Objectives: Data on the relevance of surgeon experience in liver transplant procedures are scarce. In this study, we evaluated the effects of individual surgeon experience on survival outcomes after deceased-donor liver transplant.

Materials and Methods: In this retrospective analysis of 1193 liver transplant procedures, quantile regression for survival data was performed to assess the effects of surgeon experience. Conditional quantiles of mortality and graft loss were set as primary and secondary outcome measures, respectively, which were categorized as early, midterm, and late.

Results: Greater experience of a surgeon performing hepatectomy increased the risk of early mortality (P = .005) and graft loss (P = .025) when the recipient Model for End-Stage Liver Disease was ≤ 25 and the donor Model for End-Stage Liver Disease was ≤ 1600. In conventional transplant procedures, greater experience of surgeon performing hepatectomy additionally increased the risk of midterm mortality (P = .027) and graft loss (P = .046). Conversely, a graft implant procedure performed by a more experienced surgeon was associated with better early, midterm, and late outcomes after conventional transplants
(all P < .037) and reduced the risk of early graft loss when the donor Model for End-Stage Liver Disease score was > 1600 (P = .027).

Conclusions: Unexpectedly, individual surgeon experience yields bimodal effects on posttransplant outcomes, dependent on the stage of operation, operative technique, severity of recipient status, and transplant risk profile.

Key words : Center volume, Donor model for end-stage liver disease score, Mortality, Risk profile

Introduction

Liver transplant is one of the most complex surgical procedures, with postoperative mortality rates ranging from 3% to 12% and 5-year survival rates ranging from 70% to 75%.^1-5 Numerous studies available in the transplant literature have reported risk factors for poor outcomes. Those of most relevance have reported outcomes attributable to recipients, donors, and operative procedural characteristics.^1,4,6,7 In addition, the role of combined factors, such as the donor Model for End-Stage Liver Disease (D-MELD) score introduced by Halldorson and associates and derived from recipient MELD score and donor age, has been recently advocated.^8,9 However, data on the association between the individual experience of the surgeon and patient outcomes after deceased-donor liver transplant are scarce. Notably, surgeon experience has been previously reported as a factor significantly related to postoperative outcomes in other transplant procedures and in procedures in the field of general surgery.^10-13

Given the worldwide shortage of donors, the optimal utilization of the scarce resources is of basic importance. Previously, much attention has been given to the association between case volume at a particular transplant center and posttransplant outcomes. Several groups who studied related topics have found that outcomes of liver transplants performed at high-volume centers are superior to those performed in lower-volume centers.^4,14-16 The reported differences may be at least partly due to greater experience of surgeons from high-volume centers.¹⁵ However, most importantly, these studies did not adjust for an individual surgeon’s performance, limiting these studies.^15,16

Short- and long-term outcomes after liver trans-plant have improved over time according to both single-center studies and studies based on large scientific registries.^1,2,4,17,18 However, these obser-vations obviously represent not only the increasing experience of particular surgeons but also the increasing experience of the transplant team, improved operative techniques, improved perioperative management, better immunosuppression, improved patient selection, and improved long-term patient care. Therefore, in this study, the primary purpose was to evaluate whether an individual surgeon’s experience affects patient outcomes after liver transplant.

Materials and Methods

In this retrospective exploratory analysis, we included 1193 deceased-donor liver transplant procedures performed in the Department of General, Transplant, and Liver Surgery at the Medical University of Warsaw (Poland) between 1996 and 2012. Our university’s ethics committee approved the study before it began, which conformed to the ethical guidelines of the 1975 Helsinki Declaration. Patient death was set as the primary endpoint, whereas retransplant or patient death was set as the combined secondary endpoint. These endpoints were used to calculate primary and secondary outcome measures, namely, conditional quantiles of mortality and graft loss, respectively. Cumulative mortality and graft loss were categorized as early (0.05 and 0.10 quantiles), midterm (0.15 and 0.20 quantiles), and late (0.25 and 0.30 quantiles) outcomes. Details on the operative technique and posttransplant immunosup-pression regimen have been previously discussed.⁵

All surgeons were experienced in hepatobiliary surgery before performing their first liver transplant. None of the surgeons had previously performed liver transplant procedures in any other transplant center. Separate teams routinely perform hepatectomy and graft implantation; hence, there are 2 operators for the liver transplant procedures (the first performing hepatectomy and the second performing graft implantation). Accordingly, each transplant was characterized by 2 separate covariates, namely, the individual experience of the surgeon performing the hepatectomy and the experience of the surgeon performing the graft implantation. These covariates were defined as a cumulative number of previously performed hepatectomies and implantations, respectively. Notably, surgeon experience was evaluated as a continuous risk factor; hence, effect estimates were given for increase in experience by 1 hepatectomy or graft implantation. The third covariate was overall experience of the transplant team, which was defined as the total number of previously performed transplants in the transplant center. This covariate was introduced to provide not only a measure of the increasing experience of the surgical transplant team but also a measure of the other specialist teams involved in the liver transplant program. It also provided an indirect measure of elapsing time.

To adjust the effects of the individual surgeon experience on the risk of death and graft loss, the D-MELD score was included in each of the multivariable analyses of patient and graft survival. Moreover, separate analyses were performed in patients with low and high MELD (cut-off of 25 points) and D-MELD (cut-off of 1600 points) scores, those who had piggyback and conventional transplants, and those who had end-to-end duct-to-duct or Roux-en-Y hepaticojejunostomy anastomoses.

Quantitative and qualitative variables are presented as median (interquartile range) and number (%). A Kaplan-Meier estimator was used to calculate the survival rates. The log-rank test was applied to compare survival curves. Given that surgeon experience and other covariates do not necessarily influence the risk of death and graft loss equally over time, they were evaluated for their potential impact on particular quantiles of cumulative mortality and graft loss by using quantile regression analyses for survival data (QUANTLIFE procedure of SAS; SAS Institute, Inc., Cary, NC, USA). Quantile regression for survival data provides a flexible way to capture heterogeneous effects in the sense that tails and the central location of the distribution of survival time can differentially depend on the covariates. Moreover, the proportional hazards assumption was not met; hence, we precluded the use of Cox regression. Effect estimates, survival curves, and hazard functions were presented with 95% confidence intervals. The level of statistical significance was set at .05. We used SAS version 9.4 software (SAS Institute) for statistical analyses.

Results

The baseline characteristics of the study cohort are shown in Table 1. Briefly, 14 surgeons performed 1193 liver transplant procedures. The median experience of surgeons during hepatectomies and graft im-plantations was 50 operations (interquartile range, 24-83) and 61 operations (interquartile range, 27-108), respectively. Moreover, at the conclusion of the study, the median individual experience of surgeons was 79 hepatectomies (interquartile range, 60-124) and 68 graft implants (interquartile range, 17-158). Median duration of follow-up was 4.5 years (95% confidence interval, 4.1-4.9 y).

Patient survival rates at 1, 3, 5, and 10 years after liver transplant were 84.2%, 77.6%, 74.1%, and 65.8%, respectively, and graft survival rates at the corresponding time points were 81.5%, 74.6%, 70.9%, and 62.9%, respectively. Notably, patient survival was significantly lower in the recipients with MELD score exceeding 25 points than in those with MELD score up to 25 points (P < .001; Figure 1a). Similarly, graft survival was significantly lower after liver transplants characterized by D-MELD scores exceeding 1600 points than that after those characterized by D-MELD scores up to 1600 points (P < .001; Figure 1a). Moreover, both patient and graft survival rates after conventional liver transplants were inferior to those after piggyback operations (both P < .001; Figure 1b). No significant differences in long-term patient (P = .151) and graft survival (P = .123) rates were noted after transplants with end-to-end duct-to-duct biliary anastomosis or Roux-en-Y hepaticojejunostomy (Figure 1c).

In all patients, as the experience of a surgeon performing hepatectomy increased, the mortality increased up to the 0.05 quantile (P = .002; Figure 2a), independently of the D-MELD score, experience of the surgeon performing the graft implant, and overall experience of the transplant team (Table 2). The negative independent impact of greater experience of the hepatectomy surgeon on the risk of early mortality was observed for liver transplant procedures in recipients with MELD score up to 25 points (P = .005; Figure 2b) but not in recipients with higher MELD score (P = .619; Figure 2c). There were no significant effects of the individual experience of the surgeon performing the graft implantation on patient survival regardless of the MELD score (Figure 2a-c). Notably, the D-MELD score had a significant impact on all quantiles of posttransplant mortality in the entire study cohort (all P < .001; Table 2). Moreover, greater overall experience of the transplant team was significantly associated (P = .030) with a lower risk of late mortality (0.25 quantile).

Greater experience of a surgeon performing hepatectomy independently increased the risk of early (0.05 quantile) graft loss after all liver transplant procedures (P = .019; Figure 3a) and after those characterized by a D-MELD score of up to 1600 points (P = .025; Figure 3b). This effect was not observed in liver transplants characterized by a D-MELD score exceeding 1600 points (P = .700; Figure 3c). Although the greater individual experience of the surgeon performing graft implants did not significantly influence risk of graft loss after all liver transplants (Figure 3a) and after those characterized by a D-MELD score up to 1600 points (Figure 3b), it independently reduced the risk of early (0.10 quantile) graft loss when a D-MELD score exceeded the cut-off (P = .027; Figure 3c). Notably, the D-MELD score significantly influenced the risk of graft loss in all quantiles (all P < .004; Table 2).

Conventional liver transplant procedures were associated with significant increases in the hazards of mortality and graft loss at approximately up to posttransplant years 6 and 7, respectively (Figure 4). Notably, the individual experience of the surgeon performing hepatectomy was not associated with patient or graft survival after lower-risk piggyback transplants (Figure 5a). However, it was inde-pendently associated with a higher risk of early (P = .024 for 0.05 quantile) and midterm (P = .027 for 0.20 quantile) mortality and higher risk of early (P = .027 for 0.10 quantile) and midterm graft loss (P = .046 for 0.15 quantile) after higher-risk con-ventional operations (Figure 5b). Similarly, the individual experience of the surgeon performing a graft implant did not influence patient or graft survival rates after piggyback operations (Figure 6a). However, for conventional liver transplant pro-cedures, graft implantations performed by more experienced surgeons were independently associated with lower risk of early (P = .002 for 0.05 quantile), midterm (P = .022 for 0.15 quantile, P = .024 for 0.20 quantile), and late (P = .015 for 0.25 quantile; P = .037 for 0.30 quantile) mortality, as well as with lower risk of early (P < .001 for 0.05 quantile), midterm (P = .006 for 0.15 quantile; P = .005 for 0.20 quantile), and late (P = .014 for 0.25 quantile) graft loss (Figure 6b). No specific effects of the individual surgeon experience on graft implantation were noted for liver transplants that involved end-to-end duct-to-duct (Figure 6c) or Roux-en-Y hepaticojejunostomy (Figure 6d) biliary anastomoses.

Discussion

Although numerous studies have addressed the effects of center volume on liver transplant outcomes,^4,14-16 there is lack of data on the importance of the individual surgeon’s experience. Notably, center volume is not an adequate measure of the particular experience of surgeons who participate in a transplant program because a high number of surgeons with limited individual experience may contribute to a high total volume of performed operations and vice versa. Accordingly, to the best of our knowledge, this is the first study to provide information on the relevance of individual surgeon experience on liver transplant outcomes based on a large number of operations performed at a single center.

To evaluate whether the influence of a surgeon’s experience varies with respect to the early, midterm, and long-term outcomes, we used multivariable quantile regression analyses to analyze survival data. Interestingly, the risk of early mortality and graft loss increased unexpectedly as experience of a surgeon performing hepatectomy increased. In particular, a surgeon having greater experience with hepatectomy increased the risk of both early and midterm mortality and graft loss after conventional liver transplants involving the excision of the recipient’s retrohepatic vena cava and utilization of the venovenous bypass. Although conventional operations are more frequently performed in generally sicker patients, this association was not observed in the subgroup of liver transplants characterized by high D-MELD scores or in those performed in recipients with high MELD scores, suggesting the presence of a technique-specific effect. Additionally, the negative effects of a surgeon having greater experience with hepatectomy were observed in liver transplant procedures characterized by lower recipient MELD scores and lower D-MELD scores. There are at least 2 expla-nations for this unexpected negative effect. First, this effect may resemble the U-shaped mortality curve, as shown with esophageal surgery or major liver resections,^19,20 which is commonly related to the phenomenon of “overconfidence.” This phenomenon has been reported previously, although to a lesser extent, in a renal transplant setting.^21,22 More specifically, because all surgeons who performed liver transplants in the present study were previously highly experienced in hepatobiliary surgery, the increase in early mortality rate potentially represents only the right side of the U-shaped curve. Second, the negative effect may be due to a selection bias (ie, the performance of technically more challenging operations by more experienced surgeons). However, the transplant team surgeons in our study were assigned to liver transplant procedures on a nearly randomized basis, as the assignment was made based on the 24-hour “on-call” shift. Therefore, this novel observation remains to be reconfirmed in future studies.

Although the importance of the cumulative individual surgeon experience has not been evaluated to date, a single study by Scarborough and associates focused on the individual surgeon’s annual volume of performed liver transplants.²³ The authors of that study reported that liver transplants conducted by high-volume surgeons are associated with lower postoperative complications and in-hospital mortality rates. However, because this study included data from the National Inpatient Sample database, these results could not be adjusted for MELD and D-MELD scores, important risk factor measures in the field of liver transplantation. Interestingly, operations performed by low- and intermediate-volume surgeons were associated with a decreased risk of major intraoperative events, partly supporting the “overconfidence” hypothesis. Finally, given that the group of high annual-volume surgeons comprises individuals with different cumulative case loads, both surgeon characteristics are not necessarily easily replaceable.

Contrary to the effects of greater surgeon experience with hepatectomy, increased individual experience of the surgeon performing graft implants improved early, midterm, and long-term patient survival rates, as well as graft survival rates. These observations are in line with those of other studies involving oncologic surgery, in which long-term results significantly improved with greater surgeon experience.^24-27 Moreover, these results are consistent with the primary hypothesis of this study that, whereas the immediate and perhaps midterm outcomes are equally influenced by individual experiences of surgeons during hepatectomy and graft implantation, the long-term outcomes are affected mostly by the experiences of surgeons performing graft implantation. Interestingly, the positive effects of greater experience of the surgeon performing graft implantation were observed only for conventional and not for piggyback liver transplant procedures. Although the hazards of death and graft loss were significantly increased in those who underwent conventional liver transplants with routine venovenous bypass versus those who underwent piggyback operations, this study does not provide evidence for the superiority of the latter technique. Nevertheless, conventional transplants were undoubtedly a higher-risk operation in the present study, consistent with results from a cohort of hepatocellular carcinoma patients.²⁸ Moreover, the negative effects of the conventional technique have also been reported by other authors.²⁹ Therefore, our finding of the positive effects of the experience of a surgeon performing graft implantation has mostly been observed in more technically challenging or perhaps higher-risk operations, as this effect was observed in a subgroup of liver transplants characterized by a high D-MELD score.

In addition to analyzing the effects of surgeon experience, the results of this study provide new information on the impact of D-MELD scores on posttransplant outcomes. Although contradictory results have been reported,³⁰ it is widely recognized as an important predictor of poor outcomes after liver transplant.^31,32 However, the novel finding of the present study was that the negative effects of higher D-MELD scores on patient and graft survival were present and interestingly rather similar throughout all quantiles. Accordingly, this result supports its use as the potential confounder for the adjustment of the impact of surgeon experience in the present study.

Notably, although we observed no significant effects for the experience of the surgeon performing hepatectomy in liver transplants with a D-MELD score exceeding 1600 points, we did find that greater experience of the surgeon performing graft implantations decreased the risk of early graft loss. Thus, the results of high-risk transplants seem to be less vulnerable to the potential “overconfidence” of surgeons performing hepatectomy and, at the same time, more dependent on the protective effects of graft implantations performed by more experienced surgeons. Accordingly, because there were no benefits of higher surgeon experience in liver transplants characterized by D-MELD scores not exceeding 1600 points or performed with the piggyback technique, operations characterized by these 2 parameters seem more suitable for surgeons who are still gaining experience.

We found that the only benefit of increased experience of the transplant team (or, in other words, hospital volume) was the lower risk of late mortality and a statistical tendency toward lower risk of late graft loss. The lack of any more significant effects, which were observed in other studies,^14,33 is most probably related to the adjustment for the impact of individual surgeon experience, which has not been previously performed. On the other hand, the significant positive influence in our study most certainly represents improvements not only in surgical care but also in the general multidisciplinary care of patients.

The learning curve in living-donor liver transplant has been evaluated in previous studies by Li and associates and Kim and associates.^34,35 However, both studies assessed the experience of the whole transplant team rather than that of individual surgeons and showed no difference in patient survival. In 2006, Jurgaitis and colleagues compared outcomes after liver transplants performed by surgeons who had experience of over 30 such operations (n = 106) versus those after the first operations performed by transplant fellows under the supervision of a senior transplant surgeon (n = 49).³⁶ The study indicated no significant dif-ferences in short-term patient survival. Nevertheless, the effects of experience in the surgeons who had performed over 30 previous operations were not evaluated; hence, this study was rather unlikely to reveal the significant effects of experience that were found in the present study.

Several limitations of the present study must be acknowledged. First, it is limited by its retrospective design. Second, all surgeons who performed liver transplants were previously experienced in hepato-biliary surgery and had been performing other complex operations related to this field. Accordingly, the results obtained are limited to surgeons entering the field of liver transplant surgery who are already experienced in the performance of complex hepatobiliary procedures.

In conclusion, individual surgeon experience yields a bimodal effect on liver transplant outcomes. The greater experience of a surgeon performing hepatectomy is generally associated with inferior outcomes, particularly after conventional liver transplant procedures involving venovenous bypass use and in patients characterized with lower recipient MELD and D-MELD scores. Conversely, greater experience of surgeon performing graft implantation has positive effects on posttransplant outcomes in higher risk and conventional liver transplant procedures.

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