Background:
The effectiveness and safety of laparoscopic adrenalectomy (LA) under different routes for the treatment of large pheochromocytomas (PCCs) is unknown.
Materials and methods:
This meta-analysis and systematic review was performed according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) and AMSTAR (Assessing the methodological quality of systematic reviews) Guidelines. Three databases were systematically searched, including Medline, PubMed, and Web of Science. The time frame of the search was set from the creation of the database to October 2022. Perioperative outcomes were divided into two groups according to tumor size: SMALL group (≤6 cm in diameter), LARGE group (>6 cm in diameter).
Results:
Eight studies including 600 patients were included. In the LA group, complications was comparable in both groups (SMALL group and LARGE group), and the LARGE group had longer operative time [OT weighted mean difference (WMD)=32.55; 95% CI: 11.17, 53.92; P<0.01], length of stay (LOS WMD=0.82; 95% CI: 0.19, 1.44; P<0.05), more estimated blood loss (EBL WMD=85.26; 95% CI: 20.71, 149.82; P<0.05), hypertension [odds ratio (OR)=3.99; 95% CI: 1.84, 8.65; P<0.01], hypotension (OR=1.84; 95% CI: 1.11, 3.05; P<0.05), and conversion (OR=5.60; 95% CI: 1.56, 20.13; P<0.01). In the transabdominal LA group, OT, LOS, EBL, complications, hypertension, and hypotension were the same in both groups. In the retroperitoneal LA group, complications and hypotension were the same in both groups, while the LARGE group had longer OT (WMD=52.07; 95% CI: 26.95, 77.20; P<0.01), LOS (WMD=0.51; 95% CI: 0.00, 1.01; P<0.05), more EBL (WMD=92.99; 95% CI: 27.70, 158.28; P<0.01) and higher rates of hypertension (OR=6.03; 95% CI: 1.95, 18.61; P<0.01).
Conclusions:
LA remains a safe and effective approach for large PCC. Transabdominal LA is superior to retroperitoneal LA.
Keywords: laparoscopic adrenalectomy, pheochromocytoma, retroperitoneal laparoscopic adrenalectomy, transabdominal laparoscopic adrenalectomy
Introduction
Highlights
Eight published studies were included.
For large pheochromocytomas (PCCs) (>6 cm), laparoscopic adrenalectomy (LA) was a safe and effective approach.
Transabdominal laparoscopic adrenalectomy (TLA) is superior to retroperitoneal laparoscopic adrenalectomy (RLA) for large PCCs.
PCC is a rare catecholamine-producing adrenal medullary tumor with an incidence of 0.1–0.5% in patients with hypertension1. Clinical manifestations vary widely, with the most common manifestations being headache, sweating, palpitations, and high blood pressure2. In severe cases, it can even lead to sudden death3. Surgical resection is the only curative treatment for PCC4.
LA was first reported in 1992 by Gagner et al.5. It has the advantage of reduced bleeding, shorter length of stay, and improved recovery in the management of some smaller adrenal tumors6. Today, LA has become the standard procedure for the surgical resection of small benign adrenal tumors7. However, the role of LA in the treatment of larger benign PCCs (>6 cm in diameter) is still controversial.
This meta-analysis evaluated the safety and effectiveness of LA for large PCCs by comparing the perioperative differences between two different sizes of PCCs (≤6 cm for the SMALL group, >6 cm for the LARGE group). In addition, subgroup analyses were performed for some outcome indicators according to the different laparoscopic surgical routes: TLA and RLA, with the aim of providing a more appropriate surgical route for the management of large PCCs in clinical practice.
Materials and methods
Literature search
This meta-analysis has been reported according to PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) 2020 standards and is fully consistent8. The quality assessment was performed according to AMSTAR (Assessing the methodological quality of systematic reviews) 29, with a rigorous description and full consistency for each question. This systematic review has been registered with PROSPERO.
The literature search and selection process were performed independently by two authors. When agreement could not be reached, disagreements between authors were negotiated by a third reviewer (Y.L.). Three databases including Medline, PubMed, and Web of Science were systematically searched to identify fully published studies from the date of database creation to October 2022. The search terms were as follows: (laparoscopic or minimally invasive) and large and (adrenal tumor or PCC or paraganglioma). The search was restricted by English. In addition, the references of identified studies were searched manually.
Eligibility criteria
We included only retrospective, prospective, and randomized controlled trials study designs. Inclusion criteria were: (1) adult patients diagnosed with PCC and classified by volume ≤6 and >6 cm; (2) only the following procedures are included: LA; (3) evaluation of at least one of the specified metrics, including but not limited to the following: operative time (OT), estimated blood loss (EBL), length of stay (LOS), complications, hypertension, hypotension, and conversion; and (4) search in English. The following exclusion criteria were considered for this study: (1) animal trials; (2) unavailable for search in English; (3) inability to extract data; (4) pediatric samples; (5) no relevant results; (6) not categorized by 6 cm volume; (7) single-arm studies; and (8) editorials, conference abstracts, letters, or expert opinions.
Study quality assessment
Based on the results of the initial search, the Newcastle–Ottawa Scale was used to assess the quality of the included studies10. This scale includes the three domains of selection, comparability, and exposure. Scored more than six stars were considered high-quality studies.
Data extraction
Two authors independently used standardized forms to extract the following data for each included study: author names, year, study center, sample size, procedure, age, tumor size, BMI, and metrics including OT, LOS, EBL, complications, hypertension, hypotension, and conversion.
Statistical analysis
The meta-analysis was performed using Stata statistical software version 16 (StataCorp LLC). Weighted mean difference (WMD) was used for continuous variables (effect) and odds ratio (OR) for dichotomous variables. 95% CIs and P-values are reported for all outcome metrics. The q and chi-square tests were used to verify the level of heterogeneity among the included studies. Differences were considered significant if I 2 more than 50%11. A random-effects model was used to pool the estimates. Subgroup analysis of OT, EBL, LOS, complications, hypertension, and hypotension were performed according to the laparoscopic surgical route (TLA, RLA). Mixed surgical routes (both TLA and RLA are included) were included in the MIX group. In addition, further sensitivity analyses were performed for those studies with a high degree of heterogeneity (I 2≥50% or P<0.1)12.
Results
Description of studies
A total of 498 records were retrieved from these three databases and 47 records were manually searched from the references of the relevant studies. After reading the titles and authors’ names, 42 of these studies were excluded due to duplication, 301 studies were marked as ineligible by the automated tool, and another 78 studies were excluded for other reasons. When considering study topics, abstracts, and keywords, 104 records were excluded that were not related to the study topic, five studies were not retrieved from the original text, and the remaining 15 studies were reviewed as complete studies. Three reviews, one meta-analysis, and three single-arm studies were excluded. Three reviews, one meta-analysis, and three single-arm studies were excluded. Finally, five retrospective studies and three prospective studies including 600 patients were included in the review13–20 (Fig. 1).
Figure 1.
Flow diagram of the study selection process.
Table 1 provides the baseline data extracted from each of the included studies. This includes the author’s name, year, study center, sample, procedure, BMI, tumor size, tumor laterality, age, sex, and other records.
Table 1.
Baseline data for studies included in the meta-analysis
| References | Study | Center | Procedure | Size (mean±SD) (cm) | Sample (n) | Age (mean±SD) (years) | BMI (mean±SD) (kg/m2) | Male/female | Right/left |
|---|---|---|---|---|---|---|---|---|---|
| Chung et al. 19 | Retrospective | Single center | RLA | 7.4±1.1 3.9±0.9 |
24 27 |
49.9±12.3 53.9±10.0 |
23.6±2.3 23.7±2.4 |
12/12 13/14 |
10/14 12/15 |
| Liu et al. 20 | Retrospective | Single center | LA | 8.1±1.67 4.3±1.48 |
87 166 |
47.5±13.7 46±14.8 |
23.73±3.51 23.72±3.00 |
46/41 75/91 |
NA |
| Conzo et al. 18 | Retrospective | Multicenter | TLA | 8.3 3.9 |
23 37 |
39.56 44.16 |
NA | 13/10 8/29 |
11/12 20/17 |
| Carter et al. 13 | Prospective | Single center | RLA | 7.6±0.4 3.4±0.3 |
11 15 |
57±4 51±3 |
NA | 6/5 7/8 |
6/5 8/7 |
| Perry et al. 14 | Prospective | Single center | TLA | 7.8±1.3 3.8±1.6 |
8 22 |
43.3 48.7 |
28.7 27.3 |
2/6 9/13 |
3/5 14/8 |
| Toniato et al. 17 | Retrospective | Single center | TLA | NA | 7 35 |
44 44 |
NA | NA | NA |
| Wilhelm et al. 16 | Retrospective | Multicenter | TLA | 8.15±0.41 3.8±0.16 |
25 40 |
54.5±2.9 44.8±2.7 |
NA | 10/15 15/25 |
NA |
| Kercher et al. 15 | Prospective | Single center | RLA | 7.5±1.5 4.1±1.1 |
18 63 |
47.4 45.1 |
NA | NA | NA |
LA, laparoscopic adrenalectomy; NA, not available; RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
There were no significant differences in any of the demographic variables (age WMD=3.91; 95% CI: −1.12, 8.93; P=0.13; BMI WMD=−0.02; 95% CI: −0.74, 0.70; P=0.95; sex LA OR=1.42; 95% CI: 0.90, 2.25; P=0.14, sex TLA OR=1.53; 95% CI: 0.44, 5.28; P=0.50, sex RLA OR=1.17; 95% CI: 0.47, 2.87; P=0.74; tumor laterality LA OR=0.76; 95% CI: 0.40, 1.43; P=0.40, tumor laterality TLA OR=0.62; 95% CI: 0.26, 1.50; P=0.29, tumor laterality RLA OR=0.94; 95% CI: 0.38, 2.33; P=0.90) except for inconsistency in tumor size (LA WMD=3.96; 95% CI: 3.65, 4.27; P<0.01), tumor size (TLA WMD=4.34; 95% CI: 4.18, 4.51; P<0.01), tumor size (RLA WMD=3.77; 95% CI: 3.19, 4.34; P<0.01) (Figs. 2–6).
Figure 2.
Forest plot and meta-analysis of the age between LARGE and SMALL groups.
Figure 6.
Forest plot and meta-analysis of the tumor size between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 3.
Forest plot and meta-analysis of the BMI between LARGE and SMALL groups.
Figure 4.
Forest plot and meta-analysis of the sex between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 5.
Forest plot and meta-analysis of the tumor laterality between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Quality assessment
Table 2 shows the Newcastle–Ottawa Scale study quality rating scores for the included studies. All studies were high-quality, with ratings of more than six stars.
Table 2.
Quality score of included studies based on the Newcastle–Ottawa Scale
| Selection | Comparability | Exposure | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|
| References | REC | SNEC | AE | DO | SC | AF | AO | FU | AFU | Total stars |
| Chung et al. 19 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
| Liu et al. 20 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 7 | ||
| Conzo et al. 18 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
| Carter et al. 13 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
| Perry et al. 14 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
| Toniato et al. 17 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
| Wilhelm et al. 16 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 7 | ||
| Kercher et al. 15 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 1 | 8 | |
AE, ascertainment of exposure; AF, study controls for other important factors; AFU, adequacy of follow-up of cohort (≥80%); AO, assessment of outcome; DO, demonstration that outcome of interest was not present at start of study; FU, follow-up long enough for outcomes to occur; REC, representativeness of the cohort; SC, study controls most important factors; SNEC, selection of the none posed cohort.
Perioperative outcomes
Eight studies including 600 patients were included. Perioperative outcomes included complications, conversion rates, hypertension, hypotension, OT, EBL, and LOS.
In the LA group, complications (OR=1.99; 95% CI: 0.98, 4.08; P=0.06) was comparable in both groups (SMALL group and LARGE group), and the LARGE group had longer OT (WMD=32.55; 95% CI: 11.17, 53.92; P<0.01), LOS (WMD=0.82; 95% CI: 0.19, 1.44; P<0.05), more EBL (WMD=85.26; 95% CI: 20.71, 149.82; P<0.05), hypertension (OR=3.99; 95% CI: 1.84, 8.65; P<0.01), hypotension (OR=1.84; 95% CI: 1.11, 3.05; P<0.05), and conversion (OR=5.60; 95% CI: 1.56, 20.13; P<0.01).
In the TLA group, OT (WMD=1.50; 95% CI: −21.32, 24.32; P=0.90), LOS (WMD=0.19; 95% CI: −0.41, 0.80; P=0.53), EBL (WMD=21.76; 95% CI: −42.68, 86.20; P=0.51), complications (OR=1.08; 95% CI: 0.28, 4.18; P=0.91), hypertension (OR=2.76; 95% CI: 0.95, 8.00; P=0.06) and hypotension (OR=1.16; 95% CI: 0.27, 5.01; P=0.85) were the same in both groups.
In the RLA group, complications (OR=2.20; 95% CI: 0.84, 5.78; P=0.11) and hypotension (OR=1.44; 95% CI: 0.37, 5.58; P=0.59) were the same in both groups, while the LARGE group had longer OT (WMD=52.07; 95% CI: 26.95, 77.20; P<0.01), LOS (WMD=0.51; 95% CI: 0.00, 1.01; P<0.05), more EBL (WMD=92.99; 95% CI: 27.70, 158.28; P<0.01) and higher rates of hypertension (OR=6.03; 95% CI: 1.95, 18.61; P<0.01) (Figs. 7–13).
Figure 7.
Forest plot and meta-analysis of the operative time between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 13.
A: Forest plot and meta-analysis of the conversion between LARGE and SMALL groups.
Figure 8.
Forest plot and meta-analysis of the length of stay between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 9.
Forest plot and meta-analysis of the estimated blood loss between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 10.
Forest plot and meta-analysis of the complications between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 11.
Forest plot and meta-analysis of hypertension between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Figure 12.
Forest plot and meta-analysis of the hypotension between LARGE and SMALL groups. RLA, retroperitoneal laparoscopic adrenalectomy; TLA, transperitoneal laparoscopic adrenalectomy.
Sensitivity analysis
After rigorous scoring of the quality of the literature, the included studies were of high quality (at least six stars), but there was inevitably a high degree of heterogeneity between studies. Sensitivity analysis was used to track the source of heterogeneity for each outcome metric. For outcomes with high heterogeneity (OT, EBL, and LOS), included studies were excluded one by one, and statistical merging and heterogeneity tests were performed again to elucidate changes in heterogeneity. The results showed a stable source of heterogeneity for LOS. However, OT and EBL were unstable.
Discussion
Nowadays, LA performed via a transperitoneal or retroperitoneal approach has become the treatment of choice for most adrenal tumors and is now widely used for small benign adrenal tumors21–23. Compared with other adrenal tumors, PCCs are a management challenge due to their size, vascularity, and preoperative, intraoperative, and postoperative care requirements secondary to hormone secretion13,24. One study found that minimally invasive surgery can reduce EBL, shorten LOS, and can still be used to manage large PCCs25. However, other studies have concluded that the use of LA for larger sized PCCs may lead to severe hemodynamic fluctuations and is not recommended26. This view is currently controversial. This meta-analysis aims to provide the evidence base for a more appropriate surgical approach to manage large PCCs in clinical practice. We performed the first meta-analysis of the safety and effectiveness of LA for the treatment of PCCs of different sizes (≤6 cm for the SMALL group and >6 cm for the LARGE group) and performed a subgroup analysis according to the laparoscopic surgical route. The results of this meta-analysis study found no difference in LOS and complications in the LARGE group compared with the SMALL group but required longer OT, more EBL, more occurrence of hypertension and hypotension, and possessed a higher conversion. Further subgroup analysis revealed almost no difference in outcome indicators between the LARGE and SMALL groups for TLA, leading to more differences in outcome indicators between the two groups stemming from RLA.
The results of the six included studies showed that the LARGE group required a longer OT14,15,17–20. The high heterogeneity between studies can be explained by differences in surgical route, surgeon proficiency in the procedure, and medical equipment. Subgroup analysis revealed no difference in OT between the LARGE and SMALL groups in TLA, and the results of this study were consistent with those of Conzo et al. 18, Perry et al. 14, and Toniato et al.17. However, in RLA, the OT required was longer in the LARGE group, and this result was consistent with the results of Chung et al. 19 and Kercher et al.15. They suggest that this may be related to difficulties in anatomical positioning, smaller working space, and closer proximity to the port site19. Seven studies reported EBL13–15,17–20. The heterogeneity between studies can be explained by differences in surgical routes, anatomical relationships, and the surgical proficiency of the surgeons. Subgroup analysis revealed that in the TLA, the EBL in the LARGE group was comparable to that in the SMALL group, which is the same as the findings of Conzo et al. 18 and Perry et al. 14. In the RLA group, the LARGE group had more EBL, which is consistent with the findings of Chung et al. 19. They explained it as being related to the smaller posterior abdominal space and the difficulty of dissection19. Despite the significant difference in tumor diameter between the two groups, there was no difference in LOS after LA13–15,17–20. Subgroup analysis showed the same results for TLA and RLA. It is worth noting that the sensitivity analysis showed the results for OT and EBL were not stable, and this result needs to be viewed with caution.
The results of all seven included studies found no difference in complications between the two groups13–15,17–20. The results of the subgroup analysis found the same for TLA and RLA. However, our study found that for the LARGE group, the probability of hypertension was higher13,17–19. Subgroup analysis found that in TLA, the LARGE group was the same as the SMALL group, while in RLA, there was more hypertension. Chung et al. 19 found that intraoperative hypertension tended to be more common in right adrenalectomy, which they suggested may be related to the shorter right adrenal vein and the increased likelihood of tumor manipulation. Similarly, the probability of hypotension was higher in the LARGE group13,17–20. Subgroup analysis found no difference in outcomes between the two groups in TLA and RLA. In the MIX group, only the results of Liu et al. 20 found more hypotension in the LARGE group, which they explained was related to higher catecholamine levels in patients with larger tumors. Unfortunately, there are few studies on this aspect and more high-quality randomized controlled studies are needed to support the results. Only four studies reported conversion and failed to perform subgroup analysis14,16,18,19. Conversion was higher in the LARGE group than in the SMALL group, which was mainly associated with tenacious adhesions between peritumor structures, suspected malignancy, and intraoperative bleeding14,19.
We performed this meta-analysis using the PRISMA guidelines 27. However, there are still many limitations. First, the number of included studies and patients was relatively small; second, the studies we included did not have large malignant PCCs, the management of which remains unclear; third, for conversion, we failed to perform subgroup analyses because there were too few relevant studies; and finally, there was a high degree of heterogeneity in the study metrics (OT, EBL, and LOS), and after performing sensitivity analysis, it was found that the results for OT and EBL were unstable and the reliability of this result needs further validation.
Conclusions
LA remains a safe and effective approach for large PCCs. TLA is superior to RLA. Its OT, EBL, LOS, complications, hypertension, and hypotension were the same in the two different size PCC groups. More randomized controlled studies with larger sample sizes and higher quality are needed to support our conclusions.
Ethical approval
Not applicable.
Sources of funding
This study was sponsored by Nanchong City School Science and Technology Cooperation Project NSMC20170457.
Author contribution
Conceived and designed the experiments: Y.L. Analyzed the data: L.G., L.P., and C.M. Contributed reagents/materials/analysis: L.G., Z.Z., S.G., Z.W., L.Z., and K.L. Wrote the manuscript: L.G., L.P., and C.M. All authors have read and approved the final manuscript.
Conflicts of interest disclosure
The authors declare that they have no financial conflict of interest with regard to the content of this report.
Research registration unique identifying number (UIN)
Name of the registry: PROSPERO database.
Unique Identifying number or registration ID: CRD42022319797.
Hyperlink to your specific registration (must be publicly accessible and will be checked): https://www.crd.york.ac.uk/prospero/display_record.php?ID=CRD42022319797
Guarantor
Yunxiang Li.
Data availability statement
All data generated and analyzed during this study are included in this published article. The data presented in the article may be requested by consulting the correspondence author.
Provenance and peer review
Not commissioned, externally peer-reviewed.
Acknowledgements
None.
Footnotes
L.G., L.P., and C.M. contributed equally to this work.
Sponsorships or competing interests that may be relevant to content are disclosed at the end of this article.
Published online 11 April 2023
Contributor Information
Lijian Gan, Email: 569259036@qq.com.
Lei Peng, Email: penglei933@163.com.
Chunyang Meng, Email: mengchunyang3@163.com.
Lei Zheng, Email: 194623942@qq.com.
Zhiqiang Zeng, Email: zzq2236213409@163.com.
Si Ge, Email: 1565663875@qq.com.
Zuoping Wang, Email: wzp18380207746@126.com.
Kangsen Li, Email: 2250786304@qq.com.
Yunxiang Li, Email: liyunxiang369@126.com.
References
- 1. Opocher G, Schiavi F, Conton P, et al. Clinical and genetic aspects of phaeochromocytoma. Horm Res 2003;59(suppl 1):56–61. [DOI] [PubMed] [Google Scholar]
- 2. Lenders JW, Eisenhofer G, Mannelli M, et al. Phaeochromocytoma. Lancet 2005;366:665–675. [DOI] [PubMed] [Google Scholar]
- 3. Bravo EL, Gifford RW, Jr. Pheochromocytoma. Endocrinol Metab Clin North Am 1993;22:329–341. [PubMed] [Google Scholar]
- 4. Lenders JWM, Kerstens MN, Amar L, et al. Genetics, diagnosis, management and future directions of research of phaeochromocytoma and paraganglioma: a position statement and consensus of the Working Group on Endocrine Hypertension of the European Society of Hypertension. J Hypertens 2020;38:1443–1456. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5. Gagner M, Lacroix A, Bolté E. Laparoscopic adrenalectomy in Cushing’s syndrome and pheochromocytoma. N Engl J Med 1992;327:1033. [DOI] [PubMed] [Google Scholar]
- 6. Rosoff JS, Raman JD, Del Pizzo JJ. Laparoscopic adrenalectomy for large adrenal masses. Curr Urol Rep 2008;9:73–79. [DOI] [PubMed] [Google Scholar]
- 7. Matsuda T. Laparoscopic adrenalectomy: the ‘gold standard’ when performed appropriately. BJU Int 2017;119:2–3. [DOI] [PubMed] [Google Scholar]
- 8. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Int J Surg 2021;88:105906. [DOI] [PubMed] [Google Scholar]
- 9. Shea BJ, Reeves BC, Wells G, et al. AMSTAR 2: a critical appraisal tool for systematic reviews that include randomised or non-randomised studies of healthcare interventions, or both. BMJ 2017;358:j4008. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10. Wells GA, Shea B, O’Connell D, et al. The Newcastle Ottawa 1 Scale (NOS) for assessing the quality of nonrandomized studies in meta-analyses. 2021. http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp
- 11. Higgins JP, Thompson SG, Deeks JJ, et al. 2003. Measuring inconsistency in meta-analyses. BMJ, 327:557–560. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Patsopoulos NA, Evangelou E, Ioannidis JP. Sensitivity of between-study heterogeneity in meta-analysis: proposed metrics and empirical evaluation. Int J Epidemiol 2008;37:1148–1157. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13. Carter YM, Mazeh H, Sippel RS, et al. Safety and feasibility of laparoscopic resection for large (≥6 cm) pheochromocytomas without suspected malignancy. Endocr Pract 2012;18:720–726. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 14. Perry KA, El Youssef R, Pham TH, et al. Laparoscopic adrenalectomy for large unilateral pheochromocytoma: experience in a large academic medical center. Surg Endosc 2010;24:1462–1467. [DOI] [PubMed] [Google Scholar]
- 15. Kercher KW, Novitsky YW, Park A, et al. Laparoscopic curative resection of pheochromocytomas. Ann Surg 2005;241:919–926; discussion 926–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16. Wilhelm SM, Prinz RA, Barbu AM, et al. Analysis of large versus small pheochromocytomas: operative approaches and patient outcomes. Surgery 2006;140:553–559; discussion 559–60. [DOI] [PubMed] [Google Scholar]
- 17. Toniato A, Boschin IM, Opocher G, et al. Is the laparoscopic adrenalectomy for pheochromocytoma the best treatment? Surgery 2007;141:723–727. [DOI] [PubMed] [Google Scholar]
- 18. Conzo G, Musella M, Corcione F, et al. Laparoscopic adrenalectomy, a safe procedure for pheochromocytoma. A retrospective review of clinical series. Int J Surg 2013;11:152–156. [DOI] [PubMed] [Google Scholar]
- 19. Chung HS, Kim MS, Yu HS, et al. Laparoscopic adrenalectomy using the lateral retroperitoneal approach: is it a safe and feasible treatment option for pheochromocytomas larger than 6 cm? Int J Urol 2018;25:414–419. [DOI] [PubMed] [Google Scholar]
- 20. Liu H, Li B, Yu X, et al. Perioperative management during laparoscopic resection of large pheochromocytomas: a single-institution retrospective study. J Surg Oncol 2018;118:709–715. [DOI] [PubMed] [Google Scholar]
- 21. Walz MK, Petersenn S, Koch JA, et al. Endoscopic treatment of large primary adrenal tumours. Br J Surg 2005;92:719–723. [DOI] [PubMed] [Google Scholar]
- 22. Flávio Rocha M, Faramarzi-Roques R, Tauzin-Fin P, et al. Laparoscopic surgery for pheochromocytoma. Eur Urol 2004;45:226–232. [DOI] [PubMed] [Google Scholar]
- 23. Shen WT, Sturgeon C, Clark OH, et al. Should pheochromocytoma size influence surgical approach? A comparison of 90 malignant and 60 benign pheochromocytomas. Surgery 2004;136:1129–1137. [DOI] [PubMed] [Google Scholar]
- 24. Kalady MF, McKinlay R, Olson JA, Jr., et al. Laparoscopic adrenalectomy for pheochromocytoma. A comparison to aldosteronoma and incidentaloma. Surg Endosc 2004;18:621–625. [DOI] [PubMed] [Google Scholar]
- 25. Gan L, Meng C, Li K, et al. Safety and effectiveness of minimally invasive adrenalectomy versus open adrenalectomy in patients with large adrenal tumors (≥5 cm): a meta-analysis and systematic review. Int J Surg 2022;104:106779. [DOI] [PubMed] [Google Scholar]
- 26. Inabnet WB, Pitre J, Bernard D, et al. Comparison of the hemodynamic parameters of open and laparoscopic adrenalectomy for pheochromocytoma. World J Surg 2000;24:574–578. [DOI] [PubMed] [Google Scholar]
- 27. Page MJ, McKenzie JE, Bossuyt PM, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. [DOI] [PMC free article] [PubMed] [Google Scholar]
Associated Data
This section collects any data citations, data availability statements, or supplementary materials included in this article.
Data Availability Statement
All data generated and analyzed during this study are included in this published article. The data presented in the article may be requested by consulting the correspondence author.