Feasibility of laparoscopic adrenalectomy in adrenal masses greater than 5 centimeters: a systematic review and meta-analysis

Introduction

Throughout the last decade, laparoscopic adrenalectomy (LA) has become the main treatment option for adrenal masses since minimally invasive surgery was introduced (1). It can be done through different approaches; however, laparoscopic transabdominal lateral adrenalectomy is the predominant form of surgery which is more familiar to most surgeons globally (2).

Adrenalectomy is indicated when there is a suspicion of malignancy or malignant tumors are present, as well as for non-functional tumors with malignancy risk (3). Numerous studies have shown the feasibility and safety of laparoscopic techniques for the removal of pheochromocytomas, since in 1992 first reported a lateral transabdominal LA approach (4).

While LA is the gold standard for managing small adrenal masses, its application for larger lesions (>5 cm) remains controversial due to concerns about technical feasibility, oncological safety, and limited high-quality evidence (5) Therefore, a systematic review and meta-analysis was carried out to comprehensively assess the existing literature, address knowledge gaps, and inform clinical practice, which ultimately impact patient care by establishing the efficacy and safety of LA for large masses. This study was conducted to evaluate the feasibility of LA in adrenal masses greater than 5 cm in terms of safety, effectiveness, and complications. We present this article in accordance with the PRISMA reporting checklist (available at https://gs.amegroups.com/article/view/10.21037/gs-24-69/rc) (6).

Methods

Study eligibility criteria

Local institutional ethical approval was not required as all data used in this analysis were obtained from a previously published resource. This study was prospectively registered with the International Prospective Register of Systematic Reviews and Meta-Analysis by one of the authors (Lama Alzelfawi) (PROSPERO: CRD42023462901).

For inclusion in this analysis, studies had to meet the following inclusion criteria: case-control studies, retrospective cohort studies, and prospective cohort studies published in English language. Adults with unilateral adrenal masses larger than 5 cm who went through laparoscopic unilateral adrenalectomy, including these approaches, transperitoneal, transabdominal, retroperitoneoscopic, and retroperitoneal adrenalectomy, were included. Studies failing to meet these strict eligibility criteria were excluded. The reasons for study exclusion were as follows: irrelevant intervention, i.e., bilateral adrenalectomy robotic, transvaginal, or open laparotomy, irrelevant subjects, i.e., adult patients with adrenal mass less than 5 cm, pediatric population, and animal studies, inadequate data reporting, wrong study design, repetitive publications, language limitation; and non-availability of the full text.

The main outcomes of this systematic review were safety and effectiveness. Additionally, intraoperative and postoperative measurements were tumor size, lesion localization (right/left), estimated blood loss, operation time, and hospital stay.

Complications were divided into intra-operative complications and post-operative complications. Intra-operatively, hemodynamic instability, adrenal vein avulsion, conversion to open surgery, hypotension/hypertension, estimated blood loss. Postoperatively, wound infection, gastroenteric dysfunction, bleeding, and mass recurrence.

Information sources and search strategy

A systematic review and meta-analysis of the literature were performed by a broad electronic search through PubMed, Google Scholar, Web of Science, and ProQuest databases for all relevant articles published in English for more than 5 cm adrenal tumors as shown in Figure 1. This study does not have restrictions toward date. Each database was initially searched for relevant titles. This search was performed by two independent reviewers, using a predetermined search strategy that was designed by the senior authors. The keywords used were safety, effectiveness, complications, feasibility, large adrenal mass, and LA.

Figure 1 PRISMA flow diagram.

Selection process, data collection process and analysis

All articles from the primary search were imported to Rayyan (7) for duplication removal and independently screened by two authors (E.A. & Lama Alzelfawi) based on title and abstract. Four authors reviewed the full text of all studies (E.A., Lena AlDosari, Z.A., & A.A.). Retrieved studies were reviewed to ensure inclusion criteria were met for the primary outcome at a minimum, with discordances in opinion resolved through consultation with the third reviewer (B.A.). By reading the title and abstract and applying the inclusion/exclusion criteria. Disagreements at any step of the screening process were handled through debate and consensus among all authors. The data was manually independently extracted by five authors (Lama Alzelfawi, E.A., Lena AlDosari, Z.A., & A.A.). An Excel sheet was used that included patients’ data and demographics (age, gender), study characteristics (main author’s name, year of publication, country, study design, sample size), intraoperative measurements (tumor size, tumor localization, estimated blood loss, operation time), intra-operative complications (hemodynamic instability, conversion to open, adrenal vein avulsion), and postoperative complications (bleeding, pulmonary embolism, pulmonary edema, blood transfusion, gastroenteric dysfunction, wound infection, mass recurrence). Tables were used to demonstrate included studies characteristics and results. The PRISMA chart flow figure was used to show the process of study selection. Moreover, forest plots were utilized to illustrate each outcome.

Meta-analysis was performed by random-effect models using R Studio with Meta Package (8).

Data items

The combinations and terms used included (“Adrenal Tumors Greater than” OR “Adrenal Tumors larger than” OR “Adrenal Masses Greater than” OR “Adrenal Masses larger than” OR “Adrenal Tumors >5 cm” OR “Adrenal Tumors” OR “Adrenal Masses”) AND (“transperitoneal adrenalectomy” OR “laparoscopic transabdominal adrenalectomy” OR “laparoscopic transperitoneal adrenalectomy” OR “retroperitoneoscopic adrenalectomy” OR “retroperitoneal adrenalectomy”. The search terms were identified in the title, abstract or medical subject heading.

Risk of bias

The observational studies’ methodological quality was assessed using the Newcastle-Ottawa scale (9), by three independent reviewers (Lama Alzelfawi, Lena AlDosari, Z.A.) with conflict resolution achieved through mutual consensus or, if necessary, involvement of a third party. The assessment comprised three sections, totaling nine components, examining study population selection, comparability of factors, and exposure ascertainment. Each section featured 2 to 4 questions, rated as high, low, or unclear risk of bias. Discrepancies in ratings underwent resolution through discussion among reviewers, with external mediation available if disagreements persisted. Figures 2,3 provide a comprehensive risk of bias graph and summary, revealing generally low bias risk in study selection domains, such as adequate case definition. However, comparability and exposure ascertainment displayed extremely low or negligible bias risk. Conversely, other aspects demonstrated a higher average risk of bias, underscoring the critical assessment needed in observational research.

Figure 2 Risk of bias graph.

Figure 3 Risk of bias summary, review authors’ judgments about each risk of bias item for each included study (10-34). +, low risk; −, high risk.

Results

Across the 25 studies, a comprehensive analysis of 963 patients who underwent LA for large adrenal masses revealed diverse demographic characteristics, the types of intervention, the included studies utilized various approaches for LA, as shown in Table 1. The transperitoneal LA (TLA) approach was the more prevalent choice, applied in most cases across various studies.

Intraoperative measurements

Tumor sizes varied widely in the study, as demonstrated in Table 2. Additionally, the proportion of tumors on the right side was 50% (0.50) [95% confidence interval (CI): 0.471–0.543], while on the left side, it was 45% (0.45) (95% CI: 0.404–0.508). The subgroup meta-analysis comparing the transperitoneal and retroperitoneal approaches for adrenalectomy revealed the transperitoneal approach was utilized for the largest tumor size with a mean of 12.10 cm (95% CI: 11.30–12.96).

This significant difference was supported by a test for subgroup differences (P<0.01), indicating that the tumor size differs significantly based on the surgical approach Figure 4. The operating time data across the reviewed studies exhibit variability in the duration of the surgical procedures. Marek-Safiejko et al., reported a mean total operative time of 153.1 minutes (10), while Novitsky et al., had presented an average operating time of 178±55 minutes (11). The results of random effect model for subgroup meta-analysis showed the retroperitoneal approach demonstrated a mean operative time of 140.2 minutes (95% CI: 84.45–232.98), while the transperitoneal approach required a mean operative time of 138.9 minutes (95% CI: 118.29–163.24). There was insignificant difference supported by a test for subgroup differences (P=0.97), suggesting that no advantages in terms of operative time between two approaches Figure 5. Moreover, Chen et al., study highlighted the difference in operating time between the retroperitoneal LA (RLA) approach (98.70±32.30 minutes) while the TLA approach has a longer operating time (124.36±34.62 minutes) (20). In addition, Ma et al. has observed variations in mean operative times, with TLA having the longest duration at 83.6±23.1 minutes and RLA the shortest at 49.7±13.4 minutes (27). The data collectively reflects the diverse range of operating times associated with different approaches and procedures, emphasizing the need for careful consideration of these variations in the context of the surgical interventions under investigation. Estimated blood loss during LA for adrenal masses exceeding 5 cm varied across the reviewed studies in Figure 6. The variations in blood loss are crucial indicators of the procedural intricacies and potential challenges associated with the laparoscopic approach for larger adrenal masses. Postoperative measurements in our study included hospital length stay which varied across studies in the systematic literature review, as shown in Table 2.

Figure 4 Subgroup analysis of tumor size based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

Figure 5 Operative time in minutes. (A) Overall operating times across all studies; (B) subgroup analysis of operative time based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

Figure 6 Estimated blood loss. (A) The forest plot shows the overall estimated blood loss across all the included studies; (B) sub-analysis based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

Conversely, the average blood loss was 110.6 mL (95% CI: 78.2–156.3), with a wide range of 33.7 to 334.3 mL and substantial heterogeneity (I²=98%).

As shown in Figure 6B, the analysis of blood loss revealed that the transperitoneal approach resulted in a substantially higher mean blood loss of 106.9 mL (95% CI: 67.42–169.75), compared to the retroperitoneal approach which showed a lower mean blood loss of 80.98 mL (95% CI: 14.14–463.67). This significant difference was supported by a test for subgroup differences (P<0.01), suggesting that the retroperitoneal approach may lead to less blood loss during surgery.

Notably, patients exhibited an average hospital stay of 3.72 days (95% CI: 2.97–4.66), ranging from 2 to 7.4 days, illustrated in Figure 7A. There was no significant difference in mean hospital stay between the two approaches. While the retroperitoneal approach tended to have a slightly longer mean hospital stay of 4.91 days (95% CI: 2.15–11.22) compared to 4.59 days (95% CI: 2.46–8.58) for the transperitoneal approach, this difference was not statistically significant (P=0.90). Regarding the comparison of conversion rates to open surgery between the transperitoneal and retroperitoneal approaches yielded interesting findings in Figure 7B.

Figure 7 Hospital length of stay in days. (A) Overall hospital length of stay across all studies; (B) subgroup analysis of hospital stay based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

Regarding intra-operative complications, adrenal vein avulsion, hemodynamic instability, and conversion to open surgery were included.

Only one study reported 1 case of adrenal vein avulsion (30). In addition, hemodynamic instability was defined in our study as blood pressure fluctuations during the operation, which was reported in two studies. Only seven patients out of 963 cases experienced hemodynamic instability, as shown in Figure 8. The conversion to open surgery in LA surgeries varies across studies. Out of 963 patients, 49 were converted to open surgery. Regarding the comparison of conversion rates to open surgery between the transperitoneal and retroperitoneal approaches yielded interesting findings Figure 9A. For the transperitoneal approach, the proportion of cases converted to open surgery was 7% (95% CI: 4–10%), while for the retroperitoneal approach, this proportion was notably lower at 2% (95% CI: 0–4%). The test for subgroup differences indicated a significant variation between the groups (P=0.01), suggesting that the conversion rate to open surgery is more in transperitoneal approach Figure 9B.

Figure 8 Occurrence of hypotension/hypertension. CI, confidence interval.

Figure 9 Conversion to open surgery. (A) Overall conversion to open surgery across studies; (B) subgroup analysis of conversion rate based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

Specific factors like severe adhesions, and tumor characteristics contributed to conversions. Successful laparoscopic outcomes without conversion were seen in 13 studies. Hemodynamic instability and open conversion rates were infrequent, reported at 0.00 (95% CI: 0.00–0.01, I²=0%) and 0.03 (95% CI: 0.01–0.04, I²=48%) respectively as shown in Figures 8,9.

Post-operative complications

Postoperative complications included pulmonary embolism, pulmonary edema, gastrointestinal dysfunction, bleeding, blood transfusion, mass recurrence, and wound infection. In terms of postoperative complications, the analysis revealed low prevalence rates for adverse events following LA. Pulmonary edema, gastric dysfunctions, wound infection, pulmonary embolism, and mass recurrence were reported at 0.03%, 0.04%, 0.4%, 0.03%, and 0.03% respectively. These findings collectively highlight the favorable postoperative outcomes associated with laparoscopic procedures for adrenal resection. Furthermore, one study reported mass recurrence in two patients (17). Blood transfusion was required in 1.3% of cases, while bleeding was reported in 35 cases (Table 3).

Figure 10 shows a total of 12 patients who had postoperative wound infections.

Figure 10 Occurrence of wound infection. CI, confidence interval.

Figure 11 shows blood transfusion was required in) 1.0% (0.01) of cases (95% CI: 0.00–0.02), with a wide range from 0% to 31%, accompanied by high heterogeneity (I²=51%).

Figure 11 Blood transfusion. CI, confidence interval.

The prevalence of bleeding during laparoscopic surgery was notably low at 2% (0.02) (95% CI: 0.01–0.03), with a range from 0% to 12% as shown in Figure 12.

Figure 12 Intra-operative bleeding. (A) Overall intra-operative bleeding across studies; (B) subgroup analysis of bleeding proportion based on transperitoneal laparoscopic adrenalectomy and retroperitoneal laparoscopic adrenalectomy approaches. CI, confidence interval.

As shown in Figure 12B, regarding the proportion of bleeding, the transperitoneal approach had a bleeding rate of 3% (0.03) (95% CI: 0.01–0.05), whereas the retroperitoneal approach had a slightly higher bleeding rate of 6% (0.06) (95% CI: 0.02–0.10). However, the test for subgroup differences did not show a significant variation between the two approaches (P=0.28).

Discussion

The adrenalectomy approach has evolved from an open procedure requiring large incisions to a minimally invasive approach that entails a much smaller incision (3). The diverse demographic characteristics of the 963 patients across 25 studies undergoing LA for adrenal masses more significant than 5 cm underscore the need to tailor surgical approaches to individual patient profiles. A comprehensive preoperative study is necessary for evaluating all adrenal masses, which involves clinical evaluation, hormonal assessment and imaging. Specific imaging techniques like scintigraphy or positron emission tomography may be used for suspected pheochromocytoma cases. The most important factors to evaluate during preparation were the underlying cause and the patient’s condition. After care and post-operative evaluation also highly relied on the underlying pathology. All patients were transferred to a recovery room for the first 4–6 h after surgery, to monitor their condition. Moreover, each patients’ post-surgery care plan depended on the procedural outcome and intra/post operative complications (35).

Since adrenal tumors are relatively rare, technical skills in laparoscopic surgery play a crucial part. Many surgeons have limited experience in handling them. The choice of surgical approach depends on factors such as tumor size, patient’s body type, and the surgeon’s expertise (36).

Intraoperative and postoperative complications represent crucial aspects of LA for adrenal masses exceeding 5 cm, and a deeper exploration of these outcomes is paramount for a comprehensive understanding (37,38). While our systematic review highlighted the underreporting of tumor rupture instances, the available data underscores the need for documentation to ascertain this complication’s actual occurrence or absence. Moreover, the inconsistent reporting of hypotension and hypertension during the procedure suggests a significant gap in understanding the hemodynamic stability associated with LA (39). Future studies should prioritize standardized reporting to facilitate a more detailed analysis of intraoperative complications, enabling the identification of potential risk factors and optimization of patient care strategies.

The considerable variability in operating times across studies underscores the complexity of LA for larger adrenal masses. Factors such as the surgical approach, tumor size, and the pathological diagnosis (pheochromocytoma) contribute to this diversity (40).

Several factors emerged across the studies as influential in determining operative time. Tumor size significantly impacts operative time, with larger masses associated with prolonged procedures (28). Tumor size, particularly when ≥8 cm, was a significant factor impacting operative time, as concluded by Öz et al., a longer operative time for masses ≥8 cm compared to smaller masses (31). Diagnosing pheochromocytoma further contributes to extended operative times (41).

A variety of factors contributed to the decision to convert to open surgery, including severe adhesions and tumor characteristics (34). The conversion to open surgery occurred in 49 patients out of the total of 963 patients, and all the factors contributing to conversion were not attributed to the tumor size. Successful outcomes without conversion in some studies underscore the critical role of preoperative assessment and surgical expertise (42,43). Variability in estimated blood loss across studies highlights the importance of considering factors like tumor size and surgical approach (44). Ibragimovich et al. reported a mean of 117±38 mL, while Naya et al. noted a mean of 212±165 mL (16,22).

Turning our attention to postoperative outcomes, which are integral to evaluating the overall success and safety of LA, a low prevalence of postoperative complication was observed by the overall reported complications; gastroenteric dysfunction was encountered in one case (28), pulmonary embolism was as well encountered in one case (12), pulmonary edema was seen in two cases (10,19). In contrast, wound infection has been reported in 12 cases (14,21,23,27).

The heterogeneity in hospital length of stay (LOS) across different studies, with LOS ranging from 2 to 7 days, factors such as the surgical approach (e.g., retroperitoneal vs. transabdominal), and tumor size may contribute to variations in recovery times (45,46). Novitsky et al. reported an average length of stay of 2.5±1.9 days (11). Tsuru et al. indicated a more prolonged recovery for large-tumor patients (5.4 vs. 4.5 days) (12).

Critical gaps in the literature, such as underreported intraoperative complications and varying conversion rates to open surgery, highlight the urgent need for standardized and comprehensive documentation to accurately evaluate the safety and feasibility of the procedure.

The overarching theme of our systematic review and meta-analysis revolves around the safety and feasibility of LA for larger adrenal masses. While the procedure demonstrated feasibility, findings revealed varying safety outcomes. Factors influencing safety included tumor size, surgical approach, and the occurrence of complications. Larger tumors generally correlated with longer operative times, and the transperitoneal approach was associated with increased operative duration. Conversion to open surgery significantly impacted safety, emphasizing the need for careful consideration.

Certain limitations should be acknowledged. The inherent heterogeneity across the included studies, ranging from variations in patient populations to diverse surgical techniques, introduces a level of variability that may impact the generalizability of the findings. The limited availability of detailed data in some studies, particularly regarding intraoperative complications and postoperative outcomes, hindered a comprehensive analysis.

Conclusions

In conclusion, the feasibility and safety of LA for tumors larger than 5 cm have a significant impact on several intraoperative and postoperative outcomes. Larger masses and transperitoneal approaches require a longer operation time. Conversion to open surgery was related to tumor characteristics and the presence of adhesions. Regarding hemodynamic instability, it was low among patients. These complications differ among several studies, indicating many factors affecting laparoscopic safety.

Acknowledgments

Funding: None.

Footnote

Reporting Checklist: The authors have completed the PRISMA reporting checklist. Available at https://gs.amegroups.com/article/view/10.21037/gs-24-69/rc

Peer Review File: Available at https://gs.amegroups.com/article/view/10.21037/gs-24-69/prf

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://gs.amegroups.com/article/view/10.21037/gs-24-69/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are 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.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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