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Incidence and risk factors associated with a high comprehensive complication index score after splenectomy in cirrhotic patients with hypersplenism
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Incidence and risk factors associated with a high comprehensive complication index score after splenectomy in cirrhotic patients with hypersplenism Zhaoqing Du, PhD,a,b,c Jian Dong, PhD,a,b,c Jia Zhang, PhD,a,b,c Jianbin Bi, PhD,a,b,c Zheng Wu, PhD, MD,c Yi Lv, PhD, MD,a,b,c Xufeng Zhang, PhD, MD,a,b,c,* and Rongqian Wu, PhD, MDa,b,* a
Shaanxi Provincial Center for Regenerative Medicine and Surgical Engineering, Xi’an, Shaanxi Province, China Institute of Advanced Surgical Technology and Engineering, Xi’an, Shaanxi Province, China c Department of Hepatobiliary Surgery, First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi Province, China b
article info
abstract
Article history:
Background: Postoperative complications after splenectomy are not rare and can be serious
Received 24 June 2017
in cirrhotic patients. The purpose of this study was to assess postoperative complications
Received in revised form
using the comprehensive complication index (CCI) after splenectomy in cirrhotic patients
10 August 2017
and identify risk factors for those who developed a high postoperative CCI score.
Accepted 29 September 2017
Materials and methods: This retrospective study included 208 adult patients with viral
Available online xxx
hepatitis-related cirrhosis, who underwent elective splenectomy at our hospital from January 2002 to June 2012. The primary outcome was the CCI score. A CCI score >30 was
Keywords:
considered to be a high CCI score.
Comprehensive complication index
Results: The median CCI score in this cohort was 25.6 (range: 8.7-62.9), and 66 patients
(CCI)
(31.7%) had a CCI score >30. Univariable and multivariable analyses showed that the risk
Splenectomy
factors independently associated with a high CCI score were a history of hypertension and
Cirrhosis
a model for end-stage liver disease (MELD) score 10 prior to splenectomy.
Hypersplenism
Conclusions: A high CCI score is common in cirrhotic patients undergoing splenectomy. The
Portal hypertension
CCI is a useful grading system to assess postoperative morbidity in cirrhotic patients un-
Risk factors
dergoing splenectomy. Preoperative blood pressure control is recommended and cirrhotic patients with an elevated MELD score should consider other treatment options for hypersplenism. ª 2017 Elsevier Inc. All rights reserved.
Introduction Hypersplenism is common in patients with liver cirrhosis. The presence of hypersplenism indicates more advanced liver
disease and is associated with anemia, leukopenia, thrombocytopenia, bleeding tendency, and portal hypertension. Splenectomy corrects cytopenia, improves liver function, and expands treatment choices for the underlying liver disease.1-4
* Corresponding author. Shaanxi Provincial Center for Regenerative Medicine and Surgical Engineering, First Affiliated Hospital of Xi’an Jiaotong University, 76 West Yanta Road, P.O. Box 124, Xi’an, Shaanxi Province 710061, China. Tel.: þ86 29 82657541; fax: þ86 29 85252580. E-mail addresses: [email protected] (X. Zhang), [email protected] (R. Wu). 0022-4804/$ e see front matter ª 2017 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2017.09.045
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Therefore, it remains a therapeutic option for patients with hypersplenism due to liver cirrhosis.5-8 However, the indications for splenectomy in cirrhotic patients are somewhat controversial.9 One of the major reasons for this controversy is that postoperative complications after splenectomy are not rare and can be serious in cirrhotic patients.10 However, few studies have comprehensively evaluated postoperative complications in patients with liver cirrhosis undergoing splenectomy for hypersplenism. The comprehensive complication index (CCI) was recently developed to document postoperative complications.11 It measures surgical morbidity by adding up all complications attributable to a surgical procedure and weighting them according to their severity.12 Thus, the CCI reflects the summative severity of all major and minor postoperative complications in a single patient. By avoiding underreporting minor complications, the CCI is a robust system to evaluate postoperative morbidity. Due to its consistency and completeness, the CCI has become one of the standard ways to report postoperative complications in clinical trials. To the best of our knowledge, however, there have been no reports on the incidence of a high CCI score in cirrhotic patients undergoing splenectomy for hypersplenism. The purpose of this retrospective study was to assess postoperative complications using the CCI in a large cohort of patients with viral hepatitis-related cirrhosis who received splenectomy for hypersplenism and identify risk factors for those who developed a high postoperative CCI score.
Methods Study population From January 2002 to June 2012, 1229 cirrhotic patients were hospitalized for the treatment of hypersplenism at the First Affiliated Hospital of Xi’an Jiaotong University. Of these, 241 patients (19.6%) who underwent elective splenectomy were enrolled in this study. The primary diagnosis of all cases was liver cirrhosis with hypersplenism and portal hypertension. Contraindications were uncorrectable coagulopathy and severe cardiovascular disease that prohibit the administration of general anesthesia. All clinical data of these patients, including demographics features, perioperative laboratory values, and postoperative complications were gathered from the digital medical records. Thirty-three patients had incomplete clinical data and were excluded from further analysis. The remaining 208 patients composed our study population. This retrospective, observational study was approved by the Ethics Committee of the First Affiliated Hospital of Xi’an Jiaotong University and the approval number was 2016-046. This work has been conducted in accordance with the Declaration of Helsinki of the World Medical Association. The patient’s informed written consent was waived due to the retrospective nature of this study. All data were used only for statistical analysis in this study.
Evaluation of outcomes The primary outcome was the comprehensive complication index (CCI) score.12 The CCI was calculated as the sum of all
postoperative complications that are weighted by their severity (available at www.assessurgery.com). Postoperative complications were defined as the occurrence of medical or surgical complications within 90 days of surgery. The severity of complications was evaluated using the Clavien-Dindo classification scale.13
Statistical analysis For the continuous variables, we used mean standard deviation (SD) or median (range: mindmax) to describe. And categorical variables were presented as frequency and percentage. The statistical difference between two groups was compared by the Student’s t-test or Wilcoxon test for continuous data and the chi-squared test or Fisher’s exact test for categorical variables. For the statistical analysis between three or more groups, analysis of variance was used. Factors showing significant difference in the univariate analysis were further analyzed in the final multivariate log-regression model. All statistical analyses were done using the IBM SPSS software (version 22.0). P < 0.05 was considered statistically significant.
Results Patient demographics and characteristics The demographics and baseline characteristics of the 208 cirrhotic patients who underwent splenectomy for hypersplenism were shown in Table 1. Of these patients, 151 were male (72.6%) and 57 were female (27.4%). The mean age of these patients was 44 years (range: 21-66). All patients in the study cohort had a history of viral hepatitis. There were 200 cases of hepatitis B virus (HBV)-related cirrhosis and eight cases of hepatitis C virus (HCV)-related cirrhosis. Twenty-three patients (11.1%) had a history of alcohol abuse, and 49 patients (23.6%) had a history of smoking. In terms of the underlying diseases, 33 patients (15.9%) had hypertension, and 15 patients (7.2%) suffered diabetes mellitus. On admission, 95 patients (45.7%) were found to have severe esophageal and gastric varices (>6 mm), and 13 patients (6.3%) had portal vein thrombosis. As for the liver function grade, Child-Pugh A was found in 58 patients (27.9%), Child-Pugh B in 134 patients (64.4%), and ChildPugh C in 15 patients (7.2%). In this study, 183 patients (88.0%) underwent open splenectomy, whereas 25 patients (12.0%) underwent laparoscopic splenectomy. The total estimated blood loss and transfusion during the surgery were 384 mL (range: 50-1500 mL) and 619 mL (range: 0-1400 mL), respectively. By combining preoperative imaging results with intraoperative assessment, the spleen volume and diameter were 1513 mm3 (range: 196-6800 mm3) and 160 mm (range: 12232 mm), respectively. As shown in Table 2, postoperative portal vein thrombosis (16.8%) and ascites (15.4%) were the most common complications after splenectomy. And surgical site infections happened in 10 patients (4.8%). Three patients (1.4%) were admitted to the intensive care unit due to severe postoperative complications or organ failure. One patient (0.48%) underwent reoperation due to intraabdominal bleeding and gastric leakage after splenectomy. The median length of
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du et al cci after splenectomy in cirrhotic patients
Table 1 e General clinical data of patients and laboratory information.
Table 2 e Intraoperative and postoperative characteristics of the cases.
Patients demographics and preoperative characteristics
Intraoperative and postoperative characteristics
Age (years)
Median(range)/n (percentage) 44 (21-66)
Gender (male:female)
151:57
HBV
200 (96.15%)
HCV
Intraoperative data Estimated blood loss (mL) Intraoperative transfusion (mL)
Coexisting conditions
8 (3.85%)
Spleen volume (mm3) Spleen size (mm)
23 (11.06%)
Smoking
49 (23.56%)
Laparoscopic surgery
Hypertension
33 (15.87%)
Laparotomy
Diabetes
15 (7.21%) 95 (53.37%)
Laboratory tests
384 (50-1500) 619 (0-1400) 1513 (196-6800) 160 (12-232)
Surgical methods
Drinking
Severe gastroesophageal varices (>6 mm)
Median(range)/n (percentage)
25 (12.02%) 183 (87.98%)
Postoperative complications ICU
3 (1.44%)
Reoperation
1 (0.48%) 2 (0.96%)
Leucocytes (109/L)
2.56 (0.68-13.62)
Hemorrhage
Platelet count (<50 109/L)
160 (76.92%)
Portal vein thrombosis
35 (16.82%)
ALT (>40U/L)
75 (36.06%)
Ascites
32 (15.38%)
AST (>40U/L)
98 (47.16%)
Surgical site infection
10 (4.81%)
Albumin (<35 g/L)
97 (46.63%)
Total bilirubin (>17 mmol/L) Creatinine (mmol/L)
155 (74.52%) 68 (15-188)
Laparoscopic surgery
3 (30.00%)
Laparotomy
7 (70.00%)
Pneumonia
1 (0.48%)
BUN (mmol/L)
4.86 (2.08-10.90)
SIRS
113 (54.33%)
INR
1.34 (0.95-4.51)
Comprehensive complication index (CCI)
25.6 (8.7-62.9)
APTT (>45s)
65 (31.25%)
Fibrinogen (mg/dL) AFP (mg/L)
1.88 (0.60-5.36) 10.41 (0.61-140.90)
4
HB/CV-D/RNA (10 IU/mL)
1460 (0.1-149100)
Child A
58 (27.88%)
Child B
134 (64.42%)
Child C
15 (7.21%)
Portal vein thrombosis before surgery
1 (0.48%) 13 (6.25%)
Albumin-bilirubin grade (ALBI) ALBI grade 1 (2.60) ALBI grade 2 (2.60 to 1.39) ALBI grade 3 (>1.39) MELD score (10)
35 (16.83%) 159 (76.44%) 14 (6.73%) 48 (23.08%)
ALT ¼ alanine aminotransferase; AST ¼ aspartate transaminase; BUN ¼ blood urea nitrogen; INR ¼ international normalized ratio; APTT ¼ activated partial thromboplastin time; AFP ¼ alpha fetoprotein; ALBI ¼ albumin-bilirubin grade.
27 (11-125)
Laparoscopic surgery
25 (14-45)
Laparotomy
27 (11-125)
In-hospital death
Child-Pugh score
Unavailable
Length of hospital stay
0 (0%)
ICU ¼ intensive care unit; SIRS ¼ systemic inflammatory response syndrome.
than 30. A CCI score >30 corresponds to one or more ClavienDindo classification grade III (requiring surgical, endoscopic or radiological intervention) complications. Thus, in this study, we used 30 as the cutoff value to define a high CCI score. Accordingly, patients were divided into two groups based on their CCI scores: low CCI (30) group and high CCI (>30) group. To investigate the risk factors associated with a high CCI score after splenectomy, univariable and multivariable analyses of various factors were performed. The risk factors that were significant or close to be significant (P < 0.10) in the univariable analysis were further evaluated using the multivariable analysis. As shown in Table 3, the risk factors independently associated with a high CCI score were a history of hypertension and a MELD score 10 prior to splenectomy.
hospital stay was 27 days (range: 11-125 days). No in-hospital death was observed in this cohort.
Discussion Risk factors associated with a high CCI score after splenectomy The median CCI score for the 208 cirrhotic patients who underwent splenectomy for hypersplenism was 25.6 (range: 8.7-62.9). As shown in Figure, 33 patients (15.9%) had a CCI score lower than 20, 109 patients (52.4%) had a CCI score between 20 and 30, and 66 patients (31.7%) had a CCI score higher
Postoperative outcomes were usually evaluated based on the single most severe complication as it requires the most invasive intervention. However, patients can develop various complications during the postoperative course. It is possible that several moderate complications offer more discomfort for the patient than a single severe complication. Since the CCI is a grading system that assesses the summative severity of all
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Figure e Distribution of CCI after splenectomy in cirrhotic patients.
postoperative complications, it enables a comprehensive evaluation of the patient’s postoperative well-being. Patients with liver cirrhosis exhibit high postoperative morbidity and mortality rates after surgery.14,15 The present study is the first one to report postoperative complications in cirrhotic patients undergoing splenectomy for hypersplenism using the CCI score. The CCI score ranges from 0 (no complications) to 100 (death).12 Patients with a CCI score higher than 30 are considered to have a severe postoperative condition. Here, we found that over 30% of cirrhotic patients had a postoperative CCI score >30, indicating that severe postoperative conditions are common in cirrhotic patients undergoing splenectomy for hypersplenism. The systemic inflammatory response syndrome experienced in 54% and the portal vein thrombosis experienced in 17% of the patients. Despite these severe postoperative conditions, there was no in-hospital mortality in our current study and the overall 3-year survival rate was over 90% (data not shown). Thus, good recovery is possible for cirrhotic patients who develop severe postoperative complications after splenectomy. Identification of preoperative factors associated with severe postoperative conditions is critical for developing prognostic tools to accurately pinpoint patients at risk.16-18 In the present study, we found that a history of hypertension was associated with a high CCI score after splenectomy. This is not surprising since hypertension is a well-known risk factor for postoperative complications.19-21 Patients with preexisting hypertension are more likely to experience intraoperative blood pressure lability that potentially increases the risk of surgery.22,23 Thus, postponement of elective splenectomy should be recommended if the high blood pressure is not adequately controlled.24 Cirrhotic patients with hypertension should maintain compliance to their antihypertensive treatment regimen prior to surgery, including the morning of surgery, as it may reduce intraoperative blood pressure fluctuations.25 In the current cohort, none of the other preoperative characteristics was associated with a high CCI score. There were 15 Child-Pugh C cirrhotic patients in this study. Ten of them had a postoperative CCI score less than 30, suggesting they could well tolerate an operation like
splenectomy. However, it is hard to draw any conclusive insight from 15 cases. Moreover, the preoperative Child-Pugh grade was not associated with the postoperative CCI. As to the risk assessment tools for patients with advanced liver disease, we found that patients with a MELD score higher than 10 were more likely to experience a high CCI score after splenectomy. The MELD score was developed to predict outcomes of cirrhotic patients after transjugular intrahepatic portosystemic shunt (TIPS).26 Although the MELD grading system has been strongly associated with adverse outcomes among patients with chronic liver disease,27,28 the present study is the first one to show its association with a high CCI score after splenectomy in cirrhotic patients. And cirrhotic patients with an elevated MELD score should consider other treatment options for hypersplenism. The MELD score may be a better indicator of postoperative complications than the Child-Pugh grade for cirrhotic patients undergoing splenectomy. Open splenectomy has been performed as a treatment for secondary hypersplenism since 1950.29 However, open splenectomy is excessively invasive and associated with high morbidity and mortality.30 Laparoscopic splenectomy was first reported by Delaitre and Maignien in 1991.31 Compared with open splenectomy, the laparoscopic approach reduces complications and shortens recovery.32 Therefore, laparoscopic splenectomy has gradually become the standard approach to remove normal to moderately enlarged spleens.32,33 Due to the increased risk of intraoperative hemorrhage, however, portal hypertension from liver cirrhosis remains to be considered as a contraindication to laparoscopic splenectomy in some institutions.34 In the current cohort of 208 cirrhotic patients with hypersplenism and portal hypertension, 25 patients’ spleens were removed laparoscopically. We found that laparoscopic splenectomy did not increase the risk of having a high CCI score in patients with liver cirrhosis. And there were not any converted cases in this study. However our sample size in laparoscopic splenectomy is modest. Thus, these results should be interpreted with caution. Further studies are warranted to determine whether it is feasible to laparoscopically perform splenectomy with good outcomes and minimal morbidity in cirrhotic patients with hypersplenism and portal hypertension. Several limitations of this study should be considered when interpreting the results. First, our study was conducted at a single hospital. It is possible that information on readmissions to other institutions was missing. Second, as the follow-up time in the present study was only 90 days, we were unable to comment on the longer term outcomes of patients with a high CCI score. Third, a relatively small proportion of the patients (12%) underwent laparoscopic splenectomy in this study, which might have limited the robustness of the analysis. Finally, as a retrospective study, the results are subject to a selection bias and residual confounding due to some unknown covariates. In summary, a high CCI score (i.e., >30) is common in cirrhotic patients undergoing splenectomy for hypersplenism. Patients with preexisting hypertension, a MELD score 10 was associated with a high risk of developing a high CCI score after splenectomy. Thus, preoperative assessment of liver function using the MELD score is recommended for cirrhotic patients before splenectomy. Those with an elevated MELD score should be referred for other treatment options. In addition,
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du et al cci after splenectomy in cirrhotic patients
Table 3 e Univariate and multivariate analyses of risk factors for a high CCI Score. Variables
Univariate analysis Low CCI (30)
n
142
High CCI (>30)
99 (69.72%)
52 (78.79%)
Age
43 (21-66)
45 (23-63)
Underlying liver diseases
Hypertension Diabetes
Multivariate analysis OR (95% CI)
P value
2.523 (1.141-5.583)
0.022
1.193 (0.994-3.751)
0.052
0.490 (0.231-1.040)
0.063
0.367 (0.185-0.727)
0.004
66
Gender (male)
HBV
P value
0.172 0.130 0.440
135 (95.07%)
65 (98.48%)
18 (12.68%)
15 (22.73%)
0.065
9 (6.34%)
6 (9.09%)
0.475
Coexisting conditions Drinking
15 (10.56%)
8 (12.12%)
0.739
Smoking
30 (21.12%)
19 (28.79%)
0.226
123 (86.62%)
55 (88.33%)
0.530
Severe gastroesophageal varices (>6 mm)
61 (49.59%)
34 (61.82%)
0.131
Portal vein thrombosis during perioperative period
29 (20.42%)
15 (22.73%)
0.705
2.56 (0.81-8.80)
0.973
Gastroesophageal varices
Leucocytes (109/L)
2.56 (0.68-13.62)
Platelet count at admission (<50 109/L)
112 (78.87%)
48 (72.73%)
0.327
57 (40.14%)
18 (27.27%)
0.072
ALT (>40U/L) AST (>40U/L)
70 (49.30%)
28 (42.42%)
0.355
Albumin (<35 g/L)
68 (47.89%)
29 (43.94%)
0.595
100 (70.42%)
55 (83.33%)
0.047
43 (30.28%)
22 (33.33%)
0.659
Total bilirubin (>17mmol/L) APTT (>45s) HB/CV-D/RNA (104 IU/mL)
2053 (0.1-149100)
338 (0.1-5350)
Child-Pugh score Child A
42 (29.58%)
16 (24.24%)
Child B
89 (62.68%)
45 (68.18%)
Child C
10 (7.04%)
5 (7.58%)
Unavailable
1 (0.70%)
0 (0%)
Albumin-bilirubin grade (ALBI) ALBI grade 1 (-2.60) ALBI grade 2 (-2.60 to -1.39) ALBI grade 3 (>-1.39) MELD score (10) Estimated blood loss (mL) Intraoperative transfusion (mL) Spleen volume (mm3) Spleen size (mm)
0.236 28 (19.72%)
7 (10.61%)
104 (73.24%)
55 (83.33%)
10 (7.04%)
4 (6.06%)
25 (17.61%)
23 (34.85%)
0.006
325 (50-1000)
575 (200-1500)
0.176
510 (0-1000)
675 (0-1400)
0.158
1413 (196-6800)
1428 (270-3300)
0.914
156 (12-232)
166 (14-230)
Surgical methods Laparoscopic surgery Laparotomy
0.473 0.764
0.190 0.179
20 (14.08%)
5 (7.58%)
122 (85.92%)
61 (92.42%)
The statistical difference between 2 groups was compared by the Student t-test or Wilcoxon test for continuous data and the chi-squared test or Fisher’s exact test for categorical variables. For the statistical analysis between 3 or more groups, analysis of variance (ANOVA) was used. Factors showing significant difference (P < 0.10) in the univariate analysis were further analyzed in the final multivariate analysis. Values with significant factors in univariate and multivariable analysis shows bold.
patients undergoing laparoscopic splenectomy appeared to have similar CCI scores as those undergoing open splenectomy. The CCI provides a more comprehensive evaluation of patient’s overall postoperative conditions than the conventional approach and is a useful grading system to assess postoperative morbidity in cirrhotic patients undergoing splenectomy for hypersplenism.
Acknowledgment Authors’ contributions: Z.D. participated in the data collection, statistical analysis, and paper writing; J.D., J.Z., and J.B. participated in the data collection. Z.W. and Y.L. assisted with the design of the study and interpretation of data. X.Z.
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participated in the research design and supervised the study. R.W. designed the study and revised the manuscript. All authors approved the final version of the manuscript to be published. This work was supported by a research fund for Young Talent Recruiting Plans of Xi’an Jiaotong University (R.W.).
Disclosure The authors reported no proprietary or commercial interest in any product mentioned or concept discussed in this article.
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ScienceDirect journal homepage: www.JournalofSurgicalResearch.com
Incidence and risk factors associated with a high comprehensive complication index score after splenectomy in cirrhotic patients with hypersplenism Zhaoqing Du, PhD,a,b,c Jian Dong, PhD,a,b,c Jia Zhang, PhD,a,b,c Jianbin Bi, PhD,a,b,c Zheng Wu, PhD, MD,c Yi Lv, PhD, MD,a,b,c Xufeng Zhang, PhD, MD,a,b,c,* and Rongqian Wu, PhD, MDa,b,* a
Shaanxi Provincial Center for Regenerative Medicine and Surgical Engineering, Xi’an, Shaanxi Province, China Institute of Advanced Surgical Technology and Engineering, Xi’an, Shaanxi Province, China c Department of Hepatobiliary Surgery, First Affiliated Hospital of Xi’an Jiaotong University, Xi’an, Shaanxi Province, China b
article info
abstract
Article history:
Background: Postoperative complications after splenectomy are not rare and can be serious
Received 24 June 2017
in cirrhotic patients. The purpose of this study was to assess postoperative complications
Received in revised form
using the comprehensive complication index (CCI) after splenectomy in cirrhotic patients
10 August 2017
and identify risk factors for those who developed a high postoperative CCI score.
Accepted 29 September 2017
Materials and methods: This retrospective study included 208 adult patients with viral
Available online xxx
hepatitis-related cirrhosis, who underwent elective splenectomy at our hospital from January 2002 to June 2012. The primary outcome was the CCI score. A CCI score >30 was
Keywords:
considered to be a high CCI score.
Comprehensive complication index
Results: The median CCI score in this cohort was 25.6 (range: 8.7-62.9), and 66 patients
(CCI)
(31.7%) had a CCI score >30. Univariable and multivariable analyses showed that the risk
Splenectomy
factors independently associated with a high CCI score were a history of hypertension and
Cirrhosis
a model for end-stage liver disease (MELD) score 10 prior to splenectomy.
Hypersplenism
Conclusions: A high CCI score is common in cirrhotic patients undergoing splenectomy. The
Portal hypertension
CCI is a useful grading system to assess postoperative morbidity in cirrhotic patients un-
Risk factors
dergoing splenectomy. Preoperative blood pressure control is recommended and cirrhotic patients with an elevated MELD score should consider other treatment options for hypersplenism. ª 2017 Elsevier Inc. All rights reserved.
Introduction Hypersplenism is common in patients with liver cirrhosis. The presence of hypersplenism indicates more advanced liver
disease and is associated with anemia, leukopenia, thrombocytopenia, bleeding tendency, and portal hypertension. Splenectomy corrects cytopenia, improves liver function, and expands treatment choices for the underlying liver disease.1-4
* Corresponding author. Shaanxi Provincial Center for Regenerative Medicine and Surgical Engineering, First Affiliated Hospital of Xi’an Jiaotong University, 76 West Yanta Road, P.O. Box 124, Xi’an, Shaanxi Province 710061, China. Tel.: þ86 29 82657541; fax: þ86 29 85252580. E-mail addresses: [email protected] (X. Zhang), [email protected] (R. Wu). 0022-4804/$ e see front matter ª 2017 Elsevier Inc. All rights reserved. https://doi.org/10.1016/j.jss.2017.09.045
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Therefore, it remains a therapeutic option for patients with hypersplenism due to liver cirrhosis.5-8 However, the indications for splenectomy in cirrhotic patients are somewhat controversial.9 One of the major reasons for this controversy is that postoperative complications after splenectomy are not rare and can be serious in cirrhotic patients.10 However, few studies have comprehensively evaluated postoperative complications in patients with liver cirrhosis undergoing splenectomy for hypersplenism. The comprehensive complication index (CCI) was recently developed to document postoperative complications.11 It measures surgical morbidity by adding up all complications attributable to a surgical procedure and weighting them according to their severity.12 Thus, the CCI reflects the summative severity of all major and minor postoperative complications in a single patient. By avoiding underreporting minor complications, the CCI is a robust system to evaluate postoperative morbidity. Due to its consistency and completeness, the CCI has become one of the standard ways to report postoperative complications in clinical trials. To the best of our knowledge, however, there have been no reports on the incidence of a high CCI score in cirrhotic patients undergoing splenectomy for hypersplenism. The purpose of this retrospective study was to assess postoperative complications using the CCI in a large cohort of patients with viral hepatitis-related cirrhosis who received splenectomy for hypersplenism and identify risk factors for those who developed a high postoperative CCI score.
Methods Study population From January 2002 to June 2012, 1229 cirrhotic patients were hospitalized for the treatment of hypersplenism at the First Affiliated Hospital of Xi’an Jiaotong University. Of these, 241 patients (19.6%) who underwent elective splenectomy were enrolled in this study. The primary diagnosis of all cases was liver cirrhosis with hypersplenism and portal hypertension. Contraindications were uncorrectable coagulopathy and severe cardiovascular disease that prohibit the administration of general anesthesia. All clinical data of these patients, including demographics features, perioperative laboratory values, and postoperative complications were gathered from the digital medical records. Thirty-three patients had incomplete clinical data and were excluded from further analysis. The remaining 208 patients composed our study population. This retrospective, observational study was approved by the Ethics Committee of the First Affiliated Hospital of Xi’an Jiaotong University and the approval number was 2016-046. This work has been conducted in accordance with the Declaration of Helsinki of the World Medical Association. The patient’s informed written consent was waived due to the retrospective nature of this study. All data were used only for statistical analysis in this study.
Evaluation of outcomes The primary outcome was the comprehensive complication index (CCI) score.12 The CCI was calculated as the sum of all
postoperative complications that are weighted by their severity (available at www.assessurgery.com). Postoperative complications were defined as the occurrence of medical or surgical complications within 90 days of surgery. The severity of complications was evaluated using the Clavien-Dindo classification scale.13
Statistical analysis For the continuous variables, we used mean standard deviation (SD) or median (range: mindmax) to describe. And categorical variables were presented as frequency and percentage. The statistical difference between two groups was compared by the Student’s t-test or Wilcoxon test for continuous data and the chi-squared test or Fisher’s exact test for categorical variables. For the statistical analysis between three or more groups, analysis of variance was used. Factors showing significant difference in the univariate analysis were further analyzed in the final multivariate log-regression model. All statistical analyses were done using the IBM SPSS software (version 22.0). P < 0.05 was considered statistically significant.
Results Patient demographics and characteristics The demographics and baseline characteristics of the 208 cirrhotic patients who underwent splenectomy for hypersplenism were shown in Table 1. Of these patients, 151 were male (72.6%) and 57 were female (27.4%). The mean age of these patients was 44 years (range: 21-66). All patients in the study cohort had a history of viral hepatitis. There were 200 cases of hepatitis B virus (HBV)-related cirrhosis and eight cases of hepatitis C virus (HCV)-related cirrhosis. Twenty-three patients (11.1%) had a history of alcohol abuse, and 49 patients (23.6%) had a history of smoking. In terms of the underlying diseases, 33 patients (15.9%) had hypertension, and 15 patients (7.2%) suffered diabetes mellitus. On admission, 95 patients (45.7%) were found to have severe esophageal and gastric varices (>6 mm), and 13 patients (6.3%) had portal vein thrombosis. As for the liver function grade, Child-Pugh A was found in 58 patients (27.9%), Child-Pugh B in 134 patients (64.4%), and ChildPugh C in 15 patients (7.2%). In this study, 183 patients (88.0%) underwent open splenectomy, whereas 25 patients (12.0%) underwent laparoscopic splenectomy. The total estimated blood loss and transfusion during the surgery were 384 mL (range: 50-1500 mL) and 619 mL (range: 0-1400 mL), respectively. By combining preoperative imaging results with intraoperative assessment, the spleen volume and diameter were 1513 mm3 (range: 196-6800 mm3) and 160 mm (range: 12232 mm), respectively. As shown in Table 2, postoperative portal vein thrombosis (16.8%) and ascites (15.4%) were the most common complications after splenectomy. And surgical site infections happened in 10 patients (4.8%). Three patients (1.4%) were admitted to the intensive care unit due to severe postoperative complications or organ failure. One patient (0.48%) underwent reoperation due to intraabdominal bleeding and gastric leakage after splenectomy. The median length of
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Table 1 e General clinical data of patients and laboratory information.
Table 2 e Intraoperative and postoperative characteristics of the cases.
Patients demographics and preoperative characteristics
Intraoperative and postoperative characteristics
Age (years)
Median(range)/n (percentage) 44 (21-66)
Gender (male:female)
151:57
HBV
200 (96.15%)
HCV
Intraoperative data Estimated blood loss (mL) Intraoperative transfusion (mL)
Coexisting conditions
8 (3.85%)
Spleen volume (mm3) Spleen size (mm)
23 (11.06%)
Smoking
49 (23.56%)
Laparoscopic surgery
Hypertension
33 (15.87%)
Laparotomy
Diabetes
15 (7.21%) 95 (53.37%)
Laboratory tests
384 (50-1500) 619 (0-1400) 1513 (196-6800) 160 (12-232)
Surgical methods
Drinking
Severe gastroesophageal varices (>6 mm)
Median(range)/n (percentage)
25 (12.02%) 183 (87.98%)
Postoperative complications ICU
3 (1.44%)
Reoperation
1 (0.48%) 2 (0.96%)
Leucocytes (109/L)
2.56 (0.68-13.62)
Hemorrhage
Platelet count (<50 109/L)
160 (76.92%)
Portal vein thrombosis
35 (16.82%)
ALT (>40U/L)
75 (36.06%)
Ascites
32 (15.38%)
AST (>40U/L)
98 (47.16%)
Surgical site infection
10 (4.81%)
Albumin (<35 g/L)
97 (46.63%)
Total bilirubin (>17 mmol/L) Creatinine (mmol/L)
155 (74.52%) 68 (15-188)
Laparoscopic surgery
3 (30.00%)
Laparotomy
7 (70.00%)
Pneumonia
1 (0.48%)
BUN (mmol/L)
4.86 (2.08-10.90)
SIRS
113 (54.33%)
INR
1.34 (0.95-4.51)
Comprehensive complication index (CCI)
25.6 (8.7-62.9)
APTT (>45s)
65 (31.25%)
Fibrinogen (mg/dL) AFP (mg/L)
1.88 (0.60-5.36) 10.41 (0.61-140.90)
4
HB/CV-D/RNA (10 IU/mL)
1460 (0.1-149100)
Child A
58 (27.88%)
Child B
134 (64.42%)
Child C
15 (7.21%)
Portal vein thrombosis before surgery
1 (0.48%) 13 (6.25%)
Albumin-bilirubin grade (ALBI) ALBI grade 1 (2.60) ALBI grade 2 (2.60 to 1.39) ALBI grade 3 (>1.39) MELD score (10)
35 (16.83%) 159 (76.44%) 14 (6.73%) 48 (23.08%)
ALT ¼ alanine aminotransferase; AST ¼ aspartate transaminase; BUN ¼ blood urea nitrogen; INR ¼ international normalized ratio; APTT ¼ activated partial thromboplastin time; AFP ¼ alpha fetoprotein; ALBI ¼ albumin-bilirubin grade.
27 (11-125)
Laparoscopic surgery
25 (14-45)
Laparotomy
27 (11-125)
In-hospital death
Child-Pugh score
Unavailable
Length of hospital stay
0 (0%)
ICU ¼ intensive care unit; SIRS ¼ systemic inflammatory response syndrome.
than 30. A CCI score >30 corresponds to one or more ClavienDindo classification grade III (requiring surgical, endoscopic or radiological intervention) complications. Thus, in this study, we used 30 as the cutoff value to define a high CCI score. Accordingly, patients were divided into two groups based on their CCI scores: low CCI (30) group and high CCI (>30) group. To investigate the risk factors associated with a high CCI score after splenectomy, univariable and multivariable analyses of various factors were performed. The risk factors that were significant or close to be significant (P < 0.10) in the univariable analysis were further evaluated using the multivariable analysis. As shown in Table 3, the risk factors independently associated with a high CCI score were a history of hypertension and a MELD score 10 prior to splenectomy.
hospital stay was 27 days (range: 11-125 days). No in-hospital death was observed in this cohort.
Discussion Risk factors associated with a high CCI score after splenectomy The median CCI score for the 208 cirrhotic patients who underwent splenectomy for hypersplenism was 25.6 (range: 8.7-62.9). As shown in Figure, 33 patients (15.9%) had a CCI score lower than 20, 109 patients (52.4%) had a CCI score between 20 and 30, and 66 patients (31.7%) had a CCI score higher
Postoperative outcomes were usually evaluated based on the single most severe complication as it requires the most invasive intervention. However, patients can develop various complications during the postoperative course. It is possible that several moderate complications offer more discomfort for the patient than a single severe complication. Since the CCI is a grading system that assesses the summative severity of all
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Figure e Distribution of CCI after splenectomy in cirrhotic patients.
postoperative complications, it enables a comprehensive evaluation of the patient’s postoperative well-being. Patients with liver cirrhosis exhibit high postoperative morbidity and mortality rates after surgery.14,15 The present study is the first one to report postoperative complications in cirrhotic patients undergoing splenectomy for hypersplenism using the CCI score. The CCI score ranges from 0 (no complications) to 100 (death).12 Patients with a CCI score higher than 30 are considered to have a severe postoperative condition. Here, we found that over 30% of cirrhotic patients had a postoperative CCI score >30, indicating that severe postoperative conditions are common in cirrhotic patients undergoing splenectomy for hypersplenism. The systemic inflammatory response syndrome experienced in 54% and the portal vein thrombosis experienced in 17% of the patients. Despite these severe postoperative conditions, there was no in-hospital mortality in our current study and the overall 3-year survival rate was over 90% (data not shown). Thus, good recovery is possible for cirrhotic patients who develop severe postoperative complications after splenectomy. Identification of preoperative factors associated with severe postoperative conditions is critical for developing prognostic tools to accurately pinpoint patients at risk.16-18 In the present study, we found that a history of hypertension was associated with a high CCI score after splenectomy. This is not surprising since hypertension is a well-known risk factor for postoperative complications.19-21 Patients with preexisting hypertension are more likely to experience intraoperative blood pressure lability that potentially increases the risk of surgery.22,23 Thus, postponement of elective splenectomy should be recommended if the high blood pressure is not adequately controlled.24 Cirrhotic patients with hypertension should maintain compliance to their antihypertensive treatment regimen prior to surgery, including the morning of surgery, as it may reduce intraoperative blood pressure fluctuations.25 In the current cohort, none of the other preoperative characteristics was associated with a high CCI score. There were 15 Child-Pugh C cirrhotic patients in this study. Ten of them had a postoperative CCI score less than 30, suggesting they could well tolerate an operation like
splenectomy. However, it is hard to draw any conclusive insight from 15 cases. Moreover, the preoperative Child-Pugh grade was not associated with the postoperative CCI. As to the risk assessment tools for patients with advanced liver disease, we found that patients with a MELD score higher than 10 were more likely to experience a high CCI score after splenectomy. The MELD score was developed to predict outcomes of cirrhotic patients after transjugular intrahepatic portosystemic shunt (TIPS).26 Although the MELD grading system has been strongly associated with adverse outcomes among patients with chronic liver disease,27,28 the present study is the first one to show its association with a high CCI score after splenectomy in cirrhotic patients. And cirrhotic patients with an elevated MELD score should consider other treatment options for hypersplenism. The MELD score may be a better indicator of postoperative complications than the Child-Pugh grade for cirrhotic patients undergoing splenectomy. Open splenectomy has been performed as a treatment for secondary hypersplenism since 1950.29 However, open splenectomy is excessively invasive and associated with high morbidity and mortality.30 Laparoscopic splenectomy was first reported by Delaitre and Maignien in 1991.31 Compared with open splenectomy, the laparoscopic approach reduces complications and shortens recovery.32 Therefore, laparoscopic splenectomy has gradually become the standard approach to remove normal to moderately enlarged spleens.32,33 Due to the increased risk of intraoperative hemorrhage, however, portal hypertension from liver cirrhosis remains to be considered as a contraindication to laparoscopic splenectomy in some institutions.34 In the current cohort of 208 cirrhotic patients with hypersplenism and portal hypertension, 25 patients’ spleens were removed laparoscopically. We found that laparoscopic splenectomy did not increase the risk of having a high CCI score in patients with liver cirrhosis. And there were not any converted cases in this study. However our sample size in laparoscopic splenectomy is modest. Thus, these results should be interpreted with caution. Further studies are warranted to determine whether it is feasible to laparoscopically perform splenectomy with good outcomes and minimal morbidity in cirrhotic patients with hypersplenism and portal hypertension. Several limitations of this study should be considered when interpreting the results. First, our study was conducted at a single hospital. It is possible that information on readmissions to other institutions was missing. Second, as the follow-up time in the present study was only 90 days, we were unable to comment on the longer term outcomes of patients with a high CCI score. Third, a relatively small proportion of the patients (12%) underwent laparoscopic splenectomy in this study, which might have limited the robustness of the analysis. Finally, as a retrospective study, the results are subject to a selection bias and residual confounding due to some unknown covariates. In summary, a high CCI score (i.e., >30) is common in cirrhotic patients undergoing splenectomy for hypersplenism. Patients with preexisting hypertension, a MELD score 10 was associated with a high risk of developing a high CCI score after splenectomy. Thus, preoperative assessment of liver function using the MELD score is recommended for cirrhotic patients before splenectomy. Those with an elevated MELD score should be referred for other treatment options. In addition,
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du et al cci after splenectomy in cirrhotic patients
Table 3 e Univariate and multivariate analyses of risk factors for a high CCI Score. Variables
Univariate analysis Low CCI (30)
n
142
High CCI (>30)
99 (69.72%)
52 (78.79%)
Age
43 (21-66)
45 (23-63)
Underlying liver diseases
Hypertension Diabetes
Multivariate analysis OR (95% CI)
P value
2.523 (1.141-5.583)
0.022
1.193 (0.994-3.751)
0.052
0.490 (0.231-1.040)
0.063
0.367 (0.185-0.727)
0.004
66
Gender (male)
HBV
P value
0.172 0.130 0.440
135 (95.07%)
65 (98.48%)
18 (12.68%)
15 (22.73%)
0.065
9 (6.34%)
6 (9.09%)
0.475
Coexisting conditions Drinking
15 (10.56%)
8 (12.12%)
0.739
Smoking
30 (21.12%)
19 (28.79%)
0.226
123 (86.62%)
55 (88.33%)
0.530
Severe gastroesophageal varices (>6 mm)
61 (49.59%)
34 (61.82%)
0.131
Portal vein thrombosis during perioperative period
29 (20.42%)
15 (22.73%)
0.705
2.56 (0.81-8.80)
0.973
Gastroesophageal varices
Leucocytes (109/L)
2.56 (0.68-13.62)
Platelet count at admission (<50 109/L)
112 (78.87%)
48 (72.73%)
0.327
57 (40.14%)
18 (27.27%)
0.072
ALT (>40U/L) AST (>40U/L)
70 (49.30%)
28 (42.42%)
0.355
Albumin (<35 g/L)
68 (47.89%)
29 (43.94%)
0.595
100 (70.42%)
55 (83.33%)
0.047
43 (30.28%)
22 (33.33%)
0.659
Total bilirubin (>17mmol/L) APTT (>45s) HB/CV-D/RNA (104 IU/mL)
2053 (0.1-149100)
338 (0.1-5350)
Child-Pugh score Child A
42 (29.58%)
16 (24.24%)
Child B
89 (62.68%)
45 (68.18%)
Child C
10 (7.04%)
5 (7.58%)
Unavailable
1 (0.70%)
0 (0%)
Albumin-bilirubin grade (ALBI) ALBI grade 1 (-2.60) ALBI grade 2 (-2.60 to -1.39) ALBI grade 3 (>-1.39) MELD score (10) Estimated blood loss (mL) Intraoperative transfusion (mL) Spleen volume (mm3) Spleen size (mm)
0.236 28 (19.72%)
7 (10.61%)
104 (73.24%)
55 (83.33%)
10 (7.04%)
4 (6.06%)
25 (17.61%)
23 (34.85%)
0.006
325 (50-1000)
575 (200-1500)
0.176
510 (0-1000)
675 (0-1400)
0.158
1413 (196-6800)
1428 (270-3300)
0.914
156 (12-232)
166 (14-230)
Surgical methods Laparoscopic surgery Laparotomy
0.473 0.764
0.190 0.179
20 (14.08%)
5 (7.58%)
122 (85.92%)
61 (92.42%)
The statistical difference between 2 groups was compared by the Student t-test or Wilcoxon test for continuous data and the chi-squared test or Fisher’s exact test for categorical variables. For the statistical analysis between 3 or more groups, analysis of variance (ANOVA) was used. Factors showing significant difference (P < 0.10) in the univariate analysis were further analyzed in the final multivariate analysis. Values with significant factors in univariate and multivariable analysis shows bold.
patients undergoing laparoscopic splenectomy appeared to have similar CCI scores as those undergoing open splenectomy. The CCI provides a more comprehensive evaluation of patient’s overall postoperative conditions than the conventional approach and is a useful grading system to assess postoperative morbidity in cirrhotic patients undergoing splenectomy for hypersplenism.
Acknowledgment Authors’ contributions: Z.D. participated in the data collection, statistical analysis, and paper writing; J.D., J.Z., and J.B. participated in the data collection. Z.W. and Y.L. assisted with the design of the study and interpretation of data. X.Z.
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participated in the research design and supervised the study. R.W. designed the study and revised the manuscript. All authors approved the final version of the manuscript to be published. This work was supported by a research fund for Young Talent Recruiting Plans of Xi’an Jiaotong University (R.W.).
Disclosure The authors reported no proprietary or commercial interest in any product mentioned or concept discussed in this article.
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