Research ArticleClinical Studies

Stroke Volume Variation Monitoring to Minimize Blood Loss in Hepatocellular Carcinoma Resection

RYO SAITO, HIDETAKE AMEMIYA, NAOHIRO HOSOMURA, HIROMICHI KAWAIDA, YUDAI HIGUCHI, TAKASHI NAKAYAMA, KATSUTOSHI SHODA, SHINJI FURUYA, HIDENORI AKAIKE, YOSHIHIKO KAWAGUCHI, MAKOTO SUDO, SHINGO INOUE, HIROSHI KONO and DAISUKE ICHIKAWA
Anticancer Research January 2021, 41 (1) 409-415; DOI: https://doi.org/10.21873/anticanres.14790

Abstract

Background/Aim: We aimed to evaluate the correlation between stroke volume variation (SVV) and intraoperative blood loss (IBL) in hepatocellular carcinoma (HCC) resection and examine the perioperative utility of SVV-based management. Patients and Methods: Ninety-five patients who underwent partial or sub-segmental hepatectomy for HCC between 2013 and 2019 at the University of Yamanashi Hospital were retrospectively analyzed. A correlation analysis between IBL and SVV was performed, and then all cases were divided into three groups: high, middle, and low-SVV groups. Perioperative short-term outcomes based on SVV groups were analyzed. Results: There was a weak but significant negative correlation between SVV and IBL (ρ=–0.372, p<0.001). Comparative analysis revealed that low-SVV was associated with a high incidence of postoperative complications and blood transfusion (p=0.018 and 0.037, respectively), and high-SVV was not related with postoperative complications. Conclusion: SVV-based management is a significant and feasible strategy to achieve safe and exact surgical resection of HCC.

Key Words:

Recently, minimally invasive surgeries for various malignancies have been developed to promote favorable perioperative outcomes, such as low intraoperative blood loss (IBL), avoidance of postoperative complications, and better prognoses (1, 2). In particular, surgical resection for hepatocellular carcinoma (HCC) requires special consideration to minimize IBL due to the unique procedures of HCC resection and organ characteristics of the liver. For instance, because the liver involves numerous microvessels, hepatectomy involves some degree of IBL from the resection surface, depending on various factors including venous pressure. With regards to this issue, central venous pressure (CVP) monitoring is useful for minimizing IBL and has indeed been employed in clinical practice (3, 4). While CVP monitoring is also recommended in the Japanese Clinical Practice Guidelines for HCC 2017, the risk of pneumothorax or thrombotic complications during indwelling central venous catheterization is high (5-7). Highly invasive and high-risk practices, including central venous catheterization, tend to be avoided nowadays. Therefore, the stroke volume variation (SVV) monitoring method has attracted attention as an index for systemic circulating volume due to reduced invasiveness relative to CVP monitoring (8, 9).

Several outcomes of SVV monitoring during hepatectomy have been reported to date (10, 11). A study demonstrated the close correlations between CVP and SVV, and confirmed the safety of SVV-based management during hepatectomy (12). However, most of these studies targeted healthy patients, including liver transplant donors with better liver function than patients with various liver diseases (13). Thus, it remains unclear whether SVV correlates with IBL during hepatectomy for patients with HCC and chronic liver diseases. Here, we aimed to evaluate the correlation between SVV and IBL in HCC resection and examine the perioperative utility of SVV-based management.

Patients and Methods

Patients. This study was a retrospective analysis. Between January 2013 and December 2019, 217 patients underwent surgical resection for HCC at the University of Yamanashi Hospital. This study included 106 of these patients who underwent intraoperative SVV monitoring during partial resection or sub-segmentectomy. Five patients who underwent non-curative surgery with visible residual tumors and one patient who was treated with hemofiltration dialysis were excluded. Moreover, because severe bleeding generally causes high SVV, five patients with extremely high IBL (those in the 95th to 100th percentiles) were excluded. Finally, 95 patients were analyzed in this series. This study was approved by the Ethics Committee of the University of Yamanashi (approval number, 2050) and was performed in accordance with the ethical standards of the Declaration of Helsinki and its later amendments (14). Written informed consent was obtained from all patients.

SVV monitoring. During hepatectomy, all patients were managed with general anesthesia and a ventilator. Continuous arterial pressure was monitored with an intra-arterial catheter in almost all cases based on the assessment of the anesthesiologists, except for a few patients with the minimal hepatectomy. SVV was calculated as the fluctuation of the cardiac stroke volume in 20 s, which was measured using an arterial line and breathing rhythm via the Flo Trac™ system, as described previously (12). The calculated SVV value was indicated in real time and recorded every minute. Anesthesia management, such as infusion volume adjustment, blood transfusion requirement, and evaluation of biological parameters, was performed by the anesthesiologists. All intraoperative parameters, such as amount of bleeding as well as the timing of the start and end of surgery, were recorded in our electronic medical record system. In this study, the perioperative clinical data were retrospectively collected and analyzed.

Correlation analysis between SVV and IBL. The intraoperative bleeding index was converted into IBL per hour in this study to accurately estimate the effect of high SVV for minimizing bleeding. SVV was evaluated as the average value during surgery, from the start of the operation to the completion of all procedures. The correlation was evaluated using Spearman’s rank correlation coefficient due to the characteristics of IBL as a non-normal distribution value (15).

Definition of SVV groups and comparative analyses. A total of 95 patients were divided into three groups according to the SVV quartile: the L group was the bottom quartile (SVV<6.46%), the H group was the top quartile group (SVV>11.0%), and the two middle quartiles were the M group (6.46%≤SVV≤11.0%). This classification was employed in this study to evaluate the impact of especially high or low SVV management on the perioperative outcomes. Comparative analyses were performed to reveal the effects of SVV on perioperative outcomes, including IBL and incidence of blood transfusions. The diagnosis of cirrhosis was made based on the pathological findings of the surgically resected specimen (16). Vascular invasion indicated venous, arterial, and bile duct invasion. The difficulty index was calculated according to the IWATE criteria with modification of surgical procedure parameters because both laparoscopic and laparotomy approaches were included in this study (17). In short, the laparotomy approach was awarded “-1 point” in this study similar to the HALS/Hybrid procedure, in contrast to the laparoscopic approach, which was awarded “0 points.” The total number of points was compared among groups.

Perioperative complications were evaluated based on the Clavien-Dindo classification, and grade II or higher were defined as those with clinical significance (18). Furthermore, to assess the effect on perioperative renal function of patients, which seemed one of the major adverse effects of high SVV, perioperative changes of serum creatinine levels in each group were evaluated. The change in creatinine levels was evaluated in each patient as a ratio to the preoperative value, and their average values were compared between the SVV groups.

Statistical analysis. All continuous variables are expressed as means±standard errors or the median and range, unless otherwise indicated. Statistical analyses were performed using the chi-square test and Student’s t-test. Correlation analyses were performed using Spearman’s correlation test. The correlation coefficient is indicated as ρ. All statistical analyses were performed with EZR (Saitama Medical Center, Jichi Medical University, Saitama, Japan), a graphical user interface for R (The R Foundation for Statistical Computing, Vienna, Austria), and JMP® 13 (SAS Institute Inc., Cary, NC, USA). p<0.05 was considered to indicate statistical significance (19).

Results

Correlation analysis of SVV and IBL. The median IBL was 69.3 ml/h (range=0.796-243.4 ml/h), and the median SVV was 8.33% (range=3.98-20.2%). There was a weak but significant negative correlation between SVV and IBL for all cases (ρ=–0.372, p<0.001, Figure 1). Further detailed analyses with categorization according to various situations revealed that there was a more striking correlation in patients without cirrhosis (ρ=–0.417, p=0.002) or those who underwent partial hepatectomy (ρ=–0.448, p<0.001) (Figure 2a, b). However, the correlation was similar regardless of tumor location [right liver (ρ=–0.394, p=0.002), left liver (ρ=–0.356, p=0.039)] (Figure 2c, d).

Figure 1.
Figure 1.

Correlation analysis between SVV and IBL. Spearman’s correlation test revealed a significant negative correlation between SVV and IBL (ρ=–0.372, p<0.001). SVV: Stroke volume variation; IBL: intraoperative blood loss.

Figure 2.
Figure 2.

Detailed correlation analysis in various categorizations. There was more strong negative correlation between SVV and IBL in detailed analysis for patients without liver cirrhosis (a; ρ=–0.417, p=0.002) or patients underwent partial hepatectomy (b; ρ=–0.448, p<0.001), compared with the analysis involving whole patients. The correlation was similar independent on tumor localization of whether right (c; ρ=–0.394, p=0.002) or left liver (d; ρ=–0.356, p=0.039). SVV: Stroke volume variation; IBL: intraoperative blood loss.

Comparative analyses among the three groups based on SVV. Table I shows the results of the comparative analyses of clinicopathological findings and perioperative outcomes among the subgroups classified according to the SVV value. The median SVV values in the L, M, and H groups were 5.70%, 8.41%, and 13.2%, respectively. IBL gradually decreased with increasing SVV (Figure 3a). There were significant differences in IBL between the L and H groups (p<0.001) and L and M groups (p=0.008). In contrast, the operative time was similar in all groups and was not affected by SVV values (p=0.970, Figure 3b). Although there were more patients who underwent open hepatectomy in the L group than in the H group, further detailed analyses demonstrated that there was a negative correlation between SVV and IBL with the laparotomy approach but not with the laparoscopic approach (ρ=–0.214 and –0.151, respectively).

View this table:
Table I.

Clinicopathological features of patients in each group.

Figure 3.
Figure 3.

Comparison of IBL and operative time. IBL was gradually decreased with increasing SVV with significant differences (a), in contrast to operative time, which were similar in each group and not affected by SVV values (b). IBL: Intraoperative blood loss; SVV: stroke volume variation.

Regarding postoperative outcomes, low SVV was associated with a high incidence of postoperative complications (p=0.018) and perioperative blood transfusion (p=0.037). As a result of increasing apparent or likely invisible complications, the postoperative hospital stay tended to be longer for patients with low SVV than for those with high SVV (p=0.001 between groups L and H, data not shown).

Complications associated with high SVV. Figure 4 shows the postoperative variation in relative creatinine levels, which reflected the limited intraoperative infusion volume required to maintain a high SVV. We observed an increase in creatinine levels immediately after surgery in all groups. Although there was a slight change in creatinine level of <1.2-fold in group H, no differences were observed in the creatinine levels before surgical intervention and those at the time of discharge in all groups. Additionally, no complications such as temporary or continuous hemodialysis, or thrombotic disorders including main portal vein thrombosis or cardiac and cerebral infarcts occurred due to high SVV and limited fluid transfusion.

Figure 4.
Figure 4.

Comparison of relative creatinine levels. Increased creatinine levels immediately after surgery were observed in every group. Although group H showed the relatively obvious variation, the creatinine elevation returned to baseline levels by the time of discharge. SVV: Stroke volume variation; Pre: preoperative; Post: postoperative; POD: postoperative day; Dis: discharge.

Discussion

The results of this study demonstrated that intraoperative SVV value was negatively correlated with IBL in patients who underwent partial or sub-segmental hepatectomy for HCC. Furthermore, patients with high SVV experienced fewer postoperative complications and a shorter postoperative hospital stay than those with low SVV. Therefore, monitoring SVV and maintaining a high SVV value during hepatectomy may minimize IBL and reduce the incidence of postoperative complications.

For various surgeries, it is vital to minimize IBL and keep the operative fields bloodless and clear. This helps surgeons to perform operations safely, avoid perioperative complications, and provide better postoperative outcomes and prognoses for patients (20). Hepatectomy is a surgical procedure that demands the most circumspect maneuvers due to continuous bleeding during liver resection (21). In particular, surgical resection for HCC carries a higher risk of high IBL than do other procedures due to vascular invasion, massive occupation of tumors, and the requirements of resection with sufficient margins to avoid exposure of the tumors. Moreover, HCCs generally occur due to chronic hepatitis and/or liver cirrhosis, such as virus-induced hepatitis, alcoholic hepatitis, or nonalcoholic steatohepatitis. IBL tends to be higher in livers with hepatitis and/or cirrhosis than in healthy livers (22). Therefore, strategies for minimizing IBL in HCC resection become more important than those for benign tumors in healthy livers (23).

IBL in hepatectomy is generally associated with two major causes. One is continuous bleeding from the resected surface of the liver depending on the hepatic venous pressure, which is often controlled by SVV or CVP monitoring, as described in this study. The other is unpredictable accidental bleeding from major vessels, which cannot be completely avoided using the strategies mentioned above. It is not uncommon for hepatectomy performed using an approach with intrinsically low IBL, such as the laparoscopic approach, to be affected by the latter cause of accumulated bleeding. Indeed, the correlation between IBL and SVV in patients who underwent laparoscopic surgery was weak and non-significant in this study. In these patients, both the IBL per hour and total IBL were significantly lower than those in patients who underwent open hepatectomy (39 vs. 110 ml/h, p<0.001; 258 vs. 702 ml, p<0.001; respectively. data not shown). In laparoscopic cases with low IBL, the influence of the latter bleeding cause would be relatively higher, and evaluation of the utility of SVV monitoring for minimizing IBL was difficult in these cases. This is one of the reasons underlying the difficulty in deriving definitive conclusions from recent studies, including the present study. To eliminate the effect of these differences on IBL, and to evaluate the correlation between SVV and IBL as precisely as possible, the present study focused on partial liver resection or sub-segmentectomy, in which bleeding from major vessels rarely occurs. Indeed, a further detailed analysis avoiding such uncertain variation in this study clearly demonstrated that the IBL increases with reductions in SVV (for patients without liver cirrhosis or those who underwent partial hepatectomy, Figure 2a, b). In addition, because the total amount of intraoperative bleeding is generally proportional to the duration of surgery, particularly in hepatectomies, IBL was evaluated as a converted value i.e., the total bleeding amount per hour. Exploratory analysis revealed a pronounced positive correlation between the intraoperative total bleeding amount and operation duration (ρ=–0.494, p<0.001).

During laparoscopic hepatectomy, the pneumoperitoneum helps to maintain a low relative venous pressure and minimize IBL, similar to laparoscopic surgery for other malignancies (24, 25). In order to control continuous venous hemorrhage during hepatectomy, several further procedures, such as secure compression of the hepatic resection surface and raising the liver or moving the patients to a head-up position, are attempted, in addition to maintaining a low central venous pressure. However, these hemostatic approaches can be sometimes difficult to perform in laparoscopic surgery. Therefore, even in the laparoscopic approach, high SVV should contribute to a clear surgical field and minimizing IBL to a similar extent as open hepatectomy. Furthermore, because continuous IBL predominantly occurs from the liver resection surface based on hepatic venous pressure despite the approach or extent of hepatectomy, the results of this study, which demonstrated the clinical significance of high SVV, could be applied for any type of hepatectomy.

To maintain a high SVV value, intraoperative fluid transfusion is typically limited to the fullest extent possible. Therefore, the total infusion volume was lower in the high SVV group than in the lower and middle groups, which resulted in relatively reduced urinary output and increased renal stress in the high SVV group (data not shown). Although this trend would have led to an increase in postoperative creatinine levels in the high SVV group, these levels recover to the preoperative levels with time. Indeed, fluid infusion was slightly higher in these oliguric patients in the postoperative phase than in those with low SVV and without oliguria. As a consequence, the adverse effects of intraoperative high-SVV management were transient. This demonstrated that the effect of a limited infusion volume on renal function could be temporary with careful postoperative management. Together with the lack of other complications due to hypovolemia, or rather the fact that low SVV might be associated with postoperative ascites and a longer hospital stay, the outcomes of this study supported the clinical significance and feasibility of high-SVV management.

This study had several limitations. First, it was difficult to derive definitive conclusions due to the small sample size. Second, the degree of surgical proficiency might have significantly affected the IBL in each case of this study. In addition, the universal target SVV value and the absolute significance of SVV management for extensive hepatectomy both remain to be elucidated. However, although the unique cutoff values of SVV in this study were indeed used for the analyses, the results clearly demonstrated optimal outcomes in patients with a particularly high SVV, and unfavorable ones in the especially low SVV group. Further prospective and large-scale studies would contribute to the resolution of these issues and demonstrate the significant advantages of SVV-based management for HCC resection.

In conclusion, this study indicated a significant correlation between SVV and IBL during hepatectomy for HCC, and that high-SVV management minimized IBL with few complications. SVV-based management is a significant and feasible strategy to achieve safe and exact surgical resection of HCC.

Acknowledgements

The Authors are grateful to Dr. Kazuha Mitsui & Prof. Takashi Matsukawa (Department of Anesthesiology, Faculty of medicine, University of Yamanashi, Yamanashi, Japan) for their assistance in collecting the clinical data. The Authors would like to thank Editage (www.editage.com) for English language editing. The Authors report no proprietary or commercial interest in any product mentioned or concept discussed in this article. This study was performed mainly with expenses grants from the University of Yamanashi, and partially supported by JSPS KAKENHI (20K17642).

Footnotes

  • Authors’ Contributions

    RS and HAm designed the study, and RS mainly analyzed the data and wrote the initial draft of the manuscript. DI and HAm contributed to analysis and interpretation of data, and assisted in the preparation of the manuscript. All other Authors have contributed to data collection and interpretation, and critically reviewed the manuscript. All Authors approved the final version of the manuscript and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

  • Conflicts of Interest

    The Authors have no conflicts of interest to declare regarding this study.

  • Received December 10, 2020.
  • Revision received December 16, 2020.
  • Accepted December 17, 2020.

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Stroke Volume Variation Monitoring to Minimize Blood Loss in Hepatocellular Carcinoma Resection
RYO SAITO, HIDETAKE AMEMIYA, NAOHIRO HOSOMURA, HIROMICHI KAWAIDA, YUDAI HIGUCHI, TAKASHI NAKAYAMA, KATSUTOSHI SHODA, SHINJI FURUYA, HIDENORI AKAIKE, YOSHIHIKO KAWAGUCHI, MAKOTO SUDO, SHINGO INOUE, HIROSHI KONO, DAISUKE ICHIKAWA
Anticancer Research Jan 2021, 41 (1) 409-415; DOI: 10.21873/anticanres.14790
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