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. 2024 May 15;24:593. doi: 10.1186/s12885-024-12377-5

A systematic review and meta-analysis on mortality rate following total pelvic exenteration in cancer patients

Arezoo Esmailzadeh 1,#, Mohammad Sadegh Fakhari 2,#, Nafise Saedi 3, Nasim Shokouhi 4, Amir Almasi-Hashiani 5,6,✉
PMCID: PMC11095034  PMID: 38750417

Abstract

Background

Total pelvic exenteration (TPE), an en bloc resection is an ultraradical operation for malignancies, and refers to the removal of organs inside the pelvis, including female reproductive organs, lower urological organs and involved parts of the digestive system. The aim of this meta-analysis is to estimate the intra-operative mortality, in-hospital mortality, 30- and 90-day mortality rate and overall mortality rate (MR) following TPE in colorectal, gynecological, urological, and miscellaneous cancers.

Methods

This is a systematic review and meta-analysis in which three international databases including Medline through PubMed, Scopus and Web of Science on November 2023 were searched. To screen and select relevant studies, retrieved articles were entered into Endnote software. The required information was extracted from the full text of the retrieved articles by the authors. Effect measures in this study was the intra-operative, in-hospital, and 90-day and overall MR following TPE. All analyzes are performed using Stata software version 16 (Stata Corp, College Station, TX).

Results

In this systematic review, 1751 primary studies retrieved, of which 98 articles (5343 cases) entered into this systematic review. The overall mortality rate was 30.57% in colorectal cancers, 25.5% in gynecological cancers and 12.42% in Miscellaneous. The highest rate of mortality is related to the overall mortality rate of colorectal cancers. The MR in open surgeries was higher than in minimally invasive surgeries, and also in primary advanced cancers, it was higher than in recurrent cancers.

Conclusion

In conclusion, it can be said that performing TPE in a specialized surgical center with careful patient eligibility evaluation is a viable option for advanced malignancies of the pelvic organs.

Keywords: Total pelvic exenteration, Mortality, Colorectal neoplasms, Gynecological neoplasms, Urologic neoplasms

Introduction

Total pelvic exenteration (TPE), an en bloc resection is an ultraradical operation for malignancies which was performed for the first time in 1946 by Alexander Brunschwig [1], and refers to the removal of organs inside the pelvis, including female reproductive organs, lower urological organs and involved parts of the digestive system (rectosigmoid) [2–4].

TPE procedure is used in the treatment of advanced gynecological cancers as well as primary advanced and recurrent rectal cancers [3, 5]. Even though TPE is infrequently performed, it may be considered as the last hope for the treatment of recurrent or advanced cancers [6, 7].

TPE technique was associated with significant complications and mortality in the first decades, but in recent decades due to the improvement of preoperative planning (whole-body positron emission tomography), intraoperative and postoperative care, the survival rate, surgical complications and mortality of candidate patients has improved significantly [4, 8, 9].

Overall survival and disease-free survival rate significantly improved following TPE, especially in well-selected patients [3]. To the best of our knowledge, the highest 5 years overall survival rate was reported as 65.8% [10] in cervical cancer patients following pelvic exenteration and in colorectal cancer patients, one year survival rate was more than 80% in several previous studies [11–14] and the highest five year survival rate was reported as 92.9% in a study by Mark Katory et al. in the United Kingdom [14].

Considering that this surgical technique is considered a rare and advanced technique, significant complications and mortality rate (MR) have been reported for it. Intra-operative mortality, in-hospital mortality, 30- and 90-day mortality are important consequences that are reported for the management of the complications of this surgery. In addition to the survival rate, mortality and complications are also changing over time and depend on the equipment of the surgical center as well as the experience of the surgical team, and different studies have reported different mortality rates and there is no comprehensive review in this regard. The aim of this meta-analysis is to estimate the intra-operative mortality, in-hospital mortality, 30- and 90-day mortality rate and overall mortality rate following TPE in colorectal, gynecological, urological, and miscellaneous.

Methods

Study design

This is a systematic review and meta-analysis in which international databases were searched to find the relevant studies. Standard guideline of “Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) was followed to prepared the report. This study was registered in the PROSPERO (CRD42023467479).

Eligibility criteria

In this study, all observational studies related to the MR after TPE surgery with English full-text were included in the study. There was no time limit for entering the articles, and also in terms of the study design, all the articles that reported the MR including cohort studies, cross-sectional studies and case series studies were included. However, studies which had not defined the surgical procedure of TPE routinely were excluded. Additionally, we excluded case reports, letters to the editor, and review studies from our analysis. Although, we thoroughly screened the full texts of these articles to ensure that any relevant studies that were initially overlooked, were included in our primary search. Further details of the excluded articles are defined in Fig. 1.

Fig. 1.

Fig. 1

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Flow diagram of the literature search for studies included in meta-analysis. TPE: Total Pelvic Exenteration

Information sources and search strategy

Articles published in English were searched. To retrieved relevant articles, the search was carried out using keywords for three international databases including Medline through PubMed, Scopus and Web of Science on November 2023. Different keywords were used to search the databases, and the search strategy in PubMed is given as an example.

((((“Survival“[Mesh] OR “Mortality“[Mesh] OR “mortality” [Subheading] OR “Disease-Free Survival“[Mesh] OR “Survival Analysis“[Mesh] OR “Survival Rate“[Mesh]) OR (“Survival“[tw])) OR (“Mortality“[tw])) OR (“Disease-Free Survival“[tw])) AND (((((“Pelvic Exenteration“[Mesh]) OR (“Pelvic Exenteration“[tw])) OR (“Pelvic Exenteration“[tiab])) OR (“total Pelvic Exenteration“[tw])) OR (“total Pelvic Exenteration“[tiab]))

Data collection process

To select relevant studies, retrieved articles were entered into Endnote software and duplicate articles were removed at this stage. Then the titles and abstracts of the remaining articles were screened and irrelevant articles were discarded. After that, the full text of the remaining articles was evaluated and irrelevant articles were removed. Finally, the required information was extracted from the remaining related articles.

Data items

The required information was extracted from the full text of the retrieved articles by the authors, and in cases of disagreement, decisions were made in consultation with other authors. The data extracted from each article included the name of the first author, year of publication, type of study design, sample size, type of cancer, location of the study, MR, included sample size, quality score of studies and the study population.

Our results were divided into four groups based on type of cancer: colorectal, gynecological, urological, and miscellaneous. The miscellaneous category included data on MR of TPE regardless of cancer type. Other cancers indicated for TPE in this study included squamous cell carcinoma, soft tissue sarcoma, perineal skin cancer, anal cancer, leiomyosarcoma, etc.

MR for intra-operative mortality, in-hospital mortality, 30-and 90-day mortality, was defined as reported deaths due to the surgical procedure and MR for overall mortality included death of the patients during the follow-up period due to surgery or cancer. Notably, patients who died due to other causes or were lost to follow-up were omitted from the analysis.

Study risk of bias assessment

The Joanna Briggs Institute Critical Appraisal (JBI) checklists were used to assess the quality of the included studies [15]. For each type of article, either cohort studies or case series, we utilized the relevant checklists provided by JBI. Each item on the checklist was assigned a score of 1 if the response was “yes”, and 0 if the response was “no”, “unclear”, or “not applicable”. The quality indicators were converted to 100%, Studies addressing ≥ 75% of the checklist items were considered as having a low risk of bias [16]. One author (MSF) carried out the quality assessment.

Effect measures

Effect measures in this study was the intra-operative, in-hospital, 30-day and 90-day and overall MR following TPE. The included sample size and the number of dead people were extracted from the studies, and the MR and 95% confidence interval were calculated.

Synthesis methods and statistical analysis

To check the heterogeneity among the studies, the I2 statistic was used and it was tested using the chi-square test, and if there was significant heterogeneity between the studies, the random-effects model was used to merge the data. Although, based on the heterogeneity between the studies, from a methodological point of view, the fixed effects model was used, but considering that the mortality rate may be different based on the center expertise, surgeon experience, and postoperative care, in addition to the fixed effects model, random effects model was also performed and its results were reported. Egger’s linear regression test, Begg’s test and funnel plot were used to check publication bias. All analyzes are performed using Stata software version 16 (Stata Corp, College Station, TX).

Results

Study selection

In this systematic review, 1751 primary studies (772 papers via Medline, 936 via Scopus and 43 papers via additional search) retrieved. Of the total articles, 695 duplicate articles were identified and removed. Then, the titles and abstracts of the remaining 1153 articles were screened and at this stage, 744 articles were excluded due to the lack of fulfilling the inclusion criteria and the full text of 409 remained articles was evaluated, of which 98 articles entered into this systematic review. All the process was presented in Fig. 1.

Study characteristics

As it was shown in Tables 1 and 98 studies [6, 7, 12–14, 17–102] (5343 cases) were included in the analysis. The oldest one was published in 1967 and the most recent in 2023. Both case series (23 studies) and cohort studies (75 studies) were included in the analysis. The sample size of included studies ranged from 2 to 2305 cases and colorectal, gynecological, urological and miscellaneous cancers were included in the analysis. More details in this regard were presented in Table 1.

Table 1.

Characteristics of Included Studies

Author Publish Year Country Case Series Cancer Type Cancer Origin Surgery Method Sample Size Median Follow up time (month) Inrta-operative MR In-hospital MR 30-day MR 90-day MR Overall MR
Ingiulla et al. [17] 1967 Italy Cohort Gynecological Both Open 51 NR 26
Thornton et al. [18] 1973 USA Case Series Gynecological Primary Open 7 18.5 (range: 7-114) 1 1 3
Karlen et al. [19] 1975 USA Cohort Gynecological Both Open 29 NR 7 16
Eckhauser et al. [20] 1979 USA Case Series Colorectal Primary Open 10 NR 1 1 1 1 1
Ledesma et al. [21] 1981 USA Cohort Colorectal Both Open 30 NR 3
Mori et al. [22] 1981 Japan Cohort Misc. Both Open 21 NR 1 1 3
Boey et al. [23] 1982 China Cohort Colorectal Both Open 26 NR 4 7
Takagi et al. [24] 1985 Japan Case Series Colorectal Primary Open 13 25 (range: 1-132) 0 0 1 7
Cuevas et al. [25] 1988 USA Cohort Gynecological Both Open 120 36 27
Yeung et al. [26] 1993 Canada Cohort Colorectal Both Open 50 NR 7 4
Liu et al. [27] 1994 China Cohort Colorectal Both Open 31 NR 0 0 0 0 16
Lopez et al. [28] 1994 USA Cohort Misc. Both Open 232 NR 34
Sardi et al. [29] 1994 USA Case Series Colorectal Recurrent Open 6 NR 0 0 0 0 1
Woodhouse et al. [30] 1995 UK Case Series Colorectal Primary Open 2 NR 0
Gynecological 3 0
Misc. 6 0
Urological 1 0
Luna-Perez et al. [31] 1996 USA Cohort Colorectal Primary Open 12 46 (range:3-148) 2
Shirouzu et al. [32] 1996 Japan Case Series Colorectal Both Open 26 NR 2
Russo et al. [12] 1999 USA Cohort Colorectal Both Open 47 16.83 1 20
Law et al. [33] 2000 China Cohort Colorectal Both Open 24 mean:49.8 (range:6-160) 0 0 0 0 8
Chen et al. [34] 2001 Taiwan Cohort Colorectal Primary Open 50 NR 0 1 1 1 4
Wiig et al. [35] 2002 Norway Cohort Colorectal Primary Open 47 60 0 5 2
Ike et al. [36] 2003 Japan Cohort Colorectal Primary Open 71 NR 1 3 25
Jimenez et al. [37] 2003 USA Cohort Colorectal Both Open 55 26 (range:0.26–106) 0 0 0 3 20
Recurrent 39 0 0 0
Primary 16 0 0 0
Kamat et al. [13] 2003 USA Case Series Urological Recurrent Open 14 14 (range: 3–36) 0 0 0 0 7
Vitelli et al. [39] 2003 Italy Cohort Colorectal Both Open 8 40 (range:12–120) 2
Houvenaeghel et al. [40] 2004 France Cohort Gynecological Both Open 55 NR 5
Berek et al. [6] 2005 USA Cohort Gynecological Recurrent Open 46 50 0
Leibovici et al. [42] 2005 USA Case Series Urological Recurrent Open 5 range: 5–55 0 0 0
Nguyen et al. [43] 2005 UK Cohort Colorectal Both Open 16 12.5 (range:1-120) 0 0 0
Gynecological 16 0 0 0
Misc. 41 0 0 0
Goldberg et al. [7] 2006 USA Cohort Gynecological Recurrent Open 103 NR 0 1 1 2 2
Ferron et al. [107] 2006 France Case Series Gynecological Primary MIPE 1 total 16 0 0 0 0 0
de Wilt et al. [44] 2007 Netherlands Cohort Gynecological Both Open 17 42 (range:1-155) 0 0 0
Park et al. [45] 2007 South Korea Cohort Gynecological Both Open 30 NR 0 0 0
Ungar et al. [48] 2008 Hungary Cohort Gynecological Primary Open 2 NR 0 0
Vermaas et al. [46] 2008 Netherlands Cohort Colorectal Both Open 35 mean: 28 1
Ferenschild et al. [49] 2009 Netherlands Cohort Misc. Both Open 69 43 (range:1-196) 1
Maggioni et al. [50] 2009 Italy Cohort Gynecological Both Open 48 22.3 (range:1.6–117) 0 0 0
Puntambekar et al. [51] 2009 India Case Series Gynecological Primary MIPE 7 11 (range: 4–24) 0 0 0 0 4
Spahn et al. [52] 2010 Switzerland Cohort Gynecological Both Open 6 30.5 (range:2-144) 0 0 0
Zoucas et al. [53] 2010 Sweden Cohort Misc. Both Open 32 NR 0 0 0 0
Chokshi et al. [54] 2011 USA Cohort Colorectal Both Open 36 NR 0 0 0
Gynecological 6 0 0 0
Misc. 53 0 0 0
Urological 5 0 0 0
Domes et al. [55] 2011 Canada Cohort Colorectal Both Open 28 35 (range: 1-147) 1 1 9
Guimarães et al. [56] 2011 Brazil Case Series Gynecological Recurrent Open 13 mean: 8 2 2 2 10
Mitulescu et al. [57] 2011 Romania Cohort Colorectal Both Open 48 NR 0
Gynecological 159 0
Misc. 213 0
Urological 4 0
Baiocchi et al. [58] 2012 Brazil Cohort Gynecological Both Open 56 13.8 (range: 1.09–114.3) 0
Kuhrt et al. [59] 2012 USA Cohort Colorectal Both Open 36 NR 0 0 0
Gynecological 6 0 0 0
Misc. 53 0 0 0
Urological 3 0 0 0
Ramamurthy et al. [60] 2012 India Cohort Colorectal Primary Open 3 36 (range: 11–76) 0 0 0
Gynecological 10 0 0 0
Misc. 13 0 0 0
Yoo et al. [61] 2012 South Korea Cohort Gynecological Recurrent Open 42 22 (range: 1–60) 0 0 0
Jäger et al. [62] 2013 Sweden Cohort Gynecological Recurrent Open 11 27 (range: 2-110) 0 0 0
Tan et al. [63] 2013 Australia Cohort Misc. Recurrent Open 10 26 (range: 4–169) 0 0 0
Ueda et al. [64] 2013 Japan Cohort Misc. Both Open 13 25.5 0 0 0
Ghouti et al. [71] 2014 France Cohort Colorectal Recurrent Open 14 33.5 (95%CI: 25.4–36.9) 0 0 0
milne et al. [65] 2014 Australia Cohort Misc. Both Open 68 NR 0 0 0
Pathiraja et al. [66] 2014 UK Cohort Gynecological Both Open 9 NR 0 0 0
Petruzziello et al. [67] 2014 Brazil Cohort Gynecological Both Open 14 NR 0 3
Tanaka et al. [68] 2014 Japan Case Series Gynecological Recurrent Open 3 22 (range:3-116) 0 0 0 2
Xin et al. [69] 2014 Singapore Case Series Colorectal Both Open 5 23 0 0 0
Căpîlna et al. [70] 2015 Romania Case Series Gynecological Both Open 6 NR 0
Kusters et al. [72] 2015 Netherlands Cohort Colorectal Both Open 23 62 (range: 2-191) 0 0 0
Moreno-Palacios et al. [73] 2015 Spain Case Series Gynecological Recurrent Open 8 14 (range: 5–69) 0 0 0 0 3
Rombouts et al. [74] 2015 Australia Cohort Colorectal Recurrent Open 48 NR 0 0 0
Ogura et al. [108] 2015 Japan Cohort Colorectal Both Open 15 NR 0 0 0
MIPE 9 0 0 0
Yang et al. [109] 2015 China Case Series Misc. Both MIPE 11 mean: 11.1 (range: 2–24) 0 0 0 0 2
Schmidt et al. [76] 2016 Switzerland Cohort Gynecological Both Open 34 35 (range: 1-263) 0
Chew et al. [77] 2017 Singapore Cohort Misc. Both Open 10 17.6 0 0 0
Katory et al. [14] 2017 UK Cohort Colorectal Both Open 14 30.4 (range: 0.1–83.8) 3
Aslim et al. [78] 2018 Singapore Cohort Urological Both Open 10 11.7 (range: 4.2–47.6) 0 0 0
Hagemans et al. [79] 2018 Netherlands Cohort Colorectal Both Open 126 NR 6 7 11 21
Li et al. [80] 2018 China Cohort Gynecological Both Open 20 28 (range: 12–96) 0 0 0 2
Mehta et al. [81] 2018 UK Case Series Colorectal Both Open 10 15 (IQR:8–37) 0 0 0 0
Rema et al. [89] 2018 India Cohort Gynecological Recurrent Open 17 27.5 (Range: 1.8–99.1) 0
Romeo et al. [82] 2018 Argentina Cohort Gynecological Both Open 15 20.3 (range: 1–60) 0
Tortorella et al. [91] 2018 USA Cohort Gynecological Both Open 45 NR 0 0 0
Pokharkar et al. [110] 2018 India Case Series Colorectal Primary MIPE 10 NR 0 0
Bizzarri et al. [83] 2019 Italy Cohort Gynecological Both MIPE 5 15 (range: 6–37) 0 0 0
Gregorio et al. [84] 2019 Germany Cohort Gynecological Both Open 10 0 0 0
Kiiski et al. [85] 2019 Finland Cohort Gynecological Both Open 26 35.1 (range 2.5–123) 0 0 0
Lago et al. [86] 2019 Spain Cohort Gynecological Both Open 15 18. 5 (range 1–71) 0 0 0
Lee et al. [87] 2019 Australia Case Series Colorectal Both Open 7 7 (range: 2–10) 0 0 0
Gynecological 3 0 0 0
Misc. 10 0 0 0
Nedyalkov et al. [88] 2019 Bulgaria Cohort Gynecological Both Open 9 52.3 (range, 2.3–99.3) 7
Soeda et al. [90] 2019 Japan Case Series Gynecological Both Open 7 27.5 (median: 12) 0 2
Ichihara et al. [111] 2019 Japan Cohort Colorectal Both MIPE 10 NR 0 0 0 0
Open 7 0 0 0 0
Lewandowska et al. [92] 2020 Poland Cohort Gynecological Primary Open 22 NR 0 1 0
Recurrent Open 2 0
Tuech et al. [93] 2020 France Case Series Colorectal Both Open 16 NR 2 8
Vigneswaran et al. [94] 2020 USA Cohort Colorectal Both Open 749 NR 11
Gynecological 335 4
Misc. 2305 41
Urological 1025 22
Nonaka et al. [112] 2020 Japan Cohort Colorectal Both MIPE 4 NR 0 0 0
Bogner et al. [95] 2021 Germany Cohort Colorectal Both Open 37 19.4 (IQR 10.0–32.9) 0 0
Gynecological 14 0 0
Misc. 63 0 2 0 1 2
Brown et al. [96] 2021 Australia Case Series Colorectal Recurrent Open 2 11.5 (Range: 2–18) 0 0 0 0
Kanao et al. [97] 2021 Japan Cohort Gynecological Recurrent MIPE 7 23.1 (Range: 8.7–39.0) 0 0 0 0 0
Nielsen et al. [102] 2022 Denmark Cohort Misc. Both Open 195 23 (range: 0.5–72) 1 6
Rios-Doria et al. [113] 2022 USA Cohort Gynecological Both Open 62 27.6 (range, 1.0–117.5) 0 0
Karkia et al. [114] 2022 UK Case Series Gynecological Recurrent MIPE 1 total 60 0 0 0 0 0
Abdulrahman et al. [99] 2022 UK Cohort Gynecological Both Open 5 69 (range: 2–206) 0 0 0
Quyn et al. [115] 2023 UK Cohort Colorectal Both Open 13

19.5 (IQR 7.9–

53.5 )

 0 0 0 0
Naha et al. [116] 2023 USA Cohort Misc. Both Open 792 NR 14
Ralston et al. [117] 2023 UK Cohort Colorectal Both Open 120 36 37
Saqib et al. [118] 2023 UK Cohort Misc. Both MIPE 3 21 (range: 3–53) 0 0 0
Beppu et al. [119] 2023 Japan Cohort Misc. Both MIPE 24 22 (range: 2–45) 0 0 0
Valstad et al. [120] 2023 Norway Cohort Gynecological Both Open 8 59.28 0 0 0
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Risk of bias within studies

All the articles we reviewed met over 80% of the criteria in the JBI checklists and were thus included in the study. Tables 2 and 3 describe the details of evaluating the included studies according to JBI checklist for cohort studies and case series, respectively.

Table 2.

Quality assessment of cohort studies according to JBI checklist

Author Publish Year Country Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Q10 Q11 Quality Score (%)
Ingiulla et al. [17] 1967 Italy NA NA Y Y Y Y Y Y Y Y Y 81.82
Karlen et al. [19] 1975 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Ledesma et al. [21] 1981 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Mori et al. [22] 1981 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Boey et al. [23] 1982 China NA NA Y Y Y Y Y Y Y Y Y 81.82
Cuevas et al. [25] 1988 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Yeung et al. [26] 1993 Canada NA NA Y Y Y Y Y Y Y Y Y 81.82
Liu et al. [27] 1994 China NA NA Y Y Y Y Y Y Y Y Y 81.82
Lopez et al. [28] 1994 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Luna-Perez et al. [31] 1996 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Russo et al. [12] 1999 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Law et al. [33] 2000 China NA NA Y Y Y Y Y Y Y Y Y 81.82
Chen et al. [34] 2001 Taiwan NA NA Y Y Y Y Y Y Y Y Y 81.82
Wiig et al. [35] 2002 Norway NA NA Y Y Y Y Y Y Y Y Y 81.82
Ike et al. [36] 2003 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Jimenez et al. [37] 2003 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Vitelli et al. [39] 2003 Italy NA NA Y Y Y Y Y Y Y Y Y 81.82
Houvenaeghel et al. [40] 2004 France NA NA Y Y Y Y Y Y Y Y Y 81.82
Berek et al. [6] 2005 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Nguyen et al. [43] 2005 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Goldberg et al. [7] 2006 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
de Wilt et al. [44] 2007 Netherlands NA NA Y Y Y Y Y Y Y Y Y 81.82
Park et al. [45] 2007 South Korea NA NA Y Y Y Y Y Y Y Y Y 81.82
Ungar et al. [48] 2008 Hungary NA NA Y Y Y Y Y Y Y Y Y 81.82
Vermaas et al. [46] 2008 Netherlands NA NA Y Y Y Y Y Y Y Y Y 81.82
Ferenschild et al. [49] 2009 Netherlands NA NA Y Y Y Y Y Y Y Y Y 81.82
Maggioni et al. [50] 2009 Italy NA NA Y Y Y Y Y Y Y Y Y 81.82
Spahn et al. [52] 2010 Switzerland NA NA Y Y Y Y Y Y Y Y Y 81.82
Zoucas et al. [53] 2010 Sweden NA NA Y Y Y Y Y Y Y Y Y 81.82
Chokshi et al. [54] 2011 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Domes et al. [55] 2011 Canada NA NA Y Y Y Y Y Y Y Y Y 81.82
Mitulescu et al. [57] 2011 Romania NA NA Y Y Y Y Y Y Y Y Y 81.82
Baiocchi et al. [58] 2012 Brazil NA NA Y Y Y Y Y Y Y Y Y 81.82
Kuhrt et al. [59] 2012 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Ramamurthy et al. [60] 2012 India NA NA Y Y Y Y Y Y Y Y Y 81.82
Yoo et al. [61] 2012 South Korea NA NA Y Y Y Y Y Y Y Y Y 81.82
Jäger et al. [62] 2013 Sweden NA NA Y Y Y Y Y Y Y Y Y 81.82
Tan et al. [63] 2013 Australia NA NA Y Y Y Y Y Y Y Y Y 81.82
Ueda et al. [64] 2013 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Ghouti et al. [71] 2014 France NA NA Y Y Y Y Y Y Y Y Y 81.82
milne et al. [65] 2014 Australia NA NA Y Y Y Y Y Y Y Y Y 81.82
Pathiraja et al. [66] 2014 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Petruzziello et al. [67] 2014 Brazil NA NA Y Y Y Y Y Y Y Y Y 81.82
Kusters et al. [72] 2015 Netherlands NA NA Y Y Y Y Y Y Y Y Y 81.82
Rombouts et al. [74] 2015 Australia NA NA Y Y Y Y Y Y Y Y Y 81.82
Ogura et al. [108] 2015 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Schmidt et al. [76] 2016 Switzerland NA NA Y Y Y Y Y Y Y Y Y 81.82
Chew et al. [77] 2017 Singapore NA NA Y Y Y Y Y Y Y Y Y 81.82
Katory et al. [14] 2017 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Aslim et al. [78] 2018 Singapore NA NA Y Y Y Y Y Y Y Y Y 81.82
Hagemans et al. [79] 2018 Netherlands NA NA Y Y Y Y Y Y Y Y Y 81.82
Li et al. [80] 2018 China NA NA Y Y Y Y Y Y Y Y Y 81.82
Rema et al. [89] 2018 India NA NA Y Y Y Y Y Y Y Y Y 81.82
Romeo et al. [82] 2018 Argentina NA NA Y Y Y Y Y Y Y Y Y 81.82
Tortorella et al. [91] 2018 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Bizzarri et al. [83] 2019 Italy NA NA Y Y Y Y Y Y Y Y Y 81.82
Gregorio et al. [84] 2019 Germany NA NA Y Y Y Y Y Y Y Y Y 81.82
Kiiski et al. [85] 2019 Finland NA NA Y Y Y Y Y Y Y Y Y 81.82
Lago et al. [86] 2019 Spain NA NA Y Y Y Y Y Y Y Y Y 81.82
Nedyalkov et al. [88] 2019 Bulgaria NA NA Y Y Y Y Y Y Y Y Y 81.82
Ichihara et al. [111] 2019 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Lewandowska et al. [92] 2020 Poland NA NA Y Y Y Y Y Y Y Y Y 81.82
Vigneswaran et al. [94] 2020 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Nonaka et al. [112] 2020 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Bogner et al. [95] 2021 Germany NA NA Y Y Y Y Y Y Y Y Y 81.82
Kanao et al. [97] 2021 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Nielsen et al. [102] 2022 Denmark NA NA Y Y Y Y Y Y Y Y Y 81.82
Rios-Doria et al. [113] 2022 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Abdulrahman et al. [99] 2022 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Quyn et al. [115] 2023 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Naha et al. [116] 2023 USA NA NA Y Y Y Y Y Y Y Y Y 81.82
Ralston et al. [117] 2023 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Saqib et al. [118] 2023 UK NA NA Y Y Y Y Y Y Y Y Y 81.82
Beppu et al. [119] 2023 Japan NA NA Y Y Y Y Y Y Y Y Y 81.82
Valstad et al. [120] 2023 Norway NA NA Y Y Y Y Y Y Y Y Y 81.82
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JBI: Joanna Briggs Institute, NA: not applicable, Y: yes, N: no

Q1: Were the two groups similar and recruited from the same population?

Q2: Were the exposures measured similarly to assign people to both exposed and unexposed groups?

Q3: Was the exposure measured in a valid and reliable way?

Q4: Were confounding factors identified?

Q5: Were strategies to deal with confounding factors stated?

Q6: Were the groups/participants free of the outcome at the start of the study (or at the moment of exposure)?

Q7: Were the outcomes measured in a valid and reliable way?

Q8: Was the follow up time reported and sufficient to be long enough for outcomes to occur?

Q9: Was follow up complete, and if not, were the reasons to loss to follow up described and explored?

Q10: Were strategies to address incomplete follow up utilized?

Q11: Was appropriate statistical analysis used?

Table 3.

Quality assessment of case series according to JBI checklist

Author Publish Year Country Q1 Q2 Q3 Q4 Q5 Q6 Q7 Q8 Q9 Q10 Quality Score (%)
Thornton et al. [18] 1973 USA yes yes yes yes yes yes yes yes yes yes 100
Eckhauser et al. [20] 1979 USA yes yes yes yes yes yes yes yes yes yes 100
Takagi et al. [24] 1985 Japan yes yes yes yes yes yes yes yes yes yes 100
Sardi et al. [29] 1994 USA yes yes yes yes yes unclear yes yes yes yes 90
Woodhouse et al. [30] 1995 UK yes yes yes unclear yes unclear yes yes yes yes 80
Shirouzu et al. [32] 1996 Japan yes yes yes yes yes yes yes yes yes yes 100
Kamat et al. [13] 2003 USA yes yes yes yes yes yes yes yes yes yes 100
Leibovici et al. [42] 2005 USA yes yes yes yes yes yes yes yes yes yes 100
Ferron et al. [107] 2006 France yes yes yes yes yes yes yes yes yes yes 100
Puntambekar et al. [51] 2009 India yes yes yes yes yes unclear yes yes yes yes 90
Guimarães et al. [56] 2011 Brazil yes yes yes yes yes yes yes yes yes yes 100
Tanaka et al. [68] 2014 Japan yes yes yes yes yes yes yes yes yes yes 100
Xin et al. [69] 2014 Singapore yes yes yes yes yes yes yes yes yes yes 100
Căpîlna et al. [70] 2015 Romania yes yes yes yes yes unclear yes yes yes yes 90
Moreno-Palacios et al. [73] 2015 Spain yes yes yes yes yes yes yes yes yes yes 100
Yang et al. [109] 2015 China yes yes yes yes yes yes yes yes yes yes 100
Mehta et al. [81] 2018 UK yes yes yes unclear yes yes yes yes yes yes 90
Pokharkar et al. [110] 2018 India yes yes yes yes yes yes yes unclear yes yes 90
Lee et al. [87] 2019 Australia yes yes yes yes yes unclear yes yes yes yes 90
Soeda et al. [90] 2019 Japan yes yes yes yes yes unclear yes yes yes yes 100
Tuech et al. [93] 2020 France yes yes yes yes yes yes yes yes yes yes 100
Brown et al. [96] 2021 Australia yes yes yes yes yes yes yes yes yes yes 100
Karkia et al. [114] 2022 UK yes yes yes yes yes yes yes yes yes yes 100
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JBI: Joanna Briggs Institute, U: unclear, Y: yes, N: no

Q1: Were there clear criteria for inclusion in the case series?

Q2: Was the condition measured in a standard, reliable way for all participants included in the case series?

Q3: Were valid methods used for identification of the condition for all participants included in the case series?

Q4: Did the case series have consecutive inclusion of participants?

Q5: Did the case series have complete inclusion of participants?

Q6: Was there clear reporting of the demographics of the participants in the study?

Q7: Was there clear reporting of clinical information of the participants?

Q8: Were the outcomes or follow up results of cases clearly reported?

Q9: Was there clear reporting of the presenting site(s)/clinic(s) demographic information?

Q10: Was statistical analysis appropriate?

Quantitative data synthesis and heterogeneity across studies

Colorectal cancers mortality rate

The MR following TPE in colorectal cancers was estimated and the results of meta-analysis suggested that intra-operative MR is 0.2% (n = 27, 95%CI = 0.07–1.11%, I-square = 0.0%), in-hospital MR is 3.11% (n = 31, 95%CI = 2.15–4.46%, I-square = 9.02%), 30-day MR is estimated as 2.61% (n = 35, 95%CI = 1.95–3.48%, I-square = 15.18%), 90-day MR is 6.22% (n = 12, 95%CI = 4.17–9.18%, I-square = 16.87%) and overall MR is estimated as 30.57% (n = 13, 95%CI = 26.9–34.4%, I-square = 60.6%), respectively (Table 4). All analysis was done by fixed-effects model because of no significant heterogeneity among studies. In addition, the overall MR in open surgery was 30.57%, in primary cancer 2.44%, and in primary and recurrent cancers 31.6%. There were not enough studies to perform meta-analysis for recurrent cancer.

Table 4.

Summary of meta-analysis to estimate the mortality rate following TPE in colorectal cancers

Subgroups Time Number of included studies Fixed effect models Random effect models I square
Mortality rate 95%CI Mortality rate 95%CI
Overall Intra-operative mortality 27 0.28% 0.07–1.11% 0.28% 0.07–1.11% 0.0%
In-hospital Mortality 31 3.11% 2.15–4.46% 1.44% 0.52–3.93% 9.02%
30-day Mortality 35 2.61% 1.95–3.48% 2.30% 1.17–4.49% 15.18%
90-day Mortality 12 6.22% 4.17–9.18% 2.96% 0.82–10.1% 16.87%
Overall-mortality 13 30.57% 26.9–34.4% 31.88% 23.8-41.26% 60.6%
Open surgery Intra-operative mortality 25 0.29% 0.07–1.16% 0.29% 0.07–1.16% 0.0%
In-hospital Mortality 29 3.23% 2.24–4.63% 1.59% 0.59–4.20% 10.15%
30-day Mortality 34 2.64% 1.97–3.53% 2.42% 1.25–4.64% 16.48
90-day Mortality 12 6.39% 4.28–9.43% 3.24% 0.94–10.5% 17.66%
Overall-mortality 13 30.57% 26.9–34.4% 31.88% 23.8-41.26% 60.6%
Minimally invasive surgery Intra-operative mortality 4 0% 0.00-100% - - 0.0%
In-hospital Mortality 4 0% 0.00-100% - - 0.0%
30-day Mortality 3 0% 0.00-100% - - 0.0%
90-day Mortality Insufficient data to perform meta-analysis
Overall-mortality Insufficient data to perform meta-analysis
Primary and Recurrent Intra-operative mortality 16 0.0 0-11.47% - - 0.0%
In-hospital Mortality 19 3.16% 2.0-4.96% 1.03% 0.21–4.97% 9.23%
30-day Mortality 25 2.59% 1.88–3.56% 2.08% 0.84–5.04% 17.5%
90-day Mortality 8 6.95% 4.6-10.43% 2.44% 0.33–15.76% 2.13%
Overall-mortality 8 31.6% 27.5–36.2% 34.89% 26.85–43.9% 57.2%
Primary Intra-operative mortality 8 0.91% 0.23–3.56% 0.91% 0.23–3.56% 0.0%
In-hospital Mortality 9 4.50% 2.4–8.17% 4.22% 1.82–9.47% 2.99%
30-day Mortality 7 4.64% 2.23–9.40% 4.64% 2.23–9.40% 0.0%
90-day Mortality 2 3.33% 0.84–12.3% 3.33% 0.84–12.37% 0.0%
Overall-mortality 4 27.6% 20.71–35.8% 2.44% 8.9–51.5% 72.0%
Recurrent Intra-operative mortality 5 0% 0.00-100% - - 0.0%
In-hospital Mortality 5 0% 0.00-100% - - 0.0%
30-day Mortality 5 0% 0.00-100% - - 0.0%
90-day Mortality 2 0% 0.00-100% 0% 0.00-100% 0.0%
Overall-mortality Insufficient data to perform meta-analysis
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Gynecological cancers mortality rate

Regarding MR following TPE in gynecological cancers, the obtained results showed that intra-operative MR is 0.21% (n = 40, 95%CI = 0.05–0.85%, I-square = 0.0%), in-hospital MR is 2.65% (n = 34, 95%CI = 1.61–4.36%, I-square = 1.35%), 30-day MR is estimated as 5.89% (n = 37, 95%CI = 4.65–7.43%, I-square = 0.39%), 90-day MR is 2.74% (n = 7, 95%CI = 1.03–7.07%, I-square = 0.0%) and overall MR is estimated as 25.5% (n = 12, 95%CI = 19.8–32.1%, I-square = 46.6%), respectively (Table 5). All analysis was done by fixed-effects model because of no significant heterogeneity among studies. The overall MR in open surgery was 25.5%, in minimally invasive surgery was 25.0%, and in primary, recurrent and both of them together was 53.8%, 12.7% and 55.5%, respectively.

Table 5.

Summary of meta-analysis to estimate the mortality rate following TPE in gynecological cancers

Subgroups Time Number of included studies Fixed effect models Random effect models I square
Mortality rate 95%CI Mortality rate 95%CI
Overall Intra-operative mortality 40 0.21% 0.05–0.85% 0 0–0 0%
In-hospital Mortality 34 2.65% 1.61–4.36% 0.51% 0.07–3.72% 1.35%
30-day Mortality 37 5.89% 4.65–7.43% 0.32% 0.04–2.70% 0.39%
90-day Mortality 7 2.74% 1.03–7.07% 2.74% 1.03–7.07% 0.0%
Overall-mortality 12 25.5% 19.8–32.1% 35.29% 15.3–62.1% 46.6%
Open surgery Intra-operative mortality 35 0.22% 0.05–0.87% 0 0–0 0%
In-hospital Mortality 29 2.79% 1.69–4.58% 0.59% 0.08–4.07% 2.33%
30-day Mortality 32 6.04% 4.77–7.61% 0.38% 0.05–2.99% 0.70%
90-day Mortality 3 3.08% 1.16–7.91% 3.08% 1.16–7.91% 0.0%
Overall-mortality 8 25.5% 19.7–32.5% 44.82% 19.4–73.2% 67.5%
Minimally invasive surgery Intra-operative mortality 5 0% 0.00-100% - - 0.0%
In-hospital Mortality 5 0% 0.00-100% - - 0.0%
30-day Mortality 5 0% 0.00-100% - - 0.0%
90-day Mortality 4 0% 0.00-100% - - 0.0%
Overall-mortality 4 25.0 9.71–50.8% 5.51% 0.01–96.5% 2.68%
Primary Intra-operative mortality 4 0% 0.00-100% - - 0.0%
In-hospital Mortality 7 3.85% 0.96–14.1% 3.85% 0.96–14.1% 0.0%
30-day Mortality 6 2.04% 0.29–13.1% 1.89% 0.06–39.8% 1.17%
90-day Mortality 2 0% 0.00-100% 0% 0.00-100% 0.0%
Overall-mortality 3 53.8% 28.1–77.6% 53.8% 28.1–77.6% 0.0%
Recurrent Intra-operative mortality 10 0.87% 0.19–3.05% 0% 0.00-100% 0.0%
In-hospital Mortality 8 1.54% 0.50–4.66% 0.99% 0.09–9.52% 3.23%
30-day Mortality 9 1.52% 0.49–4.61% 0.97% 0.09–9.36% 2.81%
90-day Mortality 4 1.69% 0.42–6.5% 1.69% 0.42–6.5% 0.0%
Overall-mortality 6 12.7% 8.03–19.4% 18.6% 2.63–65.8% 23.7%
Primary and Recurrent Intra-operative mortality 26 0% 0.00-100% - - 0.0%
In-hospital Mortality 19 3.14% 1.70–5.74% 0.01% 0-98.02% 0.0%
30-day Mortality 23 7.1% 5.56–8.99% 0.14% 0-5.42% 0.08%
90-day Mortality Insufficient data to perform meta-analysis
Overall-mortality 3 55.5% 40.9–69.2% 55.5% 40.9–69.2% 0.0%
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Urological cancers mortality rate

In the case of urological cancers, there have been fewer studies, but still, the results showed that 30-day MR is estimated as 2.07% (n = 4, 95%CI = 1.37–3.13%, I-square = 0.0%).

Miscellaneous cancers mortality rate

The results of meta-analysis revealed that following TPE in Miscellaneous cancers, MR of intra-operative MR is 0.16% (n = 16, 95%CI = 0.02–1.1%, I-square = 56.9%), in-hospital MR is 0.8% (n = 17, 95%CI = 0.3–2.12%, I-square = 57.6%), 30-day MR is estimated as 1.59% (n = 18, 95%CI = 1.23–2.04%, I-square = 6.01%), 90-day MR is 2.33% (n = 4, 95%CI = 1.11–4.8%, I-square = 0.0%), and overall MR is estimated as 12.42% (n = 3, 95%CI = 9.2–16.6%, I-square = 39.7%) (Table 6). These rates for surgeries are reported in Table 6, but for other cases, due to the lack of sufficient studies, meta-analysis was not performed.

Table 6.

Summary of meta-analysis to estimate the mortality rate following TPE in Misc. cancers

Subgroups Time Number of included studies Fixed effects model Random effects model I square
Mortality rate 95%CI Mortality rate 95%CI
Overall Intra-operative mortality 16 0.16% 0.02–1.10% 0.06% 0-15.87% 56.9%
In-hospital Mortality 17 0.80% 0.30–2.12% 0.78% 0.17–3.46% 57.6%
30-day Mortality 18 1.59% 1.23–2.04% 0.53% 0.09–3.18% 6.01%
90-day Mortality 4 2.33% 1.11–4.80% 2.33% 1.11–4.80 0.0%
Overall-mortality 3 12.42% 9.2–16.6% 9.90% 4.37–20.9% 39.7%
Open surgery Intra-operative mortality 13 0.17% 0.02–1.17% 0.06% 0-16.5% 76.9%
In-hospital Mortality 14 0.9% 0.3–2.3% 0.86% 0.20–3.59% 23.5%
30-day Mortality 15 1.60% 1.25–2.07% 0.60% 0.11–3.33% 9.44%
90-day Mortality 3 2.41% 1.16–4.98% 2.41% 1.16–4.98% 0.0%
Overall-mortality 2 12.2% 8.9–16.4% 12.2% 8.9–16.4% -
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Discussion

In this study, we investigated the MR after TPE using meta-analysis method, which included different types of cancers such as colorectal, gynecological, urological and miscellaneous cancers. The main findings of this study showed that the highest mortality rate was related to overall mortality. The overall mortality rate was 30.57% in colorectal cancers, 25.5% in gynecological cancers and 12.42% in Miscellaneous. In fact, the highest rate of mortality is related to the overall mortality rate of colorectal cancers. Naturally, the MR in open surgeries was higher than in minimally invasive surgeries, and also in primary advanced cancers, it was higher than in recurrent cancers.

Generally, TPE is used in the treatment of advanced gynecological cancers as well as primary advanced and recurrent rectal cancers, so it is mostly used in cases where conventional treatment modalities do not have a suitable prognosis. Due to the fact that the stage of cancer is higher and the prognosis is worse in patients who are candidates for this surgery, it is expected that the MR will be higher, on the other hand, this surgery is considered as an advanced surgery, and its success rate depends on the experience of the surgeon and the equipment of the surgical center.

In a study by Vigneswaran et al. [94] with the largest sample size conducted in the USA, 2305 cases of TPE between 2005 and 2016 were evaluated. Of these, 45% were urological malignancies, 33% colorectal, 15% gynecological and 9% other cancers. The authors have stated that despite the common complications in this surgery, the mortality rate is relatively low and the outcomes during and after the operation are dissimilar in different types of cancer. Also, the prevalence of major complications is 15%, 30-day mortality is 2%, the duration of hospitalization after surgery is 9 days, and blood transfusion is reported in 50% of cases. The results of the present meta-analysis estimated the 30-day mortality rate to be 2.61%, 5.89%, 1.59% and 2.07% in colorectal, gynecological, miscellaneous and urological cancer which is higher than the value reported in the aforementioned study in most cases. Part of this difference can be related to better equipment and care in USA medical centers and part of it to more experience of medical centers and surgical teams. In our study, the results showed that the overall mortality rate in gynecological malignancies is lower than that in colorectal cancers (25.5% vs. 30.57%). Although in the study of Vigneswaran et al. [94], no significant difference was reported in the 30-day mortality rate of different cancers, but the prevalence of complications was higher in gynecological cancers, and the return to the operating room due to complications was also higher in gynecological cancers than in colorectal cancer (12.8% vs. 8.7%), while it was 4.8% for urological cancers.

Intra-operative mortality rate in colorectal cancers with rate of 0.21% showed the highest rate among studied cancers and its value in all other cancers were 0.2% or less. In terms of in-hospital mortality, this rate was estimated at 3.11% for colorectal cancer, and the highest rate of in-hospital mortality rate was related to colorectal cancer. Therefore, the results of our study showed that in performing TPE for colorectal cancers, intraoperative, in-hospital, 30-day, 90-day and overall mortality rate is more than gynecological, urological, and miscellaneous cancers.

It is important to note that while recent advancements in surgical techniques and well-equipped surgical centers have improved mortality rates for TPE, the main rationale for such an aggressive surgery is the potential chance for a cure, which has been reported in up to 63% of patients [103]. However, the effectiveness of alternative options such as robotic-assisted or laparoscopic surgeries in achieving this goal has not been thoroughly studied [104]. One notable study by Bizzarri et al. [83] reported a 30-day mortality rate of 0% following minimally invasive TPE, demonstrating its feasibility in a small group of 5 patients. More research is needed to fully understand the outcomes of minimally invasive TPE compared to conventional surgical method.

The complexity of the TPE procedure makes it challenging to predict outcomes. Factors such as the purpose of surgery (curative or palliative), cancer type, patient comorbidities, and the expertise of the surgical team and center are known to be associated with morbidity and mortality [94, 104, 105]. Patients undergoing TPE also require strong physical and emotional support. Therefore, a skilled multi-disciplinary team is essential for evaluating patient eligibility and performing the surgery. Previous studies have emphasized the use of specific guidelines, such as the enhanced recovery after surgery (ERAS) guideline, to reduce complications [94, 106]. Ultimately, individualized patient selection is recommended before performing TPE.

To the best of our knowledge, this is the largest meta-analysis of MR following TPE. However, several limitations should be acknowledged. Our data may be biased towards reporting more studies with a 0% MR. This is mainly because if a study reported a 0% MR for a specific time period, the MR for previous periods would be assumed to be 0% as well, even if it wasn’t reported in detail. However, if a study reported a MR higher than 0% for a specific time period and didn’t report the previous MRs, those data points were labeled as missing. Furthermore, in this study we included as much studies as possible, to create a holistic picture of MR following TPE. Therefore, it might be subject to bias as all TPE performed since 1976 with proper definition of TPE were included in our analysis. Further studies are required to investigate the impact of surgical intention, surgical center expertise, post-operation care, and patients’ comorbidities on MR following TPE.

Conclusion

In conclusion, it can be said that performing TPE in a specialized surgical center with careful patient eligibility evaluation is a viable option for advanced malignancies of the pelvic organs.

Author contributions

AAH, AE, MSF, NS and NS conceived the study. AAH, AE, MSF, NS and NS contributed to the title, abstract and full-text screening. Data extraction was done by MSF, AE and AAH, and AAH and MSF analyzed the data. All authors contributed equally to the initial draft of the manuscript. All authors have read and approved the final version of the manuscript.

Funding

Not Funded.

Data availability

All data generated or analyzed during this study are included in the article.

Declarations

Ethics approval and consent to participate

Not applicable.

Consent for publication

Not applicable.

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.

Arezoo Esmailzadeh and Mohammad Sadegh Fakhari contributed equally to this work.

References

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