UNCLASSIFIED Long-Term Results of Laparoscopic Partial Versus Total Adrenalectomy for Aldosterone Producing Adenoma Jianhu Liu3,1#, Xuedong Wei1#, Chenchao Fu1,Qiaoxing Li3, Jianquan Hou1, Jinxing Lv2*, Yuhua Huang1* Purpose: Laparoscopy surgery is the gold standard for the treatment of aldosterone-producing adenomas (APA). However, the effectiveness between laparoscopic total and partial adrenalectomy is controversial. Therefore, we retrospectively analyzed the postoperative and follow-up outcomes of these two procedures. Materials and Methods: A total of 96 APA patients underwent laparoscopic surgery in our hospital between Jan- uary 2012 and December 2017. A total of 65 patients who underwent laparoscopic partial adrenalectomy (group 1) were compared with 31 patients who underwent laparoscopic total adrenalectomy (group 2). The mean follow-up time was 32.3 months and 40.8 months, respectively. Patient’s preoperative characteristics, date during surgery, and postoperative clinical results of the two groups were analyzed. Results: In both groups of patients, laparoscopic adrenalectomy was successfully carried out. The laparoscopic partial adrenalectomy group had a shorter operation time when compared to total adrenalectomy (P = .01). How- ever, patients in the laparoscopic total adrenalectomy group were older (P = .04) and had a higher proportion of multiple adenomas (P = .01) compared to partial adrenalectomy. Five patients (7.7%) who underwent partial ad- renalectomy did not show improvement in hypertension and/or serum potassium below normal levels, and review of plasma aldosterone concentration (PAC) and/or computerized tomography (CT) indicated that surgery was not successful in these patients. All 31 patients who underwent total adrenalectomy showed improvement or recovery from hypertension, and all PAC and serum potassium levels returned to normal levels after surgery. Conclusion: Although both surgical procedures were technically safe and feasible, laparoscopic partial adrenalec- tomy showed a higher failure rate (7.7%) for patients with APA. Therefore, choosing laparoscopic partial adrenal- ectomy requires careful consideration, and we selected laparoscopic total adrenalectomy in patients with unilateral APA. Keywords: adrenalectomy; aldosterone producing adenoma; hyperaldosteronism; laparoscopy; partial INTRODUCTION Primary aldosteronism (PA), described for the first time in 1955 by Conn el al., is characterized by ex- cessive aldosterone secretion, and leads to secondary hypertension, hypokalemia, hypervolemia, and met- abolic alkalosis. (1) PA accounts for ~10% of patients with hypertension, which is the most common cause of secondary hypertension.(2) Clinical subtypes of PA include aldosterone producing adenoma (APA), unilat- eral adrenal hyperplasia (UAH), and idiopathic aldos- teronism (IHA).(3) Laparoscopic adrenalectomy is the preferred treatment for APA or UAH. In case of IAH, medical treatment for mineralocorticoid receptor antag- onist (MRA) is recommended.(2) The advantage of partial adrenalectomy is that it retains 1. Department of Urology, the First Affiliate Hospital of Soochow University, No.188 Shizi Street, Suzhou 215006, China. 2. Reproductive Medicine Center, The First Affiliated Hospital of Soochow University, No.188 Shizi Street, Suzhou 215006, China 3. Department of Urology, Affiliated Kunshan Hospital of Jiangsu University, No.91 Qianjin West Road, Suzhou 215300, China # These authors contributed equally to this work. *Correspondence: Department of Urology, the First Affiliate Hospital of Soochow University, No.188 Shizi Street, Suzhou 215006, China. Tel: +8618913752992; Fax: +8651265221447; E-mail: hyhsdfyy@163.com. *Reproductive Medicine Center, The First Affiliated Hospital of Soochow University, No.188 Shizi Street, Suzhou 215006, China. Tel:18118158998; Fax: +8651265221447; E-mail: ljxsdfyy@163.com Received December 2018 & Accepted April 2019 January 2020 a portion of the adrenal gland on the affected side. This surgical procedure is minimal for adrenal function im- pairment. If the other adrenal gland develops a lesion, it can provide an opportunity for reoperation. The 2014 Chinese Urological Association(CUA) guidelines rec- ommend laparoscopic adrenalectomy for APA, thereby retaining adrenal tissue as much as possible. In recent years, several studies have shown that laparoscopic total adrenalectomy has clear beneficial effects on the treatment of APA. Unilateral adrenalectomy abolished aldosterone hypersecretion and hypokalemia in most patients with unilateral aldosterone hypersecretion. (4) Hennings et al. confirmed that after long-term fol- low-up, unilateral total adrenalectomy had a significant effect on the treatment of APA.(5) However, few reports Urology Journal/Vol 17 No. 4/ July-August 2020/ pp. 402-407. [DOI: 10.22037/uj.v0i0.4981 ] supported partial adrenalectomy of APA. Our objective was to assess the safety, feasibility, and efficacy of lap- aroscopic partial versus total adrenalectomy in patients with APA. PATIENTS AND METHODS Study Population A total of 96 patients who underwent laparoscopic partial adrenalectomy or laparoscopic total adrenalec- tomy for APA were retrospectively analyzed between January 2012 and December 2017. This retrospective study was approved by the ethics committee of the First Affiliated Hospital of Soochow University (Clinical trial identifier: 2011045). The APA procedure includ- ed the following diagnostic steps:(1) All patients had hypokalemia, persistent hypertension, and biochemical evidence of hyperaldosteronism. Biochemical evidence of hyperaldosteronism was defined as a plasma aldos- terone concentration (PAC) ≥ 20 ng/dL, and a plasma aldosterone-plasma renin activity ratio (ARR) ≥ 40 ng/ dL/ng/mL/h.(2) All patients underwent computerized tomography (CT) preoperatively. CT confirmed that all patients had unilateral adrenal adenomas, and in pa- tients with UAH, adenomas in the bilateral adrenals or IHA were excluded from the study. Procedures All patients underwent retroperitoneal laparoscopic adrenalectomy. A total of 65 out of 96 APA patients underwent laparoscopic partial adrenalectomy. The criteria for partial adrenalectomy included a single adenoma at the surface or in the lateral branch of the adrenal gland associated with lots of normal adrenal tis- sue. Laparoscopic partial adrenalectomy was executed by approaching the tumor directly without controlling the adrenal vessels. Laparoscopic partial adrenalectomy required complete resection of the tumor and normal adrenal tissue 5mm away from the tumor. In general, hem-o-lok clips were used to control bleeding from the adrenal incision. If a single adenoma tumor was present in the middle of the adrenal gland, laparoscopic total adrenalectomy was performed. In our study, 4 individ- ual surgeons performed laparoscopic adrenalectomy, whereas one surgeon performed total adrenalectomy for all APA patients. Laparoscopic unilateral total adre- nalectomy was performed in 31 out of 96 APA patients, and involved complete removal of the adrenal gland by double ligation of the central adrenal vein using hem- o-lok clips. Evaluations In this study, differences in patient characteristics of preoperative, operative time, and intraoperative blood loss were compared between the two groups. Postoper- ative follow-up included blood pressure recording, se- rum potassium levels, PAC and imaging date. Normal blood pressure without treatment was defined as hyper- tension cure, and the achievement of a normal blood pressure using fewer drugs than before adrenalectomy was defined as an improvement. in the laparoscopic partial adrenalectomy group, the mean postoperative follow-up time was 32.3 months, whereas in the lapa- roscopic total adrenalectomy group, the follow-up time was 40.8 months. Statistical Analysis Statistical analyses were performed using SPSS® ver- sion 20.0 software. Numeric data of a normal distribu- tion was expressed as the mean ± standard deviation (x ± SD) and were analyzed using the Student’s t test. Pearson’s chi-square test was used to compare categor- Table 1. Clinical characteristics of 96 patients with APA. Laparoscopic partial adrenalectomy (n = 65) Laparoscopic total adrenalectomy (n =31 ) P Age (years) 48.27 ± 11.47 56.42 ± 16.42 .04 Male / female 22 / 43 12 / 19 .64 Tumor site (Left / Right) 38 / 27 18 / 13 .97 Tumor diameter (cm) 1.86 ± 0.65 1.96 ± 0.96 .67 Blood pressure (mmHg) Systolic BP 166.52 ± 24.04 174.00 ± 36.06 .37 Diastolic BP 101.00 ± 14.12 100.75 ± 21.44 .96 Serum potassium (mmol/L) 2.55 ± 0.72 2.37 ± 0.63 .42 PAC (ng/dL) 26.65 ± 6.89 27.29 ± 7.60 .75 ARR (ng/dL/ng/mL/h) 249.16 ± 192.42 237.58 ± 259 .05 .87 Follow-up time (months) 32.32 ± 19.04 40.81±28.09 .18 Data are expressed as the mean ± SD. Abbreviations: BP, blood pressure; Serum K+ normal value 3.5–5.5 mmol/L; APA, aldosterone-producing adenoma; PAC; plasma aldosterone concentration; PAC normal value 0.7–15 ng/dL; ARR: plasma aldosterone concentration to renin activity ratio. Laparoscopic partial adrenalectomy (n = 65) Laparoscopic total adrenalectomy (n = 31) P Operative time (minutes) 76.16 ± 25.82 105.33 ± 29.60 .01 Blood loss (mL) 60.54 ± 51.91 69.55 ± 66.20 .62 Multiple adenomas (n) 0 (0%) 6 (19.4%) .01 Cured hypertension (n) 37 (56.9%) 17 (54.8%) .85 Improved hypertension (n) 23 (35.4%) 14 (45.2%) .36 No improved hypertension (n) 5 (7.7%) 0 (0%) .17 Hypokalaemia (n) 3 (4.6%) 0 (0%) .55 No improvement of PA (n) 5 (7.7%) 0 (0%) .27 Data are expressed as the mean ± SD or percentage in parentheses. Serum K+ normal value 3.5– 5.5 mmol/L; PA, primary aldosteronism. Table 2. Postoperative and follow-up outcomes when comparing laparoscopic total versus partial adrenalectomy. Laparoscopic partial vs. total adrenalectomy for APA-Liu et al. Vol 17 No 04 July-August 2020 403 ical data. P < .05 was considered statistically signifi- cant. RESULTS In our study, 96 patients were diagnosed with APA. Among these, a total of 65 patients underwent partial adrenalectomy and 31 patients underwent total adre- nalectomy. Clinical characteristics of APA patients are presented in Table 1. No statistical significant differ- ences were observed in gender, tumor site, size of the APA at imaging techniques, preoperative blood pres- sure levels, serum potassium levels, PAC, ARR, and follow-up time between the 2 groups. Statistical differ- ences were observed in patients’ age (P = .04). Table 2 lists surgical and follow-up results of patients in both groups. Statistical significant differences were observed in operative time (P = .01) and number of multiple adenomas (P = .01) between the 2 groups. All laparoscopic procedures were successfully performed without conversion to open operations. None of the study subjects showed major intraoperative or postop- erative complications, such as injury of adjacent organs or major vessels and long-term supplementation of cor- tisol. During follow-up, all patients in the laparoscopic total adrenalectomy group showed cure or improvement of hypertension. No patients required potassium supple- mentation, and plasma aldosterone levels returned to normal levels after surgery. However, in 5 out of 65 patients who underwent laparoscopic partial adrenalec- tomy, the clinical symptoms of PA failed to improve. None of the 5 patients had improved hypertension, and 3 out of these 5 patients remained hypokalemic and re- quired potassium supplementation. However, the dif- ference in failure of PA between the two groups was not statistically significant. Nevertheless; the failure rate of PA of the laparoscopic partial adrenalectomy group was as high as 7.7%, which was unacceptably high. Table 3 shows the no improvement of PA in 5 APA patients who underwent laparoscopic partial adrenal- ectomy. These 5 patients remained hypertensive and showed a high PAC after laparoscopic partial adrenal- ectomy. Moreover, in 3 of 5 patients, serum potassium levels were not normalized after surgery. Furthermore, 2 of 5 patients were followed up with CT, which con- firmed tumor recurrence (Figures 1, 2). The other 3 patients refused to undergo CT. It is worth mentioning that in a patient it was found that the PAC was 15.21 ng/ dL during follow-up, and the plasma aldosterone levels was 12.59 ng/dL ( > 10 ng/dL) after the saline infusion test.(6) Survival analysis showed no statistically signif- icant difference in postoperative relapse-free survival between the two groups (P = .079) (Figure 3). DISCUSSION The purpose of this report was to compare the postop- erative and follow-up outcomes in 2 groups of APA patients who underwent either laparoscopic partial or total adrenalectomy. With advances in surgical tech- niques, laparoscopic adrenalectomy has gradually be- come the gold standard for the treatment of unilateral PA.(7-9) However, the method used to cure APA is still controversial, namely laparoscopic partial or total ad- renalectomy. Laparoscopic partial vs. total adrenalectomy for APA-Liu et al. Table 3. No improvement of primary aldosteronism in 5 aldosterone-producing adenoma patients who underwent laparoscopic partial adrenalectomy. Blood pressure Serum potassium levels PAC and others Case 1 Remained hypertensive 3.0 mmol/L at one month after surgery; 2.21 mmol/L at CT confirmed tumor recurrence (FIG. 1). 12 months after surgery; continuous oral potassium The PAC was 25.7 ng/dL after 36 months of follow-up. supplementation. Case 2 Remained hypertensive 2.9 mmol/L at one month after surgery; CT confirmed tumor recurrence (FIG. 2). continuous oral potassium supplementation. The PAC was 15.21 ng/dL after 22 months of follow-up. The PAC after the saline perfusion test was 12.59 ng/dL ( >10 ng/dL). Case 3 Remained hypertensive Normal serum potassium. The PAC was 20.44 ng/dL after 30 months of follow-up. Case 4 Remained hypertensive 3.2 mmol/L at one month after surgery; continuous oral The PAC was 18.74 ng/dL after 15 months of follow-up. potassium supplementation. Case 5 Remained hypertensive Normal serum potassium. The PAC was 21.01 ng/dL after 64 months of follow-up. PAC, plasma aldosterone concentration; PAC normal value 0.7– 15 ng/dL. Figure 1. A. Preoperative computerized tomography (CT) demonstrates unilateral single aldosterone-producing adenoma (APA) (arrow). B. Pathological results of the postoperative specimen confirmed as adenoma. C. 13 months after surgery, CT showed postoperative tumor recurrence (arrow). Unclassified 404 Chen et al. reported that the mean operative time for total adrenalectomy in 47 patients with PA was 103.5 minutes, which is almost consistent with the mean op- erative time determined in our study (105.33 minutes). However, our findings showed that the time for partial adrenalectomy was shorter compared to the time re- ported in their study (76.16 vs 95.9 minutes).(10) In our study, partial adrenalectomy was performed in younger patients. Probably, the surgeon considered partial adre- nalectomy for younger patients to retain more adrenal function. However, if older patients have recurrenc- es after surgery, reoperation may be difficult due to physical conditions. So this may be the reason for the difference in age between the two groups. In addition, both surgical procedures were safe, no significant dif- ferences were observed in postoperative recovery, and no major complications occurred intraoperatively or postoperatively.(7,11,12) There are controversies between the two surgical methods. The main reason is that laparoscopic partial adrenalectomy has the advantage of retaining part of the ipsilateral adrenal tissue. However, it also has the disadvantage that the tumor may not be completely re- moved and residual microadenomas may remain after surgery. Chen,(10) Fu,(11) and Al-Sobhi(13) et al. reported the results of 16 and 104 laparoscopic partial adrenal- ectomies. The average follow-up time was 1 year and 8 years, respectively. None of the patients in their studies had recurrent PA and retained more normal ipsilateral adrenal tissue. In addition, none of the patients’ serum cortisol levels were reduced and no exogenous steroid replacement therapy was required after surgery. How- ever, reports on postoperative recurrence of patients with laparoscopic partial adrenalectomy are available. Ishidoya et al. reported that postoperative hypertension and hyperaldosteronism did not improve in 2 out of 29 patients who underwent laparoscopic partial adrenal- ectomy.(14) We performed 65 laparoscopic partial adre- nalectomies and experienced 5 cases that did not show improvement of PA after surgery. In 2 of these 5 cases postoperative tumor recurrence was confirmed by CT. In some reports on adrenalectomy in patients with uni- lateral PA, unilateral single APA was confirmed to ac- count for only 26%-46% by the postoperative patholog- ical results.(5,15,16) Although patients were diagnosed by high resolution CT and adrenal vein sampling (AVS) before surgery as unilateral single APA, the postopera- tive pathological results showed that some patients had multiple adenomas/nodules.(11,12) Wiel et al. reported that small adrenal gland micro-nodules were frequently ignored by routine histopathology.(17) Using hematox- ylin and eosin (HE)-stained sections combined with ex-vivo MRI, macroscopic sections, the pathologist morphologically classified 12 of 15 adrenals as multi- nodular. In general, partial adrenalectomy may not com- pletely remove microadenomas. Residual microadeno- mas, which secrete aldosterone may cause PA to fail or recur. In our study, 6 out of 31 patients that underwent total adrenalectomy were pathologically confirmed as multiple adenomas after surgery. Although all patients that underwent partial adrenalectomy were confirmed as APA before and after surgery, 5 out of 65 patients did not improve or relapse, which might confirm the above viewpoint. Laparoscopic total adrenalectomy is safe and feasible for most adrenal diseases.(18) It has fewer perioperative complications and rare postoperative mortality.(19,20) In our study, patients who underwent laparoscopic total and partial adrenalectomy did not require cortisol sup- plementation therapy after surgery. In the partial adre- nalectomy group, a total of 5 patients did not achieve improvement of APA, however, all patients in the total adrenalectomy group were cured. No significant differ- ences were observed in surgical outcome between the Figure 2. A. Preoperative computerized tomography (CT) demonstrates unilateral single aldosterone-producing adenoma (APA) (arrow). B. Pathological results of the postoperative specimen confirmed as adenoma. C. 14 months after surgery, CT showed postoperative tumor recurrence (arrow). Figure 3. Survival analysis: Comparison of relapse-free survival in postoperative follow-up between the two groups. Notes: Survival analysis showed no statistically significant differ- ence in postoperative relapse-free survival between the two groups (P = .079) Laparoscopic partial vs. total adrenalectomy for APA-Liu et al. Vol 17 No 04 July-August 2020 405 two groups, however total adrenalectomy prevented ipsilateral recurrence due to partial adenoma remnants. Although survival analysis showed no statistically sig- nificant difference in postoperative relapse-free surviv- al between the two groups (P > .05), the P value was close to a significant level. If the follow-up time is prolonged and the number of cases are increased, there may be statistically significant differences in postoper- ative recurrence between the two groups. Our study has several limitations. First, our study is a retrospective study, and the decision criteria for partial or total adrenalectomy procedure were not randomized. Preoperatively, our patients were not selected for AVS, and underwent a CT scan, which might have resulted in diagnostic bias. AVS is an invasive procedure, and if the preoperative imaging scans confirmed unilateral adrenal masses, AVS was not always necessary.(21-22) In our study, we have fewer cases of laparoscopic total ad- renalectomy and in both total adrenalectomy and partial adrenalectomy, the follow-up time was relatively short. In future studies, we will increase the number of cases and extend the follow-up time. CONCLUSIONS This study showed that laparoscopic partial and total ad- renalectomy are technically safe and feasible. 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Laparoscopic partial vs. total adrenalectomy for APA-Liu et al.