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Original article
Abstract
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 1
Laparoscopic enucleation of renal masses. González-León T., et al.
Resumen
Introduction
Renal carcinoma (RC) represents 2% of the complete organ, has progressively changed sin-
diagnoses and deaths from malignant tumors ce 1980 when partial nephrectomy (PN) began
in adults. This incidence has increased in the to show excellent results as far as survival and
past years. Approximately 75% are diagnosed in recurrence, particularly in ≤4 cm tumors, but
patients over 60 years of age and are more fre- indicated even for ≥7 cm tumors.(3)
quent in males.(1,2) Compared to radical nephrectomy (RN),
The classic treatment for renal masses re- PN is associated with a marked reduction of the
gardless their size, consisting of removing the incidence of chronic kidney disease (CKD) and
2 Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14.
Laparoscopic enucleation of renal masses. González-León T., et al.
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 3
Laparoscopic enucleation of renal masses. González-León T., et al.
Statistical Analysis
The SPSS program, version 23.0 was utilized. Frequencies and percentages were estimated for qua-
litative variables; means and SD for quantitative variables. Student´s t-test was used to compare pre
and postoperative creatinine (p<0.05), and the Kaplan Meier curve for survival.
Ethical Considerations
This research is part of a Project approved by the CNCMA Institution Review Board and Ethical
Review Board. The ethical principles of the Declaration of Helsinki for Medical Research with
human beings were followed.(8)
Results
Laparoscopic TE has increased since it was introduced at the CNCMA, in 2010 (Figure 1).
Mean age was 58.0 years (±11.1 years). Most were male patients (60.0%). 73.2% of renal masses
were diagnosed incidentally. Physical status classification ASA II and ECOG 0 or I were the most
frequent (69.0%, 54.9%, 42.3%, respectively). 87.3% of the patients had comorbidities; arterial
4 Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14.
Laparoscopic enucleation of renal masses. González-León T., et al.
hypertension was the most frequent. Mean tumor size was 33.6 mm. cT1a clinical stage, in co-
rrespondence with renal masses ≤4 cm and most masses were of low surgical complexity (64.8%).
Mean R.E.N.A.L score was 6.1 (Table 1).
Variables Results
Mean SD
Age (years) 58.0 ±11.1
Tumor size (mm) 33.6 ±12.07
R.E.N.A.L. score 6.1 ±1.9
Preoperative Creatinine (mmol/L) 92.4 ±20.8
No. %
Males 43 60.6
Comorbidities 62 87.3
ASA II 49 69.0
ECOG 0/I 39/30 54.9/42.3
Incidental Diagnosis 52 73.2
Surgical Complexity (low/moderate) 46/16 64.8/22.5
cT1a/cT1b N0 M0 46/23 64.8/32.4
Hand-assisted laparoscopic approach without warm ischemia (WI) was used in most patients
(92.9%), one required conversion to open surgery and 5.6% needed surgical reintervention, which
was performed by laparoscopic surgery. Other perioperative outcomes are presented in Table 2.
Six patients had renal function damage estimated by their preoperative level of creatinine and
increased to seven postoperatively (measure at the end of the study). Mean postoperative crea-
tinine was 97.6 mmol/l vs 92.4 mmol/l preoperatively, but this difference was not statistically
significant (p=0.082) (Table 3).
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 5
Laparoscopic enucleation of renal masses. González-León T., et al.
Postoperative
Elevated Normal Total
Creatinine
No. % No. % No. %
Elevated 3 50.0 3 50.0 6 100
Preop
Normal 4 6.2 61 93.8 65 100
Total 7 9.9 64 90.1 71 100
Perioperative Mean SD Difference t p
Preoperative 92.4 20.8
-5.2 -1.776 0.082
Postoperative 97.6 28.0
16% of the patients presented complications, most postoperatively (14.0%). Bleeding prevailed
(8.4%), resolved with medical measures in two patients (grade II); two others required laparos-
copic exploration (one underwent RN, also by laparoscopy) and admittance in the intensive care
unit (grade IV); and in two others that presented vascular lesions (a pseudoaneurysm and an arte-
riovenous fistula), the solution was selective arterial renal embolization (SRAE) (grade IIIb). One
patient required laparoscopic exploration for prolonged paralytic ileus and was also admitted in the
intensive care unit (grade IV). Reintervention was performed in an obese patient for eventration at
the hand-assistance port (grade IIIb) (Table 4).
6 Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14.
Laparoscopic enucleation of renal masses. González-León T., et al.
Malignant tumors were more frequent (71.8%) and 52.1% classified as clear-cell renal carcino-
ma (ccCR). Stage pT1a prevailed (74.8%); overall survival (OS) and cancer specific survival (CSS)
at one and five year was 100%, respectively, and recurrence-free survival decreased at five years
because two patients recurred with malignant tumors in the same renal unit. They underwent RN
by the laparoscopic approach. Mean time follow-up was 7.4 years (Table 5 and Figure 2).
Variables No. %
Histology
Benign Masses
• Oncocytoma 10 14.2
• Angiomyolipoma 4 5.6
• Complex Cyst 4 5.6
• Others 2 2.8
Subtotal 20 28.2
Malignant Masses
• Chromophobe Carcinoma 3 4.2
• Papillary Carcinoma 11 15.5
• Clear Cells Carcinoma 37 52.1
Subtotal 51 71.8
Tumor Stage*
• pT1a/pT1b/pT2a 40/10/1 78.4/19.6/1.9
Overall Survival and Cancer Specific
51 100
Survival*
Recurrence-free Survival 1/5 years* 51/49 100/96.07
Positive Surgical Margins 0 0
Mean time follow-up: 7.4 years (Standard Error 0.5)
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 7
Laparoscopic enucleation of renal masses. González-León T., et al.
8 Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14.
Laparoscopic enucleation of renal masses. González-León T., et al.
sis at the expense of manual compression of the growing need to measure the complexity of
renal parenchyma, in those operated on by the renal masses objectively, the R.E.N.A.L nephro-
transperitoneal approach without WI. Those metric system is one of the most widely used
who underwent the retroperitoneal approach, because it is an excellent tool to predict if the
without hand-assistance, were strictly selected minimally invasive approach is safe as well as
(when the tumor was posterior, located towards the kind of nephrectomy required.(13,14)
the lower pole, predominantly exophytic); Studies on laparoscopic PN have reported a
however, the impossibility of controlling the prevalence of low-complexity tumors, as in this
bleeding quickly in a patient operated on by this series. In a study of small renal masses, Kons-
approach, resulted in the conversion to open tantinidis et al.(15) found a mean R.E.N.A.L score
surgery reported in this series. of 5.6±1.52. Dong et al.(7) reported a mean size
The transperitoneal approach is considered of 3.4cm and a R.E.N.A.L score of 7 (moderate
having the advantages of greater workspace, complexity) in their series of laparoscopic TE
greater instrument maneuverability and better in 108 patients. Nevertheless, the experience of
anatomical orientation, which is one of the the team in this type of surgery also plays an
disadvantages of the retroperitoneal approach. important role in the surgical decision.
The advantages described in this approach are The indication for PN has moved from
more direct access to the kidney and the renal imperative, when in presence of a solitary
hilum which avoids the need of mobilizing the functional or anatomical kidney, and relative,
intestine. As other authors, we choose the re- when the patient has a sick contralateral renal
troperitoneal approach for TE when the mass unit (lithiasis, chronic pyelonephritis or with
is posterior, postmedial or postlateral and also diseases that affect renal function and here-
predominantly exophytic and small to achieve ditary tumors), to elective, which currently
its enucleation successfully without utilizing prevails and was the indication for the patients
WI. This approach is also recommended for in this series. Today, PN is recognized as the
patients with previous abdominal surgery, gold standard according to the clinical guideli-
although no significant differences have been nes for T1a-T1b exophytic renal masses with
found in the percentage of complications and the aim to preserve more renal function.(6)
conversion to open surgery, when they are Most laparoscopic TE reports use WI, be-
approached transperitoneally.(11) ing the reason for reporting less bleeding than
Nevertheless, the study carried out by in this series, which was only utilized in 23.9%
Porpiglia et al. reports not having found any of the patients, as Tsivian et al.(16) who reported
differences between the transperitoneal and a blood loss of 125 ml while Rinott et al.(17) re-
retroperitoneal approaches when PN is per- ported 100 ml.
formed regardless tumor location and surgical Other researchers suggest that TE does not
complexity.(12) increase complications and is safe when dea-
There are two main aspects to keep in mind ling with small renal masses, despite absence
when assessing the surgical complexity of PN: of hilar control. The oncological outcome is
the size of the tumor mass and the proportion similar to that of standard on-clamp PN and the
of the endophytic component. In view of the outcome of renal function is better.(18,19)
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 9
Laparoscopic enucleation of renal masses. González-León T., et al.
Off-clamp simple enucleation of renal mas- there were five major complications, grade IIIa
ses is feasible by laparoscopic approach and has and only two related to the urinary tract. In
produced comparable oncological outcomes this series, 6 (8.4%) patients presented major
with standard on-clamp partial nephrectomy, complications (≥grade III). Minervini et al.(23)
with an incremental advantage for the preser- confirmed similar results, as this investigation,
vation of renal function. with 8.9% complications.
In a meta-analysis that included 13 The complications of laparoscopic PN are
studies and 1 796 patients who underwent la- potentially serious, among them renal paren-
paroscopic TE, when compared to PN showed chyma bleeding, with an incidence between 1%
significantly less operative time, length of and 2%, being more frequent postoperatively.
hospital stay, blood loss, diminished eGFR and Arterial pseudo aneurysm and fistulas of the ar-
less complications in the TE group. There were teriovenous system are, frequently, the cause of
no significant differences between TE and PN bleeding and their incidence is between 3% and
regarding ischemia time, positive margins, re- 10%. The bleeding can spread to the retroperito-
currence and survival.(20) neal space or the collecting system, conditioning
Postoperative renal function (RF) was the appearance of a retroperitoneal hematoma
assessed in the investigation by creatinine and and/or hematuria. They can be treated conserva-
the postoperative outcomes were satisfactory, tively and require blood transfusions, but SRAE
as in other investigations, and there was no is the treatment of choice for hemodynamically
significant decrease of postoperative creatinine stable patients, with good outcomes controlling
values. Blackwell et al.(21) did not observe statis- the hemorrhage and preserving most of the renal
tically significant differences in a study where parenchyma viable. In the study, three patients
they compare RF between TE and PN, but it were treated conservatively and only required
was better for TE. In one study, mean eGFR blood transfusion; two others needed SRAE due
was preserved in 93% of the patients at one to the presence of an arteriovenous fistula and
year, and in another which compared RN with an arterial pseudo aneurysm, respectively. Occa-
PN mean postoperative eGFR was significantly sionally, surgical reintervention for the suturing
higher for PN.(7,17) of the renal parenchyma or nephrectomy will be
Urological complications have been des- required, as occurred in one of the patients of
cribed in PN, which are, in general, persistent the series.(24,25)
hematuria, hemorrhage, renal vascular damage, Less complications have been reported
urinary loss, renal failure and infection (uri- when comparing PN to TE which is why it is
nary infection, perirenal abscess and sepsis). recommended for treating localized tumors
It is considered that they occur in 23% of the even for complex renal masses.(26)
patients and approximately 1/3 is Clavien gra- Other authors in TE studies have reported
de I–II.(22) a similar behavior regarding the histological
Rinott et al.(17) reported 23% minor compli- classification of the tumors: ccCR prevailed,
cations (Clavien-Dindo ≤III) and Zhao et al.(10) followed by papillary and chromophobe car-
reported 1.4% major complications (grade cinoma. They also found a prevalence of pT1a
IIIb) in 108 patients, whereas in another study tumors (64.4%) and 31.5% pT1b, as well as
10 Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14.
Laparoscopic enucleation of renal masses. González-León T., et al.
very low pT2 percentage, and unlike the results robotic approach and enucleoressection VS
of the series, one pT3 was reported. They also enucleation were predictors of complications
coincide with tumor recurrence in two pa- higher than Clavien-Dindo grade II, ischemia
tients.(23) time and trifecta (negative surgical margins, no
The patients in the series developed re- perioperative grade II Clavien-Dindo, greater
currences after the first year, one at the first surgical complications and no postoperative
tumor bed and another patient developed mul- acute kidney injury) were predictors of acute
tifocal tumors in the same renal unit, similar to post-operative renal damage.(29)
what Minervi et al.(23) reported in two patients TE is a safe and effective technique for
with recurrence. When robot-assisted and la- treating T1 tumors and the short-term oncolo-
paroscopic TE were compared, no differences gical outcomes are acceptable, although Dong
were found regarding recurrence.(10) W et.al. confirm these results after a follow-up
Positive surgical margins (PSM) is one of of more than five years.(7)
the issues still discussed regarding TE becau-
se the PSM rate is significantly higher when
compared to PN, although it has not been de- Conclusions
monstrated that this phenomenon corresponds
with a significant increase of recurrence.(26,27) Laparoscopic TE is a feasible surgical alterna-
Nevertheless, a recent systematic review did tive for select renal masses, with satisfactory
not find significant differences between both perioperative, oncological and functional
techniques regarding occurrence of PSM.(28) outcomes. Most complications were posto-
No positive margins were reported in this perative, grade II or IIIb and related with ble-
series unlike other authors. Minervi et al.(23) eding. The patients with complications had
reported positive surgical margins in 3 (2.4%). a significantly higher ECOG and these were
The existence of a pseudocapsule in every pa- related with the increase of tumor diameter
tient of the present series contributed to these size, higher R.E.N.A.L. score, longer operative
outcomes, as other researchers believe. TE has time and bleeding, but these differences were
not shown an increase in recurrence nor mor- not significant. Malignant tumors and clear-cell
tality either, when compared with PN.(7,17,20) renal carcinoma, pT1 masses prevailed, and an
The oncological outcomes obtained were elevated overall and cancer-specific survival
satisfactory and similar to those published in were confirmed.
medical literature. 95.7% CSS has been repor-
ted, 89.6% recurrence-free survival and 91.9%
OS at 5 years. In another study CSS was 95.9% Taxonomy CRediT
and OS 92.5%, in a 62-month mean-follow-up.
Another investigation only reported one recu- Tania González León, MD: conceptualization,
rrence after a 44.5-month follow-up.(17,23) data organization, formal analysis, investiga-
A recent multi-center study which asses- tion, methodology, supervision, validation,
sed the impact of tumoral resection techniques writing
found that the laparoscopic approach VS the Isabel García Morales, MD: conceptualization,
Revista Mexicana de Urología ISSN: 2007-4085, Vol. 82, núm. 3, mayo-junio 2022:pp. 1-14. 11
Laparoscopic enucleation of renal masses. González-León T., et al.
investigation, data organization, formal analysis analysis. BMC Urology. 2019 Jun 7;19(1):48. doi:
Anet López Chacón, MD: data organization, https://doi.org/10.1186/s12894-019-0480-6
formal analysis, methodology 5. Leppert JT, Lamberts RW, Thomas I-C, Chung
Indira López Rodríguez, MD: edition and writing BI, Sonn GA, Skinner EC, et al. Incident CKD
after Radical or Partial Nephrectomy. J Am Soc
Financing Nephrol. 2018 Jan;29(1):207–16. doi: https://
doi.org/10.1681/asn.2017020136
No sponsorship was received to write this ar- 6. García AG, León TG. Simple Enucleation for
ticle. Renal Tumors: Indications, Techniques, and
Results. Curr Urol Rep. 2016 Jan;17(1):7. doi:
Conflict of interest https://doi.org/10.1007/s11934-015-0560-4
7. Dong W, Chen X, Huang M, Chen X,
The authors declare no conflicts of interest. Gao M, Ou D, et al. Long-Term Oncologic
Outcomes After Laparoscopic and Robotic
Tumor Enucleation for Renal Cell Carcinoma.
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