Radical versus conservative surgical treatment of liver hydatid cysts: a meta-analysis

Abstract

To date, the efficacy of radical surgery (RS) versus conservative surgery (CS) for liver hydatid cysts (LHC) remains controversial. This meta-analysis was conducted to compare the two interventions. PubMed, Embase, and Web of Science were searched from their inceptions until June 2016. Meta-analysis was performed using STATA 12.0 software. We identified 19 eligible studies from 10 countries by retrieval. In total, 1853 LHC patients who received RS were compared with 2274 patients treated by CS. The risk of postoperative overall complication, biliary fistula, and recurrence was significantly lower, and operation time was significantly longer in the RS group. However, no statistically significant differences were found in terms of mortality risk and the duration of hospital stay between RS and CS. No significant publication biases were observed in all the above analyses. In conclusion, RS reduces the rates of postoperative complications and recurrence, whereas no trend toward such a reduction in mortality was observed in LHC patients.

Keywords

liver hydatid cysts / radical surgery / conservative surgery / meta-analysis / complications

Introduction

Hydatid cyst (HC) is a rare but life-threatening parasitic disease caused by the larval form of Echinococcus granulosus. HC has been regarded as a public health threat and an economic burden in sheep-raising regions, such as South America, Australia, North Africa, Turkey, China, and the Mediterranean countries [¹,²]. Clinical features of human HC may vary from an asymptomatic condition to severe morbidities or even mortality.

The cysts of hydatid grow slowly, and approximately 50% to 77% of which will infiltrate the liver [³,⁴]. The management of liver hydatid cysts (LHC) mainly depends on patients’ general condition, size and localization of cysts, pathological involvement, available expertise, and equipment [⁵–⁷]. Chemotherapy, such as benzimidazole, could not eliminate cysts entirely and is not an ideal treatment for LHC when used alone [¹,⁸]. By contrast, surgical procedures, including radical (pericystectomy and hepatic resection) and conservative (unroofing, drainage, marsupialization, and omentoplasty) approaches, are widely practiced and were considered to be the first choice for LHC [⁴,⁹]. However, regardless of what kind of surgery, the high probability of postoperative complications and recurrence remains a major obstacle affecting the quality of patients’ life. The incidence of postoperative complications is over 60% [¹⁰], recurrence rate is around 10% [¹¹,¹²], and mortality rate ranges from 0% to 7.5% after operation [¹⁰].

However, the efficacy of radical surgery (RS) versus conservative surgery (CS) approaches remains controversial to date. Several studies showed a significant improvement in the RS of LHC in view of a substantial decrease in the rates of morbidity, reoperation, recurrence, and mortality compared with CS [²,¹³]. Meanwhile, a recent propensity score matching study highlighted that no statistically significant differences were observed between RS and CS in terms of these outcomes [¹⁴]. To clarify this controversy, we reviewed all the relevant studies to further compare the efficacy of RS with CS.

Search strategy and selection criteria

Two investigators (PQ and ZL) independently searched the databases of PubMed, Embase, and ISI Web of Science from their inceptions until June 2016. Our core search consisted of terms (echinococcos* or hydatid*) and (liver or hepatic) and (radical or resection or hepatectomy or pericystectomy or segmentectomy or “subadventitial cystectomy” or “subadventitial total exocystectomy”) and (conservative or endocystectomy or drainage or unroofing or omentoplasty or capitonnage or “partial pericystectomy” or marsupialization). We also manually retrieved the references of relevant studies and reviews.

Studies were eligible provided they met the following inclusion criteria: (1) subjects were liver hydatid cysts; (2) published as an original article in English; (3) randomized clinical study or cohort study (either prospective or retrospective) that compared RS with CS in patients with LHC; (4) primary outcomes were complications (morbidity), recurrence, reinterventions, mortality, hospital stay, or operative time; (5) reported the value of odds ratio (OR) or standardized mean difference (SMD) with 95% confidence intervals (CI) or provided sufficient data to deduce it. We excluded the following studies: (1) hepatic alveolar echinococcosis patients or only children as subjects; (2) only provided P value or other conditions that effect size could not be calculated; (3) review, conference abstract, and letter to the editor. If two or more publications recruited duplicated population, we included the one with the largest number of patients.

Data abstraction of the included studies

Two researchers (PQ and ZL) independently explored the eligible articles, and Kappa statistic was used to assess the variability between them. Discrepancy was solved by another author (JH). For each eligible study, we extracted the following information: first author, publication year, country where patients were hospitalized, study period, duration of follow-up, number and characteristics of patients, characteristics of cysts, OR or SMD value with 95% CI, and outcomes measured. The study quality was assessed by using Newcastle–Ottawa Scale (NOS) score [¹⁵]. We referred the Meta-analysis of Observational Studies in Epidemiology guidelines for reporting this meta-analysis [¹⁶].

Statistical methods of meta-analysis

STATA 12.0 statistical software was used to analyze data. The primary outcome that we analyzed and compared was postoperative overall complication, and the secondary outcomes included several common complications, recurrence, mortality, duration of hospital stay, and operative time. Random-effects model was applied to pool estimated effect sizes.

We assessed heterogeneity between studies using P value of Cochran’s Q test, and it was considered to be significant provided P<0.10. The I² metric was used to quantify the proportion of the total variation, and 25%, 50%, and 75% of I² statistic corresponded to cut-off points for low, moderate, and substantial heterogeneity, respectively. Subgrouped analyses and meta-regression were conducted to determine the potential factors that might bring in heterogeneity.

We subsequently performed influence analyses to evaluate whether the results could be markedly affected by any single study. We also compared the summary effect sizes between using fixed- and random-effects models. Publication bias was determined by Begg’s funnel plot and Egger’s test. Eventually, the Galbraith plot was performed to detect outliers, which might bias the results.

Characteristics of the included studies

The database searches returned 537 unique citations after removing duplications. Of these citations, 70 full text articles were further assessed and 51 were excluded according to the selection criteria. Thus, a total of 19 articles were included in this meta-analysis. The flow chart of our literature search and selection is shown in Fig. 1. Agreement between the two observers on which studies must be included was nearly perfect (κ: 0.891).

The baseline characteristics of the 19 studies, 18 of which published after 2000, are summarized in Table 1. All the included studies were retrospective except the one by Yuksel et al. [¹⁷], which belonged to prospective study. A total of 4127 LHC patients, 1853 of which received RS and 2274 people underwent CS, were included in this meta-analysis. The mean or median follow-up time ranged from 2 to 148.8 months. Six studies were conducted in Italy, five in Turkey, and the rest were from eight different countries. The median NOS score for the quality of our included studies was 6, with a range from 4 to 8.

Comparison of surgery-related complications between RS and CS

All the included studies, except one, estimated postoperative overall complication [²³]. In total, 309 of the 1675 (18.4%) patients in the RS group and 921 of the 2236 (41.2%) in the CS group developed complications after surgery. Meta-analysis showed that RS was significantly associated with a lower risk of postoperative overall complication (Fig. 2A, OR= 0.32; 95% CI 0.19–0.56) while with a substantial between-study heterogeneity (I² = 86.3%, P<0.001).

Then, we analyzed several specific complications, and the pooled analyses showed that patients with RS had a reduced risk of biliary fistula (Fig. 2B, 11 studies, OR= 0.24; 95% CI 0.14–0.39, I² = 29.9%, P = 0.161) and residual/abdominal cavity abscess (Fig. 2C, 8 studies, OR= 0.29; 95% CI 0.11–0.77, I² = 60.7%, P = 0.013). No statistical differences were found in terms of pulmonary complications (Fig. 2D), wound infection, pleural effusion, bleeding, cardiovascular complication, and reinterventions between the two groups when a random-effects model was adopted (Supplementary Fig. S1A–S1E).

Comparison of postoperative recurrence risk between RS and CS

All the 19 studies compared the postoperative recurrence between RS and CS. Overall, postoperative recurrence was identified in 34 of the 1742 (2.0%) patients treated by RS and 270 of the 2202 (12.3%) patients treated by CS. The risk of postoperative recurrence was significantly lower in the RS group than in CS (Fig. 3A, OR= 0.16; 95% CI 0.11–0.23). Heterogeneity was limited in this meta-analysis (I² = 0%, P = 0.516).

Comparison of postoperative mortality risk between RS and CS

Mortality was compared between the two groups in 16 studies (except studies [³,⁹,²⁷]). In general, 60 out of 1753 (3.4%) patients with RS and 64 out of 2026 (3.2%) patients with CS died after surgery. We pooled the 16 studies together and found similar risk of mortality between the two groups (Fig. 3B, OR= 0.79; 95% CI 0.46–1.35). A low heterogeneity arose between these studies (I² = 25.3%, P = 0.188).

Comparison of hospital stay and operative time between RS and CS

A total of 12 studies collected and compared the duration of hospital stay. However, only six of them were analyzed in our meta-analysis as the rest failed to provide enough data to calculate SMD. By pooling the six included studies, we found that no significant difference was observed in the duration of hospital stay between RS and CS (Fig. 4A, SMD= -1.04; 95% CI -2.19–0.11), and a high degree of heterogeneity was presented (I² = 96.6%, P<0.001).

Five studies reported the operation time and three of them were eligible finally. This meta-analysis demonstrated that patients went through a significantly longer time of operation in the RS group (Fig. 4B, SMD= 1.51; 95% CI 0.74–2.28). Similarly, a high heterogeneity emerged among the three studies (I² = 79.9%, P = 0.007).

Exploration of heterogeneity in the meta-analysis

The meta-analysis in terms of the comparison of overall complications between the two groups produced a substantial heterogeneity with more than ten included studies. To explore the potential source of heterogeneity, we performed subgrouped analysis and meta-regression analysis. The covariates that we analyzed included publication year, study region, size of cysts, proportion of patients with multiple cysts, number of patients, and follow-up time, which might bring in heterogeneity and no less than three studies were conducted in each subgroup. We demonstrated that postoperative complications were significantly less in the RS group in all pooled subgroups except the ones with larger cysts and unclear proportion of multiple cysts. In addition, subgrouped analyses identified the publication year, region, follow-up, cyst size, and multiple cysts as potential sources of heterogeneity (Table 2, P<0.05 for Q statistic). The benefit of RS in reducing the risk of morbidity was significantly greater in studies published after 2006, conducted in Europe, with a higher proportion of multiple cysts and with a shorter duration of follow-up. Univariable meta-regression showed that the proportion of multiple cysts was the only factor that produced heterogeneity. However, no independent factor was identified when we performed multivariable meta-regression.

Sensitivity analysis and test of publication bias

Sensitivity analysis was conducted to validate the steady of our findings. First, we compared all the above pooled OR or SMD values (by a random-effects model) with estimated effect sizes by using a fixed-effects model (Table 3). Unlike the above findings, RS showed a statistically significant reduced risk of bleeding, reinterventions, and a significant shorter duration of hospital stay in comparison with CS, when a fixed-effects model was used. The rest of the meta-analyses revealed similar results between the two models. Influence analysis suggested that no any single study could markedly affect the summary estimations (Supplementary Fig. S2A–S2E).

Begg’s funnel plots were drawn to detect the existence of publication bias and all the plots reflected basic symmetry (Fig. 5A–5F). We found no statistically significant publication bias in terms of all the above outcomes (all P>0.10 in both Begg’s and Egger’s test).

Eventually, Galbraith’s plots identified four [²,¹⁴, ²⁵,²⁸], one [⁹], two [¹⁴, ²⁸], zero, two [⁹, ²⁴], and one [⁹] outliers for the meta-analyses in terms of overall complications, biliary fistula, recurrence, mortality, duration of hospital stay, and operative time, respectively (Supplementary Fig.S3A–S3F). After removing the four outliers in overall complications, the heterogeneity nearly disappeared in the updated meta-analysis (Supplementary Fig. S4, I² = 0.4%, P = 0.444).

Current debate on the treatment of LHC

In 2004, Dziri et al. systematically reviewed the evidence for the treatment of LHC and deduced that chemotherapy alone was not an ideal approach [⁸]. By contrast, surgical interventions, including radical and conservative approaches, are the cornerstone for eliminating cysts of hydatid. Dziri et al. concluded that the level of evidence was very low in the choice between RS and CS because of the lack of relevant randomized trials or well-designed cohort studies [⁸]. Thus far, no consensus regarding the optimal surgery approach for LHC remains, although several related well-designed retrospective, prospective, and propensity score matching studies gradually appeared.

Recently, He et al. reviewed only five studies (1 in Chinese) with 1267 patients and demonstrated that RS showed a favorable outcome compared with CS [³⁰]. The purpose of our current meta-analysis was to further compare the efficacy of RS versus CS. Based on our selection criteria, a total of 19 original studies (all in English) with 4127 patients were available. Both the magnitudes of included studies and evaluated patients in our study were more than three times larger than in He et al. [³⁰]. Very few included studies in the similar meta-analysis by He et al. may be due to the inexact search strategy and the obsolete deadline (to Dec 2013). By contrast, our meta-analysis showed strong benefits of RS in reducing the risk of overall complications and recurrence after operation. In addition, we found no significant difference in mortality risk between the two groups. The incidence of postoperative bile leaks is high in LHC, especially in patients with conservative operations. With four eligible studies, Hu et al. found no significant difference in the risk of bile leakage between RS and CS (P>0.05) [³⁰]. However, after pooling 11 relevant studies, we concluded that the risk of surgery-related biliary fistula was statistically significantly lower in patients who received RS, regardless if fixed- or a random-effects model was used. Our findings might be useful to further clarify the debate in the efficacy of RS versus CS.

Apart from therapeutic method, the outcomes of LHC were also determined by several other crucial factors, such as patients’ characteristics, namely, age [¹⁰,³¹], cysts diameter [¹⁰,³¹–³⁴], number [³⁵] and location of cysts [³⁶], duration of hospital stay [³¹], study period [¹⁰], and so forth. Meanwhile, the above factors might confuse the comparison between RS and CS. In our meta-analysis, publication year, region, follow-up time, and size and number of cysts were identified as potential sources of variation between studies.

In view of a high probability of morbidity and recurrence (31.3% and 7.7%, respectively, in our meta-analysis) after surgery especially CS in LHC, taking interventions to improve these unfavorable outcomes is critical. Although the effect of benzimidazole alone was unsatisfactory, treatment with surgery plus benzimidazole appeared to be effective in lowering complications and recurrence [¹,³⁷]. Omentoplasty was also effective in improving outcomes in patients who received CS [¹]. Our results showed RS as a beneficial method in obtaining better outcomes. However, management of LHC still should be mainly dependent on patients’ characteristics, size and location of cysts, and pathological involvement [⁵–⁷].

Recently, LHC management has evolved from open surgery to the increasing application of laparoscopic approach. In selected LHC patients, laparoscopic treatment is feasible and safe with low conversive rate [³⁸]. Jabbari et al. compared the efficacy of open surgery versus laparoscopic treatment and found that the operative time, postoperative pain, and hospitalization time were significantly lower in the laparoscopic group [³⁹]. Zaharie et al. recruited 333 patients with LHC and also showed the superiority of laparoscopic treatment [⁴⁰]. However, larger, prospective cohort studies, or randomized trials are still necessary to confirm its superiority.

Summary

In conclusion, our meta-analysis concerning a total of 4127 patients from 19 studies demonstrated that RS may reduce the risk of postoperative complications and recurrence, whereas no trend was observed toward such a reduction in mortality.

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