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. 2022 May 26;12:732714. doi: 10.3389/fonc.2022.732714

A Systematic Review and Meta-Analysis of Minimally Invasive Partial Nephrectomy Versus Focal Therapy for Small Renal Masses

Lin Dong 1, Wang You Liang 2, Lu Ya 3, Liu Yang 1,*, Wei Qiang 4
PMCID: PMC9178090  PMID: 35692758

Abstract

Background

Minimally invasive partial nephrectomy (MIPN) and focal therapy (FT) are popular trends for small renal masses (SRMs). However, there is currently no systematic comparison between MIPN and FT of SRMs. Therefore, we systematically study the perioperative, renal functional, and oncologic outcomes of MIPN and FT in SRMs.

Methods

We have searched the Embase, Cochrane Library, and PubMed for articles between MIPN (robot-assisted partial nephrectomy and laparoscopic partial nephrectomy) and FT {radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation (CA), irreversible electroporation, non-thermal [irreversible electroporation (IRE)] ablation, and stereotactic body radiation therapy (SBRT)}. We calculated pooled mean difference (MD), odds ratios (ORs), and 95% confidence intervals (CIs) (CRD42021260787).

Results

A total of 26 articles (n = 4,420) were included in the study. Compared with MIPN, the operating time (OP) of FT had significantly lower (SMD, −1.20; CI, −1.77 to −0.63; I2 = 97.6%, P < 0.0001), estimated blood loss (EBL) of FT had significantly less (SMD, −1.20; CI, −1.77 to −0.63; I2 = 97.6%, P < 0.0001), length of stay (LOS) had shorter (SMD, −0.90; CI, −1.26 to −0.53; I2 = 92.2%, P < 0.0001), and estimated glomerular filtration rate (eGFR) of FT was significantly lower decrease (SMD, −0.90; CI, −1.26 to −0.53; I2 = 92.2%, P < 0.0001). However, FT possessed lower risk in minor complications (Clavien 1–2) (OR, 0.69; CI, 0.45 to 1.07; I2 = 47%, P = 0.023) and overall complications (OR, 0.71; CI, 0.51 to 0.99; I2 = 49.2%, P = 0.008). Finally, there are no obvious difference between FT and MIPN in local recurrence, distant metastasis, and major complications (P > 0.05).

Conclusion

FT has more advantages in protecting kidney function, reducing bleeding, shortening operating time, and shortening the length of stay. There is no difference in local recurrence, distant metastasis, and major complications. For the minimally invasive era, we need to weigh the advantages and disadvantages of all aspects to make comprehensive choices.

Systematic Review Registration

https://www.crd.york.ac.uk/PROSPERO/#recordDetails, identifier PROSPERO (CRD42021260787).

Keywords: minimally invasive, focal therapy, ablation techniques, kidney, nephrectomy, meta-analysis

Introduction

Small renal masses (SRMs) represent a group of heterogeneous tumors covering the entire metastatic potential, including malignant, indolent, and benign tumors. Among them, kidney cancer already accounts for 2%–3% of all cancers, and the incidence is increasing year by year (1, 2). The American Urological Association (AUA) and European Association of Urology (EAU) guidelines both recommend partial nephrectomy for SRMs (3). In addition, minimally invasive partial nephrectomy (MIPN) including robot-assisted partial nephrectomy (RAPN) and laparoscopic partial nephrectomy (LPN) is the current trend. However, OPN is selected, most of which are intraoperatively converted from LPN or RAPN to OPN for SRMs. In addition, it has recently been fully developed in the clinic.

With the clinical application of ablation techniques, focal therapy (FT) {radiofrequency ablation (RFA), microwave ablation (MWA), cryoablation (CA), irreversible electroporation, and non-thermal [irreversible electroporation (IRE)] ablation} has been fully developed (4). FT has the advantages of less trauma, less bleeding, and shorter hospital stay (5). The guidelines of AUA and EUA recommend FT replacing PN for kidney mass < 3 cm in size, and it is suitable for patients with kidney masses who are forbidden to operate or have serious comorbidities (6, 7). Therefore, the comparative study on MIPN and FT is very meaningful. However, there are main systematic reviews about ablative therapies versus partial nephrectomy for small renal masses at present (8). Therefore, the purpose of this study is to compare the perioperative period, renal function, and oncologic outcomes of MIPN and FT in SRMs.

Methods

Protocol and Guidance

The study was performed according to Preferred Reporting Items for Systematic Reviews and the meta-analysis (PRISMA) (9). The protocol for this review has been registered on PROSPERO (CRD42021260787).

Search Strategy

This study involved literature published in the Embase, PubMed, and Cochrane Library up to January 26, 2022. We defined the eligibility criteria according to the population (P), intervention (I), comparator (C), outcome, and study design approach (O). P, the patients with SRMs; I, undergoing MIPN; C, FT was performed as a comparator; O, one or more of the following outcomes: perioperative, renal functional, and oncologic outcomes. The search terms included (robot-assisted partial nephrectomy OR robotic partial nephrectomy OR RAPN OR RPN OR laparoscopic partial nephrectomy OR LPN OR Minimally invasive) AND [“Renal Neoplasm” (MeSH) OR renal masses] AND [“radiofrequency ablation” (MeSH) OR “Cryoablation” (MeSH) OR microwave ablation OR RFA OR irreversible electroporation OR CRA OR MWA OR IEP OR “Stereotactic body radiation therapy” (MeSH) OR SBRT]. The search strategy was not limited by language or year. It was not requested by the ethics or institutional review committee due to the study being designed as a systematic review and meta-analysis.

Inclusion and Exclusion Criteria

We have included the literature by the following criteria. Comparative data were available on the treatment of SRMs through MIPN (RAPN and LPN) and FT (RFA, CA, MWA, and IRE). Outcome indexes should include at least one of the following: perioperative period, renal function, and oncologic outcomes. Any study that did not confirm the above inclusion criteria was excluded.

Data Extraction and Outcome Measures

Two researchers (LY and LX) independently have reviewed the retrieved literature by the inclusion and exclusion criteria. The third researcher (ZZJ) was asked to participate in the discussion to decide whether to include when disagreements were encountered. The extracted data included the first author, publication, country, study type, group, age (if mentioned), follow-up, female proportion, and renal nephrectomy score ( Table 1 ).

Table 1.

Characteristics of the included studies.

Author Year End points Publication Country Study design Study interval Group Cases Malignant tumour, n (%) Tumour grade (1-2),n (%) Clinical T1, n(%) Clavien grade (0-2), n (%) Age Male proportion(%) BMI(Body mass index) (kg/m2) Comorbidities ASA(%) tumour size(cm) Pathology (Ma/Be/Un) R.E.N.A.L Nephrometry score Follow-up (months) Confounders adjustment NOS score(max:9)
Bensalah (10) 2007 Survival, recurrence, complications BJU international USA R 2000-2006 LPN 50 41 (82) 37 (90)     56.5 ± 11.7 62 31.1 ± 8.0 ≥3(53%) 2.6 ± 0.9 N/A N/A 25 No 8
LRFA 38 29 (80) 20 (95)     62 ± 17.5 58 29.6 ± 4.8 ≥ 3(26%) 2.3 ± 0.7 15
Bertolo (11) 2019 Survival, recurrence, complications, renal function Urologic Oncology USA R 2006-2016 RAPN 65     65(100) 16 (25) 79.3 ± 3.3 66 27.4 ± 4.9 3.0 (0.5) 2.9 ± 1.0 54/11/0 6.9 ± 1.9 37 (29-44) No 7
CA 65     65(100) 5 (8) 79.3 ± 4.1 60 27.9 ± 5.9 2.9 (0.6) 3.0 ±1.0 48/17/0 6.4 ± 2.0 46 (38-53)
Bianchi, L (12). 2021 Survival, recurrence, complications, renal function Int J Urol Italy R 2007-2019 MIPN 137 2.4 (2–3)       72 (62–77) 66.4 26 (24–29)   2.4 (2–3) 107/30/0   52 (32–99) Yes (propensity score matching) 7
Ablation 137 2.3 (1.8–2.9)       72 (65–79) 65.7 26 (24–28)   2.3 (1.8–2.9) 106/19/12   62 (47–79)
Bird (13) 2009 Survival, recurrence, complications, renal function Journal of Endourology USA R 2002-2007 LPN 33 20 (60.6)       57.8 (27–77) 55 28.45 2.2 3.1 .20/13/0 N/A 27 (6–58) No 7
LRFA 36 26 (72.3)       75.2 (56–86) 61 30.08 2.8 2.8 26/13/0 12 (6–23)
Caputo (14) 2017 Survival, recurrence, complications European Urology USA P 1999-2014 RAPN 31 28 (90) 8 (36.5) 31 (100) 30 (96.8) 61 (52–68) 67 30.6 (26.6–35.4) 3 (2–3) 5.0 (4.5–5.6) 28/3/0 9.0 (8–10) 13.0 (3.19–19.2) Yes (propensity score matching) 8
CA 31 22 (71) 12 (42.6) 31 (100) 27 (87.1) 68 (64–76) 81 30.6 (26.3–37.4) 3 (3–3) 4.3 (4.2–4.7) .22/8/1 8.0 (6–9) 30.1 (13.2–64.0)
Desai (15) 2005 Survival, recurrence, complications Urology USA P 1999-2003 LPN 153         60.59 ± 13.19 58 29.06 ± 6.42 ≥3(46) 2.25 ± 0.67 N/A N/A 5.8 (1–36) No 6
LCA 89         65.55 ± 12.69 69 27.43 ± 5.59 ≥3(75) 2.05 ± 0.56 24.6 (1–60)
Emara (16) 2014 Survival, recurrence, complications, renal function BJU international UK P 2010-2012 RAPN 47 33 (70)       60.5 (38–80) 80 N/A N/A 3.278 ± 1.787 33/14/0 5.77 ± 0.25 16.50 ± 0.946 No 8
CA 56 39 (70)       69.75 (42–90) 66 2.559 ± 0.958 .9/9/8 5.75 ± 0.23 31.30 ± 1.802
Fossati (17) 2015 Survival, recurrence, complications, renal function European urology focus Italy R 2000-2013 MIPN 206 153 (74)     194 (94) 60 (51–70) 69 26 (23–28) ≥3(17) 2.5 (2.0–3.4) 153/53/0 N/A 43 No 8
LCA 166 105 (63)     136 (82) 66 (57–73) 73 25 (23–29) ≥3(30) 2.0 (1.5–2.5) 105/43/18 39
Garcia, R. G (18). 2021 Recurrence, complications CardioVascular and Interventional Radiology Brazil R 2008-2017 RAPN 69     69 (100) 2 (3) 54.8 ± 11.9 72.4 27.5 ± 3.8 ≥3(0) N/A N/A N/A 22.1 No 7
PCA 63     63 (100) 0 (0) 62.5 ± 14.1 76.2 28.3 ± 4.5 ≥3(24.5) 22.1
Guillotreau (19) 2012 Recurrence, complications, renal function European Urology USA R 1998-2010 RAPN 210 156 (74)     36 (17) 57.8 ± 11.8 58 30.1 ± 6.4 ≥3(51) 2.4 ± 0.8 N/A N/A 4.8 (1–7.9) Yes (multivariable logistic regression for complications) 8
LCA 226 181 (77)     19 (8) 67.4 ± 11.3 71 29.3 ± 6.2 ≥3(80) 2.2 ± 0.9 44.5 (8.7–66.8)
Haber (20) 2012 Survival, recurrence, complications, renal function BJU international USA R 1998-2008 LPN 48     48 (100)   60.6 ± 13.7 52.1 30.1 ± 6.2 2.7 ± 0.5 3.2 ± 1.33 31/17/0 N/A 42.7 ± 30.8 No 8
LCA 30     30 (100)   60.9 ± 11.4 73.3 31.5 ± 5.8 2.7 ± 0.8 2.6 ± 1.08 25/5/0 60.2 ± 46.3
Haramis (21) 2012 Survival, recurrence, complications Journal of Laparoendoscopic and Advanced Surgical Techniques USA R 2005-2008 LPN 92       10 (10.9) 58.8 (37–85) 60.8 N/A N/A 1.9 (0.3–4.5) N/A N/A 21.8 (1–48) No 6
LCA 75       5 (0.07) 69.2 (19–84) 62.7 1.9 (1–3) 2.0 (0.4–7.5) 14 (1–34)
Ji (22) 2016 Recurrence, complications Urologia internationalis China R 2006-2015 LPN 74         57.3 (25–76) 55.4 N/A 1.7 (1–3) 2.9 (1.4–3.8) 103/2/0 N/A 2.2 (1.7–3.3) No 6
LRFA 105         64.2 (42–81) 62.9 2.3 (1–3) 2.2 (1.7–3.3) 71/3/0 78 (60–106)
Kim (23) 2015 Survival, recurrence, complications, renal function Asian journal of surgery South Korea R 2005-2011 RAPN 27         60.33 ± 15.61 70.4 25.9 ± 3.4 N/A 1.77 ± 0.96 24/3/0 6.5 ± 1.7 10.9 ± 7.0 Yes (propensity score matching) 6
RFA 27         58.67 ± 11.60 81.5 26.6 ± 3.1 1.8 ± 0.81 .3/2/24 6.3 ± 1.6 16.7 ± 10.5
Kiriluk (24) 2011 Complications, renal function Journal of Endourology USA P 2002-2008 LPN 51 41 (80.3)     6 (11.8) 66.0 (23–83) 51 29.1 (18.2–24) N/A 2.27 (0.80–5.10) N/A N/A 18.3 (13.0–26.8) No 7
LAT 51 26 (50.9)     12 (23.5) 65.7 (27–75) 51 30.0 (12.1–56.9) 2.35 (0.99–4.90) 27.9 (0.4–40.0)
Lian (25) 2010 Recurrence, complications, renal function Chinese journal of surgery China R 2005-2009 LPN 29         61 (55-68) 66 N/A N/A 2.8 (2.0-4.5) N/A N/A 27 (3-36) No 6
LCA 18         63 (41-73) 78 2.9 (1.5-5.0) 16 (6-21)
Link (26) 2006 Recurrence Journal of Endourology USA R 2004-2005 LPN 217         N/A N/A N/A N/A 2.6 ± 1.3 N/A N/A N/A No 7
LCA 28         2.4 ± 0.9
Liu (27) 2021 Survival, recurrence, complications, renal function Diagnostics China R 2008, 2015 RAPN 55 32 (58.2)   53 (96.4) 0 (0) 57.27 ± 13.28 52.7 25.29 ± 4.58 ≥3(23.6) 4.06 ± 2.01 N/A N/A 33.20 ± 19.55 Yes: matching 7
LCA 55 27 (49.1)   54 (98.2) 3 (5.5) 59.44 ± 14.77 52.7 25.04 ± 4.23 ≥3(20) 3.86 ± 2.13 54.96 ± 34.59
O'Malley (28) 2007 Recurrence, complications BJU International USA R 2003-2005 LPN 15         75.7 ± 4.6 79 27.1 ± 3.9 ≥3(53) 2.5 ± 1.0 N/A N/A 9.83 ± 8.8 Yes: matching 8
LCA 15         76.1 ± 4.5 57 29.1 ± 6.8 ≥3(62) 2.7 ± 1.3 11.9 ± 7.2
Pantelidou (29) 2016 Recurrence, complications, renal function CardioVascular and Interventional Radiology UK R 2005-2013 RAPN 63 59 (93.7)     10 (15.9) 54 ± 7 N/A N/A 2 (2–3) 2.88 ± 0.13 63/0/0 7.38 ± 0.16 18.5 (6.2–29.5) No 7
RFA 63 63 (100)     4 (6.3) 61 ± 21 2 (2–3) 2.11 ± 0.19 59/0/4 7.38 ± 0.16 47.5 (11.8–80.2)
Park (30) 2018 Survival, recurrence, complications European radiology Republic of Korea R 2008-2016 RAPN 63 54 (85.7)     3 (4.8) 57.7 ± 10.8 75 N/A 1.8 ± 0.3 2.0 ± 0.6 63/0/0 7.1 ± 1.7 24.6 (1-90) Yes: matching 8
RFA 63 48 (76.2)     3 (4.8) 57.1 ± 13.1 65 1.8 ± 0.7 2.1 ± 0.5 63/0/0 7.2 ± 1.5 21 (1-65)
Tanagho (31) 2013 Recurrence, complications, renal function Journal of Endourology USA R 2007-2012 RAPN 233 80 (52.3)       57.4 ± 11.9 54.5 30.1 ± 6.0 N/A 2.9 ± 1.5 185/48/0 7.3 ± 1.9 21.9 ± 18.8 No  
2000-2003 CA 267 185 (79.4)       69.3 ± 11.0 61 30.4 ± 7.8 2.5 ± 1.0 80/73/114 6.4 ± 1.7 39.8 ± 34.3
Turna (32) 2009 Survival, recurrence, complications, renal function The Journal of urology USA R 1997-2006 LPN 36 23 (63.8)       60.3 ± 15.5 58 30.5 ± 7.1 ≥3(66.7) 3.7 ± 1.9 N/A N/A 80 No 8
RFA 36 22 (73.3)       64.1 ± 11.1 64 31.3 ± 5.7 ≥3(77.7) 2.5 ± 1.1 80
Uemura, T (33). 2021 Survival, recurrence, complications, renal function In Vivo Japan R 2016-2019 RAPN 78 58 (74.3)   78 (100) 76 (97.4) 61 (52-69) 63 23 (21-25) ≥3(1.3) 1.9 (1.5-2.3) N/A ≥10(3.8) 18.5 (12-30) No 7
PCA 48 41 (85.4)   48 (100) 47 (97.9) 78 (70-82) 41 23 (21-26) ≥3(33.3) 2.6 (2.0-3.4) ≥10(10.8) 12 (6-32)
Yanagisawa (34) 2020 Survival, recurrence, complications, renal function Urologic oncology Japan R 2011-2019 LPN 90 65 (72)   90 (100) 87 (96.7) 69.5 (63-75) 81 N/A N/A 28.8 ± 9.5 88/0/2 6 (5-8) 18 Yes: matching 7
PCA 90 88 (97.8)   90 (100) 89 (98.9) 68.5 (61−76) 76 27.6 ± 9.7 65/25/0 6 (5-7) 26.5  
Yu (35) 2020 Survival, recurrence, complications, renal function Radiology China R 2006-2017 LPN 185     185 (100)   60.4 ± 14.1 74.6 N/A N/A 2.3 ± 0.9 185/0/0 N/A 40.6 (25.1–63.4) Yes: matching 8
MWA 185     185 (100)   63.2 ± 15.2 74 2.3 ± 0.5 185/0/0 42.0 (23.5–69.3)  
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Matching: 1 - Age; 2 - BMI; 3 - ASA; 4 - Charlson; 5 - Gender; 6 - Pathological stage; 7 - Urinary diversion type. RARC, robot-assisted partial nephrectomy; LPN, laparoscopic partial nephrectomy; RFA, Radiofrequency ablation; CRA, Cryoablation; MWA, Microwave ablation; RCT, randomized controlled trial; R, Retrospective; P, Prospective; NA, data not available; NOS, score; Newcastle-Ottawa Scale score.

Statistical Analysis

Statistical analysis was performed by Review Manager, version 5.2 (The Cochrane Collaboration, Oxford, UK) Stata v.12.0 (Stata Corp LLC, College Station, TX, USA). For this meta-analysis, if the heterogeneity test was I2 > 50%, P < 0.1, then we used the random effect model; if the heterogeneity test was I2 < 50%, P > 0.1, then we used the fixed utility model. The combined r-values and 95% confidence intervals (CIs) of each study were calculated, and the forest map displayed the characteristics of each study result. The quality of the included literature was evaluated using the Newcastle–Ottawa scale (NOS). The Begg’s and Egger’s tests were used to test the publication bias. The P < 0.05 was indicated statistically significant.

Results

Eligible Studies and Study Characteristics

We initially searched 1,206 records. A total of 385 literature studies that were published repeatedly and cross-published were deleted. After reading the title and abstract, 760 articles were excluded. After the remaining 61 pieces of literature were searched for full text, reading, and quality assessment, 26 pieces of literature (10–35) (4,420 participants: MIPN: 2031 vs. FT: 2389) were eventually included ( Figure 1 ). The detailed information of this literature was listed in Table 1 .

Figure 1.

Figure 1

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Flowchart for records selection process of the meta-analysis [According to PRISMA template: Moher D, Liberati A, Tetzlaff J, Altman DG, The PRISMA Group (2009). Preferred Reporting Items for Systematic Reviews and Meta-Analyses: The PRISMA Statement. PLoS Med 6(7): e1000097. doi:10.1371/journal. Pmed 1000097].

Perioperative Outcomes

Data on OP were reported in 17 studies (10, 11, 15, 17, 18, 20, 22, 24–28, 30–32, 34, 35). Compared with MIPN, patients who underwent FT had significantly lower OP (SMD, −1.20; CI, −1.77 to −0.63; I2 = 97.6%, P < 0.0001) ( Figure 2A ). Owing to high heterogeneity (I2 = 95%), we chose subgroup analysis. Compared with FT, patients who underwent LPN had significantly higher OP (SMD, −1.14; CI, −1.26 to −1.02; I2 = 97.6%, P < 0.0001) and patients who underwent RAPN had significantly higher OP (SMD, −0.67; CI, −0.83 to −0.51; I2 = 97.5%, P < 0.0001) ( Figure 2B ). Sensitivity analysis and subgroup analysis cannot reduce heterogeneity.

Figure 2.

Figure 2

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Forest plots of perioperative outcomes: perioperative outcomes. Forest Plot Estimates of MIPN VS FT for OP (A), EBL (C), LOS (E), minor complications (G), overall complications (H), and major complications (I). Forest Plot Estimates subgroup analysis of MIPN VS FT for OP (B), EBL (D), and LOS (F). MIPN, minimally invasive partial nephrectomy; FT, focal therapy; OP, operating time; EBL, estimated blood loss; LOS, length of stay.

We included 13 studies (11, 15–17, 20, 22, 24, 25, 27, 28, 31, 32, 35) about EBL. Compared with MIPN, patients who underwent FT had significantly less EBL (SMD, −0.90; CI, −1.26 to −0.53; I2 = 92.2%, P < 0.0001) ( Figure 2C ). Owing to high heterogeneity (I2 = 92.2%), we chose subgroup analysis. Compared with FT, patients who underwent LPN had significantly higher EBL (SMD, −0.97; CI, −1.36 to −0.58; I2 = 87.8%, P < 0.0001) and patients who underwent RAPN had significantly higher EBL (SMD, −1.00; CI, −1.44 to −0.55; I2 = 73.4%, P = 0.01) ( Figure 2D ). We subgroup analysis by nephropathy recently published 2022 back to 2017 (5 years) vs. older studies. There is only subgroup analysis by nephropathy recently published in 2022 back to 2017 (5 years) (SMD, −0.95; CI, −1.11 to −0.78; I2 = 26.8%, P = 0.247) vs. older studies (SMD, −0.44; CI, −0.56 to −0.32; I2 = 92.2%, P = 0.0001) difference here for estimated blood loss (EBL). Sensitivity analysis cannot reduce heterogeneity.

We included 18 studies (10, 11, 13, 15–18, 20, 22–28, 30, 32, 34) on LOS. Compared with MIPN, patients who underwent FT had significantly less LOS (SMD, −0.90; CI, −1.26 to −0.53; I2 = 92.2%, P < 0.0001) ( Figure 2E ). Owing to high heterogeneity (I2 = 92.2%), we chose subgroup analysis. Compared with FT, patients who underwent RAPN had significantly higher LOS (SMD, −0.86; CI, −1.26 to −0.46; I2 = 90.1%, P < 0.0001) and patients who underwent LPN had significantly higher LOS (SMD, −1.23; CI, −2.68 to 0.22; I2 = 98.4%, P < 0.0001) ( Figure 2F ). Sensitivity analysis cannot reduce heterogeneity.

Compared with MIPN, patients who underwent FT had significantly less minor complication (Clavien 1–2) (OR, 0.69; CI, 0.45 to 1.07; I2 = 47%, P = 0.023) ( Figure 2G ) and overall complication (OR, 0.71; CI, 0.51 to 0.99; I2 = 49.2%, P = 0.008) ( Figure 2H ). There is a similarity between MIPN and FT for major complications (Clavien 3–5) (OR, 0.91; CI, 0.60 to 1.39; I2 = 0%, P = 0.504) ( Figure 2I ).

Renal Functional Outcomes

For the functional results, we conducted a systematic analysis of eGFR. Data on eGFR were reported in seven studies. Compared with MIPN, patients who underwent FT had significantly reduced in eGFR (SMD, −0.94; CI, −1.32 to −0.57; I2 = 83.9%, P < 0.0001) ( Figure 3A ). Owing to high heterogeneity (I2 = 83.9%), we chose sensitivity analysis. After omitting the studies by Bensalah et al. (10), Kim et al. (23), and Tanagho et al. (31), as samples that were left out, the pooled results change substantially, but the heterogeneity was significantly reduced (SMD, −0.850; CI, −1.050 to −0.650; I2 = 5.1%, P = 0.367) ( Figure 3B ).

Figure 3.

Figure 3

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Forest plots of perioperative outcomes: renal functional outcomes. Forest Plot Estimates of MIPN VS FT for eGFR (A) (I2=83.9%) and (B) (I2=5.1%). MIPN, minimally invasive partial nephrectomy; FT, focal therapy.

Oncological Outcomes

The median or mean follow-up period of oncological outcomes of MIPN was 2.2 to 42.7 months, and FT was 14 to 78 months. Fourteen studies recorded on local recurrence rate, and six studies recorded on distant metastasis rate. There is a similarity between MIPN and FT for local recurrence rate (OR, 4.54; CI, 2.59 to 7.96; I2 = 1.6%, P = 0.431) ( Figure 4A ) and distant metastasis rate (OR, 2.37; CI, 0.87 to 6.47; I2 = 29.1%, P = 0.217) ( Figure 4B ).

Figure 4.

Figure 4

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Forest plots of perioperative outcomes: renal functional outcomes. Forest Plot Estimates of MIPN VS FT for local recurrence rate (A) and distant metastasis rate (B). MIPN, minimally invasive partial nephrectomy; FT, focal therapy.

Publication Bias

We conducted publication bias on more than 15 included studies using Egger’s test. For OP, Egger’s test results revealed that t = −2.39, P = 0.051 in Supplementary Figure 1A and funnel plots in Supplementary Figure 1B . For LOS, Egger’s test results revealed that t = −1.73, P = 0.106 in Supplementary Figure 1C and funnel plots in Supplementary Figure 1D . For overall complication, Egger’s test results revealed that t = 1.11, P = 0.281 in Supplementary Figure 1E and funnel plots in Supplementary Figure 1F . For major complications (Clavien 3–5), Egger’s test results revealed that t = 0.97, P = 0.345 in Supplementary Figure 1G and funnel plots in Supplementary Figure 1H . There is no publication bias in the above.

Discussion

In recent years, with the development of minimally invasive technology, SRMs were mainly treated by MIPN. For the clinical application of ablation technology, SRM ablation therapy has thus entered a new era (36, 37). The purpose of SRMs by MIPN or FT was to treat tumors while reducing perioperative complications, protecting the function of the kidney, and decreasing the postoperative recurrence rate (38). Therefore, the best treatment plan depends on the perioperative period, renal function, and tumor outcome. At present, there are few reports on the relationship between MIPN and FT.

MIPN has replaced the traditional radical nephrectomy with the increase of SRMs patients’ willingness to protect the kidney and the progress of corresponding surgical techniques in urology. A study has concluded that it is no statistically significant difference between MIPN and radical nephrectomy in terms of tumor control effects (39). At the same time, MIPN not only preserves the patient’s nephrons but also is minimally invasive. Therefore, MIPN has become the main treatment for SRMs and early renal cancer. However, because MIPN requires renal artery block during the operation, the long-term renal function damage caused by this has also become a deficiency of MIPN (40–42). There have always been controversies regarding the treatment of SRMs between FT and MIPN, but unfortunately, due to the shortcomings of retrospective research, the level of credibility of the relevant conclusions is not high. To our knowledge, this study provides a new systematic review and meta-analysis comparing MIPN and FT for SRMs. Because of the lack of RCTs, we have investigated 25 non-randomized observational studies comparing MIPN and FT. The primary endpoint is the oncology outcome (local tumor recurrence and distant metastasis). The secondary endpoints are renal function and perioperative outcomes. Because of the short follow-up period, the meta-analysis of CSS and OS is inappropriate. However, a multi-center retrospective analysis showed that RAPN has good long-term oncologic and functional outcomes of the procedure, which duplicate those achieved in historical series of laparoscopic surgery (43).

The meta-analysis emphasizes that FT has a disadvantage in Oncological control compared to MIPN. Compared with patients who received MIPN, patients who have received FT had an OR of 2.43 for distant metastases and an OR of 6.59 for local recurrence. For the reasons, on the one hand, the overall follow-up period of the oncologic outcomes in the FT group is long, which may lead to a relatively high recurrence rate, especially metastasis rate. The different follow-up periods between MIPN and FT affect both distant metastasis rate and local recurrence rate. In addition, considering the secondary efficacy, which is the confirmed oncologic outcomes after the second FT, the risk of recurrence can be reduced (44). In one study, compared with MIPN, secondary FT seemed to be effective for cancer control and the metastasis rate was not high (45). However, there is no second FT in the included literature. Interestingly, matching studies with similar basic characteristics showed no difference in local recurrence rates between MIPN and FT (23, 29, 35). On the other hand, the firing diameter of FT covers the tumor edge 0.5–1 cm (46). In some anomalistic tumors, FT cannot guarantee complete coverage of the entire tumor. MIPN only needs to ensure that the tumor capsule is intact. Several studies have confirmed that MIPN is more effective in local recurrence rate and distant metastasis rate compared with FT (20, 35).

Conversely, for the meta-analysis results, we mainly describe the perioperative outcomes of MIPN and FT in SRMs. Patients who underwent FT had significantly lower OP of MD (60.34 min), lower EBL of MD (50.28 ml), and LOS of MD (1.95 day) compared with MIPN. For the renal functional outcomes, patients who underwent FT had significantly lower eGFR of WD (8.56 ml/min/1.73m2) compared with MIPN. There are two main reasons that FT has a lower OP, BEL, LOS, and eGFR than MIPN. On the one hand, FT has the advantages of convenient operation and small trauma (47). Research by Park et al. also confirmed that FT has the above results (30). On the other hand, compared with MIPN, FT does not need to block the renal artery, thereby reducing the renal warm ischemia time and ischemia-reperfusion injury and further preserving the advantages of renal function. A system analysis study also confirmed this view (44). Moreover, the EAU guidelines suggest that FT is feasible for renal insufficiency or isolated renal tumors (7). However, there is only subgroup analysis by nephropathy recently published in 2022 back to 2017 (5 years) vs. older studies difference here for EBL. The possible reason is that with the improvement of minimally invasive surgical techniques, the amount of surgical bleeding in 2022 back to 2017 has been significantly controlled. Therefore, compared with FT, there was no difference in the amount of EBL. In addition these are also explained in the discussion section of the article.

We used postoperative complication graded by Clavien Dindo classification for complication analysis (48). Interestingly, no matter one of the minor complications (Clavien 1–2), major complications (Clavien 3–5), and overall complications are similar between MIPN and FT. MIPN has a higher complication rate compared with FT in many studies (31, 35). Although the management of SRMs by MIPN has developed rapidly, the incidence of major complications is still higher than that of FT but not statistically significant. However, all overall complication rates, max complication rates, and minor complication rates in the FT group and MIPN group were lower. Moreover, it did not reach statistical significance.

Choosing MIPN or FT requires comprehensive consideration of the patient’s underlying disease, tumor characteristics (size, number, and anatomical relationship), kidney disease stage, life expectancy, comorbidities, and other related factors (49, 50). The diameter of tumors reported in literature studies is about 2–3 cm, and a few studies are up to 7 cm in size (13, 51). Compared with MIPN, patients receiving FT have smaller average tumor size, relatively uncomplicated anatomical location, multiple renal tumors, endogenous tumors, and other factors (52, 53). Among the SRMs patients treated with FT, most of the patients’ R.E.N.A.L nephrectomy scores showed that the complexity of the operation was Low or medium (11, 34). In adition, part of the literature included in this meta-analysis uses renal measurement scores to assess the complexity of surgery also confirms the appeal argument (11, 14, 16, 23, 29–31, 34). Therefore, we are considering whether to choose MIPN or FT treatment. The Charlson comorbidity index and tumor complexity score can replace the age and tumor size reference factors to make the most profitable decision (54).

Our meta-analysis has several limitations. First, none of the literature in this meta-analysis is a randomized controlled trial. Second, the meta-analysis mainly recorded observational studies and may be affected by factors such as bias and confounding. Third, the OP and LOS in this article are highly heterogeneous. The heterogeneity could not be ruled out after sensitivity analysis and subgroup analysis, so the random-effects model was selected. Fourth, we did not distinguish the surgical approach (laparoscopic vs. percutaneous vs. robotic). Moreover, the long-term prognosis of tumors cannot be fully assessed due to the lack of long-term and follow-up control studies of large cases.

Conclusion

FT has more advantages in protecting kidney function, reducing bleeding, shortening operating time, and shortening the length of stay. There is no difference in local recurrence, distant metastasis, and major complications. For the minimally invasive era, we need to weigh the advantages and disadvantages of all aspects to make comprehensive choices.

Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/ Supplementary Material .

Author Contributions

Conceptualization: LD and LiY. Data curation: LD, LuY, WLL, and WQ. Formal analysis: LD and LuY. Funding acquisition: LD. Methodology: LiY. Investigation: LD and LuY. Resources: WLL. Writing—original draft: WLL. Writing—review and editing: WQ. All authors contributed to the article and approved the submitted version.

Funding

This work was supported by the Scientific Research Foundation of Health and Family Planning Commission of Sichuan Province (20PJ236).

Conflict of Interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Publisher’s Note

All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher.

Supplementary Material

The Supplementary Material for this article can be found online at: https://www.frontiersin.org/articles/10.3389/fonc.2022.732714/full#supplementary-material

Supplementary Figure 1

Egger’s publication bias plot to detect publication bias and Funnel plot to detect publication bias.

Click here for additional data file. (579.9KB, jpeg)
Click here for additional data file. (647.2KB, pdf)

Abbreviations

MIPN, minimally invasive partial nephrectomy; FT, focal therapy; SRMs, small renal masses; RFA, radiofrequency ablation; MWA, microwave ablation; CA, cryoablation; IRE, irreversible electroporation; SBRT, stereotactic body radiation therapy; MD, mean difference; ORs, odds ratios; CIs, confidence intervals; AUA, American Urological Association; EAU, European Association of Urology; RAPN, robot-assisted partial nephrectomy; LPN, laparoscopic partial nephrectomy; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analysis; NOS, Newcastle–Ottawa scale; OP, operating time; EBL, estimated blood loss; LOS, length of stay.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

Supplementary Figure 1

Egger’s publication bias plot to detect publication bias and Funnel plot to detect publication bias.

Click here for additional data file. (579.9KB, jpeg)
Click here for additional data file. (647.2KB, pdf)

Data Availability Statement

The datasets presented in this study can be found in online repositories. The names of the repository/repositories and accession number(s) can be found in the article/ Supplementary Material .

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