Anemia After Kidney Transplantation Is Not CompletelyExplained by Reduced Kidney Function
Steven J. Chadban, MD, PhD, Laura Baines, MD, PhD, Kevan Polkinghorne, MD,Andrew Jefferys, MD, Sharan Dogra, MD, PhD, Claire Kanganas, MD, PhD, Ashley Irish, MD,
Josette Eris, MD, PhD, and Rowan Walker, MD
Background: Anemia is prevalent among kidney transplant recipients and likely contributes tomortality and morbidity. Prevalence of anemia is associated strongly with degree of kidney graftdysfunction; however, it remains unclear whether additional transplant-associated factors alsocontribute.
Methods: The aim of this study is to compare the prevalence of anemia between 2 cohorts, 1 ofkidney transplant recipients (n � 851) and another from the general population (n � 732), sourced fromsubjects of the AusDiab study and selected by means of propensity score to provide a cohort matchedfor kidney function (Cockcroft-Gault creatinine clearance).
Results: Average hemoglobin level in kidney transplant recipients was (13.1 g/dL [131 g/L]; range,9.0 to 18.0 g/dL), significantly less than in the general population (14.3 g/dL [143 g/L]; range, 9.7 to 20.0g/dL). The prevalence of anemia (hemoglobin � 12.0 g/dL [�120 g/L] for females; �12.5 g/dL [�125g/L] for males) was almost 10-fold greater in kidney transplant recipients (30.8%) versus the generalpopulation (3.4%). Average hemoglobin level was lower in the kidney-transplant-recipient cohort at alllevels of creatinine clearance. Considering both cohorts pooled, multivariate analysis showed thattransplant status had the strongest association with anemia, followed by sex, creatinine clearance, andage.
nemia is a frequent consequence of decreas-ing kidney function, which at best is debili-
ating, but at worst may contribute to the excessardiovascular mortality observed in patients withrogressive kidney failure.1 Successful kidneyransplantation may be associated with completeorrection of anemia; however, recent studiesescribed persistence of anemia in approxi-ately one third of kidney transplant recipients.2
idney function was identified as the key deter-inant of anemia posttransplantation; however,
ther factors unique to transplantation also mayontribute.
The aim of this study is to compare the preva-ence of anemia between a cohort of Australianidney transplant recipients versus a cohort ofhe general Australian adult population with simi-ar kidney function and thereby determinehether kidney function completely accounts
or anemia posttransplantation.
METHODS
This study is a retrospective case-control study of therevalence of anemia in kidney transplant recipients versus
eneral-population subjects matched for creatinine clear-
merican Journal of Kidney Diseases, Vol 49, No 2 (February), 20
nce (CrCl). Anemia is defined as hemoglobin (Hb) concen-ration less than 12.5 g/dL (�125 g/L) in males and less than2.0 g/dL (�120 g/L) in females. CrCl was calculated usinghe Cockcroft and Gault formula.3
idney Transplant Recipients
Cross-sectional data were obtained from patients from 4ustralian kidney transplant centers. All patients at each
enter who were older than 16 years and had a functioning
From the Renal Medicine and Transplantation, Royalrince Alfred Hospital and University of Sydney, Camper-own; Department of Nephrology, Monash Medical Centre,layton; Department of Kidney Medicine, Royal Perth Hos-ital, Perth; and Department of Kidney Medicine, Royalelbourne Hospital, Parkville, Australia.Received June 28, 2006; accepted in revised form Novem-
er 9, 2006.Originally published online as doi:10.1053/j.ajkd.2006.11.034
n January 4, 2007.Support: None. Potential conflicts of interest: None.Address reprint requests to Steven J. Chadban, MD, PhD,
ransplantation, Level E9, Royal Prince Alfred Hospital,amperdown, NSW 2050, Australia. E-mail: [email protected]
raft for longer than 3 months at the time of the survey werencluded. Patients recorded as receiving erythropoietinherapy and those who received a combined kidney-pancreasransplant were excluded from the study.
Demographic and clinical data were collected during routineutpatient visits between October and December 2001 andncluded age, sex, weight, date of kidney transplantation, hospi-al where the transplantation was performed, primary kidneyisease, and presence or absence of diabetes. Laboratory dataollected included serum creatinine and Hb concentrations.ime from transplantation was calculated as the differenceetween the date of the survey and date of transplantation.
Maintenance immunosuppression was recorded as the usef individual agents, including steroids, cyclosporine, tacroli-us, mycophenolate mofetil (MMF), azathioprine, and rapa-ycin. Use of angiotensin-converting enzyme (ACE) inhibi-
ors and/or angiotensin II receptor antagonists (ARAs) andrythropoietin therapy was recorded.
ohort of the General Population
Subjects were selected from participants of the AusDiaburvey. This cross-sectional study of a representative samplef the noninstitutionalized Australian adult population wasndertaken in 1999 to 2000 and included measurement ofb and CrCl (Cockcroft-Gault) at a single time point.4 Of
1,247 subjects who completed the survey, glomerular filtra-ion rate (GFR) less than 60 mL/min/1.73 m2 (�1.00 mL/s/.73 m2) was present in 11.2%.5 For the present study, aohort was selected by using propensity score based on CrClnd sex (see Statistical Analysis). Data used for the presentnalysis include age, sex, weight, serum creatinine level, Hboncentration, and presence or absence of diabetes. Dataegarding drug therapy and the presence or absence ofreviously identified kidney disease were unavailable forhese patients.
tatistical Analysis
Using logistic regression, propensity scores were calcu-ated by using the combined AusDiab and kidney transplantohorts to estimate the probability (propensity) for theresence of a kidney transplant based on CrCl and sex.ropensity scores were used to obtain a matched cohort inhich kidney transplant recipients were matched to a control
ubject (without a transplant) based on propensity score.atching was performed by means of Mahalanobis metricatching within calipers defined by the propensity score5
sing the publicly available matching algorithm “psmatch2.”6
verall quality of matching was assessed by calculating theercentage of bias reduction among variables used to calcu-ate the propensity score and assessing the mean CrCletween 2 groups. Sample size decreases as the adequacy ofatching increases; therefore, the final propensity-matched
ohorts were determined by balancing adequacy of matchingithout decreasing the sample size excessively.Chi-square test was used to test the difference in propor-
ions in 2 or more groups. Differences between groups werenalyzed using Student t-test. Linear regression analysis wassed to explore the relationship between anemia and theollowing variables: age, sex, weight, time from transplanta-
ion, primary kidney disease, presence or absence of diabe- m
es, CrCl, and categorical use of individual immunosuppres-ive agents, including steroids, cyclosporine, tacrolimus,zathioprine, and MMF, and use of ACE inhibitors andRAs together. A multivariate model was used to confirm
he contribution of associations, and unrelated variables wereemoved from the model. For all statistical tests, P of 0.05 oress is considered significant. All analyses were performedsing SPSS, version 11.5 (SSPS Inc, Chicago, IL).
RESULTS
emographic and Clinical Characteristics
Kidney Transplant RecipientsA total of 1,222 kidney transplant recipients
ere evaluated. Excluded from the final analysisere 88 patients recorded as receiving erythropoi-
tin therapy, 150 patients with missing data, and1 patients who had received their transplant lesshan 3 months before data collection. An addi-ional 92 patients were excluded during match-ng by propensity score to subjects with chronicidney disease.Demographic and clinical characteristics of
he 851 kidney transplant recipients included inhe final analysis are listed in Table 1. Averageransplant recipient age at the time of survey was8 years, with average time from transplantationf 8 years. CrCl was higher in male comparedith female transplant recipients (P � 0.01).The distribution of primary kidney disease is
isted in Table 2. Glomerulonephritis was theost prevalent underlying pathological state, ac-
ounting for 43% of all cases. Diabetes was leastommon, accounting for only 6.2% of kidneyailure in this Australian population. Diabetesas present as a comorbidity in a substantiallyreater proportion at the time of the survey, in1% of the 528 subjects for whom these dataere available.Proportions of kidney transplant recipients ad-inistered individual immunosuppressive agents
t the time of survey are listed in Table 3.yclosporine was the most commonly pre-
cribed individual agent, used in 76% of allatients and equally between sexes. An antiprolif-rative agent was used by 90% of all patients,ith similar use of MMF and azathioprine. Ste-
oids were administered to 47% of patients, witho sex difference. Rapamycin was administeredo a small minority.
Use of ACE inhibitors and/or ARAs was docu-
ented in only 37% of all patients. However, of
to
7awrC
P
tFwan
j
tskCw(e
K
ggC
K
G
m
GDP
OU
P
C
CTA
AMR
Anemia in Kidney Transplant Recipients 303
hese, 54% of patients were administered eitherr both of these drugs.
General-Population CohortDemographic and clinical characteristics of
32 subjects selected from the AusDiab cohortre listed in Table 1. General-population subjectsere significantly older than kidney transplant
ecipients (P � 0.01), but were well matched forrCl (P � not significant).
revalence of AnemiaKidney Transplant RecipientsMean Hb concentration and number of pa-
ients with anemia are listed in Table 4 (Fig 1A).or the entire cohort, mean Hb concentrationas 13.1 g/dL (131 g/L), and prevalence of
nemia was 30.8%. Anemia was present in sig-ificantly more women than men (P � 0.01).
General-Population CohortMean Hb concentration and number of sub-
ects with anemia are listed in Table 1. Overall,
Table 1. Demographic
All
idney transplant recipientsNo. of subjects 851Age at survey (y) 48 (16-79)Time from transplantation (y) 7.6 (0.25-33.2)Serum creatinine (mg/dL) 1.45 (0.46-4.59)CrCl (mL/min) 65 (18-168)eneral population cohortNo. of subjects 732Age at survey (y) 64 (25-95)Time from transplantation (y) 1.07 (0.68-3.17)Serum creatinine (mg/dL) 68 (19-156)
Note: Data expressed as mean (range). To convert creatultiply by 0.01667.Abbreviation: NS, not significant (P � 0.05).
Table 2. Primary Kidney Disease in KidneyTransplant Recipients by Sex
he prevalence of anemia in general populationubjects was 3.4%, almost 10-fold less than inidney transplant recipients with equivalentrCls. In general-population subjects, womenere 4.5-fold more likely than men to be anemic
P � 0.01), whereas in kidney transplant recipi-nts, the excess risk was l.3-fold.
Prevalence of Anemia Stratified byidney FunctionThe prevalence of anemia was significantly
reater for kidney transplant recipients versuseneral-population subjects within each strata ofockcroft-Gault CrCl, with a near–10-fold ex-
Note: Data expressed as number (percent).*Six patients excluded because of incorrect calcineurin-
and C
477.5
1.5570
641.15
71
inine in
nhibitor data coding.
cmToetwcRlrnlmmamv
CH
rtioaatH
e(smtmr
gcc
CT
kstd1dgHi0hwogv0s
aang0cgctta1
les and
Chadban et al304
ess seen for CrCl greater than 60 mL/min (�1.00L/s) and 30 to 60 mL/min (0.50 to 1.00 mL/s;able 5). Because recent data showed the superi-rity of the Modification of Diet in Renal Dis-ase equation over Cockcroft-Gault as an estima-or of true GFR in kidney transplant recipients,7
e recalculated estimated GFR (eGFR) for bothohorts by using the Modification of Diet inenal Disease equation and determined the preva-
ence of anemia by eGFR strata. Prevalenceemained approximately 10-fold greater for kid-ey transplant recipients versus the general popu-ation for eGFR greater than 60 mL/min (�1.00L/s; 18.7% versus 2.4%) and eGFR of 30 to 60L/min (0.50 to 1.00 mL/s; 34.8% versus 3.8%),
lthough it was similar for GFR less than 30L/min (�0.50 mL/s) for both groups (58.3%
ersus 50%).
linical Associations Withb Concentration
For the combined cohort of kidney transplantecipients and general-population subjects, a mul-ivariate model showed that clinical factors affect-ng Hb concentration were, in order of the strengthf relationship, transplant status, sex, CrCl, andge, with each factor individually significantlyssociated with Hb concentration (P � 0.01) andogether responsible for 56% of the variability inb concentration (Fig 2).Hb concentration was related to CrCl within
ach group in both kidney transplant recipientsr � 0.33; P � 0.01) and general-populationubjects (r � 0.27; P � 0.01). However, theagnitude of this relationship was different be-
ween groups. For CrCl of 120 mL/min (2.00L/s), Hb concentration in kidney transplant
Note: Data expressed as mean (range) or number (perce*Anemic defined as Hb level less than 12.0 g/dL for fema
ecipients was only 0.6 g/dL (6 g/L) less than in b
eneral-population subjects; however, at a de-reased CrCl of 40 mL/min (0.67 mL/s), Hboncentration was 1.4 g/dL (14 g/L) less (Fig 3).
linical Associations With Hb in Kidneyransplant Recipients
Clinical associations with Hb concentration inidney transplant recipients according to sex arehown in Fig 2A and B. The relationship be-ween Hb concentration and CrCl was indepen-ent of sex (P � 0.01), and a decrease in CrCl of0 mL/min (0.17 mL/s) was associated with aecrease in Hb concentration of 0.23 g/dL (2.3/L) in men and 0.20 g/dL (2.0 g/L) in women.b concentration also was related weakly to age
n both men and women (r � 0.13 overall; P �.01). Men with polycystic kidney disease had aigher Hb concentration compared with thoseith glomerulonephritis as the underlying causef kidney failure (mean Hb, 14.3 versus 13.5/dL [143 versus 135 g/L]; 95% confidence inter-al of the difference, 0.28 to 1.46 g/dL; P �.01). Neither time from transplantation nor diagno-is of diabetes was related to Hb concentration.
Regarding the use of immunosuppressivegents, Hb concentration was higher in mendministered azathioprine compared with thoseot administered azathioprine (13.9 versus 12.8/dL [95% confidence interval of the difference,.40 to 1.67 g/dL] or 139 versus 128 g/L [95%onfidence interval of the difference, 4.0 to 16.7/L]; P � 0.01), whereas MMF had no signifi-ant effect on Hb level in men or women. Impor-antly, CrCl also was higher for those adminis-ered azathioprine versus those not administeredzathioprine (78 versus 68 mL/min [1.30 versus.13 mL/s]), and this may have contributed to
convert Hb in g/dL to g/L, multiply by 10.less than 12.5 g/dL for males.
centra
.0)
.0)
nt). To
etter Hb concentrations. Cyclosporine use was
amvc
gamg
and (Bf
Anemia in Kidney Transplant Recipients 305
ssociated with a lower Hb concentration in bothen and women compared with no use (12.9
ersus 13.6 g/dL [129 versus 136 g/L]; 95%onfidence interval of the difference, 0.38 to 0.10
Figure 1. Histograms of Hb concentrations in (A) maleemale subjects with chronic kidney disease.
Table 5. Prevalence of Anemi
CrCl (mL/min)
Transplant Recipients (n � 851)
No. of Patients Anemia (n) A
�60 463 10130-60 369 149�30 19 12
Note: To convert CrCl in mL/min to mL/s, multiply by 0.01667.
/dL; P � 0.01 overall), and tacrolimus use wasssociated with a lower Hb concentration in onlyen (13.4 versus 14.1 g/dL [134 versus 141
/L]; 95% confidence interval of the difference,
) female kidney transplant patients and (C) male and (D)
ified By Cockcroft-Gault CrCl
General Population (n � 732)
%) No. of Patients Anemia (n) Anemia (%)
425 7 1.7293 14 4.814 4 28.6
a Strat
nemia (
21.840.463.2
0diic
tl
w1em
C
Chadban et al306
.05 to 1.38 g/dL; P � 0.036). CrCls were notifferent between those administered calcineurinnhibitors or those not administered calcineurinnhibitors. There was no relationship between Hboncentration and use of steroids.
Use of ACE inhibitors and/or ARAs in pa-ients with available data was associated with a
ower Hb concentration in women compared C
ith no use (12.2 versus 12.9 g/dL [122 versus29 g/L]; 95% confidence interval of the differ-nce, 0.20 to 1.22 g/dL; P � 0.01), whereas inen, there was no significant effect.
linical Associations With CrCl
There was an inverse relationship between
Figure 2. Clinical associa-tions with Hb concentrations in(A) male and (B) female trans-plant recipients.
rCl and age (r � 0.30; P � 0.01). CrCl was
ukA
lAoAwcaAtpetpmtos
o
3pstejsCi
whfeermp
tAnbw
stpw
Anemia in Kidney Transplant Recipients 307
nrelated to time from transplantation, primaryidney disease, diagnosis of diabetes, and use ofCE inhibitors and/or ARAs.
DISCUSSION
This study is designed to document the preva-ence of anemia in kidney transplant recipients inustralia and compare this with the prevalencef anemia in a cohort of the general population ofustralian adults matched for CrCl to determinehether kidney function could completely ac-
ount for posttransplantation anemia. The over-ll prevalence of anemia of 31% in this cohort ofustralian kidney transplant recipients is similar
o that reported in American,8 Korean,9 and Euro-ean cohorts.2 Australian kidney transplant recipi-nts have demographic characteristics similar toheir European counterparts, including a lowrevalence of diabetic nephropathy as the pri-ary kidney disease compared with patients in
he United States.10 The female preponderancef anemia observed here also was noted byome,9 but not others.11
Conversely, the overall prevalence of anemia
Figure 3. Graph of relation-hip between Hb concentra-ion and CrCl for kidney trans-lant recipients and subjectsith chronic kidney disease.
bserved in general-population subjects was t
.4%, almost 10-fold less than in kidney trans-lant recipients with an equivalent CrCl. Fewtudies documented the epidemiological charac-eristics of anemia in the general population witharly stages of CKD; however, Australian sub-ects appear to have rates similar to Americanubjects with similar ethnicity and calculatedrCls, including the observed excess of anemia
n women.12
CrCl is related directly to Hb concentrationithin both groups; however, because the 2 co-orts were matched for CrCl, it is clear thatactors other than this contribute to the 10-foldxcess of anemia seen in kidney transplant recipi-nts. In the combined cohort of kidney transplantecipients and general-population subjects, theost powerful determinants of anemia are the
resence of a kidney transplant and female sex.The endocrine capacity of the kidney is related
o its excretory function, measured by CrCl.fter transplantation, an early peak in endoge-ous erythropoietin level is observed, followedy a smaller, but sustained, increase associatedith the start of graft function.13 Anemia within
he first 6 months after transplantation is well
rtfigopw
tIvptcacpammclatadtwtswClumaaeciaco
kaeHrT
ugfl
taoitoCar
ssadcthstpssaTawdp
actdpsvchvtuiacp
Chadban et al308
ecognized and commonly relates to blood losshrough surgery and venipuncture, delayed graftunction, and such acute inflammatory events asnfection or rejection.2 Restoration of normalraft function does not always ensure correctionf anemia, and variations in endogenous erythro-oietin production in kidney transplant patientsith normal kidney function were reported.14
Immunosuppressive drugs administered toransplant recipients also may cause anemia.nterpretation of the association between indi-idual agents and the prevalence of anemia isrone to bias in such cross-sectional studies ashis because Hb concentration may affect a clini-ian’s choice of drug; agents known to causenemia may be avoided or discontinued if Hboncentration is low or may be selected for use inatients with polycythemia. The antiproliferativegent azathioprine is well known to cause bonearrow depression, and despite a differentechanism of action, MMF was observed to
ause similar levels of anemia.15 In this Austra-ian cohort, azathioprine use in men was associ-ted with a higher Hb level, perhaps reflectinghe observed association between both male sexnd azathioprine use on CrCl. MMF use had noemonstrable association with anemia here, con-rary to findings of others.2,8 Cyclosporine useas associated with lower Hb levels, an observa-
ion previously described in children16 and ob-erved in only men in this study. Tacrolimus alsoas associated with lower Hb levels in men.yclosporine and tacrolimus may cause hemo-
ytic anemia; however, this is uncommon andnlikely to account for these findings in theaintenance-phase subjects in this study. The
ssociation between calcineurin inhibitors andnemia may be caused by nephrotoxicity; how-ver, no consistent relationship between cal-ineurin-inhibitor use and CrCl was evident. Thenverse relationship between Hb concentrationnd use of calcineurin inhibitors observed in thisohort may be explained by their negative effectn erythropoiesis.17
ACE inhibitors are known to cause anemia inidney transplant recipients and, for this reason,re used in the treatment of posttransplantationrthyrocytosis.18 Consistent with this is the lowerb concentration observed in female transplant
ecipients administered these agents in this study.
he absence of a relationship between CrCl and k
se of ACE inhibitors/ARAs in this study sug-ests this effect to be independent of allograftunction and likely caused by an erythropoietin-owering effect of ACE inhibitors.18
Factors other than transplant-related drugherapy also may be contributory to the excess ofnemia observed in kidney transplant recipientsver general-population subjects. Iron deficiencys relatively common after kidney transplanta-ion and may explain a proportion of the anemiabserved, particularly in women in this study.9
hronic infection,9 advanced donor age, andcute rejection2 are other identified factors notecorded in this study.
Certain limitations inherent in the design of thistudy must be acknowledged. This study was retro-pective and cross-sectional and therefore unable tossess the contribution to anemia of alterations inrug treatment over time and progression of clini-al events. This is highly pertinent to the contribu-ion of antiproliferative drugs, which are likely toave been discontinued in patients who developedignificant anemia before the survey point, and alsoo that of ACE inhibitors, which may have beenrescribed to treat polycythemia. In addition, notatistical attempt to account for multiple compari-ons has been made; therefore, a proportion of thessociations observed may have arisen by chance.he 2 cohorts were chosen by propensity score,ttempting to match for CrCl and sex. Althoughell matched for these 2 parameters, the cohortsiffered significantly by age, which may have im-acted on the results.
The high prevalence of late posttransplantationnemia described in the kidney transplant recipientohort is likely to be detrimental. In dialysis pa-ients, anemia is associated strongly with echocar-iographic evidence of left ventricular hypertro-hy.19 In kidney transplant recipients, anemia washown to be a risk factor for increased Cornelloltage on the electrocardiogram, a marker of in-reased left ventricular mass.20 Left ventricularypertrophy is an independent risk factor for cardio-ascular death in the general population and pa-ients treated with hemodialysis20 and may contrib-te to the excess of cardiovascular death observedn kidney transplant recipients.21 Not least are thedverse effects of anemia on exercise capacity,ognition, and quality of life described in dialysisatients, which are likely to be similar in anemic
idney transplant recipients.
pppHeapsrsitee
fantboset
tc
Wafi2
Pr2
c
os
rr
fac
gt
aal
i
RoM
WaN
oaNS
Np
Kte1
trS
hy4
NP
na9
Rt2
Pio4
up
cw
Anemia in Kidney Transplant Recipients 309
Achieving optimal allograft function is indis-utably the ideal solution in the management ofosttransplantation anemia, but this will not beossible in a significant proportion of patients.owever, treatment with recombinant erythropoi-
tin was effective in the correction of anemiafter transplantation.22 Despite this and the highrevalence of anemia found in this study, only amall number of patients were treated with eryth-opoietin therapy and hence excluded from thistudy. The European experience appears similarn that only 17.8% of severely anemic kidneyransplant patients were treated with erythropoi-tin.2 Similar evidence suggests that erythropoi-tin also is underused in subjects with CKD.
In conclusion, for a given level of kidneyunction, kidney transplantation is associated with
dramatic excess of anemia compared withontransplantation subjects, an effect that is likelyo be multifactorial. Widespread recognition ofoth the scale of the problem and consequencesf posttransplantation anemia combined with pro-pective intervention studies are needed if theffect of anemia upon survival of the kidneyransplant recipient is to be addressed.
ACKNOWLEDGMENTThe authors wish to acknowledge the AusDiab investiga-
ors for the provision of data for the general populationohort examined in this study.
REFERENCES1. Jurkovitz CT, Abramson JL, Vaccarino LV, WeintraubS, McClellan WM: Association of high serum creatinine
nd anemia increases the risk of coronary events: Resultsrom the prospective community-based Atherosclerosis Riskn Communities (ARIC) Study. J Am Soc Nephrol 14:2919-925, 20032. Vanrenterghem Y, Ponticelli C, Morales JM, et al:
revalence and management of anemia in kidney transplantecipients: A European survey. Am J Transplant 3:835-845,0033. Cockcroft DW, Gault MH: Prediction of creatinine
learance from serum creatinine. Nephron 16:31-41, 19764. Chadban SJ, Briganti EM, Kerr PG, et al: Prevalence
f kidney damage in Australian adults: The AusDiab kidneytudy. J Am Soc Nephrol 14:S131-S138, 2003
5. D’Agostino RB Jr: Propensity score methods for biaseduction in the comparison of a treatment to a non-andomized control group. Stat Med 17:2265-2281, 1998
6. Leuven E, Sianesi B: Psmatch2: Stata module to per-orm various types of propensity score matching. Availablet: http://ideas.repec.org/c/boc/bocode/s432001.html. Ac-
essed March 1, 2004 p
7. Poggio ED, Wang X, Weinstein DM, et al: Assessinglomerular filtration rate by estimation equations in kidneyransplant recipients. Am J Transplant 6:100-108, 2006
8. Yorgin PD, Scandling JD, Belson A, Sanchez J, Alex-nder SR, Andreoni KA: Late post-transplant anemia indult kidney transplant recipients. An under-recognized prob-em? Am J Transplant 2:429-435, 2002
9. Kim HC, Park SB, Han SY, Whang EA: Anemia follow-ng kidney transplantation. Transplant Proc 35:302-303, 2003
10. US Renal Data System: USRDS 1998 Annual Dataeport. The National Institutes of Health, National Institutef Diabetes and Digestive and Kidney Diseases, Bethesda,D, 199811. Lorenz M, Kletzmayr J, Perschl A, Furrer A, HorlH, Sunder-Plassmann G: Anemia and iron deficiencies
f anemia associated with chronic kidney insufficiencymong adults in the United States: Results from the Thirdational Health and Nutrition Examination Survey. J Amoc Nephrol 13:504-510, 200213. Sun CH, Ward HJ, Paul WL, Koyle MA, Yanagawa
, Lee DB: Serum erythropoietin levels after kidney trans-lantation. N Engl J Med 321:151-157, 198914. Nampoory MR, Johny KV, al Hilali N, Seshadri MS,
anagasabhapathy AS: Erythropoietin deficiency and rela-ive resistance cause anaemia in post-kidney transplant recipi-nts with normal kidney function. Nephrol Dial Transplant1:177-181, 1996
15. Sollinger HW: Mycophenolate mofetil for the preven-ion of acute rejection in primary cadaveric kidney allograftecipients. US Kidney Transplant Mycophenolate Mofetiltudy Group. Transplantation 60:225-232, 199516. Yorgin PD, Belson A, Sanchez J, et al: Unexpectedly
igh prevalence of posttransplant anemia in pediatric andoung adult kidney transplant recipients. Am J Kidney Dis0:1306-1318, 200217. Saito S, Fujiwara T, Sakagami K, Matsuno T, Tanaka
: Anemia following kidney transplantation. Transplantroc 30:3025-3026, 199818. Gossmann J, Thurmann P, Bachmann T, et al: Mecha-
ism of angiotensin converting enzyme inhibitor-relatednemia in kidney transplant recipients. Kidney Int 50:973-78, 199619. Silberberg JS, Rahal DP, Patton DR, Sniderman AD:
ole of anemia in the pathogenesis of left ventricular hyper-rophy in end-stage kidney disease. Am J Cardiol 64:222-24, 198920. Rigatto C, Foley R, Jeffery J, Negrijn C, Tribula C,
arfrey P: Electrocardiographic left ventricular hypertrophyn kidney transplant recipients: Prognostic value and impactf blood pressure and anemia. J Am Soc Nephrol 14:462-68, 200321. Kasiske BL, Chakkera HA, Roel J: Explained and
nexplained ischemic heart disease risk after kidney trans-lantation. J Am Soc Nephrol 11:1735-1743, 200022. Vanrenterghem Y, Vanwalleghem J: Benefits and con-
erns of treating pre-dialysis and kidney transplant patientsith recombinant human erythropoietin. Nephrol Dial Trans-
