Value of liver stiffness measured by transientelastography in the liver transplantpre-operative evaluation of the potentialdeceased liver donors: preliminary study

According to the annual reports of harvesting andof grafts established by the Biomedical Agency[Agence de la biomedecine (ABM)] in France, for anidentical number of potential donors and despitethe expansion of the acceptation criteria of thedonors, a decrease is noted in the number of livergrafts harvested since 2005 with only two cadavericdonors of three who had their livers harvested(73% in 2005, 67% in 2008) (1). The selection ofthe liver graft is crucial for the success of atransplantation as experience has shown that notonly is it important to carefully select the recipient,but also essential to carefully select the organavailable (2). One of the limitations for practition-ers assessing the quality of liver grafts is to be ableto determine objectively the degree of steatosisduring selection (3). Ideally, they should haveaccess to a reliable, reproducible, simple and rapid

tool, which allows to assess objectively the qualityof liver grafts and the quantitative evaluation ofthe degree of hepatic steatosis. Considering theexperimental arguments supporting the hypothesisof a good predictive elastometry value of theFibroScan� on the functional nature of the liver,the authors present the interest of measuring liverstiffness (LS) using the FibroScan� as an objectiveevaluation criterion in the pre-operative selectionof liver grafts of potential donors.

Materiel and methods

In this single center prospective study over a periodof eight months, 16 successive brain dead patients(eight due to stroke, seven due to head trauma, onedue to cerebral anorexia) apt for liver harvest-ing underwent a FibroScan� in the polyvalent

Pichon N, Loustaud-Ratti V, Clavel M, Carrier P, Amiel JB, Labrousse F.Value of liver stiffness measured by transient elastography in the livertransplant pre-operative evaluation of the potential deceased liver donors:preliminary study.Clin Transplant 2011: 25: E205–E210. ª 2010 John Wiley & Sons A/S.

Abstract: The selection of a liver graft is crucial for the success of atransplantation. One of the determinant factors in the selection of a livergraft of quality is to assess the degree of steatosis. The aim of this study wasto evaluate the feasibility of a FibroScan� during the liver retrieval proce-dure and to determine the interest of measuring liver stiffness (LS) using theFibroScan� as a criterion of objective assessment in the pre-donationselection of liver grafts. Of 16 FibroScan� performed on 16 livers of donorsmeeting conventional French criteria for the selection of liver grafts, the LSvalues were considered as abnormal in three donors (18.75%). The corre-spondence with the histologic analysis of the biopsies in terms of elevatedsteatosis was excellent. For 13 other liver grafts, the values of LS werenormal as were the histologic analyses of the biopsies. A supplementarymulticenter study is required in order to position the transient elastographyas the objective examination in the pre-operative selection of liver grafts.

Nicolas Pichona,b,c, VeroniqueLoustaud-Rattid, Marc Clavela,Paul Carriere, Jean Bernard Amiela

and Francois Labroussef

aDepartment of Critical Care, Dupuytren

University Hospital, Limoges, France, bCIC-P

0801 Inserm, Limoges, France, cCoordination

Hospitaliere des Prelevements d�Organes et de

Tissus, dHepatitis Federation, Departments ofeHepatology and fPathology, Dupuytren

University Hospital, Limoges, France

Key words: graft evaluation – hepatic steatosis –

liver stiffness – liver transplants – transient

elastography

Corresponding author: Nicolas Pichon,

Department of Critical Care, Dupuytren

University Hospital, Limoges, France.

Tel.: (33)5 55 05 62 40; fax: (33)5 55 05 62 44;

e-mail: nicolas.pichon@chu-limoges.fr

Conflict of interest None.

Accepted for publication 29 October 2010

Clin Transplant 2011: 25: E205–E210 DOI: 10.1111/j.1399-0012.2010.01386.xª 2010 John Wiley & Sons A/S.

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intensive care unit of the University Hospital inLimoges before the conventional surgical multi-organ harvesting procedure. In France, the selec-tion of liver grafts from cadaveric donors prior tothe donation uses two levels of selection (4, 5). Thelevel 1 selection is based on various criteria:demographical data (past medical history, age,sex, body mass index [BMI], weight), recentmedical history (medication requirements, days inICU), time course of biologic parameters untilsurgical hepatic harvesting (natremia, hepatic bio-chemistry) and on evaluation of hepatic steatosisby abdominal echography (4, 5). The level 2selection is based on the macroscopic characteris-tics of the liver assessed by the surgeon during theharvesting (organ-shine, consistency, surface, edge,color, presence of steatosis or atheromatosis) andon a histologic analysis of a liver biopsy (LB)analyzed extemporaneously by a pathologist ifnecessary (4, 5). The demographical data of the 16donors, together with the results of the variousconventional parameters of the pre-operative selec-tion of liver grafts used in France, were collected(Table 1).LS was measured as early as possible after the

paraclinical confirmation of brain death diagnosedclinically. The French National Register of Refusal

(FNRR) was consulted systematically (mandatoryin France) before carrying out the FibroScan�, soas to eliminate any opposition of the donor toperforming clinical research or organ harvesting.The families of the donors, unopposed to harvest-ing of organs of their relatives, were informed ofthe study.

Each FibroScan� examination uses a new pat-ented technology called ‘‘ultrasound impulsedelastography’’ and explores a volume of more than3 cm3 of the liver to measure LS. Its principleconsists in directing a mechanical pulse at the skinsurface (a shear wave obtained with a vibratorplaced in a probe) that propagates through theliver in the form of an elastic wave, the velocity ofwhich is measured by ultrasound (transducerplaced in the head of the probe that emits andreceives the ultrasounds). The velocity of this waveis determined by the stiffness of the medium itcrosses: the faster the vibration spreads, the stifferthe liver. The measurement is made on the rightlobe of the liver through the intercostal route(intersection of the mid axillary line and thexyphoid appendix) using an ultrasound probefollowing application of a conduction gel to theskin. The examination includes at least 10 validacquisitions and lasts an average of five min. The

Table 1. Demographical data and results of the various conventional parameters of the pre-operative selection of liver grafts used in France for the 16 potentialdonors

16 Potential donors

Age (yr)

SexDaysin ICU

BMI(kg/m2)

Abdominalechography

Biology the day of multi-organ harvesting

GGT (UI/L)

INR

AP (UI/L)ASAT(UI/L)

Total bilirubin(mg/dL)

Natremie(mmol/L)

49 ± 18m ± SD

22 ± 3m ± SD

29 ± 35m ± SD

60 ± 23m ± SD

43 ± 21m ± SD

1.18 ± 1.1m ± SD

150 ± 11m ± SD

Livers harvested/transplanted (12)1 19 F 3 21 A, B, C <N 1.50 <N 63 1.53 1422 25 F 2 20 A, B, C <N 1.46 <N 48 2.47 1393 73 M 3 24 A, B, C <N 1.37 <N 29 1.06 1394 48 F 3 16 A, B, C <N 1.41 <N 14 0.24 1275 48 M 7 26 A, B, C <N 1.29 <N 34 3.94 1456 45 M 2 28 A, B, C 4N 1.51 <N 62 0.76 1477 74 F 2 21 A, B, C <N 1.22 <N 54 0.88 1398 39 M 3 22 A, B, C <N 1.18 <N 49 0.59 1369 46 F 4 20 A, B, C <N 1.46 <N 28 0.29 140

10 52 F 3 20 A, B, C 2N 1.27 <N 21 0.76 13511 43 M 4 25 A, B, C <N 1.32 <N 85 0.41 14012 74 M 2 24 A, B, C <N 1.42 <N 30 1.24 130

Non-transplanted livers (4)Harvested (2) 18 F 2 22 A, B <N 2.11 <N 73 0.59 154

24 M 10 22 D, E <N 1.65 2N 2024 1.71 165Not harvested (2) 57 M 3 17 A, B N 1.43 <N 25 0.65 147

63 M 4 29 D, E <N 1.36 <N 13 0.71 144

M, male; F, female; ICU, intensive care unit; AP, alkaline phosphatases; BMI, body mass index; INR, international normalized ratio; GGT, gamma glutamyl transpeptidase;N, upper normal limit (ASAT: 36 UI/L and alkaline phosphatases: 104 UI/L); A, normal size; B, homogenous parenchyma; C, regular contours; D, slight hepatomegaly; E,hyperechogenic parenchyma.

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result obtained is expressed in kilopascals (kPa)and corresponds to the median of the 10 validacquisitions. The values observed were comprisedbetween 2.5 and 75 kPa. When interpreting theresults, two elements must be taken into account:the number of valid measurements and the vari-ability of the valid measurements determined bythe value of the interquartile range (IQR), whichmust be lesser than 30% of the median to considerthe examination as qualitatively satisfactory (6).The failure rate of the measurements is of around6% with, as essential limitation, the obesity ofthe patient which impedes the progression ofthe ultrasounds (7). A BMI >28 kg/m2 increasesthe failure rate of the LS measurements using theFibroScan� (8). Age does not alter LS, therefore,permitting the use of the FibroScan� in theassessment of liver grafts in elderly donors (9).The FibroScan� was performed by two hepatolo-gists using this apparatus daily in the monitoring oftheir patients with hepatitis.

A LB, the reference in the assessment of steatosis,was taken systematically by the transplant teams inthe operating theater, before aortic clamping andgraft harvesting, in order to compare the pathologyresults with the elastometric values. All the biopsieswere analyzed blind by two pathologists.

Finally, a purely descriptive analysis of corre-spondence was established between the results ofLS obtained with the FibroScan� and the results ofthe hepatic biologic assessment, the echographicalexamination and the histologic analysis of the liverbiopsies of the 16 organ donors.

Results

Among the 16 potential liver donors (nine men[56.3%] and seven women [43.7%]), no restrictionwas put forward by the Biomedical Agency regard-ing the harvesting of the liver grafts in view of theconventional level 1 selection criteria (Table 1). Themean age of the donors was of 46.8 ± 18.7 yr(range, 18–74 yr), the mean BMI was of22.3 ± 3.6 kg/m2 (range, 16–29 kg/m2) and theduration in intensive care before harvesting was of3.6 ± 2.1 d (range, 2–10 d). The mean fluid over-load prior to harvesting was of 2900 ± 4200 mL,and all the patients were treated with catechola-mines (2 with epinephrine alone, 2 with epinephrineand norepinephrine and 12 with norepinephrinealone) prior to harvesting.

Of the 16 potential liver grafts, 14 were harvestedand, finally, only 12 livers were transplanted(Table 1).

The FibroScan� was performed in the 16 donorswithout any complications or failures despite two

patients with a BMI ‡28 kg/m2 which increase thefailure rate of the LS measurements (Table 1). Themean duration of the FibroScan� examination wasof 6 ± 4 min (range, 3–18 min), the mean numberof measurements was of 17 ± 10 (range, 10–40),bearing in mind that 10 valid acquisitions perexamination are required to consider the latter asinterpretable and, the mean time lapse between theFibroScan� and aortal clamping in the operatingtheater was of 17 ± 24 h (range, 3 ± 10 h)(Table 2). Fourteen of the 16 examinations exhib-ited a mean IQR of 13 ± 5% of the respectivemedian for each value (range, 4–21%), that is tosay 30% inferior to the median, allowing them tobe considered as qualitatively satisfactory. Twoexaminations revealed an IQR >30% (respectively45% and 65% of the two respective medians) andwere hence considered as qualitatively unsatisfac-tory (6). One of these two examinations (IQR of45% of the median) corresponded to a measure-ment of one of the four non-transplanted livers,and the other examination (IQR of 65% of themedian) corresponded to a measurement made onone of the livers harvested and transplanted(Table 2) (6).Once the transplant teams had arrived on site,

the macroscopic aspect of the liver assessed by thesurgeon during harvesting, according to the level 2selection criteria, revealed four macroscopicallyabnormal livers with steatotic aspect for two ofthem, fibrotic for one and ischemic for the last one(Table 2). Of these four livers, two liver grafts werenot harvested on the basis of this macroscopiccriterion alone. The two other livers were harvestedbut, finally, not transplanted following histologicanalysis of a LB analyzed extemporaneously by thepathologists of the two transplant centers con-cerned. In these two cases, the LB measurementrequired by the protocol was carried out inaddition to the LB performed for the extempora-neous examination. In the end, four liver trans-plant teams (25% of the liver transplant teams)had been called in unnecessarily since the trans-plantation could not be finalised.Of the four non-transplanted livers, the pre-

operative value of LS was greater than 10 kPa inthree cases. There was a correspondence betweenthe abnormal values of LS and the liver macro-scopic aspect for three of the four liver grafts. Thehistologic analysis of the liver biopsies of thesethree livers was also abnormal, notably in terms ofsteatosis, with rates >50%, and one of them alsopresented a degree of fibrosis that was difficult toassess (Table 2). For the three values of LS greaterthan 10 kPa, there are wide ranges in LS values(29.9, 17.8, and 10.1 kPa) and no correlation with

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the abnormal histologic degrees of macrosteatosis(50%, 30% and 50%, respectively). The authorscannot explain such a wide range between LSvalues for a same degree of steatosis in theirpreliminary study with only 16 cadaveric donors.In the development of their next study on the sametopic with much larger patient population (635patients will be included), the authors hope theywill be able to explain such wide ranges for samevalues of steatosis and if the FibroScan� candistinguish significant steatosis if the LS is nearnormal. Nevertheless, this correspondence betweenan abnormal value of LS greater than 10 kPa andan abnormal histologic examination confirms thenotion of the interest of the pre-operative use ofFibroScan� and measurement of LS in the evalu-ation of liver grafts at the stage of selection of livergrafts from potential cadaveric donors.The fourth non-transplanted liver had an abnor-

mal ischemic macroscopic aspect but a far lowervalue of LS (5.4 kPa), and the histologic analysisdid not reveal severe steatosis. This graft wasrejected by the liver transplant team because thevisual inspection revealed macrosteatotis. TheFibroScan� readings and the LB result wouldsuggest otherwise.

Among the 12 livers harvested and transplanted,the conventional selection criteria used in France(level 1 and 2) were valid and sufficient. The LSvalue of each liver was recorded with a mean of6.8 ± 2.4 kPa. The pathology analyses of the LBperformed within the protocol framework werealso, a posteriori, normal (Table 2).

Discussion

The criteria presently available to assess the degreeof steatosis of liver grafts are imaging (ultrasonog-raphy [US], multi-detector row computed tomog-raphy [MDCT] or magnetic resonance imaging[MRI]) and the macroscopic aspect of the liverduring the pre-operative selection (10). Neverthe-less, the hepatic biopsy remains the only objectiveexamination of reference to quantify the degree ofsteatosis. The benefits of a supplementary objectiveevaluation of the liver before harvesting surgicalprocedure, such as measurement of the LS, shouldenable a better assessment of the quality of thepotential liver graft.

A high degree of steatosis (macro- or microstea-tosis) of a liver graft increases the severity of theischemic-reperfusion lesions observed during the

Table 2. Macroscopic aspect, histologic analysis of a liver biopsy and measurements obtained from the FibroScan for each liver of the 16 potential donors

16 Potentialdonors

Age(yr)/sex

Livermacroscopicaspect

Liver biopsy FibroScan�

Fibrosis

SteatosisMiS/MaS(%) Cholestasis

Duration ofexamination(min)

Number ofmeasurements(number ofvalidacquisitions)

Successrate (%)

Interquartilerange/medianvalue (%)

Measuredelasticity(KPa)

0/12 4/12 2/127 ± 5m ± SD

18 ± 11m ± SD

77 ± 25m ± SD

18 ± 15m ± SD

6.4 ± 2.2m ± SD

Livers harvested/transplanted (12)1 19/F Normal No No/no No 4 10 (10) 100 16 9.12 25/F Normal No 10%/no No 3 10 (10) 100 13 6.13 73/M Normal No 10%/no No 12 39 (10) 26 9 3.34 48/F Normal No No/no No 18 40 (17) 43 64 9.35 48/M Normal No No/5% No 7 22 (16) 73 21 8.46 45/M Normal No No/1% No 6 19 (14) 74 8 5.37 74/F Normal No No/no No 6 19 (10) 53 16 2.58 39/M Normal No No/no No 6 11 (10) 91 11 7.99 46/F Normal No No/no Discreet 7 13 (10) 77 9 6.710 52/F Normal No No/no No 7 12 (10) 83 15 4.611 43/M Normal No No/no No 3 10 (10) 100 12 7.712 74/M Normal No No/no Discreet 3 10 (10) 100 21 5.6

Non-transplanted livers (4)Harvested (2) 18/F Ischemic No 10%/no No 13 10 (10) 100 15 5.4

24/M Steatotic No 10%/50% No 8 22 (15) 68 45 29.9Not harvested(2)

57/M Fibrotic Yes 20%/30% No 5 13 (10) 77 4 17.863/M Steatotic No 10%/50% No 10 10 (10) 100 18 10.1

MiS, microvesicular steatosis; MaS, macrovacuolar steatosis.

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liver transplantation procedure with, consequently,a delay in the return to the graft�s functioning (11).Because of this, some liver transplant teamssystematically reject the grafts that appear steatoticduring the pre-operative selection in the hospitalconcerned (12). Although the microsteatoticdegree, whatever the severity, does not appear tohave an impact on the return to functioning andsurvival of the graft (12), the situation is less clearregarding macrosteatosis, with the considerablerisk of delay in the return to functioning of thegraft in the case of more than 30% of steatosis (13).Between 30% and 60%, the decision to harvest ortake a liver graft or not remains debatable (14).Assessment of the degree of steatosis on theechogenicity of the hepatic parenchyma is onlyvisual and therefore qualitative (15). There isfrequent discordance between the pre-operativeechographical result, the macroscopic observationsof the transplant teams during harvesting, and theresults of the extemporaneous histologic analyses,sometimes conducted in the operating theater whenthe first two criteria are discordant (10). MDCT orMRI makes it easier to comprehend the evaluationof the steatosis than the US (16, 17). These twoexaminations are easy to conduct in potentialliving donors but cannot be performed at thepatient�s bedside, which implies the involvement ofextensive logistics in order to move the brain deaddonors, intubated and ventilated, to the imagingunits (10). The macroscopic aspect of the liver canonly be assessed by the transplant team at theharvesting site. It is a qualitative and subjectiveimpression that can be a source of considerableerror. The extemporaneous examination that maybe performed during harvesting is an operator-dependent examination that can lead to incorrectreading or interpretation by the pathologist. Thepresence of the transplant team at the sampling siteimplies very extensive logistics: night air travel andat the week end, flight teams on call for take-offand landing of the planes transporting the trans-plant teams, mobilisation of complete transplantteams, monopolisation of operating theaters andtheir teams. Furthermore, this great mobilisationof staff and material does not always result in liverharvesting when the macroscopic and/or extempo-raneous histologic examination reveals steatosis. Inthis context, it would be interesting to haveavailable a paraclinical examination allowing theprecise and objective quantification of the eventualsteatosis of a potential liver graft. The advantagesof using a FibroScan� in this population ofdeceased patients are the following: the measure-ment is taken at the patient�s bedside and is totallynon-invasive; the examination is simple, rapid,

similar to a Doppler, the result of the measurementis instantaneous and the examination is reproduc-ible and non-operator dependent (18). Today, theacknowledged fields of application of the Fibro-Scan� are hepatitis C virus (HCV, HBV, coinfec-tions HIV–HCV) and the monitoring of fibrosis orcirrhosis (19). In liver transplantation, otherauthors have demonstrated the interest of theFibroScan� in the follow-up of transplantedpatients (20–22). Regarding steatosis, some teamshave showed a correlation between LS and steato-sis, and also between fibrosis and necrotic inflam-matory activity of the liver (23, 24). Other studieson living liver donors, or patients suffering fromnon-alcohol related chronic hepatic diseases, didnot find this correlation (25, 26). Our preliminarystudy cannot confirm this correlation because ourpopulation is clearly insufficient to come to anyfinal conclusion.In order to optimise the evaluation of hepatic

steatosis using the FibroScan�, a new specificparameter, the controlled attenuation parameter(CAP) measured through ultrasound signalsacquired by the FibroScan�, in the process ofvalidation, has been developed (27–29). Thisparameter was not yet validated and availablewhen the authors performed their preliminarystudy, but in their larger work in progress theauthors will include the measure of CAP.In view of the results of this preliminary study

and the data in the literature, the authors underlinethe need to conduct a larger, multicenter study witha consequent population, to determine whether theFibroScan�, with the determination of the value ofLS and CAP, could help in the pre-operativeselection of liver grafts from brain dead donors.

Conclusion

In liver transplantation, the functional conse-quences for the transplanted patient stem fromthe quality of the graft, and one of the essentialproblems lies in the selection of the liver graft inpotential organ donors. The present selectioncriteria are not sufficient and remain hardly objec-tive. It is necessary for the practitioners, in the pre-operative selection period at the bedside of braindead donors, to have access to an objectivediagnostic tool that is simple, reproducible andquick, allowing not only the evaluation of thequality of the hepatic parenchyma but also thedegree of hepatic steatosis of the potential graft.The FibroScan� appears to meet some of thesecriteria, even if the authors cannot make anyconclusion on the feasibility of using theFibroScan� to assess the degree of steatosis. The

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FibroScan� presents no risk for the outcome of thepotential liver graft since it is a non-invasiveexamination using ultrasound vibrations. Our pilotstudy has shown the feasibility of performing aFibroScan� at the bedside of a brain dead patient,during the pre-operative selection of grafts beforeorgan harvesting. The LS value determined by theFibroScan�, with its quantitative and objectivenature, will probably never replace surgeon visu-alisation and LB if necessary but could be useful asanother tool for graft assessment. Determinationof the optimal threshold values based on LSenabling the discrimination of livers that can begrafted or not should, eventually, bring about areduction in the pointless moving around oftransplant teams obliged to reject a graft becauseof the macrosteatotic aspect of the liver and shouldoptimise the number of liver grafts harvested inFrance from brain dead donors and hence thenumber of liver transplanted patients.

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