Nephrol Dial Transplant (2010) 25: 270–274doi: 10.1093/ndt/gfp459Advance Access publication 11 September 2009 What is the relevance of systematic aorto-femoral Doppler ultrasound
in the preoperative assessment of patients awaiting first kidney
transplantation: a monocentric prospective study

Guillaume Ploussard1,∗, Pierre Mongiat-Artus1,2,∗, Paul Meria1, Edouard Tariel1, Franc¸ois Gaudez1,Eric De Kerviler3, Christophe Legendre4, Marie-Noelle Peraldi5,6, Denis Glotz5 and Franc¸oisDesgrandchamps1 1Department of Urology and Paris 7 University, Saint Louis Hospital, 2CNRS U944 – UMR 7212, 3Department of Radiology andParis 7 University, Saint-Louis Hospital, 4Department of Nephrology and Paris 5 University, Necker Hospital, 5Department ofNephrology and Paris 7 University, Saint-Louis Hospital and 6INSERM U662, Paris, France Correspondence and offprint requests to: Pierre Mongiat-Artus; E-mail: [email protected]∗Both authors equally contributed to the study.
examination. Nevertheless, in the case of arterial physical Background. The purpose of our study was to study the
abnormality, ‘for case’ DUS is critical and helps in the relevance of a systematic aorto-femoral colour Doppler ul- surgical strategy in ∼20% of cases.
trasound (DUS) in the evaluation of first renal transplantreceivers.
Keywords: atherosclerotic infiltration; cardiovascular risk factors;
Doppler ultra sound; recipient; renal transplantation Methods. We prospectively studied 100 consecutive first
renal transplant (RT) receivers. All patients had a preoper-
ative physical examination with a careful vascular system
evaluation including assessment of risk factors and colour
DUS of aortic, iliac and femoral arteries. Renal transplanta-tion was planned in the right iliac fossa with end-to-lateral The increasing number of renal transplantation (RT) in- vascular anastomoses. Clinical parameters, DUS results, dications has lead to a larger number of recipients with operative and post-operative parameters at 3 months were vascular disease and more advanced ages [1]. Patients with compared according to the vascular assessment.
chronic renal insufficiency often exhibit at least some de- Results. Among the 84 patients presenting with a nor-
gree of atherosclerosis and arterial wall calcifications due to mal preoperative physical arterial examination, 12 patients end-stage renal failure, associated cardiovascular risk fac- (14.3%) had an abnormal DUS, revealing atherosclerotic tors and/or hyperparathyroidism. The reliable pre-operative arteries, but no case of arterial stenosis. Among the 16 vascular assessment of a renal graft recipient is warranted patients with abnormal physical arterial examination, 10 and must be performed prior to patient inclusion of the patients (62.5%) had abnormal DUS, including 4 cases of patient on the waiting list [2]. Initial arterial assessment in- iliac stenosis. In 3 of the 16 patients (18.8%), DUS revealed cludes at least vascular physical examination with femoral right iliac artery stenosis requiring a modification in the artery palpation. Nevertheless, colour Doppler ultrasound surgical procedure. No additional vascular procedure was (DUS) is performed by most of the transplantation teams reported in the case of normal preoperative vascular exam- in order to identify external iliac artery atheroma that could ination. No technical problems during arterial anastomosis compromise anastomosis viability, which is a key factor for and no post-transplantation arterial complications were re- a good functional result of RT [3]. In some patients, exter- ported. In multivariate analysis, abnormal physical exami- nal iliac artery atheroma may require an additional surgical nation was the most significant risk factor of atherosclerotic vascular procedure during RT, and published series have demonstrated that better results are obtained when preop- Conclusion. The abnormality of arterial physical examina-
erative endarterectomy is planned [4,5,6]. Colour Doppler tion is the best clinical predictor of abnormal DUS in preop- sonography is also applied after RT to assess the vascular erative assessment of renal transplant receivers. However, integrity of the allograft. The intrarenal resistance index the low sensitivity and positive predictive value of the phys- has been shown to be a strong predictor for renal allograft ical examination do not support the conclusion that DUS and patient survival [7]. The allograft intrarenal index was can be avoided in patients with normal arterial physical closely correlated with recipient age and vascular stiffness C The Author 2009. Published by Oxford University Press [on behalf of ERA-EDTA]. All rights reserved.
For Permissions, please e-mail: [email protected] The relevance of systematic aorto-femoral Doppler ultrasound of the recipient, which confirms the need for a good assess- Table 1. Causes of chronic renal insufficiency
ment of recipient vascular state [8].
The management of a waiting list for RT is expensive be- cause of detailed evaluation of the recipient and regular con- trols and incites cost reduction [9]. The cost-effectiveness of a DUS screening test for vascular evaluation of RT can- didates, compared to physical arterial examination, has not In this study, we analysed the diagnostic interest of colour DUS for the vascular assessment of renal transplant candi- dates according to clinical parameters.
Subjects and methods
Neurological bladder, systemic lupus, cystinosis We conducted a prospective study to evaluate the utility of a systematicaorto-femoral DUS in the vascular assessment of primary cadaver renal and 38 females with a median age of 43.1 years (range: 19– 66 years; SD 11.48; 31% >50 years). The most current The study was approved by the local ethical committee. Inclusion crite- ria were indication of a first renal or combined renal and pancreatic trans- causes of chronic renal insufficiency (Table 1) were high plantation and acceptance to participate. Exclusion criteria were previous blood pressure (20%), IgA nephropathy (15%), polycys- renal or combined renal and pancreatic transplantation or living donor tic kidney disease (13%) and diabetic nephropathy (13%).
transplantation or refusal to participate. We enrolled 100 consecutive can- Ninety patients were waiting for RT and 10 for a com- didates for a first kidney or combined kidney and pancreas transplantation.
Each patient received in addition to the usual preoperative evaluation, bined renal and pancreatic transplantation. The mean time (i) a complete clinical examination by a senior urologist with special on haemodialysis was 4.2 years (range: 1–16).
emphasis on the vascular system (palpation and auscultation of carotid, Group 1 comprised 16 patients with abnormal arterial femoral and distal arteries) and thereafter, (ii) a colour DUS of aorta, iliac physical examination: the absence of distal pulse in 7 cases and femoral arteries by a senior radiologist.
(43.8%), the absence of femoral pulse in 2 cases (12.5%), Cardiovascular risk factors were defined as severe arterial hyperten- sion, complicated diabetes, heavy smoking habits (current or past smoking femoral arterial murmur in 5 cases (31.3%) and carotid with a number of pack years >2), hyperchlolesterolaemia (LDL choles- artery murmur in 2 cases (12.5%). Group 2 comprised 84 terol >4.14 mmol/L and/or HDL <1.04 mmol/L), hyperuricaemia (cut- patients with normal arterial physical examination. Abnor- off 416 µmol/L), hypertriglyceridaemia (cut-off 1.7 mmol/L) and obesity mal DUS was reported in 10 patients (62.5%) in Group 1 (body mass index >30). Physical arterial examination was considered ab- normal in the case of absent arterial pulse and/or in the case of arterial and in 12 patients (14.3%) in Group 2 (Table 2). The differ- murmur during auscultation. The quantification of atherosclerosis degree ence between both groups was statistically significant (P < was made using velocity (low-peak systolic and diastolic flows and high resistance index) and/or morphological (measurements of intima–media When analysing the factors associated with abnormal thickness, plaque volume index and degree of stenosis) criteria.
DUS in a univariate analysis (Table 3), abnormal physical In the case of normal arterial physical examination, the renal implan- tation was planned on the right external iliac artery for RT or on the examination was significantly associated with atheroscle- left iliac artery for combined pancreatic and kidney transplantation, with rotic infiltration in DUS (OR 10; 95% CI: 3.1–32.6). Age end-to-side arterial anastomosis. In the case of abnormal arterial physical was also significantly associated with abnormal DUS (OR examination, the left external iliac artery or the primary iliac artery was 4.1; 95% CI: 1.5–11.1). On the other hand, diabetes did not considered for implantation sites. DUS was unblinded to the urologistonly after he made the first decision on the surgical strategy. The final differ in the two groups (P = 0.08). The positive predictive decision was made considering both clinical evaluation and DUS. Pre- value of HTA and diabetes for abnormal DUS was 24.2 and postoperative complications and functional results at 3 months were and 42.9, respectively. Sensitivity and specificity of abnor- mal examination were 41.6 and 94.7. Positive and negative Patients were separated into two groups depending on vascular clinical predictive values of abnormal examination for abnormal examination: group 1 with ‘abnormal vascular physical examination’ and group 2 with ‘normal vascular physical examination’. The two groups DUS were 62.5 and 85.7, respectively. In the multivariate were initially compared according to cardiovascular risk factors, age and analysis, abnormal physical examination (P = 0.001) and time on dialysis. They were then compared according to the change be- age (P = 0.009) remain significant as the two independent tween initial and final decision on surgical strategy. Finally, they were predictive factors of abnormal DUS. DUS was abnormal compared according to surgical complications and functional results ofthe transplantation. Statistical analysis was performed using a chi-square in 22 cases revealing atherosclerotic infiltration in 18 cases test or Fisher’s exact test for qualitative data. Continuous variables were (81.8%) and stenosis in 4 cases (18.2%) (Table 4). Arterial studied with Student’s t-test or a Mann–Whitney test in the case of no stenosis was found only in patients with abnormal physical normal distribution. Binomial logistic regression was used to perform the examination (100%, P = 0.03) and accounted for 25% of multivariate analysis in order to determine the most relevant risk factors of abnormal DUS. Statistical difference was defined as P < 0.05, usingthe SPSS 13.0 (Chicago, IL, USA) software.
In the sub-group of patients >50 years, abnormal phys- ical examination was the only significant predictor of ab-normal DUS in univariate (P = 0.007; OR: 18.0) and mul- tivariate (P = 0.008; HR: 36.8) analyses. None of the otherparameters were significant predictors of abnormal DUS.
No patient refused participation in the study. From January In Group 1, the surgical strategy was modified in three 2002 to June 2008, we included 100 consecutive primary ca- patients as a result of DUS (arterial stenosis). The re- daver renal transplant recipients. The patients were 62 males nal graft was implanted in another site in two patients Table 2. Characteristics of patients according to arterial physical examination (n = 100)
Table 3. Risk factors of abnormal DUS: univariate and multivariate anal-
fossa haematoma following arterial puncture. He received the renal transplant in the left iliac fossa. In this group, no additional surgical vascular procedure was required during There was a significant difference between the Groups Univariate analysisHigh blood pressure 1 and 2 concerning the rate of change in surgical strategy Time on haemodialysis >10 years 0.97 (18.8% versus 1.2%, P = 0.01; see Table 2).
No unsuspected technical problem has been re- ported during arterial anastomosis. No immediate post- transplantation arterial complication has been reported.
With 3 months of follow-up, mean post-operative serum creatine was 1.89 mg/dl (range: 0.76–4.84 mg/dl). In the case of stenosis or atherosclerotic arteries in DUS, post- operative serum creatine was not different in the case of nor- mal or abnormal DUS (respectively, 1.70 and 1.62 mg/dl, Time on haemodialysis >10 years 0.42 Discussion
During the last 15 years, the number of renal transplants per- formed in older patients has dramatically increased. Cardio- vascular disease is more prevalent in older renal transplantrecipients. Atherosclerotic disease represents a technical Table 4. Type of abnormality of DUS (n = 22) and dispatching according
challenge for RT. All candidates for RT undergo preop- to arterial physical examination and modification of surgical strategy erative vascular assessment to determine the presence ofatherosclerosis of the iliac arteries. Such diagnosis could contraindicate the transplantation or requires pretransplan- tation vascular surgery or a medical preparation. Physical examination is the first step of the assessment. Some centres routinely perform DUS of the aortoiliac arteries to ascertain the integrity of the arterial anastomosis site. Colour DUSmakes it possible to distinguish moderate atheroscleroticinfiltration from severe, which could compromise anasto- (transplantation in the left iliac fossa for one patient and mosis viability and graft survival. Burgos et al. reported othotopic real transplantation for the other patient). An 3% of candidates excluded from RT because of severe endarterectomy was planned and performed for the third vascular disease diagnosed with DUS [3]. Another advan- patient (with an end-to-side anastomosis on the right com- tage of a complete preoperative vascular assessment is that mon iliac artery). However, one patient had an abnormal additional surgical vascular procedure or modification of arterial examination and a stenosis on DUS, but the anas- the implantation site can be planned before transplantation tomosis was conducted on the external iliac artery without and that better results are expected [3]. However, the cost- effectiveness of a screening test by DUS has not yet been In Group 2, the surgical strategy was modified in one evaluated. Systematic vascular assessment by abdominal patient as a result of DUS despite a normal arterial ex- aortic angiography revealed < 2% of candidates who were amination. The patient was diagnosed with a right iliac found to have aortoiliac disease severe enough to require The relevance of systematic aorto-femoral Doppler ultrasound surgical reconstruction [10]. So routine aortoiliac angiogra- ical examination’ for an abnormal DUS. For patients with phy is not warranted [1]. The aim of our present study was abnormal arterial physical examination, helical computed to determine the diagnostic yield of colour DUS regarding tomography angiography is critical in the context of com- plete pretransplantation evaluation [2]. It is of note that In our study, abnormal arterial physical examination was atherosclerotic lesions may also progress asymptomatically the most significant predictive factor of abnormal DUS after the initial assessment when the patient is on the wait- (P = 0.001; OR 10.4). In our patients, severe atheroscle- ing list for a long time. Waiting time on the list is a recog- rosis infiltration with arterial stenosis represented 40% of nized risk factor for postoperative complications, poor graft abnormalities in DUS. Age was also a significant risk factor survival and death during the first year following transplan- of abnormal DUS in multivariate analysis (P = 0.009; OR tation [12]. The timing of systematic vascular reassessment 6.9). We chose a cutoff of 50 years that was often reported should be determined in each patient according to age and in the literature. Abnormal DUS was more often reported cardiovascular risk factors. As recommended, the medical in diabetic patients, but the difference did not reach signif- status of patients on the cadaveric transplantation waiting icance (P = 0.07). Other cardiovascular risk factors were list should be reviewed at least every 2 years. Advancing age not relevant to anticipate abnormal DUS. Both advanced and diabetes increase the need to periodically re-evaluate age and diabetes were major risk factors abnormal DUS at patients on the waiting list at least annually [2,13]. How- initial assessment. For these patients, vascular evaluation ever, the clinical examination of the patients will remain by the means of a combination of physical examination and mandatory if not the only useful evaluation. It remains to DUS was probably not sufficient. Additional radiological study the cost-efficiency of such care.
techniques with helical computed tomography angiogra-phy could be useful to depict more accurately the extent Conclusion
of arterial disease. Indeed, even in the absence of stenosis,vascular calcifications in the iliac area are frequent in the elderly diabetic population. The location or the extent of The abnormality of arterial physical examination is the best arterial wall calcifications can compromise the anastomo- clinical predictor of abnormal aorto-femoral DUS in pre- sis of the renal transplant. The most efficient procedure operative assessment of renal transplant receivers. Partic- to assess importance and distribution of atherosclerotic le- ularly, in patients >50 years, an abnormal physical exam- sions in the elderly population is computed tomography ination is the only significant predictor of abnormal DUS with reconstruction [11]. According to Andres et al. 29% in univariate and multivariate analyses. However, the low of candidates have been excluded from the waiting list due sensitivity and the positive predictive value of the physical to universal calcifications [11]. The site of the arterial anas- examination limit strong conclusions and do not support the tomosis can be selected according to computed tomography statement that DUS can be avoided in patients with normal results in the case of partial arterial calcifications. In the arterial physical examination. In the case of arterial phys- case of abnormal DUS revealing severe vascular disease, ical abnormality, vascular assessment with aorto-femoral an additional procedure by helical computed tomography Doppler ultrasound is mandatory and helps to modify the is also critical. Burgos et al. noted that some patients were surgical procedure in ∼20% of the cases.
excluded from the waiting list due too an abnormal DUSresult. However, they also noted that some have been rein- Conflict of interest statement. None declared.
tegrated onto the waiting list after helical computed to-mography allowed for modification of the surgical strategy References
(modification of the implantation site) [3].
In our series, severe atherosclerosis was reported only 1. US Department of Health and Human Services Annual report of the in patients with abnormal vascular physical assessment and US scientific registry for transplant recipients and the Organ pro- was responsible for a change in surgical strategy in 18.8% of curement and transplantation network. US Department of Health andHuman Services, Division of Transplantation, Rockville, MD, UNOS, the cases. The main interest of our study is that no additional surgical vascular procedure was performed for any patient 2. Kasiske B, Cangro C, Harikam S. The evaluation of renal transplant with normal arterial physical examination. The short-term candidates: clinical practice guidelines. Am J Transplant 2002; 2: 3–95 efficiency of this strategy was controlled by postoperative 3. Burgos FJ, Pascual J, Marcen R et al. The role of imaging techniques serum creatine level and absence of immediate complica- in renal transplantation. World J Urol 2004; 22: 399–404 tions. After dispatching patients in groups depending on 4. Droupy S, Eschw`ege P, Hammoudi Y et al. Consequences of iliac colour DUS results and clinical evaluation, no difference arterial atheroma on renal transplantation. J Urol 2006; 175: 1036–1039 was found between groups concerning the complication rate 5. Galazka Z, Szmidt J, Nazarewski S et al. Kidney transplantation in of surgery and the serum creatine levels of patients. How- recipients with atherosclerotic iliac vessels. Ann Transplant 1999; 4: ever, long-term follow-up results may change this result, 6. Van Der Vliet JA, Naafs DB, van Bockel JH et al. Fate of renal According to our results, in patients without a specific allografts connected to vascular prostheses. Clin Sci 1996; 10: 199– risk factor, preoperative DUS might be optional when ar- 7. Radermacher J, Mengel M, Ellis S et al. The renal arterial resistance terial physical examination is normal. However, in order index and renal allograft survival. N Engl J Med 2003; 349: 115–124 to discuss the limitations of our study, we would like to 8. Schwenger V, Keller T, Hofmann N et al. Color Doppler indices of re- emphasize the relatively small cohort of patients and the nal allografts depend on vascular stiffness of the transplant recipients.
low sensitivity (41.6) of only the criterion ‘abnormal phys- Am J Transplant 2006; 6: 2721–2724 9. Jeantet A, Piccoli GB, Malfi B et al. Preparation of candidates for in the iliac arterial sector in renal transplant candidates. Transplant renal transplantations: cost analysis. Transplant Proc 2004; 36: 455– 12. Gill JS, Pereira BJ. Death in the first year after kidney transplantation: 10. Brekke IB, Lien B, Jakobsen A et al. Aortoiliac reconstruction in implications for patients on the transplant waiting list. Transplantation preparation for renal transplantation. Transplant Int 1993; 6: 161– 13. Matas AJ, Kasiske B, Miller L. Proposed guidelines for re-evaluation 11. Andres A, Revilla Y, Ramos et al. Helical computed tomography of patients on the waiting list cadaver transplantation. Transplantation angiography is the most efficient test to assess vascular calcifications Received for publication: 4.8.09; Accepted in revised form: 13.8.09 Nephrol Dial Transplant (2010) 25: 274–277doi: 10.1093/ndt/gfp486Advance Access publication 19 September 2009 Nail changes in kidney transplant recipients
Abeer M. Abdelaziz1, Khaled M. Mahmoud2, Essam M. Elsawy2 and Mohamed A. Bakr2 1Department of Dermatology and 2Urology and Nephrology Center, Mansoura University, Mansoura, Egypt Correspondence and offprint requests to: Khaled Mahmoud; E-mail: [email protected] Abstract
Background. Nail changes are common complications of
end-stage renal disease, and reports of nail changes in kid-
A significantly higher incidence of nail changes was re- ney transplant recipients (KTR) are rare. Few reports have ported in end-stage renal disease (ESRD) patients [1,2] documented a higher prevalence of onychomycosis in KTR and in those on haemodialysis [2,3]. Several nail changes compared with controls, while others found no significant have been described which may occur in up to 60.3% of pa- differences. In this study, we investigated the prevalence tients with ESRD and in up to 62.3–69.8% of haemodialysis and nature of nail changes in a large series of KTR.
Methods. Three hundred and two KTR (216 males and
Whether similar nail changes could be present after 86 females) were included in this study, and the mean trans- kidney transplantation, there is only one published case- plant duration was 6.57 years (range 1.5 month–23 years).
control study of 205 patients that showed that 56.6% of They were screened for the presence of nail changes. Nail kidney transplant recipients (KTR) had at least one type of clippings were collected when indicated and cultures were nail pathology [4]. On the other hand, there are a few re- performed for patients with suspected onychomycosis. The ports on nail changes in patients receiving immunosuppres- patients were compared with 302 age- and sex-matched sive drugs for indications other than kidney transplantation healthy controls (220 males and 82 females).
Results. One hundred and twenty-one KTR (40.1%) had
The aim of this study was to determine the prevalence nail changes compared with 104 (34.4%) in controls. Ony- and the nature of nail lesions in a large series of KTR.
chomycosis, Muehrcke’s nail and leuconychia were signif- icantly more common in KTR [23 (7.6%), 13.3 (4.3%),11 (3.6%), respectively] compared with controls [7 (2.3%), Subjects and methods
1(0.3%), 2 (0.66%), P = 0.002, 0.001 and 0.02, respec-tively]. However, the most frequent nail change among KTR This study was conducted on two groups of patients, group I which in-cluded 302 kidney transplant patients (216 males and 86 females) and and controls was absent lunula, 90 (29.8%) and 80 (26.5%), group II which included 302 healthy individuals who served as a control respectively P = 0.36. Longitudinal ridging was also a fre- quent nail pathology among KTR and controls, 21 (6.9%) Group I received kidneys from living-related donors in the Urology and and 19 (6.3%), respectively, P = 0.74.
Nephrology Center, Mansoura University, Egypt. They were followed upand examined in the out-patient clinic during the period from July 2004 to Conclusion. KTR have higher prevalence rates of ony-
July 2006. Their ages ranged from 11 to 64 years (mean 35.9 ± 11.3). They chomycosis, Muehrcke’s nail and leuconychia than the were receiving immunosuppressive protocols in different combinations of healthy population. On the other hand, absent lunula could steroid, azathioprine, mycophenolate mofetil, cyclosporine and tacrolimus.
be a normal variation among Egyptian people.
The time since transplantation ranged from 1.5 months to 23 years (mean6.57 ± 5.2 years).
Keywords: kidney; nail; transplantation
Group II was randomly selected from healthy hospital staffs and from healthy companions of ill patients. Controls were matched with cases bysex and age. Their ages ranged from 14 to 66 years (mean 33.9 ± 11.2).
C The Author 2009. Published by Oxford University Press [on behalf of ERA-EDTA]. All rights reserved.
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