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Laparoscopic partial nephrectomy in obese patients: how can the body mass index influence the surgical and functional outcomes?
* Corresponding author: Francesco Greco
Mailing address: Department of Urology, Policlinico S Pietro, Gruppo San Donato and Centro Salute Uomo, Bergamo, Italy.
Email: francesco_greco@ymail.com
Received: 28 September 2023 / Revised: 27 October 2023 / Accepted: 13 November 2023 / Published: 25 December 2023
DOI: 10.31491/UTJ.2023.12.014
Abstract
Objective: To evaluate the impact of body mass index (BMI) on surgical and functional outcomes of laparoscopic partial nephrectomy (LPN) for T1 renal tumors.
Patients and methods: In this single-center retrospective study, 240 consecutive patients underwent LPN for localized, incidentally discovered renal masses of < 7 cm (cT1). Patients were categorized into four groups according to their BMI, as follows: group 1, normal weight (BMI < 25 kg/m2); group 2, overweight (BMI 25–29.9 kg/m2); group 3, obese (BMI 30–39.9 kg/m2); and group 4, morbidly obese (BMI ≥ 40 kg/m2).
Results: Median operative time presented no statistically significant differences between BMI groups, whereas estimated blood loss was higher in morbidly obese patients than in all other groups. Warm ischemia time (WIT) and changes in eGFR were not influenced by the BMI groups but a decrease in the WIT was reported in obese and morbidly obese patients when an early unclamping technique (EUT) was used. An increase in BMI was not significantly associated with the occurrence of postoperative complications. In fact, the median complication rate was 3.3% for normal BMI, 4.5% for overweight patients, 4.8% for obese patients, and 3.6% for morbidly obese patients.
Conclusion: LPN could be considered a viable treatment option for renal masses amenable to nephron-sparing surgery in patients with higher BMI. An EUT should always be used in obese and morbidly obese individuals, considering the statistically significant decrease in WIT and the higher risk of chronic renal insufficiency in these patients.
Keywords
Kidney cancer, partial nephrectomy, laparoscopy, obesity, surgical outcomes
Introduction
The widespread use of modern imaging methods has led to the earlier diagnosis and improved staging of renal cell
carcinoma (RCC), resulting in a marked increase in the number of renal tumors detected incidentally in patients
with no urological symptoms [1]. These tumors are often
of lower grade and stage, and the need for RN for such asymptomatic, locally confined lesions has therefore been
questioned. Nephron-sparing surgery (NSS) could offer
a good alternative for small renal lesions (< 4 cm) [1-3].
Whereas open NSS represents the gold standard in the surgical therapy of T1 renal tumors [1], with the advances
in mini-invasive surgery, the refinement of intracorporeal suturing, and the availability of hemosealant substances,
the robotic and laparoscopic approaches have gained popularity for NSS. If robotic surgery represents the most preferred approach in the treatment of uro-oncologic disease,
the high cost associated with this technique remains an important issue for many urologic centers. Laparoscopic
partial nephrectomy (LPN) is surely less expensive than robotic surgery but it is currently performed in a few highvolume referral centers, as its diffusion has been limited
by the steep learning curve [1]. Since laparoscopy is generally less invasive than an open surgical technique, laparoscopy may be preferable if it can be shown to achieve
the same results, with the same safety for the patient.
Obesity represents a major health problem in industrialized countries, where its prevalence has increased dramatically over the past two decades. In the United States,
25.6% to 29% of adults aged 40 years and older were
considered obese in 2005 [4]. A higher risk of developing renal cell carcinoma (RCC) has been found in obese
patients than in non-obese patients [5-7], and currently,
most patients undergoing surgical treatment for RCC are overweight or obese. On the other hand, improved survival after partial nephrectomy has been reported in obese
patients with organ-confined disease [8-10]. The objective
of the present study was to investigate whether LPN could be safely performed in obese and morbidly obese patients compared with non-obese ones.
Patients and methods
This was a retrospective, single-center study including 240 patients who underwent LPN between May 2001 and
April 2013. Patients were categorized into four groups according to their BMI, as follows: group 1, normal weight (BMI < 25 kg/m2); group 2,
overweight (BMI 25–29.9 kg/m2); group 3, obese (BMI 30–39.9 kg/m2) and group
4, morbidly obese (BMI ≥ 40 kg/m2) [8, 11]. The study
was approved by the institutional review board. Written informed consent was obtained from all patients.
All operations were performed for localized incidentally discovered renal masses of < 7 cm (cT1); all indications
were elective. Before surgery, all patients underwent renal ultrasonography and CT to give detailed information on
tumor size, location, extent of parenchymal infiltration, and proximity to the pelvicocalyceal system. Patients with
severe heart failure (New York Heart Association functional class III–IV), chronic renal insufficiency, and/or
with an American Society of Anesthesiology (ASA) score of ≥ 3 were excluded from this study.
Demographic data, peri- and postoperative variables, including operative duration, estimated blood loss, warm
ischemia time (WIT), complications, hospital stay, renal function, histological tumor staging, and surgical margins
were collected and analyzed. Kidney function was evaluated by measuring estimated glomerular filtration rate
(eGFR) preoperatively and at 1-year follow-up. eGFR was calculated using the modification of diet renal disease
(MDRD) equation. All complications were recorded with a grade (I, II, IIIa, IIIb, IVa, IVb, or V) assigned according to the modified
Dindo-Clavien classification [12]. The R.E.N.A.L (tumor size-[R]adius, location and depth-[E]
xophytic or endophytic; nearness to the renal sinus fat or collecting system [N]; anterior or posterior position [A],
and polar vs non-polar location [L]) nephrometry score was used to assess the characteristics of the tumors in all
groups [13]. All operations were performed by two surgeons (F.G., P.F.), each of whom had completed at least
100 LPNs each before the beginning of the study, thus reducing the learning curve effect.
Our surgical techniques have been reported previously [14]. Shortly, a transperitoneal approach was used in all
patients. The renal artery was clamped with one laparoscopic bulldog clamp. The tumor was excised with cold
scissors in a near-bloodless field. Targeted excisional biopsies of the tumor bed were sent for frozen section in
case of suspicion regarding margin status. Collecting system was repaired with a running 2-0 Vicryl on a CT-1 needle. Renal parenchymal repair was performed with three
to five interrupted sutures. A Hem-o-Lok clip was secured on the suture to prevent pull-through. Another Hem-o-Lok
clip was applied to the suture flush with the opposite renal surface, compressing the kidney. The bulldog clamp was
then removed and fibrin glue was applied to the cut renal parenchymal surface. The en bloc specimen is extracted in
an Endocath (Covidien formerly Tyco Healthcare GmbH, Neustadt/Donau, Germany) and a flat suction drain was
placed in the renal lobe. Since 2008, we have adopted an early unclamping technique to minimize warm ischemia
time. In patients who underwent LPN with early unclamping, only the initial collecting system suturing was performed under ischemia and the renal parenchymal repair
of the bolstered renorrhaphy was performed in the revascularized kidney. The median follow-up was 45.7 ± 18.4
months. Follow-up was calculated from the date of surgery to the date of the last documented examination. All
patients underwent physical examination and ultrasonography every 3 months during the first year, every 6 months
during the second and third years, and annually thereafter. CT or MRI was performed every 6 months during the first
and second years, and annually during the third, fourth, and fifth years after surgery.
Statistical analysis was performed with SigmaPlot® software version 11.0 (SPSS Inc., Chicago, IL, USA).
Patient baseline characteristics and surgical outcomes were reported as frequencies (percentages) for categorical variables, median, and interquartile range (IQR) for
continuous ones and statistical significance was accepted at P < 0.05. Fisher’s exact test was applied to evaluate statistical differences
between groups in pathological stages.
Results
The baseline characteristics of the patients are summarized in Table 1. Of the 240 patients, 60 (25% of the entire cohort) were non-obese, 110 (45.8%) were overweight, 42 (17.5%) were obese, and 28 (11.7%) were morbidly obese. The ASA score was higher in obese and morbidly obese patients than in others (P = 0.03). The median (IQR) R.E.N.A.L nephrometry score per group was 7 (5–9) for normal BMI, 7 (5–9) for overweight patients, 7 (6–9) for obese patients and 7 (6–8) for morbidly obese patients (P = 0.5).
Table 1
IHC of NE differentiation in prostate tumors.
| Variables | Normal weight (n = 60) |
Overweight (n = 110) |
Obese (n = 42) |
Morbidly obese (n = 28) |
P-value |
|---|---|---|---|---|---|
| Median (IQR) age, years | 56 (40–67) | 58 (44–77) | 58 (49–74) | 56.5 (50–73) | 0.3 | Median (IQR) ASA score | 2 (2–3) | 2 (2–3) | 3 (2–3) | 3 (2–3) | 0.03 |
| Men/women, n | 42/18 | 70/40 | 23/19 | 16/12 | 0.18 |
| Left/right kidney, n | 39/21 | 53/57 | 24/18 | 17/11 | 0.16 |
| Median (IQR) tumor size, cm | 3.2 (2–6) | 2.8 (1.5–6) | 3.3 (2–5) | 3.1 (2–5) | 0.4 |
| Median (IQR) R.E.N.A.L. nephrometry score | 7 (5–9) | 7 (5–9) | 7 (6–9) | 7 (6–8) | 0.5 |
| Median (IQR) preoperative GFR, mL/min/1.72m2 | 92 (82–98) | 89 (73–97) | 88.5 (72–95) | 88 (70–93) | 0.07 |
Median operative time presented no statistically significant differences between BMI groups (P = 0.4), whereas estimated blood loss was higher in morbidly obese patients than in all other groups (median 200 mL vs 150, 155, and 160 mL for normal weight, overweight, and obese patients, respectively, P = 0.03) (Table 2). Warm ischemia time and changes in eGFR were not influenced by BMI groups, and no kidney was lost postoperatively due to warm ischemic injury. Regarding WIT, we noted statistically significant differences only in groups 3 and 4 in the presence of delayed (DUT) vs. early unclamping technique (EUT) [group 3: median DUT/WIT: 16.2 min; median EUT/WIT: 11.5 min (P = 0.03); group 4: median DUT/WIT: 17 min; median EUT/WIT: 12.2 min (P = 0.02)] (Table 2). The mean (IQR) length of hospital stay did not present a statistically significant difference between the 4 groups (P = 0.2). Furthermore, an increase in BMI was not significantly associated with the occurrence of postoperative complications. In fact, the median complication rate was 3.3% for normal BMI, 4.5% for overweight patients, 4.8% for obese patients, and 3.6% for morbidly obese patients (P = 0.2). There were no grade 4 or 5 complications and no conversion to radical nephrectomy was necessary.
Table 2
Intra- and postoperative patient data.
| Variables | Normal weight (n = 60) |
Overweight (n = 110) |
Obese (n = 42) |
Morbidly obese (n = 28) |
P-value |
|---|---|---|---|---|---|
| Median operating time, min | 145 (90–180) | 150 (110–210) | 155 (130–210) | 160 (145–230) | 0.4 | Median (IQR) EBL, mL | 150 (100–210) | 155 (100–250) | 160 (150–280) | 200 (180–450) | 0.03 |
| Median (IQR) WIT, min | 11 (7–18) | 11 (7–18) | 13 (11–20) | 15 (12–20) | 0.06 |
| EUT, min | 9.7 (7–14) | 10.7 (7–14) | 11.5 (9–15) | 12.2 (10–15) | 0.06 |
| DUT, min | 11.1 (9–14) | 12.1 (10–15) | 16.2 (14–20) | 17 (15–20) | 0.03 |
| Postoperative transfusion, n (%) | 1 (1.67) | 1 (0.9) | 1 (2.4 | 1 (3.6) | 0.5 |
| Complication rates, n (%) | 2 (3.3) | 5 (4.5) | 2 (4.8) | 1 (3.6) | 0.2 |
| Median (IQR) hospital stay, days | 4 (3–6) | 4 (3–7) | 4.5 (4–6) | 5 (4–7) | 0. 2 |
| Median (IQR) postoperative GFR, mL/min/1.72m2 (at 1-year-follow-up) |
88 (79–95) | 85 (69–95) | 84.5 (69–90) | 84 (65–90) | 0.07 |
Definitive pathological results showed a high incidence of clear cell tumors in all groups. Surgical margins were positive in only 2 (1.8%) overweight patients and 1 obese patient (2.3%) (P = 0.3, Table 3). One overweight patient developed tumor seeding at the port site 24 months after surgery.
Table 3
Oncologic outcomes.
| Variables | Normal weight (n = 60) |
Overweight (n = 110) |
Obese (n = 42) |
Morbidly obese (n = 28) |
P-value |
|---|---|---|---|---|---|
| Median tumor size, cm | 3.7 (2.5–6) | 3.3 (2–6) | 3.6 (2–6) | 3.4 (2–6) | 0.4 |
| Cell type, % | |||||
| clear-cell | 78 | 82 | 84 | 83 | 0.2 |
| chromophobe | 12 | 10 | 9 | 12 | |
| oncocytoma | 6 | 5 | 5 | 3 | |
| angiomyolipoma | 4 | 3 | 2 | 2 | |
| Positive margins, n (%) | 0 | 2 (1.8%) | 1 (2.3%) | 0 | 0.3 |
Discussion
Obesity is a medical condition in which excess body fat (BMI of 30 or greater) has accumulated to the extent that
it may have an adverse effect on health, leading to reduced life expectancy and/or increased health problems [15].
Obese or elderly patients often have associated medical conditions (e.g., diabetes, heart failure, hypertension, and
renal failure) that tend not to improve. Furthermore, obesity has been associated with an increased incidence of
several cancers, including esophageal, pancreatic, colorectal, breast, and kidney cancer [8, 16]. There is no direct
explanation as to the role of obesity in the development of cancer, but it has been related to chronic tissue hypoxia,
insulin resistance, compensatory hyperinsulinemia, obesity-induced inflammatory response, and lipid peroxidation [8, 17], an increased concentration of adipokines that
support tumor growth, and a lower concentration of the
tumor suppressor adiponectin [8, 18]. Such patients have
diminished reserves and tolerance to complications, and
are usually assigned a higher ASA score. These abovementioned comorbidities increase the risk of postoperative
complications and make anesthesia more risky [15].
Laparoscopic surgery in obese patients is likely to be
more technically demanding, with the possible need for longer trocars, decreased range of motion, and an increase
in the volume of retroperitoneal adipose tissue surrounding the kidney [19]. Nevertheless, it is well known that
these patients can extremely benefit from a minimally invasive surgical approach, which, through a minor surgical
trauma, decreases postoperative morbidity [20-23]. NSS
was initially reserved for patients at high risk of developing renal failure after kidney surgery to treat renal cancer
and open partial nephrectomy (OPN) to be equivalent to
open radical nephrectomy in terms of long-term cancerfree survival with unilateral renal involvement, unifocal
disease, and tumor size < 4 cm [2]. In recent years, LPN
has been proposed as a valid alternative to OPN for the
therapy of T1 RCC [14, 24, 25]. The anatomical
characterization of renal tumors before LPN is fundamental for a
correct evaluation of the outcomes [26]. The first anatomical characterization to evaluate the predictable difficulty
of NSS was reported by Kutikov et al. [13].
After categorizing the patient population into four groups based on BMI according to the WHO classification of
obesity, the BMI groups did not present statistically significant differences in tumor size and R.E.N.A.L. nephrometry score, and they were equivalent in relation to age
and gender distribution. In 2007, Gong et al. [21] reported
their experience with laparoscopic kidney surgery in the obese population. They also separated their cohort based
on BMI and found that laparoscopy was feasible in obese
patients. Nevertheless, the authors did not find any correlation between BMI, R.E.N.A.L. scores, surgical techniques (EUT vs. DUT), WIT and renal function.
The more widespread use of grading schemes in reporting complications has facilitated standardization to some
extent. Dindo et al. [12] proposed a modification of the
Clavien system of surgical complications. When we applied this system to the present data, an increase in BMI
was not significantly associated with the occurrence of postoperative complications, with a median complication rate of 3.3% for normal BMI, 4.5% for overweight
patients, 4.8% for obese patients, and 3.6% for morbidly obese patients. Moreover, all grade 4 or 5 complications
could be registered. Moreover, although the median operative time presented no statistically significant differences between the BMI groups (P = 0.4),
the median estimated blood loss was higher in morbidly obese patients
than in all other groups. WIT ≤ 20 min was achieved in all patients, whereas WIT ≤ 15 min was achieved using an
EUT. This is an advantage of the laparoscopic technique,
where the presence of pneumoperitoneum, with intraabdominal pressure set at 15-20 mmHg, avoids possible
bleeding from small vessels, allowing resection of the tumor even with unclamped renal vessels [14]. Interestingly,
an important advantage in terms of WIT was noted when
an EUT was used in obese and morbidly obese patients.
The best cut-off time to consider for a safe NSS procedure
has been debated over the past few years and has recently
been suggested to be 20 min. In general, the concept that every minute of ischemia may count is recognized, considering that WIT may affect postoperative renal function
[27]. This is an important aspect to consider when performing LPN, as obesity increases the risk of developing
chronic renal insufficiency, especially in elderly patients
[28]. Nevertheless, there was no statistically significant
difference in eGFR between groups at 1-year follow-up,
which can be explained by the young age of the recruited
patients. Our data are comparable to the outcomes described in the literature in obese patients after LPN [4-9].
Colombo et al. [7] compared the perioperative outcome
of laparoscopic partial nephrectomy in obese and nonobese patients, using a cohort of patients who underwent
retroperitoneal or transperitoneal approach. There was no
significant difference between groups regarding EBL, operative time, WIT, conversion rate, or hospital stay for the
transperitoneal approach group.
In another study by Feder et al. [29], which analyzed
patients who underwent laparoscopic partial or radical
nephrectomy, there was also no significant difference between obese and non-obese groups with regard to EBL,
operation duration, hospital stay, and number of open
conversions or complications. Concerning oncologic data,
we noted a higher incidence of clear cell tumors in all 4
groups. Surgical margins were positive in only 2 (1.8%)
overweight patients and 1 obese patient (2.3%). Moreover, one overweight patient developed tumor seeding at
the port site 24 months after surgery, which was due to a
rupture of the specimen during the procedure and not to
positive margins. However, there are several limitations
to the present study that must be acknowledged. First, this
is a retrospective study, which introduces an inherent selection bias that cannot be overcome. It is also limited by
the small number of patients in the obese BMI and morbidly obese groups, which limits the ability to determine
a precise correlation between obesity and complexity of
the operation. Finally, this experience is from a tertiary
referral center with a high volume of LPN procedures
and therefore the current findings may not apply to other
populations in different hospital settings.
Conclusions
Although it may require greater surgical skill, LPN in obese and morbidly obese individuals presents similar surgical outcomes to normal and overweight individuals. An EUT should always be used in obese and morbidly obese individuals, considering the statistically significant decrease in WIT and the higher risk of chronic renal insufficiency in these patients.
Declarations
Acknowledgments
None.
Financial support and sponsorship
None.
Conflict of interest statement
No conflict of interests.
Ethical Approval and Informed consent
The study was approved by the institutional review board. Written informed consent was obtained from all patients.
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