asked, “Based on the information you know

bout this patient, do you recommend that the PCP refer [theatient] to a nephrologist at this time?” with possible an-wers of “yes” or “no.” For participants recommendingeferral, we also asked them their preferences regarding: (1)he optimal time frame for referral, (2) whether the nephrolo-ist should take over the patient’s care or the PCP shouldaintain primary supervision, (3) the desired frequency of

ephrologist input, and (4) types of guidance the PCP shouldeek from a nephrologist. To further assess physicians’hresholds for referral of patients, we asked them to identifyhe estimated GFR at which they believed the PCP shouldefer a patient such as the patient featured in the scenario to aephrologist by using a visual analogue scale in whichhysicians could circle the GFR level (ranging from 0 to2 mL/min/1.73 m2 [0 to 0.20 mL/s]) they believed was

Table 1. Example of Information Provided to

Clinical History an

istory of present illness 50-year-old Africanarea and is seeinmedications regu

ast medical history Hypertension (10-yocial history Married, has 3 chil

(fee-for-service)specialist if need

eview of systems Negativeedications Daily diuretic and a

angiotensin 2 rewith hypertensio

hysical examination Blood pressure, 12unremarkable (in

Labor

omplete blood countlectrolytes and liver function studiesrinalysis (gross dipstick)erum creatinine (mg/dL)

NOTE. To convert serum creatinine in mg/dL to �mol/L, m*Hypothetical patient scenarios randomly varied patient r†Estimated GFR, 32.1 mL/min/1.73 m2 (using modifiL/min/1.73 m2 (using Cockcroft-Gault equation) for Africa‡Estimated GFR, 28.9 mL/min/1.73 m2 (using modifiL/min/1.73 m2 (using Cockcroft-Gault equation) for Africa

ppropriate for referring the patient. a

uideline AwarenessWe assessed physicians’ awareness of existing clinical

ractice guidelines for CKD by providing them with a list ofeveral professional medical organizations and asking themf they were aware of clinical guidelines published by any ofhe organizations. Answers could be “yes” or “no.”

arriers to CareTo assess perceptions regarding potential barriers in the

are of their patients with CKD, we assessed physicians’greement with the statements, “The medical care I imple-ent for patients such as this helps slow the progression ofKD and improve outcomes over time,” and “I believe Iave enough clinical and administrative resources availableo provide all the appropriate care that my patients withKD need based on their current conditions.” We alsossessed reasons why participants did not completely agreeith these statements. We asked PCPs, “How much of the

ime do you experience difficulties referring patients likehis [referring to the patient scenario] to a nephrologist?”nd their reasons for difficulties.

tatistical AnalysisWe used bivariate (chi-square) statistics to identify differ-

nces (according to physician specialty) in physicians’ char-

Physicians in Hypothetical Patient Scenario

ical Examination

ican (Caucasian*) woman who recently moved to theP for the first time. She takes her previously prescribedemainder of history of present illness is unremarkable.

on) only (or with diabetes [5-y duration]),* obesityorks as administrative assistant, nonsmoker, indemnityinsurance plan that does not restrict receipt of referral to

inophen (for patient with hypertension only) orblocking agent and oral hypoglycemic agent (for patientiabetes)m Hg; weight, 154 lb; height, 5= 2�; otherwise

g eye, cardiovascular, and neurological examinations)

udies

onths Before Visit 1 Week After Visit

Normal NormalNormal Normal1� protein 1� protein

2.1† 2.3‡

by 88.4; GFR in mL/min to mL/s, multiply by 0.01667.d patient comorbid disease status.dification of Diet in Renal Disease equation) and 35.4rican patient.dification of Diet in Renal Disease equation) and 32.3rican patient.

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PHYSICIAN CARE OF PATIENTS WITH CKD 195

heir recommendations regarding the diagnostic evaluationnd referral of the patient, including their preferences regard-ng the optimal time frame for referral of the patient to aephrologist, primary supervision of the patient’s care, fre-uency of nephrologist input regarding the patient’s care,nd types of guidance physicians believed nephrologistshould provide the PCP. To address test-retest reliability, wencluded questions in different sections of the questionnairehat allowed us to test the consistency of scenario responsesith regard to recognition of CKD and recommendations for

eferral. We assessed consistency in individual physicians’ssessments of patients’ kidney function by comparing re-ponses to separate questions requiring a response of a rangef GFR versus a qualitative descriptive response (eg, “severeidney dysfunction”). We also assessed the median GFR athich physicians of different specialties recommended theatient be referred for nephrologist care. We used logisticegression to estimate the proportion of physicians recom-ending specific diagnostic testing after adjustment for

atient race and comorbid conditions.We performed multivariable logistic regression to identify

hysician (years in practice, physician specialty, practiceetting, and proportion of time spent in clinical settings) oratient scenario (patient race and comorbid disease statushypertension only versus hypertension and diabetes]) char-cteristics independently associated with recognition of CKDnd referral of hypothetical patients. We also performedultivariable logistic regression to determine whether poten-

ial differences in physicians’ recommendations for referralf the patient remained after adjustment for physicians’ recog-ition of stages 3 to 4 CKD. In separate multivariable logisticegression models, we assessed whether PCPs’ awareness ofKD or perceived barriers to the care of patients with CKDas associated with their recommendations for referral.

RESULTS

esponse Rate, Scenario Randomization, andhysician Characteristics

Of 1,200 physicians initially targeted, 131 hadoved, were no longer contactable, or had incor-

ect addresses; 52 were not PCPs or nephrolo-ists; and 58 were dead or no longer practicingedicine (total, 241 ineligible physicians). Of

he remaining 959 eligible physicians, 304 physi-ians responded (comprising 178 PCPs [89 fam-ly physicians and 89 general internists] and 126ephrologists; 28% response rate for family phy-icians, 28% for general internists, 39% for neph-ologists). There were no differences betweenesponding and nonresponding physicians withegard to age (mean, 46 � 11 [SD] versus 47 �1 years, respectively; P � 0.05), sex (29% menersus 27% women, respectively; P � 0.05),ears in clinical practice (mean, 14 � 12 versus4 � 11 years, respectively; P � 0.05), or

eographic census region of residence (North- P

ast, 23% versus 26%; North Central, 24% ver-us 23%; South, 32% versus 34%; and West,0% versus 19%, respectively; P � 0.05).

Hypothetical patient characteristics (hyperten-ion alone versus hypertension plus diabetes andfrican-American versus white race) were dis-

ributed equally among study physicians. PCPsnd nephrologists were similar with respect toheir self-reported ethnicity, race, and years inractice. PCPs were more likely than nephrolo-ists to be women, practice in solo or grouprivate practice settings, spend more time inlinical settings, and spend the majority of theirime caring for patients with diseases other thanidney disease. PCPs also were more likely thanephrologists to turn to non–kidney disease–pecific professional organizations for clinicalractice guidelines (Table 2).

uccessful Identification of CKD andecommendations for Evaluation

In bivariate analyses, PCPs were statisticallyignificantly less likely to recognize the hypotheti-al patient as having CKD compared with neph-ologists, with nearly 30% of family physiciansnd 15% of general internists reporting theyere “unsure” of the patient’s GFR (versus 2%f nephrologists unsure; P � 0.01; Table 3).ifferences in recognition persisted after adjust-ent for practice setting, years in practice, per-

entage of clinical time, patient scenario, andensus region (Fig 1). There was a strong correla-ion between physicians’ separate assessmentsf patients’ kidney dysfunction: 98% of neph-ologists who recognized the patient as havingKD assessed the patient as having “moderate”r “severe” kidney dysfunction, 85% of general-sts who recognized the patient as having CKDssessed the patient as having “moderate” orsevere” kidney dysfunction, and 59% of familyedicine physicians who recognized the patient

s having CKD assessed the patient as havingmoderate” or “severe” kidney dysfunction, all� 0.01.There was a graded relation between degree of

dult and kidney disease specialization and phy-icians’ recommendations for many diagnostictudies, with family physicians and general inter-ists less likely than nephrologists to recommendany diagnostic tests with certainty (Fig 2).

CPs were more likely than nephrologists to

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xpress uncertainty regarding recommendationsf urine microscopic examination (11% of fam-ly physicians versus 1% of general internistsnd 3% of nephrologists; P � 0.01), magneticesonance angiography of the renal arteries (23%f family physicians, 19% of general internists,% of nephrologists; P � 0.01), and renal ultra-ound (18% of family physicians, 14% of gen-ral internists, and 5% of nephrologists; P � 0.01).

hysicians’ Preferences for Referral

PCPs were statistically significantly less likelyhan nephrologists to recommend referral to a

Table 2. Characteristics of Responding Physi

Characteristic

FamP

ears in practice0-10�10

exMaleFemale

thnicityHispanicNon-HispanicaceAsianAfrican AmericanWhite�2 racesOtheregionNortheastNorth centralSouthWest

ractice setting*Solo privateGroup privateHealth maintenance organization, staff modelUniversityCommunity hospitalGovernment health care facility

ercentage of time spent inClinical activitiesResearch activitiesAdministrative activities

ercentage of time spent seeingPatients with kidney diseasePatients with other diseases

NOTE. Values expressed as number (percent) or mean � SAbbreviation: NS, not significant.*Options were not mutually exclusive; physicians may ha

ephrologist (Table 3). This finding remained m

obust after adjustment for physicians’ recogni-ion of the patient’s CKD (Fig 1). Among physi-ians recommending referral, most preferred thateferral occur within 2 to 3 months of the pa-ient’s evaluation by the PCP. Among physicianselieving the PCP should continue to assumerimary supervision of the patient’s care withuidance from the nephrologist, PCPs were moreikely than nephrologists to recommend less fre-uent input from referring nephrologists (16% ofamily physicians and 20% of general internistsersus 6% of nephrologists recommending refer-ing nephrologist input monthly to every 6

Selected Randomly Across the United States

ctices

)General Internists

(n � 89)Nephrologists

(n � 126) P

NS) 50 (56) 56 (44)) 39 (44) 64 (51)

0.03) 62 (70) 95 (75)) 27 (30) 26 (21)

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27 (30) 31 (25)2 (2) 5 (4)

) 54 (61) 78 (62)1 (1) 2 (2)3 (3) 8 (6)

NS) 28 (31) 30 (24)) 19 (21) 27 (21)) 25 (28) 50 (40)) 17 (19) 19 (15)

) 14 (16) 11 (9) 0.03) 36 (40) 68 (54) NS

7 (8) 5 (4) NS) 21 (24) 40 (32) �0.01) 22 (25) 32 (25) NS) 8 (9) 7 (6) NS

7 89 � 20 76 � 26 �0.019 � 20 15 � 22 �0.01

6 11 � 17 15 � 18 NS

17 � 13 86 � 20 �0.010 81 � 18 15 � 18 �0.01

centages may not equal 100% because of missing values.

cted more than 1 option.

cians

ily Prahysician(n � 89

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PHYSICIAN CARE OF PATIENTS WITH CKD 197

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

Family PracticePhysicians(n � 89)

General Internists(n � 89)

Nephrologists(n � 126) P

stimation of GFR (mL/min/1.73 m2) �0.0190-120 1 (1) 0 060-89 8 (9) 7 (8) 2 (2)30-59 44 (49) 47 (53) 107 (85)15-29 6 (7) 16 (18) 14 (11)�15 2 (2) 1 (1) 0I am unsure 27 (30) 13 (15) 2 (2)orrect recognition of CKD 50 (56) 63 (71) 121 (96) �0.01ecommendation for referral �0.01Yes 63 (71) 66 (74) 121 (96)No 23 (26) 21 (24) 3 (2)ptimal time frame* NSNext 1-4 wk 32 (51) 33 (50) 63 (52)Next 2-3 mo 26 (41) 26 (39) 52 (43)Next 4-6 mo 1 (2) 3 (5) 4 (3)Next 7-9 mo 0 0 0Next 10-11 mo 0 0 0Within 1 y 1 (2) 1 (2) 0

rimary supervision of care* NSLet PCP continue care with nephrologist’s guidance 51 (81) 54 (82) 113 (93)Let nephrologist take over care 9 (14) 10 (15) 7 (6)

requency of input† 0.01Once and then later if needed 8 (16) 11 (20) 7 (6)Every mo 2 (4) 0 4 (4)Every 2-3 mo 8 (16) 15 (28) 34 (30)Every 4-6 mo 24 (47) 22 (41) 60 (53)Every 7-9 mo 2 (4) 2 (4) 0Every 10-12 mo 6 (12) 2 (4) 2 (2)Every 1-2 y 1 (2) 1 (2) 1 (1)Every 2� y 0 0 0

ypes of guidance desired from nephrologist (v notdesired)†

Confirmation of appropriate evaluation 48 (94) 51 (94) 107 (95) NSAdditional evaluation and testing 50 (98) 49 (91) 105 (93) NSNutritional advice 41 (80) 41 (76) 101 (89) NSAdvice about medication regimen 50 (98) 46 (85) 109 (96) NSPredialysis/renal replacement therapy preparation 25 (49) 30 (56) 83 (73) �0.01Electrolyte management 25 (49) 23 (43) 91 (81) �0.01Assessment/management of anemia 0 (0) 0 (0) 14 (12) �0.01Assessment/management of metabolic bone disease 0 (0) 0 (0) 14 (12) �0.01Assessment/management of cardiovascular disease

risk factors 0 (0) 1 (2) 8 (7) NSManagement and assessment of kidney disease

severity 0 (0) 3 (6) 5 (4) NSPatient education 0 (0) 0 (0) 4 (4) NS

NOTE. Values expressed as number (percent). Percentages may not equal 100% because of missing values. To convertFR 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

atient with nephrologist’s guidance.

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uestion about referral to assess physicians’ con-istency, nephrologists recommended that pa-ients similar to the patient in the scenario beeferred earlier than general internists and familyedicine physicians (median estimated GFR for

eferral, 39 mL/min/1.73 m2 (interquartile range,4 to 44 mL/min/1.73 m2 [0.65 mL/s; interquar-ile range, 0.57 to 0.73 mL/s] versus 32 mL/min/.73 m2; interquartile range, 26 to 36 mL/min/.73 m2 [0.53 mL/s; interquartile range, 0.43 to.60 mL/s] and 32 mL/min/1.73 m2; interquartileange, 26 to 36 mL/min/1.73 m2 [0.53 mL/s;nterquartile range, 0.43 to 0.60 mL/s], respec-ively; P � 0.001).

Physicians recommending referral most fre-uently believed the following types of guidancehould be sought from nephrologists: confirma-ion of appropriate evaluation of the patient byhe PCP (95%), additional evaluation and testing94%), advice about the patient’s medicationegimen (94%), nutritional advice (84%), adviceegarding electrolyte management (64%), andredialysis/renal replacement therapy prepara-ion (63%). Family physicians and general inter-ists were less likely than nephrologists to be-ieve advice should be sought from consultingephrologists on predialysis/renal replacement

Fig 1. Correct identification of CKD and recommendn practice, practice setting, percentage of clinical time*Adjusted for correct identification of stages 3 to 4 CKime, census region, and patient race and comorbid co

herapy preparation, advice on electrolyte man- (

gement, assessment/management of anemia, andssessment/management of metabolic bone dis-ase (Table 3).

haracteristics Associated With Correctdentification of CKD Severity andecommendation of Referral

After adjustment, family physicians with morehan 10 years in clinical practice were least likelyo recognize CKD (Table 4). Family physiciansnd general internists with more than 10 years inlinical practice were least likely to recommendatient referral (Table 4).

erceived Barriers to Patient Referral andelation of Perceived Barriers to Referral

PCPs were less likely than nephrologists to:1) be aware of existing clinical practice guide-ines, (2) believe the medical care they imple-ent for patients with CKD slows CKD progres-

ion and improves clinical outcomes, and (3)elieve they have enough clinical and administra-ive resources to provide appropriate care foratients with CKD. Family physicians were moreikely than general internists to report that theyxperience difficulties referring patients withKD to nephrologists at least a little of the time

for referral by physician specialty. *Adjusted for yearsus region, and patient race and comorbid conditions.rs in practice, practice setting, percentage of clinicals.

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PHYSICIAN CARE OF PATIENTS WITH CKD 199

Among family physicians, those agreeing thatheir care improves the health of patients had

Fig 2. Diagnostic studies recommended* by phyrogressive CKD. (A) Serological and hematologic stund radiological studies. *Adjusted for patient race anesonance angiography. □ � Family practice physician

-fold greater odds (odds ratio, 6.1; 95% confi- t

ence interval [CI], 1.2 to 31.6) of recommend-ng referral of patients with CKD compared with

s for the evaluation of a hypothetical patient withB) immunologic and virological studies, and (C) urineorbid conditions. †Complete blood count. ‡Magneticgeneral internists; � � nephrologists.

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mproves clinical outcomes. Among general in-ernists, those aware of existing clinical guide-ines had 14-fold greater odds (odds ratio, 14.5;5% CI, 1.1 to 186.3) of recommending referralompared with their counterparts who were notware of guidelines, whereas those stating thathey have enough clinical and administrativeupport to care for patients with CKD were 90%ess likely (odds ratio, 0.10; 95% CI, 0.02 to.68) to recommend referral compared with theirounterparts reporting that they do not havenough support.

DISCUSSION

In this study of physicians sampled randomlyrom across the United States, our findings suggesthat efforts to raise physicians’ awareness of pro-

Table 4. Physician and Patient CharacteristicsRecommen

Physician Characteristic

Correct Identificof Stage 3-4 C

Adjusted* % (95

pecialty and years in practiceFamily practice physician, 0-10 y 64 (46-79)Family practice physician, � 10 y 55 (42-69)General internist, 0-10 y 77 (62-87)General internist, �10 y 78 (61-89)Nephrologist, 0-10 y 96 (87-99)Nephrologist, �10 y 99 (92-100

ractice setting‡Community hospital 90 (80-95)All other settings 88 (80-93)

ime spent in clinical setting (%)�50 87 (79-92)�50 98 (87-100

atient scenario characteristic§atient raceAfrican American 90 (83-95)Caucasian 86 (77-92)

atient comorbid conditionsHypertension only 91 (83-95)Diabetes and hypertension 86 (77-92)

Abbreviation: NS, not significant.*Adjusted for years in practice, physician specialty, practi

f questionnaire (patient race and comorbid conditions).†Adjusted for correct identification of stage 3 to 4 CKD, y

f clinical time, census region, and version of questionnaire‡No significant differences in other practice settings.§For patient scenario characteristics: adjusted for years

linical time, census region, patient comorbid conditions (hAfrican American or Caucasian).

ressive CKD and disseminate recently developed m

linical practice guidelines have not been as effec-ive as hoped.17,18 Our findings highlight that PCPsnd nephrologists have different perceptions ofow the evaluation of patients with progressiveKD should be undertaken and the intensity withhich specialists should be involved in their care.his national study is consistent with results ofarlier regional studies showing that patients withKD who receive care in primary care settings

requently do not receive care in accordance withKF-KDOQI guideline recommendations released

n 2000.12,20 Our study also extends previous re-earch by assessing physicians’ care for a standard-zed patient, thereby eliminating potential confound-ng caused by practice setting or unmeasured patientharacteristics. Most importantly, it identifies phy-ician-related mechanisms through which subopti-

ciated With Correct Identification of GFR andof Referral

P Trend

Recommendation forPatient Referral

Adjusted† % (95%CI) P Trend

�0.01 �0.0185 (68-93)69 (54-81)88 (75-95)66 (48-81)98 (90-99)99 (92-100)

NS NS91 (81-96)92 (86-96)

NS NS90 (84-94)99 (89-100)

NS NS92 (85-96)90 (82-95)

NS NS92 (85-96)90 (83-95)

ing, percentage of clinical time, census region, and version

practice, physician specialty, practice setting, percentagent race and comorbid conditions).

ctice, physician specialty, practice setting, percentage ofsion only or diabetes and hypertension), and patient race

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PHYSICIAN CARE OF PATIENTS WITH CKD 201

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

Characteristic

Family PracticePhysicians(n � 89)

GeneralInternists(n � 89)

Nephrologists(n � 126) P

o your knowledge, have any [organizations] issued guidelinesregarding referral of patients with CKD? �0.01

Yes 30 (34)* 29 (33)* 100 (79)No 8 (9) 11 (12) 3 (2)I am unsure 48 (54) 49 (55) 22 (17)

he medical care I implement for patients such as this helps to slowprogression of CKD and improve outcomes over time �0.01

Completely agree 22 (25)* 41 (46) 66 (52)Less than completely agree 64 (72) 47 (53) 59 (47)easons for incomplete agreement with the above question†Many patients are nonadherent (Agree [v not agree]) 48 (72) 33 (69) 46 (77) NSSee little evidence that treatments slow disease (Agree [v not agree]) 6 (9)* 4 (8) 1 (2) NSAlthough improvement is shown in studies, I do not see improvement

in my patients (Agree [v not agree]) 13 (19) 5 (10) 7 (12) NSMy patients have so many important clinical issues to address that I

have little time to address their kidney disease (Agree [v not agree]) 11 (16)* 7 (15)* 2 (3) �0.01believe I have enough clinical and administrative resources available

to provide all the appropriate care that my patients with CKD needbased on their current conditions �0.01

Completely agree 20 (22)* 22 (25)* 50 (40)Less than completely agree 67 (75) 67 (75) 74 (59)easons for incomplete agreement with the above question‡No electronic patient records (Agree [v not agree]) 17 (25) 14 (21) 28 (37) NSNo electronic laboratory studies (Agree [v not agree]) 11 (16) 10 (15) 14 (18) NSNeed ancillary support (Agree [v not agree]) 18 (26)* 22 (33) 38 (50) NSNot enough secretarial support (Agree [v not agree]) 14 (27) 14 (21) 24 (32) NSMany patients cannot afford appropriate medications (Agree [v not

agree]) 40 (58) 42 (63) 57 (75) NSow much of the time do you experience difficulties referring patients

like this to a nephrologist? 0.02Not at all 45 (51) 61 (69) NAAt least a little of the time 42 (47) 28 (31) NA

greement with statements among those facing difficulty§Nephrologists are not interested in seeing these patients (Agree [v

not agree]) 6 (14) 6 (21) NA NSThere are no (few) nephrologists in my geographic area (Agree [v not

agree]) 23 (52) 8 (29) NA NSNephrologists are overbooked and often cannot accommodate

patients like this in their practice (Agree [v not agree]) 18 (41) 16 (57) NA NSNephrologists may want to completely take over the patient’s care

(Agree [v not agree]) 6 (14) 5 (18) NA NSInsurance companies restrict my abilities to refer patients to

nephrologists (Agree [v not agree]) 15 (34) 4 (14) NA NS

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: “Theedical 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

ypothetical 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

uch of the time do you experience difficulties referring patients like this to a nephrologist?”

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BOULWARE ET AL202

Suboptimal recognition of progressive CKDould be attributed to a variety of potential rea-ons, including lack of knowledge regardingethods to calculate estimated GFR, lack of

ime, and inadequate knowledge of CKD riskactors. A recent regional study showed thatCPs were not aware of significant risk factorsor CKD, suggesting that targeted education ofCPs is needed.21 Provider differences in recom-endations for referral of patients with more

apid progression of CKD (as presented in ourypothetical scenarios) may represent an evenore clinically relevant problem than lack of

ecognition of CKD on the part of generalistsecause referral to nephrologist care and institu-ion of appropriate therapies for such persons haseen shown to improve clinical outcomes.5,14,22-25

ossible explanations for differences in recom-endations for referral include lack of knowl-

dge of or uncertainty regarding clinical recom-endations regarding specialty referral, lack of

nowledge of risk factors for CKD progres-ion,21,26 or lack of agreement with clinical rec-mmendations (shown in other diseases to affecthysician practice adherence to clinical practiceuidelines).27 Our findings that general internistsware of recent clinical guidelines and familyractice physicians who believe their care couldnhance patients’ clinical outcomes were moreikely to recommend referral support this hypoth-sis. Although this study did not directly measurehe effectiveness of efforts by the National Insti-utes of Health’s National Kidney Disease Edu-ation Program (which began in 2003) and oth-rs to implement uniform laboratory reporting ofFR and expose physicians to educational mate-

ials and clinical decision aids for CKD care thatould help PCPs estimate the severity of CKDore accurately, provide support for decisions to

efer patients, and enhance some physicians’onfidence in the likelihood of improving clini-al outcomes by instituting recommended care, itrovides evidence that physicians may not havead adequate exposure to these or similar effortst the time of this study.28

Our results also suggest mechanisms for varia-ion in recommendations for referral. Generalnternists who reported that they had enoughlinical and administrative support were lessikely to recommend referral. Some general inter-

ists may have confidence in their abilities to t

rovide appropriate care for these patients anday not perceive added benefit to referring pa-

ients for specialty care. Prior work indicates thathysicians may not seek referrals if they believehey have informal access to clinical specialistsho can provide answers to needed questions

egarding management of patients with chronicllnesses.29,30 General internists may have moreeady access to medical specialists than familyhysicians. Family physicians more often re-orted a lack of nephrologists in their geographicrea. Whereas evidence suggests early referralor appropriate care of patients with CKD canmprove clinical outcomes,13,14 it remains un-lear whether appropriate care delivered by PCPsith limited nephrologist input leads to worse

linical outcomes.Disagreement regarding when and why pa-

ients with CKD should be referred for specialistare may reflect not only a lack of uniformityegarding information disseminated to physi-ians, but also differences in how physicianserceive their roles in the care of such patients.CPs may desire to maintain continuity of careor their patients with chronic illnesses whileinimizing unnecessary testing. In addition, theyay be faced with balancing competing priori-

ies among other chronic illnesses. However,isagreement between PCPs and specialists couldontribute to confusion regarding care and poten-ially lead to omissions or redundancies in care,ltimately decreasing overall quality of care orncreasing costs. Recent research indicates thatmplementation of models with shared clinicalare by PCPs and nephrologists may enhanceutcomes without overburdening nephrolo-ists.31 Thus, efforts to achieve consensus withegard to optimal management strategies couldmprove clinical outcomes. Although existingKD clinical practice guidelines in the Unitedtates were generated from within the nephrol-gy community, the development of additionaluidelines simultaneously endorsed by familyedicine, general internal medicine, and neph-

ologist groups could move efforts to reach con-ensus forward. Physicians in other countriesave sought to develop guidelines incorporatingeneralist and specialist input into care of pa-ients with CKD, but similar efforts have not yetccurred within the United States.32 Collabora-

ive efforts in guideline development for other

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PHYSICIAN CARE OF PATIENTS WITH CKD 203

llnesses may have helped achieve broader dis-emination of clinical practice guidelines forhese illnesses among specialists and generalistsn the United States.33-36

It is noteworthy that PCPs with more than 10ears of clinical practice experience were leastikely to recognize CKD and also least likely toecommend referral. These findings strongly con-rm other studies indicating that more recently

rained physicians are more aware of currentreatment guidelines and potentially deliver bet-er quality care.37,38 Physicians with more yearsn practice should be targeted for disseminationf information regarding the identification andppropriate referral of patients with CKD.

Limitations of this study deserve mention.lthough we studied a national sample of UShysicians and made many follow-up contacts,ur response rate was suboptimal, potentiallyimiting generalizability. However, our analysesomparing participating with nonparticipatinghysicians indicate that the only difference washysician specialty. The lower primary care re-ponse may indicate lack of awareness or interestn CKD as an important clinical problem. Sec-nd, we asked physicians to provide advice re-arding a hypothetical patient. Clinicians seeingatients in real life might act differently, al-hough scenarios have been shown to have valid-ty in quality or care assessment.39 Although weere interested in assessing physicians’ re-

ponses when evaluating patients with progres-ive kidney disease, one of our scenarios fea-ured a patient with hypertension. It is possiblehat some physicians believed this patient wasot likely to experience a further rapid decreasen kidney function because such rapid decrease isot observed as frequently in patients with hyper-ension. Third, our questionnaire asked physi-ians about a brief episode of care with a singleatient. Practice patterns might vary for patientseen over longer periods. Fourth, we did notrovide physicians with tools to estimate GFR ornformation on where to find tools.40 Comparinghysicians with no information on tools for cal-ulating estimated GFR with physicians withrompting to use tools would help ascertain theffect of ongoing efforts to enhance both calcula-ion of estimated GFR by clinicians and report-

ng of GFR among clinical laboratories.28 2

Notwithstanding these limitations, we foundhat PCPs were less likely to recognize CKD orecommend referral of patients and differed frompecialists with regard to their recommendedvaluation of patients and preferences regardinghe degree of specialist involvement in patients’are. Awareness of clinical guidelines, confi-ence in the effectiveness of care, and percep-ions regarding the amount of available clinicalnd administrative support were related stronglyo primary care referral recommendations. Greaterissemination of existing clinical guidelines, tar-eted education of PCPs, and work to involveoth PCPs and nephrologists in consensus-uilding efforts that more clearly delineate strat-gies for diagnosing and managing patients withrogressive CKD, including collaboration toevelop joint clinical practice guidelines, couldnhance the care of these high-risk patients.

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