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. 2023 Jan 6;13:273. doi: 10.1038/s41598-023-27430-9

Meta-analysis of laparoscopic radical hysterectomy, excluding robotic assisted versus open radical hysterectomy for early stage cervical cancer

Greg Marchand 1,✉, Ahmed Taher Masoud 1,2, Ahmed Abdelsattar 2, Alexa King 1, Hollie Ulibarri 1, Julia Parise 1, Amanda Arroyo 1, Catherine Coriell 1, Sydnee Goetz 1, Carmen Moir 1, Atley Moberly 1, Malini Govindan 1
PMCID: PMC9822966  PMID: 36609438

Abstract

Recent evidence has shown an increase in recurrence and a decrease in overall survival in patients treated with laparoscopic radical hysterectomy (LRH) and robotic assisted radical hysterectomy (RRH) open techniques (ORH). In addition, several high quality trials were recently published regarding the laparoscopic treatment of early stage cervical cancer. We sought out to reassess the recurrence rates, overall survival, complications and outcomes associated with laparoscopic radical hysterectomy (LRH) techniques against open techniques (ORH) when robotic assisted techniques were excluded. We searched PubMed, Medline, Cochrane CENTRAL, SCOPUS, ClinicalTrials.Gov and Web of Science for relevant clinical trials and observational studies. We included all studies that compared with early stage cervical cancer receiving LRH compared with ORH. We included randomized clinical trials, prospective cohort, and retrospective cohort trials. We included studies that included LRH and RRH as long as data was available to separate the two arms. We excluded studies that combined LRH and RRH without supplying data to differentiate. Of 1244 total studies, we used a manual three step screening process. Sixty studies ultimately met our criteria. We performed this review in accordance with PRISMA guidelines. We analyzed continuous data using mean difference (MD) and a 95% confidence interval (CI), while dichotomous data were analyzed using odds ratio (OR) and a 95% CI. Review Manager and Endnote software were utilized in the synthesis. We found that when excluding RRH, the was no significant difference regarding 5-year overall Survival (OR = 1.24 [0.94, 1.64], (P = 0.12), disease free survival (OR = 1.00 [0.80, 1.26], (P = 0.98), recurrence (OR = 1.01 [0.81, 1.25], (P = 0.95), or intraoperative complications (OR = 1.38 [0.94, 2.04], (P = 0.10). LRH was statistically better than ORH in terms of estimated blood loss (MD = − 325.55 [− 386.16, − 264.94] (P < 0.001), blood transfusion rate (OR = 0.28 [0.14, 0.55], (P = 0.002), postoperative complication rate (OR = 0.70 [0.55, 0.90], (P = 0.005), and length of hospital stay (MD = − 3.64[− 4.27, − 3.01], (P < 0.001). ORH was superior in terms of operating time (MD = 20.48 [8.62, 32.35], (P = 0.007) and number of resected lymph nodes (MD = − 2.80 [− 4.35, − 1.24], (P = 0.004). The previously seen increase recurrence and decrease in survival is not seen in LRH when robotic assisted techniques are included and all new high quality is considered. LRH is also associated with a significantly shorter hospital stay, less blood loss and lower complication rate.

Prospero Prospective Registration Number: CRD42022267138.

Subject terms: Cervical cancer, Outcomes research

Introduction

Cervical cancer is the third most common malignancy and the second most common cause of death from cancer among women in the USA1. The incidence and mortality of cervical cancer have a large geographic variation as it is more common and more fatal in developing countries2. Cervical cancer is classified into early-stage and advanced-stage cancer3. Although staged clinically, the surgical treatment of early-stage cervical treatment is critical for optimizing patient survival4,5. Radical hysterectomy with pelvic lymphadenectomy is a commonly performed procedure for the treatment of cervical cancer6. Patients who are found to be candidates for surgical intervention may see 5-year survival rate increased to as high as 87%7. Abdominal, laparoscopic, robotic-assisted laparoscopic and vaginal approaches to radical hysterectomy have all been described and performed by many authors8. Secondary to the risk of spreading cancers, several authors have stated that gynecologic oncology has been slower to adopt minimally invasive techniques than other specialties, sometimes reserving these techniques for only risk reducing procedures9. The first laparoscopic radical hysterectomy was performed in 199310 and since that time the minimally invasive surgery (both laparoscopic and robotic-assisted laparoscopic) have been increasingly used.11,12. Over the last two decades, many studies have compared the survival outcomes and operative morbidity of the minimally invasive and open surgery for the management of cervical cancer13. Open radical hysterectomy shows significant morbidity including bladder dysfunction, blood loss, and complications of blood transfusion14. Many retrospective studies15–19 have shown that laparoscopic surgery causes perioperative complications less than open surgery. Complicating this, a recent randomized clinical multicenter trial proved that minimally invasive surgery was accompanied by a high rate of recurrence and a worse disease-free survival rate than open surgery20. In addition, a recent retrospective study that included 2461 patients with cervical cancer showed that minimally invasive surgery is associated with a higher risk of death than open surgery21. The culmination of these results was a change in the National Comprehensive Cancer Network (NCCN) guidelines with regards to minimally invasive radical hysterectomy22. The current NCCN guidelines and European Society of Gynaecological Oncology (ESGO) guidelines recommended that the standard surgical approach for management of early-stage cervical cancer is abdominal radical hysterectomy23.

In addition to this recent evidence against minimally invasive radical hysterectomy techniques, several new high quality trials regarding LRH and RRH have been published. For this reason, we were motivated to investigate LRH versus ORH while excluding robotic assisted techniques. We conducted this meta-analysis with late breaking, high quality data to again compare the efficacy and safety of laparoscopic radical hysterectomy with that of open radical hysterectomy for the management of cervical cancer. We have meticulously excluded all robotic assisted cases, and attempted to obtain data to use as many high quality trials as possible, while excluding robotic assisted cases.

Method

This meta-analysis was performed following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)24 and the guidelines reported in the Cochrane Handbook for Systematic Reviews of Interventions25.

Eligibility criteria

The inclusion criteria included studies that met all of the following:

  1. Population: women with early stage cervical cancer

  2. Intervention: Laparoscopic radical hysterectomy (LRH)

  3. Comparator: Open radical hysterectomy (ORH)

  4. Included Study Designs: randomized clinical trials, prospective cohort, and retrospective cohort studies.

And included at least one of our primary or secondary outcomes.

Primary outcomes included:

(1.) Operative time, (2.) Estimated blood loss, (3.) Rate of intraoperative complications, (4.) Rate of postoperative complications, (5.) Rate of blood transfusions.

Secondary outcomes included:

(1.) Rate of recurrence, (2.) Postoperative or intraoperative mortality (defined as within 90 days of surgery), (3.) Five-year survival rate, (4.) Disease-free survival rate, (5.) Number of resected lymph nodes.

We made all efforts to obtain all data possible from all included studies in order to include as many high quality trials as possible, but ultimately excluded those trials that failed our inclusion critieria because they did not publish, or despite our best efforts we could not obtain the necessary data to differentiate which cases included robotic assistance and which did not. We excluded all secondary works, such as meta-analyses and reviews, all animal studies, conference abstracts, and studies with incomplete reported data.

Search and study selection

We searched PubMed, Medline, Scopus, Web of Science, ClinicalTrials.Gov and Cochrane CENTRAL databases from database inception until January 2nd 2022 for articles that matched our inclusion criteria.

We used the following search strategy in our search: (laparoscopic OR laparoscopy) AND (open OR abdominal) AND ((cervical cancer) OR (cancer cervix)) AND (hysterectomy). We screened the included articles in three steps. The first step implied importing the results from electronic databases to a Microsoft Excel26 sheet using EndNote Software27. The second step included a manual title and abstract screening of the articles imported to the Excel sheet. The third step was the full-text screening of the included citations from step 2. Additionally, we manually searched the references of the included papers for possible missed studies. Two researchers separately performed the literature search and eligibility match. Disagreements in the included studies was reached by consensus. A third member of the research team was assigned to settle disputes if consensus could not be reached on any study's eligibility, but was ultimately never needed.

Data collection

We collected three categories of data from each included study: the first category is the baseline and demographic characteristics of the included participants, such as the author, year, country, sample size, age, BMI, included stages, follow up period, time period, adenocarcinoma, squamous cell carcinoma, and positive lymph nodes. The second category included the outcomes of analysis, mainly: Operative time, estimated blood loss, Intraoperative complication, Postoperative complication, Blood transfusion rate, Recurrence, mortality, Five-year survival rate, Disease-free survival, and Resected lymph nodes. The third category included data for risk of bias assessment. The process of data collection was done using Microsoft Excel26.

Risk of bias assessment

We used the quality assessment tools from the National Heart, Lung, and Blood Institute (NHLB) to assess the risk of bias of observational studies28. We followed The Grading of Recommendations Assessment, Development and Evaluation (GRADE) Guidelines in assessing the quality of this study. We assessed the risk of bias of included trials using Cochrane’s risk of bias tool29. The tool assesses proper randomization of patients, allocation concealment, and adequate blinding through seven domains. Each domain was judged to be either “low”, “unclear”, or “high” risk of bias. The details of the GRADE assessment of each outcome can be found in Supplementary Table S1.

Analysis

We performed the meta-analysis of this study using Review Manager Software27. Our study included continuous and dichotomous outcomes. We analyzed continuous data using mean difference (MD) and 95% confidence interval (CI), while dichotomous data were analyzed using odds ratio (OR) and 95% CI. The fixed-effects model was used when data were homogeneous, while heterogeneous data were analyzed under a random-effects model. To measure the presence of inconsistency among the studies, we used the I2 and the p-value of the Chi-square tests30. Values of P < 0.1 or I2 > 50% were significant indicators of the presence of heterogeneity. We tried to solve the inconsistency of heterogeneous outcomes using Cochrane’s leave-one-out method30.

Ethics approval and consent to participate

This Manuscript has been reviewed by the institutional IRB board at Marchand Institute and was found to be exempt from IRB review. (January 2022). Data used was exempt from consent to participate or publish secondary to the nature of the study being a systematic review, retrospectively looking at previously published data.

Commitment to diversity

The Marchand Institute remains committed to diversity and tolerance in its research, and actively maintains a workplace free of racism and sexism. Greater than half of the authors for this study are female and many represent diverse backgrounds and under-represented ethnic groups.

Results

Summary of included studies

The literature search results are illustrated in the PRISMA flow diagram in Fig. 1. We included sixty studies that met our eligibility criteria from the different databases11,15,16,31–87. We analyzed 42,994 patients with cervical cancer in different stages according to FIGO staging (2009 edition)3. A total of 15,995 patients were allocated to the laparoscopic group, while 26,999 patients were allocated to the laparotomy group. The mean age of patients in the laparoscopic group and laparotomy group was 46.5 and 46.7 years, respectively. A summary of the included studies, the demographic data of patients, the included stages, and follow-up duration are described in detail in Tables 1 and 2.

Figure 1.

Figure 1

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PRISMA flow diagram of our literature search.

Table 1.

Summary of the included studies.

Study ID Country Study design Included stages Follow up (mo), (median) Time period Sample size, n
LH OH
Abu-Rustum 2003 USA Retrospective cohort IA1, 2–IB1 NR 2000–2002 19 195
Anagnostopoulos 2017 UK Retrospective cohort IA2–IIA1–IB1 36 2011–2013 36 36
Anchora 2019 Italy Retrospective cohort IA1 49 2016 206 217
Bogani 2014 Italy Prospective cohort IA2, IIA, IB2, IIB 36 2004–2011 65 65
Bogani 2020 Italy Retrospective matched IB1–IIA 59 2013–2014 70 35
Campos 2013 Brazil Clinical trial IA2–IB NR 1999–2004 16 14
Campos 2021 Brazil Clinical trial IA2–IB–IIA 60 1990–2004 16 14
Chen 2014 Taiwan Retrospective cohort IA–IIB NR 2005–2013 32 44
Chen 2019 China Retrospective cohort IB1 50 2010–2018 129 196
Chen 2020 China Retrospective cohort IB1 36 2004–2016 963 1634
Chen 2021 Italy Retrospective matched IB1 42 2008–2018 87 174
Corrado 2018 Italy Retrospective cohort IB1 82 2001–2016 152 101
Estape 2009 USA Retrospective cohort IA2, IB1, IB2 45 2006–2008 17 14
Ditto 2015 Italy Retrospective cohort IA2–IB1 40 2002–2013 60 60
Frumovitz 2007 USA Retrospective cohort IA1, 2–IB1, 2 13 2004–2006 35 54
Ghezzi 2007 Italy Retrospective cohort IA2, IIA, IB1, IB2 58 2004–2007 50 48
Gil-Moreno 2018 Spain Prospective cohort IA2, IIA2–IB1, IIB 112 1999–2016 90 76
Gortchev 2012 Bulgaria Retrospective cohort IB1 26 2006–2010 46 175
Guangyi 2007 China Retrospective cohort IB–IIA 26 1998–2005 90 35
Guo 2018 China Retrospective cohort IA–IIA 39 2000–2003 412 139
He 2020 China Retrospective matched IA1–IA2–IB1 42 2004–2016 739 739
Kanao 2019 Japan Retrospective cohort IB1–IIB 30 2014–2017 80 83
Kim 2018 Korea Retrospective NR NR 2011–2014 3100 3235
Kim 2019 Korea Retrospective cohort IB1–IB2 59.1 2000–2018 122 122
Kim 2020 Korea Retrospective cohort Ia1—IIa1–Ib1–Ib2–IIa2 NR 2006–2016 26 22
Kong 2014 Korea Retrospective cohort IB–IIA 28/58 2006–2013 40 48
Lambaudie 2010 France Prospective Cohort IA1, IA2, IB1 NR 2007–2009 16 22
Laterza 2016 Italy Retrospective cohort IA1, IA2, IB1, IIA2 121.2/43.6 1997–2015 82 68
Lee 2002 Taiwan Prospective cohort IA2–IB 60 2002 30 30
Lee 2011 Korea Retrospective cohort IA2, IIA, IB1, IB2 78 1994–2001 24 48
Li 2021 China Retrospective cohort IA2–IB1–IIA1 33 2009–2016 546 661
Liang 2019 China Retrospective cohort IA1–IA2–IB1–IB2–IIA1–IIA2–IIB NR 2004–2015 5491 12,956
Lim 2019 Singapore Prospective cohort IA1–IIA 29 (0–79) 2009–2014 51 85
Liu 2019 China Retrospective cohort IB1–IB2 NR 2001–2015 271 135
Malzoni 2009 Italy Retrospective cohort IA1 with LVSI–IB 53 (4–89) 1995–2007 65 62
Margina 2008 USA Prospective cohort IB, IC, IIA, IIB, IIIC 40 1993–2006 31 35
Mendivil 2016 USA Retrospective cohort IA2–IIB 39 2009–2013 39 49
Naik 2010 UK Clinical trial IB1 NR 2005–2007 7 6
Nam 2012 Korea Retrospective cohort IA2–IIA 92 1997–2008 263 263
Paik 2019 Korea Retrospective cohort IB–IIA 63.6 2000–2008 133 605
Park 2013 Korea Retrospective cohort IB2–IIA2 33 1997–2011 31 30
Park 2016 Korea Retrospective cohort IA2–IIA 58.8 1997–2013 186 107
Qin 2020 NR Retrospective cohort IA1, IA2, IB1 59 59 172 84
Rodriguez 2021 Colombia Retrospective cohort IA1–IIA2–IIB1 52.35 2006–2017 681 698
Sert 2011 Norway Retrospective cohort IA1–IB1 /IA1–IB1 63.2 2005–2009 7 26
Shanmugam 2020 India Retrospective cohort IA1, IA2, IB1, IB 33.5 2012–2018 82 89
Sharma 2006 England Retrospective cohort IA2–IIB 38.25 1999–2005 35 32
Soliman 2011 Brazil Retrospective cohort NR NR 2007–2010 31 30
Steed 2004 Canada Retrospective cohort IA–IB 20 1996–2003 71 205
Suh 2015 Korea Retrospective cohort IA2–IIA 44 2003–2011 55 106
Taylor 2011 USA Retrospective cohort IA2–IB1 /IA2–IB1 NR 2003–2009 9 18
Topatas 2014 Turkey Retrospective cohort IA2–IB2 43 2007–2010 22 46
Wang 2019 China Retrospective cohort IA1, IA2, IB1, IB 41.3 (6–193.5) 2001–2015 217 179
Wright 2012 USA Retrospective cohort NR NR 2006–2010 217 1610
Xiao 2015 China Retrospective cohort IA–IIB 106 48
Xiao 2016 China Retrospective cohort IA–IIA 48.6 2001–2014 42 16
Xu 2020 China Clinical trial IA1, IA2, IB1, IB NR NR 84 84
Yuan 2019 China Retrospective cohort IA2–IB2 64 2012–2014 99 99
Zhang 2017 China Retrospective cohort IA2–IIB 54 2008–2012 35 42
Zhao 2021 China Retrospective cohort IA2–IIA2 60 2013–2016 148 939
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NR not reported, mo month.

Table 2.

Baseline characteristics of participants.

Study ID Age (years), (mean, SD) (median, range) BMI, (mean, SD) (median, range) Squamous n (%) Adenocarcinoma n (%) Positive lymph nodes n (%)
LH OH LH OH LH OH LH OH LH OH
Abu-Rustum 2003 42.6 (30–69) 43.6 (20–85) 23.1 (18–30) 24.6 (18–40) 10 (53%) 132 (67%) 7 55 NR NR
Anagnostopoulos 2017 44.6 (12.2) 41.2 (12.7) 25.8 (3.8) 26.4 (4.7) 25 (69%) 20 (55%) 11 (31%) 16 (45%) NR NR
Anchora 2019 46 (19–85) 46 (26–83) 29 (17–40) 26 (18–39) 139 (67.5) 141 (65.0 67 (32.5) 76 (35.0) 17 (8.3) 43 (19.8)
Bogani 2014 48.9 (± 13.5) 50.9 (± 14) 25.1 (± 5.2) 25.9 (± 6.1) 20 (31%) 22 (34%) 45 (69%) 43 (66%) 18 (28%) 17 (26%)
Bogani 2020 45 (25–82) 45 (25–68) 22.4 (15.8–39.8) 23.1 (15.7–33.3) 24 (68%) 59 (84%) 7 (20%) 8 (11%) 10 (28%) 28 (40%)
Campos 2013 36.19 ± 9.78 39.64 ± 6.23 NR NR 12 (75%) 12 (86%) 4 (25%) 2 (14%) NR NR
Campos 2021 NR NR NR NR NR NR NR NR NR NR
Chen 2014 51.2 (11.9) 51.9 (11.3) 23.2 (3.4) 24.9 (4.6) 26 (81.3) 33 (75) 1 (3.1) 1 (2.3) 3 (9.4) 9 (20.5)
Chen 2019 49.29 ± 9.31 51.69 ± 10.25 22.99 ± 3.29 22.98 ± 3.14 103 (79.84) 165 (84.18) 19 (14.73) 23 (11.73) 1 (0.78) 11 (5.61)
Chen 2020 47.0 ± 9.3 46.7 ± 9.6 NR NR 784 (100%) 1393 (100%) 0 0 78 (9.9%) 106 (7.6%)
Chen 2021 49.00 ± 12.00 48.00 ± 14.00 NR NR 66 (75.86) 140 (80.46) 18 (20.69) 27 (15.52) 4 (4.60) 8 (4.60)
Corrado 2018 45 (23–78) 50 (28–76) 23.5 (17–35) 24.8 (18–51) 110 (72.3%) 68 (67.3%) 37 (24.3%) 23 (22.8%) 148 (97.3%) 97 (96%)
Estape 2009 52.8 (4.8) 42 (12) 28.1 (4.8) 29.5 (6.4) 11 (64.7%) 10 (71.4%) 6 (35.3%) 2 (14.3%) NR NR
Ditto 2015 46 (29.79) 45.5 (15.78) 24.3 (2.9) 24.0 (4.3) 36 (60%) 35 (58%) 24 (40%) 25 (42%) 3 (5%) 6 (10%)
Frumovitz 2007 40.8 (28–63) 42.5 (27–68) 28.1 (18–40) 28.2 (17–46) 15 33 17 16 NR NR
Ghezzi 2007 47 (24–78) 53 (28–75) 23 (17.4–35) 25 (19–43) 38 (76%) 33 (68.7%) 7 (14%) 13 (27.1%) 7 (14%) 9 (18.7%)
Gil-Moreno 2018 46.31 (11.04) 50.5 (13.6) 26 (18–38) 26.5 (18–40) 57 (63.3) 47 (61.8) 27 (30) 23 (30.2) 10 (11.11) 12 (15.79)
Gortchev 2012 42.5 ± 9.9 49.0 ± 11.0 NR NR 41 (89.1%) 167 (95.4%) 5 (10.9%) 8 (4.6%) 5 (10.9%) 42 (24.0%)
Guangyi 2007 42 ± 9 44 ± 11 NR NR 81 25 5 4 18 4
Guo 2018 44.19 (25–76) 40.52 (23–62) 22.81 (14.33–35.61) 23.19 (13.88–36.63) 340 (82.52) 110 (79.14) 72 (17.48) 29 (20.86) 53 (12.86) 20 (14.39)
He 2020 46.80 ± 9.460 46.69 ± 9.367 NR NR 641 641 89 89 71 71
Kanao 2019 44.0 ± 10.2 49.0 ± 11.5 20.5 (19.1–23.3) 21.4 (19.7–23.7) 37 (46.3) 44 (53.0) 43 (53.7) 39 (47.0) 9 (11.2) 12 (14.5)
Kim 2018 40 sd is NR 45 NR NR NR NR NR NR NR NR
Kim 2019 49.5 ± 11.2 49.0 ± 11.0 148 (66.7) 167 (75.2) 62 (27.9) 42 (18.9) 19 (8.6) 23 (10.4)
Kim 2020 48.77 (11.82) 53.82 (11.13) 23.80 (3.47) 24.43 (2.77) 21 (80.8) 15 (68.2) 5 (19.2) 6 (27.3) NR NR
Kong 2014 45.0 ± 10.6 48.0 ± 11.0 22.3 ± 2.9 23.4 ± 3.3 30 (75.0) 39 (81.3) 7 (17.5) 7 (14.6) 7 (17.5) 8 (16.7)
Lambaudie 2010 45 (32–57) 53 (31–72) 21.9 (14.3–39.4) 21.9 (17.2–34) 11 (68.7%) 17 (85.0%) 4 (25.0%) 3 (15.0%) NR NR
Laterza 2016 43 (24–77) 48 (26–85) 23.44 (16.9–39.76) 24.52 (19.3–43.3) NR NR NR NR 2 (2.4) 1 (1.6)
Lee 2002 46.2 ± 7.2 48.0 ± 6.8 NR NR 27 25 3 5 14 5
Lee 2011 48.4 (39–68) 50.2 (34–67) 23.4 (18.2–32.4) 23.9 (15.8–34.6) 19 (79.2%) 38 (79.2%) 4 (16.7%) 8 (16.7%) 4 (16.7%) 10 (20.8%)
Li 2021 46.94 ± 9.367 47.03 ± 9.354 NR NR 451 (85.6) 565 (58.48) 82 (15.02) 78 (11.8) 51 (9.34) 46 (6.96)
Liang 2019 NR NR NR NR 4691 (85.4) 11,404 (88) 559 (10.2) 1006 (7.8) NR NR
Lim 2019 47 (28–70) 49 (30–70) 22.9 (12.9–33.7) 23.4 (14.7–33.9) 21 (41.2) 50 (58.8) 25 (49.0) 27 (31.8) 7 (13.7) 12 (14.1)
Liu 2019 42.9 ± 9.1 42.6 ± 7.9 23.1 ± 2.8 23.7 ± 3.0 217 (80.1) 119 (88) 42 (15.5) 12 (8.9) 42 (15.5) 15 (11.1)
Malzoni 2009 40.5 ± 7.7 42.7 ± 8.6 26 (19–35) 29 (19–35) 56 (86) 53 (85) 7 (10.5) 6 (10) 23.5 ± 5.1 25.2 ± 6.2
Margina 2008 54.9 (14.3) 50.9 (8.6) 26.8 (4.6) 27.3 (5.8) 12 14 6 7 NR NR
Mendivil 2016 47.8 ± 12.02 51.3 ± 12.48 27.9 ± 5.71 29.2 ± 6.00 38 (69) 27 (77) 9 (18) 5 (12.8) NR NR
Naik 2010 38.5 (33.5–53.5) 37 (29.5–46) 24.8 ± 1.3 25.0 ± 1.8 6 (85) 5 (83) 1 (14) 1 (16) NR NR
Nam 2012 46.4 46.5 23.9 23.2 214 (81.4) 207 (78.7) 41 (15.6) 46 (17.5) 252 (95.8) 252 (95.8)
Paik 2019 45.2 ± 10.8 48.9 ± 11.2 NR NR 91 (68.4) 453 (74.9) 42 (31.6) 152 (25.1) 0 0
Park 2013 48.5 (25–77) 48.1 (25–84) 23.1 (15.6–34.8) 23.7 (17.6–34.7 90 (78.3) 154 (81.9) 25 (21.7) 34 (18.1) 46 (40) 71 (37.8)
Park 2016 45.3 (27–71) 47.3 (28–73) 23.69 (17.1–34.9) 23.58 (17.1–35.9) 0 (0) 0 (0) 186 (100) 107 (100%) 29 (15.6) 16 (15.0)
Qin 2020 44.3 ± 8.2 42.8 ± 8.3 23.1 ± 2.8 23.2 ± 3.0 72 (85.7) 72 (85.7) 35 (20.3) 35 (20.3) 15 (8.7) 9 (10.7)
Rodriguez 2021 NR NR NR NR 451 (66.2%) 462 (66.3%) 206 (30.3%) 208 (29.8%) 77 (11.3) 56 (8)
Sert 2011 45.0 ± 12.9 44.8 ± 11.8 22.5 ± 1.84 25 ± 3.0 5 (71.4) 19 (73) 2 (28.6) 6 (23) NR NR
Shanmugam 2020 52.5 50.3 NR NR 74 (43.3%) 79 (46.2%) 7 (4.1%) 7 (4.1%) 7 (12.1%) 4 (6.8%)
Sharma 2006 43.4 (28–60) 42.8 (28–66) NR NR 18 (51.4) 16 (50) 9 (25.7) 11 (34.3) NR NR
Soliman 2011 44.2 (23.55–64.9) 48.1 (25.5–82.2) 29.5 (18.7–47.8) 26.2 (20.9–44.5) 16 (51.6) 13 (43.33) 12 (38.7) 16 (53.3) 3 (10) 9 (31)
Steed 2004 43 (30–69) 44 (24–86) NR NR 31 (44) 111 (54) 40 (56) 94 (46) 5 (7) 18 (9)
Suh 2015 49.1 ± 11.3 48.7 ± 11 23.1 ± 3.25 23.55 ± 3.7 NR NR NR NR 5 (9) 39 (36.8)
Taylor 2011 41.4 (31–60) 41.1 (25–61) 26.3 (20.6–36.1) 26.9 (17–38.3) 5 (55.5) 11 (61.1) 4 (44.44) 7 (38.88) NR NR
Topatas 2014 46.5 (40–57) 50 (46–58) 18 (81.8) 29 (63.0) 1 (4.6) 5 (10.9) 2 (9.1) 3 (6.7)
Wang 2019 45.95 ± 7.331 44.76 ± 7.743 23.25 ± 2.629 23.56 ± 3.286 188 (86.6) 160 (89.4) 25 (11.5) 9 (5.0) 87 (40.1) 71 (39.7)
Wright 2012 NR NR NR NR NR NR NR NR NR NR
Xiao 2015 43.7 ± 9.3 45.7 ± 11.3 23.8 ± 3.9 24.7 ± 3.8 96 (90.6%) 42 (87.5%) 6 (5.7%) 5 (10.4%) 9 (8.5%) 9 (18.8%)
Xiao 2016 47.1 ± 9.9 55.1 ± 7.6 23.0 ± 3.0 23.8 ± 2.6 42 (100) 16 (100) 0 (0) 0 (0) NR NR
Xu 2020 46.67 ± 9.49 44.9 ± 8.08 NR NR 65 64 14 16 NR NR
Yuan 2019 43.58 ± 8.86 44.56 ± 7.60 44.56 ± 7.60 24.56 ± 1.50 82 (82.8%) 82 (82.8%) 14 (14.1%) 13 (13.1%) 11 (11.1% 10 (10.1%)
Zhang 2017 45 (29–64) 46.6 (27–75) 22.68 ± 3.15 24.07 ± 3.3 32 (91.4) 40 (95.2) 3 (5.6) 2 (4.8) NR NR
Zhao 2021 47.02 ± 8.70 49.53 ± 9.32 NR NR NR NR NR NR NR NR
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NR not reported, n number, SD standard deviation.

Results of risk of bias assessment

The result of the quality assessment yielded an overall moderate risk of bias according to Cochrane`s tool and the mean score for observational studies was 10.57 out of 14 according to NHLB. All clinical trials44,55,56,83 reported proper randomization therefore they were categorized as low risk of bias. All clinical trials were at low risk of bias regarding attrition bias and selective reporting. A detailed illustration of the quality assessment of the included studies is illustrated in Supplementary Table S2.

Analysis of outcomes

Operative time (minutes)

Operating time was reported by 42 studies. We found that ORH operating time was significantly lower than LRH operative time (MD = 20.48 [8.62, 32.35], (P = 0.007). Pooled data were heterogeneous (P < 0.001); I2 = 98% which could not be solved by the leave-one-out method or subgroup analysis (Fig. 2).

Figure 2.

Figure 2

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Forest plot of operative time.

Estimated blood loss (ml)

We analyzed 6410 patients from 39 studies that reported the estimated blood loss. The overall mean difference showed that blood loss was significantly lower in LRH group than ORH group (MD = − 325.55 [− 386.16, − 264.94] (P < 0.001)), Pooled analysis was heterogeneous (P < 0.001); I2 = 97% (Fig. 3).

Figure 3.

Figure 3

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Forest plot of estimated blood loss (EBL).

Intraoperative complication

Thirty two studies reported the rate of intraoperative complications. We found no significant difference between both groups (OR = 1.38 [0.94, 2.04], (P = 0.10)). Data was heterogeneous (P < 0.001); I2 = 69% as shown in Fig. 4A. We solved the heterogeneity by excluding Liang et al.87 (P = 0.15); I2 = 21%, the overall odds ratio after solving heterogeneity did not show any significant difference between both groups (OR = 1.14 [0.86, 1.51], (P = 0.37)) (Fig. 4B).

Figure 4.

Figure 4

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Forest plot of the rate of intraoperative complications before (A) and after (B) solving for heterogeneity by excluding the Liang et al. study.

Postoperative complication

A total of 33,563 patients were analyzed from 43 studies that reported postoperative complications. The overall odds ratio showed that the LRH group had a postoperative complications rate significantly lower than that of ORH (OR = 0.70 [0.55, 0.90], (P = 0.005)). Pooled data was heterogeneous (P < 0.001); I2 = 78%. We could not solve heterogeneity by the leave-one-out method or subgroup analysis (Fig. 5).

Figure 5.

Figure 5

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Forest plot of the rate of postoperative complications.

Length of hospital stay (days)

Forty-one studies reported length of hospital stay. We found that patients in the LRH group stayed at hospital fewer days than patients in the ORH group (MD = − 3.64 [− 4.27, − 3.01], (P < 0.001)). We found heterogeneity which could not be solved by the leave-one-out method or subgroup analysis (Fig. 6).

Figure 6.

Figure 6

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Forest plot of the average length of hospital stay.

Resected lymph nodes

Thirty six studies reported the number of resected lymph nodes as an outcome. Pooled analysis showed that the LRH group was associated with fewer resected lymph nodes than the ORH group (MD = − 2.80 [− 4.35, − 1.24], (P = 0.004)). We found heterogeneity among studies (P < 0.001); I2 = 93% (Fig. 7).

Figure 7.

Figure 7

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Forest plot of the number of resected lymph nodes.

Five-year Overall Survival

A total of 8610 patients were analyzed from 22 studies. The combined analysis did not show any significant difference between both groups (OR = 1.24 [0.94, 1.64], (P = 0.12)). A little heterogeneity was found among studies (P = 0.03); I2 = 40% (Fig. 8A). We solved the heterogeneity by excluding Corrado et al.59 (P = 0.21); I2 = 19%. The overall analysis after solving heterogeneity also showed no significant difference between both groups (OR = 1.10 [0.87, 1.40], (P = 0.43)) (Fig. 8B).

Figure 8.

Figure 8

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Forest plot of five-year overall survival before (A) and after (B) solving for heterogeneity by excluding the Corrado et al. study.

Disease free survival

Twenty seven studies reported DFS. Pooled analysis did not show any difference between both groups (OR = 1.00 [0.80, 1.26], (P = 0.98)). Data was heterogeneous (P = 0.002); I2 = 50% (Fig. 9).

Figure 9.

Figure 9

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Forest plot of the rate of disease free survival.

Postoperative or Intraoperative Mortality (Defined as within 90 days postop)

Twenty four studies reported mortality as an outcome. The overall odds ratio showed no significant difference between either group (OR = 0.86 [0.69, 1.06], (P = 0.15). Pooled analysis was homogeneous (P = 0.14); I2 = 24% (Fig. 10).

Figure 10.

Figure 10

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Forest plot of the postoperative or intraoperative mortality rate.

Recurrence

A total of 19,610 patients were analyzed from 40 studies. We found no significant difference between the two groups (OR = 1.01 [0.81, 1.25], (P = 0.95). Data was heterogeneous (P < 0.001); I2 = 56% (Fig. 11).

Figure 11.

Figure 11

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Forest plot of recurrence of disease.

Blood transfusion rate

The combined analysis of 12,673 patients from 29 studies favored the LRH group significantly (OR = 0.28 [0.14, 0.55], (P = 0.002). Pooled analysis was heterogeneous (P < 0.001); I2 = 96% (Fig. 12).

Figure 12.

Figure 12

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Forest plot of the rate of blood transfusion.

A funnel plot and Egger test of all outcomes can be found in Supplementary File S1. A separate sensitivity analysis involving only the studies with a low risk of bias can also be found in Supplementary File S2. The sensitivity analysis showed different findings only in the outcome of postoperative complications, where the result changed from statistically significant to insignificant. There were no changes in any other outcomes within the sensitivity analysis.

Discussion

This is the largest scale meta-analysis to date that has compared LRH to ORH through an evaluation of the available evidence, and the first, to our knowledge, to attempt to do so while specifically excluding robotic assisted techniques. In our study, we found that LRH was associated with a significantly lower incidence of estimated blood loss, postoperative complications. In addition, predictably, the LRH group had a short period of postoperative hospital stay. The number of the resected in the LRH group lymph node was significantly fewer than that of the ORH group. The combined analysis did not show any significant difference between both groups regarding 5-year overall survival, disease-free survival, and postoperative or intraoperative mortality. The duration of the surgical procedure was significantly longer in the LRH compared to ORH. This stands in contrast to previous studies that showed decreased survival as a result of minimally invasive radical hysterectomy techniques20.

Although isolated studies have disagreed with these results, the majority of previous systematic reviews and meta-analyses have not. In 2015, Wang et al.88 performed a meta-analysis of 12 cohort studies. They demonstrated similar results to our study. They conclude that LRH was better than ORH regarding the short-term outcomes such as faster functional recovery, estimated blood loss, and postoperative complications. The survival outcomes were also similar in both groups.

Smith et al.89 performed another meta-analysis to compare the minimally invasive hysterectomy with abdominal radical hysterectomy. They found that in more than 22,000 women with early-stage cervical cancer the progression-free survival was significantly worse for women who underwent the minimally invasive radical hysterectomy. This finding is strengthened with longer follow-up. The pooled relative risk for postoperative or intraoperative mortality was lower in the minimally invasive group.

In 2020, Kampers et al.90 performed the first meta-analysis stratifying the patients subjected to different operation techniques according to their risk factors. They compared the survival rates of open hysterectomy and laparoscopic hysterectomy in different risk groups. The study demonstrated that protective techniques in laparoscopy result in improved survival.

Kong et al.84 conducted a retrospective analysis of 88 patients with a cervical cancer diameter of 3 cm or greater. They found that LRH can be a feasible alternative surgical procedure for the management of FIGO stage IB and IIA cervical cancer. However, the institution at which the study was performed was introduced with the laparoscopic approach much later than the laparotomy approach. This in turn made the follow-up period in the LRH group relatively short to make any conclusive remarks on survival benefits.

Liang et al.87 reviewed the records of 18,447 patients undergoing radical hysterectomy for cervical cancer. They demonstrated that laparoscopic hysterectomy was associated with a higher risk of major complications than conventional laparotomy. Prior to our review, this study probably represented the largest scale evidence that assessed surgical complications after radical hysterectomy. Other studies to attempt this were single-center studies with small sample sizes15,60,74. In reconciling why the findings of Liang et al. did not also appear as statistically significant in our analysis, we hypothesize that this had to do with limitations on Liang’s study design. This study relied on inpatient medical records or readmission records to obtain information on complications without regular follow-up of the patients. Therefore, without any first-hand knowledge of the circumstances of this study we would hypothesize that perhaps this their conclusion may not have been as statistically significant if direct outreach to patients had been attempted, consistent with other cohort analyses.

In 2021, Campos et al.55 performed a single-center randomized controlled trial on 30 patients with cervical cancer and lymphovascular invasion. They demonstrated a non-significant trend of worse outcomes for LRH. The overall survival time and disease-free survival time were longer in the LRH group. However, the main limitation facing the study was the small sample size.

In 2018, the LACC study by Ramirez et al.20 found that the minimally invasive radical hysterectomy had lower rates of overall survival and disease-free survival than abdominal radical hysterectomy. It was largely based on this study that the National Comprehensive Cancer Network (NCCN) recommended careful counseling of the patient about short-term versus long-term outcomes and oncologic risks of the different surgical approaches.

Limitations

Although the main limitation facing us in this study is the heterogeneity in some outcomes, we managed to understand most of the attributing factors. We believe the use of studies with different designs and disparity in follow-up periods was responsible for the heterogeneity, which is understandable. Another possible limitation of our study includes selection bias, which is difficult to account for. With observational studies, there is always the possibility that surgeons have intentionally selected out cases for laparoscopic radical approaches that appear easier or have different characteristics than those chosen to be performed open. This could affect data. Our analysis represents the most recent and wide-scale evidence that compares LRH to ORH among women with cervical cancer. In light of this controversy it would be desirable to have more well designed prospective randomized trials in order to strengthen the evidence and dissolve any remaining controversy.

Conclusion

We conclude that LRH is associated with a significantly lower incidence of estimated blood loss, postoperative complications. In addition, the LRH had a short period of postoperative hospital stay. In contrast to previous studies that mixed robotic assisted cases we found no difference regarding 5-year overall survival and recurrence excluding robotic assisted cases.

Supplementary Information

Supplementary Table S1. (551KB, docx)
Supplementary Table S2. (16.5KB, docx)
Supplementary Information 3. (392.1KB, docx)
Supplementary Information 4. (283.6KB, docx)
Supplementary Legends. (14.7KB, docx)

Acknowledgements

The Marchand Institute for Minimally Invasive Surgery would like to acknowledge the efforts of all of the students, researchers, residents and fellows at the institute who put their time and effort into these projects without compensation, only for the betterment of women’s health. We firmly assure them that the future of medicine belongs to them.

Author contributions

All authors attest to significant contributions to this work. In particular the following duties were performed by the listed authors. This list does not preclude these authors from making other significant contributions to other portions of this work, and this Institute values all of the effort from our valuable team. (Middle initial corresponds to the second letter of the first name to avoid ambiguity.) Conceptualization was performed mostly by G.M., A.H.M., and A.H.A. Initial draft was composed mostly by A.K., H.U., A.M.A., C.C., S.G., C.M. and A.T.M. Data collection was performed mostly by C.C., S.G., and C.M. Data analysis was performed mostly by J.P., A.M.A., C.C., C.M., and A.T.M. Final draft and discussion was written mostly by G.M., A.H.M., and S.G. Data used was exempt from consent to participate or publish secondary to the nature of the study being a systematic review, retrospectively looking at previously published data.

Data availability

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

Competing interests

The authors declare no competing interests.

Footnotes

Publisher's note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

The online version contains supplementary material available at 10.1038/s41598-023-27430-9.

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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 Table S1. (551KB, docx)
Supplementary Table S2. (16.5KB, docx)
Supplementary Information 3. (392.1KB, docx)
Supplementary Information 4. (283.6KB, docx)
Supplementary Legends. (14.7KB, docx)

Data Availability Statement

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

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