Laparoscopic Aspiration for Fat-Rich Renal Angiomyolipoma: A Retrospective Analysis of Chinese Patients at a Single-Institute

doi:10.21203/rs.3.rs-1498206/v1

Background: This retrospective analysis was aimed at evaluating the clinical data of patients with renal angiomyolipoma who were treated by laparoscopic aspiration in our institution and summarizing our experience of preliminary surgery at a single center.

Methods: We retrospectively analyzed clinical data of 13 female patients with renal angiomyolipoma who were admitted to and treated in Shengjing hospital from January 2016 to December 2019. We analyzed the patients’ preoperative, intraoperative, and postoperative data and performed renal function tests and CT during the follow-up.

Results: Postoperative pathologic tests revealed renal angiomyolipoma in all patients. Twelve patients were successfully treated with laparoscopic aspiration, while one underwent laparoscopic partial nephrectomy half-way due to the small amount of fat in the tumor. The average maximum tumor diameter was 4.4 cm (range: 1.6–9.8). The average operation duration, blood loss, and postoperative hospitalization duration were 112.2 minutes (range: 60–180), 104.6 ml (range: 10–200), and 6.2 days (range: 5–10), respectively. Preoperative and postoperative creatinine levels were below the upper limit of normal values, with the mean preoperative and postoperative creatinine levels were 0.56 mg/dl (range: 0.44–0.98) and 0.57 mg/dl (range: 0.46–0.95), respectively. No postoperative complications or recurrence occurred during the average follow-up of 27.1 months.

Conclusion: Our preliminary results indicate laparoscopic aspiration is safe, effective, and minimally invasive for treating renal angiomyolipoma, particularly for the rich-fat type.

Laparoscopic aspiration

Fat-rich

Renal angiomyolipoma

Zero ischemia

Laparoscopic aspiration is safe, effective, and minimally invasive for treating renal angiomyolipoma.

Renal angiomyolipoma is a common benign disease in urology. According to statistics, the probability of its occurrence in the population is approximately 0.13% [1]. Renal angiomyolipoma originates from the mesoderm renal mesenchymal tissue, which is a mature specific cell tissue, mainly composed of smooth muscle, adipose tissue, and blood vessels [2]. Because renal angiomyolipoma has no specific clinical manifestations, it was hard to detect in the past. However, with the development of medical imaging technology and increased awareness about health in general, the detection rate for renal angiomyolipoma is increasing gradually. Renal angiomyolipoma is mostly discovered accidently on color doppler ultrasound of the urinary system or abdominal CT during health checkups [3]. In most cases, renal angiomyolipomas do not become malignant; however, the large ones are at the risk of rupture and hemorrhage. The main symptoms of acute rupture and hemorrhage of renal angiomyolipoma are acute lumbar abdominal pain, abdominal tenderness, and intraperitoneal hemorrhage. In nearly 33% of the cases, the rupture and bleeding of renal angiomyolipomas result in hypovolemic shock [4-5], which may endanger life if not treated in a timely manner [6].

Renal angiomyolipomas with a maximum diameter of >4 cm or with the tendency to rupture and bleed or turn malignant can be treated with drugs or surgery. The International TSC Consensus Group recommends the use of mTOR inhibitors as the first-line treatment for renal angiomyolipomas ≥ 3 cm [7]. The surgical treatment of renal angiomyolipomas mainly includes partial nephrectomy, nephrectomy, selective renal artery embolization, microwave ablation (MWA), laparoscopic cryoablation, and radiofrequency ablation [8]. Since renal angiomyolipoma is a benign tumor, partial nephrectomy by laparotomy, laparoscopy, or robotic surgery is mainly performed [9-11]. Partial nephrectomy has great significance in maintaining renal function by preserving the nephron as much as possible.

Partial nephrectomy by laparotomy, laparoscopy, or robotic surgery are all associated with risks of hemorrhage and mortality. Traditional partial nephrectomy requires temporary closure of renal pedicle vessels during the operation. This inevitably results in renal ischemia and reperfusion injury, which could irreversibly damage renal function [12]. In addition, this operation involves suture of the surgical wound, which causes trauma to the normal kidney tissue and may even result in secondary bleeding. Therefore, we propose treatment by laparoscopic aspiration. Laparoscopic aspiration is a safe, effective, and minimally invasive surgical approach and has been previously used in the treatment for simple renal cysts. The feasibility of laparoscopic aspiration for central renal angiomyolipomas has been confirmed [13]. In this study, we retrospectively evaluated the clinical data of patients with renal angiomyolipoma who were treated by laparoscopic aspiration at a single center. We also assessed whether laparoscopic aspiration could have the advantages of affording minimal invasion, decreasing bleeding, and protecting renal function. Herein, we summarize our experience of preliminary surgery.

From January 2016 to December 2019, 13 women with a mean age of 49.2 years (range: 21–67) were diagnosed with renal angiomyolipoma and underwent laparoscopic aspiration in Shengjing Hospital affiliated to China Medical University. Relevant data were obtained from the hospital database with the consent of our institute's research and ethics committee. All patients voluntarily provided informed consent. Preoperative blood cell analysis, urinalysis, liver function test, renal function test, urological ultrasound, and computed tomography (CT) were performed for all patients. A typical Fat-Rich renal angiomyolipoma is depicted in Figure 1A-C. Indications for surgical intervention included a maximum tumor diameter of >4 cm (seven patients [54%]) and symptoms caused by renal angiomyolipoma (six patients [46%]). Six patients (46%) had tumors on the left, while seven (54%) had tumors on the right. Seven patients (54%) had tumors in the upper pole and six (46%) in the lower pole. Six patients with symptomatic renal angiomyolipoma complained of lumbar and abdominal discomfort, pain, and hematuria. The average maximum tumor diameter in these patients was 2.5 cm (range: 1.6–3.9). On the basis of CT findings, the mean maximum tumor diameter in the 13 patients was determined to be 4.4 cm (range: 1.6–9). The preoperative mean creatinine level was 0.56 mg/dL (range: 0.43–0.98; normal range: 0.59–1.04). Patients with bilateral and multiple renal angiomyolipomas were excluded. All patients denied a history of urinary surgery and were treated only for isolated renal angiomyolipomas.

Based on the patient's physical condition, preoperative examinations, and surgical experience of the surgeon, several alternative surgical methods were discussed with the patient. Finally, laparoscopic aspiration was performed on all the patients according to their choice. The patients were positioned in a healthy lateral position with a high waist pad. An incision of approximately 2 cm was made under the 12th rib at the posterior axillary line. The retroperitoneal cavity was pushed open using the index finger and a cavity was separated. A self-made inflatable balloon was placed into the separated extraperitoneal cavity. Pneumoperitoneum was maintained at 13-15 mm Hg (1 mm Hg = 0.133 kPa). Next, three trocars were placed below the costal margin at the axillary front, approximately 2 cm above the midaxillary iliac crest at the axillary front, and above the horizontal iliac crest at the axillary front. Gerota's fascia (Gerota's FAScia) was dissected cautiously to expose the renal artery to prevent renal hemorrhage and timely clamp the renal artery. Subsequently, the retroperitoneal fat was incised, and renal fat sac was separated by using ultrasonic knives. The adhesion between the tumor and surrounding tissue was intraoperatively explored to fully reveal the tumor, which had an obvious fat component(Fig.2a). To separate along the surface of tumor until the junction with the normal tissue of the kidney, the tumor capsule was incised with an ultrasonic knife. The suction device was then inserted into the tumor to completely aspirate the fat components(Fig.2b-c); Monopolar electrocoagulation using spray mode (U.S., Valley) and power of 100 W was used to fully stop bleeding on the wound at the base of the tumor(Fig.2d). Furthermore, the pressure of the pneumoperitoneum was reduced to confirm that there was no active bleeding on the wound, and biological glue and hemostatic gauze were applied. Complete blood routine and liver and kidney function tests were performed after surgery. When the drainage tube was successfully removed and the diet returned to normal, the patient was discharged. Renal function test and CT were performed at intervals of 3 months after discharge followed by every 6 months or 1 year.

Detailed patient demographics and perioperative data are presented in Table 1. Laparoscopic aspiration could not be completed in only one of the 13 patients due to the small fat content of the tumor, and the procedure was converted to laparoscopic partial nephrectomy during the operation. The remaining patients all underwent laparoscopic aspiration successfully. None of the patients required blood transfusions or showed complications. The average estimated blood loss was 104.6 mL (range, 10–200). The average retroperitoneal drainage volume was 301.5 mL (range, 5–890 mL). The average postoperative hospital stay was 6.2 days (range, 5–10 days). The average drainage tube placement time was 4.9 days (range, 3–8 days). Only one patient underwent conversion to laparoscopic partial nephrectomy during the operation, requiring transient clipping of the renal artery and a hot ischemia time of 16.3 min. Postoperative pathological assessments reported renal angiomyolipomas in all patients. We analyzed the imaging data of the patient who had undergone conversion to laparoscopic partial nephrectomy during surgery and found that the tumor in this patient contained less fat. The preoperative mean creatinine value of the 13 patients was 0.56 mg/dL (range, 0.44–0.98 mg/dL) and the postoperative mean creatinine value was 0.57 mg/dL (range, 0.46–0.95 mg/dL), and the differences was not statistically significant (P > 0.05). All patients were followed up for the renal function tests and CT examination. Creatinine was in the normal range, and no recurrence or metastasis was found. The mean follow-up time was 27.1 months (range, 14–54 months).

Table 1. Demographic and perioperative data of patients

Variable	Value
No. of patients	13
Age (years)	49.2±13.0
Height (m)	1.67±0.35
Weight (kg)	64.5±7.7
BMI (kg/m²)	23.1±2.9
Tumor location
Right/left	7/6
Upper/lower	7/6
Tumor size (cm)	4.4±2.6
Preoperative SCr level (mg/dL)	0.56±0.14
Operation time (min)	112.2±42.6
Aspiration time (min)	3.8±1.3
Conversion to NSS	1
WIT (min)	16.3
EBL (ml)	104.6±59.0
Drainage (ml)	301.5±258.4
Drainage days	4.9±1.4
Hospitalization days	6.2±1.3
Postoperative SCr level (mg/dL)	0.57±0.15
Complications	0
Recurrence	0
Follow-up duration (mo)	27.1±10.6

BMI, body mass index; EBL, estimated blood loss; SCr, serum creatinine; WIT, warm ischemia time

Table 2. A synopsis of published series on the treatment of RAML

Reference	Lin et al ^[3⁰^]	He et al^[3¹^]	Castle et al^[32]	Kara et al^[3³^]	Present
Treatment	SAE	LPN	RFA	RPN	L-Aspiration
No. of patients	45	15	15	53	13
Age（yrs）	38.6 ±12.5	41.6 ± 10.3	56.7(31-81)	54.1±13	49.2±13.0
Tumor size（cm）	10.7±6.2	7.8 ± 2.8	2.6 (1-3.7)	2.8(1.8-4.6)	4.4±2.6
Pre-SCr(mg/dL)	0.82±0.15	0.53 ± 0.77	NS	0.93±0.22	0.56±0.14
Post-SCr(mg/dL)	0.84±0.17	0.56 ± 0.73	NS	0.85±0.22	0.57±0.15
Operative time(min)	60(60-120)	101 ± 15	NS	169.1±68.8	112.±42.6
WIT(min)	NA	28 ± 5	NS	17.5(14.2-20.1)	16.3
EBL(ml)	NA	311 ± 217	NS	198±194	104.6±59.0
Hospitalization(d)	NA	4.7 ± 1.1	NS	3±1.3	6.2±1.3
Follow-up days(mo)	14(6.5-40.5)	24.1 ± 13.2	21.2(1.3-71.7)	7 (1–17)	27.1±10.6
Complication	NS	1	4	8	0
Recurrence	NS	0	0	0	0

NS, non-significant; SAE, selective arterial embolization; LPN, laparoscopic partial nephrectomy; RFA, radiofrequency ablation; RPN, robotic partial nephrectomy

Renal angiomyolipoma was first defined and discovered by Fischer in 1911 [14], accounting for 0.44% of solid renal tumors with a male:female incidence of 2:1 [15]. Renal angiomyolipomas are divided into simple sporadic and hereditary, of which hereditary disease is generally associated with tuberous sclerosis or lymphangioleiomyomatosis. Approximately 10% of renal angiomyolipoma patients with tuberous sclerosis [16] have genes located in tuberous sclerosis 1 (TSC1) and tuberous sclerosis 2 (TSC2) [17]. Renal angiomyolipoma with tuberous sclerosis shows multiple, bilateral, larger, and younger features. The typical clinical symptoms are facial sebaceous tumors, refractory epilepsy, and mental retardation. Most single renal angiomyolipomas are non-heritage, with a diameter of <4 cm and no clinical symptoms. Conservative observation is recommended, but there is currently no standard monitoring plan. We generally recommend that patients undergo imaging examinations such as color ultrasound or CT at 6-month intervals [18]. When the mass grows rapidly and presents the risk of rupture and bleeding, surgical treatment is recommended. The risk of mass rupture and bleeding may be closely related to mass diameter and female hormone secretion. The typical triple sign is lumbago, hematuria, and mass, which may be accompanied by other symptoms such as fever, nausea, vomiting, shock, hypertension, renal insufficiency, and anemia. For renal angiomyolipomas with a large diameter, early intervention is recommended.

The gold standard for renal angiomyolipoma is pathological examination, but the puncture biopsy process may cause the tumor to rupture and hemorrhage, so it is rarely used clinically. At present, the main examination methods are color Doppler ultrasound, CT, and MRI. Since renal angiomyolipomas mostly contain adipose tissue, their imaging manifestations are different from those of renal cell carcinoma. Ultrasonography is easy to perform and does not require radiation; it is often used as an important technique for preliminary screening and follow-up. Color ultrasound of renal angiomyolipomas showed that a large difference in acoustic resistance and the acoustic beam could produce strong echo reflections among substances with a large acoustic resistance difference, while renal cell carcinoma showed hypoechogenicity due to the small difference in acoustic resistance between the masses. CT enhancement is the most frequently used imaging method for renal angiomyolipomas. The vascular and smooth muscle components were significantly enhanced under enhancement CT scanning, while fat showed an extremely low-density shadow, generally <10–20HU. Therefore, in comparison with color Doppler ultrasound, CT has higher sensitivity and specificity. MRI shows higher resolution of small amounts of fat than ultrasound or CT. T1-weighted imaging shows a high signal and T2-weighted imaging shows a low signal, reflecting the internal structure of the tumor more sensitively.

The clinical classification of renal angiomyolipomas is mainly based on their size and symptoms. On the basis of their maximum diameter, the tumors are categorized into <4 cm and ≥4 cm; for cases with maximum tumor diameter ≥4 cm or obvious clinical symptoms, surgical intervention is recommended as the first choice. Song et al. [20] divided renal angiomyolipomas into three types according to their fat content: fat-rich, fat-poor, or fat-invisible. The fat content is the largest in the fat-rich renal angiomyolipoma and the least in the fat-invisible. Nearly 5% of renal angiomyolipomas cannot be identified by CT and MRI due to the lack of fat [21-22]. The fat CT attenuation of fat-rich renal angiomyolipoma is generally ≤-10 HU [20]; the CT attenuation of invisible renal hamartomas is >10 HU; their signal intensity index (SII) is ≤16.5%; and the ratio of mass to spleen (TSR) is ≥0.71 [20]; in contrast, the CT attenuation of lipid-poor renal angiomyolipomas is >-10 HU, TSR is <0.71, and SII is >16.5% [20]. The reasons why I specifically describe the classification of renal angiomyolipoma in imaging are as follows: (1) There is no significant difference between the imaging findings of some fat-invisible and fatty-poor renal angiomyolipomas and renal cell carcinoma. It may be necessary for experienced clinicians to determine the scope of surgical resection according to the shape of the tumor and the frozen pathological return. (2) We found that laparoscopic aspiration of fat-rich renal angiomyolipomas proceeded very smoothly; however, some fat-poor renal angiomyolipomas did not even require aspiration.

At present, there are few articles on the application of laparoscopic aspiration in the treatment of renal angiomyolipoma. Xu et al. [13] reported 10 cases of central renal angiomyolipoma treated by laparoscopic aspiration, and the operation process was smooth. We believe that the renal angiomyolipomas of these 10 patients may have been fat-rich renal hamartomas. Laparoscopic aspiration for renal angiomyolipomas is still a relatively novel technique. We hope to evaluate patient imaging data in detail before surgery to clarify the type of fat distribution and thereby determine the appropriate surgical target.

Although renal angiomyolipomas are benign tumors and grow slowly, we believe that timely surgical intervention is needed when the diameter of the tumor is ≥4 cm or symptoms such as pain and bleeding occur. Since renal angiomyolipomas are benign tumors, surgical intervention is performed to protect renal function as much as possible based on the approach of solving the patient's clinical symptoms and preventing rupture and bleeding. At present, the most frequently used surgical intervention is selective renal artery embolization [23]. However, some patients may show phenomena such as fever, nausea, pain, and renal infarction after selective renal artery embolization [24, 25, 26]. Moreover, embolization is associated with a high postoperative recurrence rate [26, 27]. With the advancements in surgical technology and equipment, the curative effect of partial nephrectomy has been gradually recognized. Liu et al [28] studied 35 patients treated with RLNSS, and their results showed that RLNSS was technically feasible and safe, and renal function was largely preserved. Traditional partial nephrectomy needs to block the renal pedicle, so it is difficult to avoid affecting renal function. Mic [29] et al found that renal function decreased by about 20% on average after partial nephrectomy. The most important factor affecting renal function in LPN is renal ischemia-reperfusion. The longer the warm ischemia time of the kidneys, the greater the effect on renal function and even irreversible damage. In this context, we continue to explore whether the operation can be made even less invasive. We have noticed that the suction device can suck fat in urinary tract surgery, and there is rich clinical experience for the application of a laparoscopic aspiration technique to simple renal cysts. Therefore, we proposed the application of laparoscopic aspiration in the treatment of renal angiomyolipomas.

Xu et al [13] reported that during laparoscopic aspiration for central renal angiomyolipomas, due to the special location of the renal hilum, partial nephrectomy under traditional laparoscopic surgery may easily damage the kidney collection system, and laparoscopic aspiration can achieve good results without damaging the normal renal parenchyma. Traditional partial nephrectomy temporarily clamps the renal artery, and reconstruction of the renal parenchyma with suture lines is also harmful to renal function to some extent. In contrast, laparoscopic aspiration of renal angiomyolipomas performed by our research center is performed without clamping the renal artery and without suture reconstruction, yielding zero ischemia in a sense. This finding has important clinical significance for patients with isolated renal insufficiency. Due to the unique histological characteristics of renal angiomyolipomas, there is a layer of mesh with fibrous tissue between the part of the tumor that protrudes into the renal parenchyma and the renal parenchyma, which is generally free of blood vessels. The external attractor in this area absorbs the tumor completely, reducing the contact with renal parenchyma and the risk of intraoperative bleeding. Although the renal artery was not blocked by this method, it was routinely free to be blocked if necessary. One patient in this group was unable to undergo aspiration of the mass intraoperatively with an aspirator and subsequently underwent laparoscopic partial nephrectomy. The postoperative imaging data showed that the patient had a fat-poor renal angiomyolipoma. We think that the effects of this technique are better in fat-rich renal angiomyolipomas, so we emphasize the need to carefully evaluate the imaging data of patients before the operation. The other patients successfully completed laparoscopic aspiration. The creatinine value of all patients was in the normal range without complications. We suggest that laparoscopic aspiration should be considered for fat-rich renal angiomyolipomas with a maximum diameter of ≥4 cm and clinical symptoms such as pain and bleeding. We found that the use of monopolar electrocoagulation and biological hemostatic agents can achieve sufficient hemostasis of the wound and avoid the renal function damage caused by suturing of the wound. In comparison with traditional techniques, laparoscopic aspiration for renal angiomyolipoma is more minimally invasive. The postoperative bedtime is shorter, recovery is faster, and effect on renal function is the least.

In table 2, laparoscopic aspiration has been compared with other surgical methods, including SAE, LPN, RFA, and RPN. We found that laparoscopic aspiration shows less bleeding, fewer complications, and better protection of renal function. Only one patient in this group required temporary clamping the renal artery, which may cause a warm ischemic injury; none of the patients needed suturing of the wound, which can affect normal renal parenchymal function; in addition, during the long-term follow-up, no recurrence or metastasis was found. Laparoscopic aspiration offers more advantages, especially for patients with renal insufficiency and isolated kidney. However, our study also has some limitations, including its retrospective and single-center nature, the low patient number, and the limited follow-up time. We hope that this technology can be popularized in more institutions, allowing exploration of its possible problems, further improving the technology, and benefitting more patients.

Laparoscopic aspiration can achieve zero ischemia to some extent. Due to its surgical characteristics of not requiring temporary clipping of the renal artery or suturing of the wound surface, laparoscopic aspiration has an extremely good therapeutic effect for such cases of renal insufficiency and solitary kidney. We believe that it is an alternative treatment for renal angiomyolipoma.

NS, non-significant; SAE, selective arterial embolization; LPN, laparoscopic partial nephrectomy; RFA, radiofrequency ablation; RPN, robotic partial nephrectomy

ACKNOWLEDGEMENTS

Not applicable.

AUTHORS’CONTRIBUTIONS

(I) Conception and design: B Yin; (II) Administrative support: B Yin; (III) Provision of study materials or patients: B Yin, J Xie; (IV)Collection and assembly of data: J Xie, G Luo; (V) Data analysis and interpretation: X Wang, J Li; (VI) Manuscript writing: All authors; (VII) Final approval of manuscript: All authors.

FUNDING

345 Talent Project of Shengjing Hospital of China Medical University.

AVAILABILITY OF DATA AND MATERIALS

The datasets used and analyzed during the current study available from the corresponding author on reasonable request.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

The study was approved by the Ethics Committee and IRB of Shengjing Hospital of China Medical University. Healthcare providers’ informed consent was provided on the electronic survey before data collection. The study was conducted in accordance with the Declaration of Helsinki (as revised in 2013). Informed consent was not required since this was a retrospective study and all data with personal identifiers were kept confidential.

CONSENT FOR PUBLICATION

Not applicable.

COMPETING INTERESTS

The author declares that there is no competing interest.

CONTRIBUTOR INFORMATION

Jianwei Xie, Email: [email protected].

Bo Yin*, Email: [email protected].

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No competing interests reported.

Laparoscopic Aspiration for Fat-Rich Renal Angiomyolipoma: A Retrospective Analysis of Chinese Patients at a Single-Institute

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Abstract

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Version 1