{"paper_id":"9c7e5a92-d148-4d7a-bb59-519d8931ad3f","body_text":"O R I G I N A L A R T I C L E Open Access\nSurgical outcomes of laparoscopic\nhysterectomy with concomitant\nendometriosis without bowel or bladder\ndissection: a cohort analysis to define a\ncase-mix variable\nEvelien M. Sandberg 1, Sara R. C. Driessen 1, Evelien A. T. Bak 1, Nan van Geloven 2, Judith P. Berger 1,3,\nMathilde J. G. H. Smeets 3, Johann P. T. Rhemrev 3 and Frank Willem Jansen 1,4,5*\nAbstract\nBackground: Pelvic endometriosis is often mentioned as one of the variables influencing surgical outcomes of\nlaparoscopic hysterectomy (LH). However, its additional surgical risks have not been well established. The aim of\nthis study was to analyze to what extent concomitant endometriosis influences surgical outcomes of LH and to\ndetermine if it should be considered as case-mix variable.\nResults: A total of 2655 LH ’s were analyzed, of which 397 (15.0%) with concomitant endometriosis. For blood loss and\noperative time, no measurable association was found for stages I ( n = 106) and II ( n = 103) endometriosis compared to\nLH without endometriosis. LH with stages III ( n =9 3 )a n dI V(n = 95) endometriosis were associated with more intra-\noperative blood loss (p = < .001) and a prolonged operative time ( p = < .001) compared to LH without endometriosis.\nNo significant association was found between endometriosis (all stages) and complications ( p =. 6 2 ) .\nConclusions: The findings of our study have provided numeric support for the influence of concomitant endometriosis\non surgical outcomes of LH, without bowel or bladder dissection. Only stages III and IV were associated with\na longer operative time and more blood loss and should thus be considered as case-mix variables in future\nquality measurement tools.\nKeywords: Concomitant endometriosis, Laparoscopic hysterectomy, Case-mix correction, Surgical outcome measures\nBackground\nMeasuring surgical outcomes to improve quality of\nhealth care has received increasing attention over the\npast decades. Consequently, many national registra-\ntion systems have been developed to collect hospital\ndata and compare surgical outcomes between hospi-\ntals or even surgeons. An important limitation of\nmost of these registrations is the lack of correction of\ncase-mix variables [ 1]. Case-mix variables are defined\nas specific patient characteristics that are known to\nindependently influence surgical outcome measures\nand that are potentially explaining the differences in\noutcomes between hospitals and/or surgeons [ 1, 2].\nThus, for an appropriate and reliable interpretation of\nthe surgical outcomes, a case-mix correction is abso-\nlutely mandatory.\nSpecific for the laparoscopic hysterectomy (LH),\nstudies have demonstrated that BMI, uterine weight,\nand previous procedures influence surgical outcome\nmeasures [ 1, 2]. As a result, a case-mix correction\nfor these variables has been recommended when\ncomparing outcomes of LH [ 1, 2]. In a recent sys-\ntematic review on this top ic, pelvic endometriosis\n* Correspondence: f.w.jansen@lumc.nl\n1Department of Gynecology, Leiden University Medical Centre, Leiden, the\nNetherlands\n4Department BioMechanical Engineering, Delft University of Technology,\nDelft, the Netherlands\nFull list of author information is available at the end of the article\nGynecological Surgery\n© The Author(s). 2018 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0\nInternational License ( http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and\nreproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to\nthe Creative Commons license, and indicate if changes were made.\nSandberg et al. Gynecological Surgery  (2018) 15:8 \nhttps://doi.org/10.1186/s10397-018-1039-3\n\nwas also found to be a potential factor influencing\nsurgical outcomes of LH [ 2]. However, no further\nconclusions on concomita nt endometriosis could be\ndrawn in this review as available evidence was lim-\nited. Indeed, only three retrospective studies were\nfound that demonstrated an association between\nendometriosis and prolonged operative time and in-\ncreased complication risk of LH [ 3–5]. Furthermore,\nnone of these studies applied a correction for the\nknown case-mix variables, which may have poten-\ntially resulted in an over- or underestimation of the\nimpact of endometriosis.\nThe objective of this study was firstly to analyze to\nwhat extent concomitant endometriosis influences\nsurgical outcomes of LH and secondly, to determine\nif concomitant endometriosis should be considered\nas case-mix variables in future quality tools.\nMethods\nIn this study, all hysterectomies registered, between\nApril 2014 and September 2016, in the web-based ap-\nplication of QUSUM ( https://www.qusum.org )w e r e\nincluded [ 1]. Detailed information on this database\nhas been described elsewhere [ 1], but briefly, data\nwere obtained by asking gynecologists performing lap-\naroscopic surgery to register anonymously their con-\nsecutive LH ’s for benign indication and low-grade\nmalignancy (e.g., cervical and endometrial dysplasia).\nAll Dutch gynecologists performing LH ’s were re-\ncruited via a personal e-mail invitation, and gynecolo-\ngists from abroad were asked to participate in the\nstudy at international meetings and conferences. The\nInstitutional Review Board (IRB) of Leiden University\nMedical Centre, Leiden, the Netherlands reviewed the\nstudy and exempted it from IRB approval.\nTo evaluate the association between endometriosis\nand surgical outcomes, we retrospectively compared\nsurgical outcomes of patients undergoing LH with\nand without concomitant endometriosis. Only proce-\nd u r e sw i t hh y s t e r e c t o m i e sa so n l ys u r g e r yw e r ec o n -\nsidered, including LH ’s with concomitant adnexal\nsurgery. Hysterectomies including bowel or bladder\ndissection of endometriosis were excluded. Indeed, it\ndid not seem fair to compare these operations to\n‘simple ’ LH’s for benign indication or low-grade\nmalignancy.\nWe considered as primary outcomes the following\nthree surgical outcome measures: intra-operative\nblood loss (ml), operative time (listed as time from\nincision to closure), and complications (up to 6 weeks\npostoperatively). Complications were defined accord-\ning to the internationally accepted classification of\nthe Dutch Society of Obstetrics and Gynecology\n(Appendix 1 )[ 6]. The severity of the complications\nwas graded according to the following classification:\nlevel A, recovery without reoperation; level B, reop-\neration indicated; level C, permanent injury and loss\nof function; level D, death [ 6]. Only reactive conver-\nsions to laparotomy, as defined by Blikkendaal et al.,\nwere included [ 7]. To adequately compare LH ’sw i t h\nand without endometriosis, a correction of the three\nknown case-mix variables BMI (kg/m 2), uterine\nweight (grams), and previous abdominal procedures\n(previous laparotomy and therapeutic laparoscopy)\nwas applied [ 2].\nFor each LH registered in the QUSUM database, we\nabstracted the data of the three primary outcomes,\nthe three case-mix variables, and the following base-\nline characteristics: the presence and stage of con-\ncomitant endometriosis, the age of the patients at\nprocedure (years), the type of hysterectomy (total lap-\naroscopic hysterectomy (TLH)), supracervical laparo-\nscopic hysterectomy (SLH), laparoscopic-assisted\nvaginal hysterectomy (LAVH) and robotic hysterec-\ntomy (RH)), and the experience of the surgeons (years\nof experience, number of LH ’s per year, and total\nnumber of LH ’s performed). Gynecologists were asked\nto enter the information on experience at initial regis-\nt r a t i o ni nt h ew e ba p p l i c a t i o n[1].\nEndometriosis was classified into four stages, ac-\ncording to the revised definition of the American\nSociety for Reproductive Medicine [ 8]. Stage I was\ndefined as minimal endometriosis with only superfi-\ncial lesions and a few filmy adhesions; stage II, the\nmild variant, included additional deep lesions in the\nDouglas cavity; stage III was a moderate stage where,\nin addition to the previous stages, endometriomas on\nthe ovary are observed together with more dense\nadhesions. Finally, stage IV , the severe endometriosis,\nincluded large endometriomas and extensive\nadhesions.\nStatistics\nFor the statistical analysis, SPSS version 23.0 (SPSS\nInc., Chicago, IL, USA) and R statistical software ver-\nsion 3.3.1 were used [ 9]. Categorical data were pre-\nsented as frequency with percentages (%) and\ncontinuous data were presented as mean with stand-\nard deviation (SD) or as geometric mean with geo-\nmetric standard deviation (GSD), if data were\nskewed. To assess significant differences between the\nbaseline characteristics of the group with endometri-\nosis and the one without, independent sample t tests,\nFisher ’s tests, and chi-square with trends were used\nas appropriate. Statistical significance was defined as\na p value < .05. A (generalized) linear mixed model\nregression (univariable and multivariable analysis) was\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 2 of 9\n\nperformed to define the association between endo-\nmetriosis and surgical outcomes. The case-mix vari-\nables BMI, uterine weight, and previous procedures\nwere included as co-variables [ 1, 10]. The characteris-\ntic “previous procedures ” was dichotomized into no\nprevious procedures or at least one. Data with a\nskewed distribution were transformed for analysis\ninto log values. We found t hat blood loss, operative\ntime, and uterine weight needed a log transformation,\nwhich resulted in normalization of the distribution.\nIn 55 cases (including five patients with endometri-\nosis) surgeons reported no blood loss after procedure\n(0 ml). Blood loss was ther efore transformed into\nlog(x +1 ) .\nTo correct for the fact that surgeons entered various\nprocedures, analyses were performed with a random\nintercept for the performing surgeon. For blood loss and\noperative time, findings of the regression analyses were\npresented as percentage increase or decrease with 95%\nconfidence interval (95% CI). The results for complica-\ntion risk were reported as odds ratio with 95% CI. To\nmake data easier to interpret, an index patient was used\nto demonstrate the additional effect of the different\nstages of endometriosis on surgical outcomes. The other\ncase-mix characteristics of this index patient were fixed\nand based on the mean values of the entire cohort.\nResults\nDuring the study period, a total of 2655 LH ’sw e r e\nanalyzed of which 397 cases (15.0%) with concomitant\nendometriosis. Table 1 gives an overview of the base-\nline patient characteristics and surgical outcomes. Pa-\ntients in the endometriosis group were younger (43.5\nTable 1 Baseline patient characteristics and surgical outcomes\nof LH with and without endometriosis\nLH with\nendometriosis\nn = 397\nLH without\nendometriosis\nn = 2258\np value\nPatient characteristics\nAge, years, mean ± SD 43.5 ± 7.7 49.8 ± 11.9 < .001\nBMI, kg/m2, mean ± SD 27.9 ± 5.5 28.6 ± 6.4 .04\nUterine weight, gram,\ngeometric mean; GSD*\n149.31 ± 1.8 162.5 ± 2.1 < .001\nPrevious abdominal\nprocedures, n (%)\n< .001\nNone 152 (38.3) 1290 (57.1)\nOne 124 (31.2) 592 (26.2)\nTwo 64 (16.1) 234 (10.4)\n> Two 57 (14.4) 142 (6.3)\nStage of endometriosis, n (%)\nStage I 106 (26.7) –\nStage II 103 (25.9)\nStage III 93 (23.4)\nStage IV 95 (23.9)\nProcedure type, n (%) .03\nTLH 376 (94.7) 2036 (90.2)\nSLH 13 (3.3) 109 (4.8)\nLAVH 6 (1.5) 88 (3.9)\nRobotic 2 (0.5) 25 (1.1)\nSurgical outcomes\nBlood loss (ml), geometric\nmean; GSD*\n80 ± 3.1 67 ± 3.4 ɸ\nOperative time (min),\ngeometric mean; GSD*\n94 ± 1.5 91 ± 1.5 ɸ\nComplications, n (%) 24 in 22\npatients (5.5%)\n175 in 153\npatients (6.8%)\nɸ\nLesion\nBladder 3 (0.8) 27 (1.2)\nUreter 1 (0.3) 9 (0.4)\nVessel – 1 (< 0.1)\nBowel 2 (0.5) 7 (0.3)\nHemorrhage 5 (1.3) 41 (1.8)\n> 1000 mL intra-operative 5 (1.3) 13 (0.6)\nWound dehiscence – 6 (0.3)\nThrombosis – 3 (0.1)\nDysfunction ileus – 2 (0.1)\nInfections 1 (0.3) 50 (2.2)\nDysfunction incontinence – 10 (0.4)\nOther 2 (0.5) 11 (0.5)\nConversion 10 (2.5) 8 (0.4)\n.16\nTable 1 Baseline patient characteristics and surgical outcomes\nof LH with and without endometriosis (Continued)\nLH with\nendometriosis\nn = 397\nLH without\nendometriosis\nn = 2258\np value\nSeverity of complications,\nn (%)\nLevel A–recovery 18 (4.5) 113 (5.0)\nLevel B–reoperation 3 (0.8) 39 (1.7)\nLevel C–permanent injury 1 (0.3) 0\nLevel D–death 0 1 (< 0.1)\nData are presented as number (percentage) or as mean ± standard deviation\nor as geometric mean (GM) with geometric standard deviation (GSD)\n*Interpretation of the GSD: 95% of the data are expected to lie in the range of\nGM/(GSD)2 to GM*(GSD) 2\nStatistics: independent t test for continuous data; Fisher ’s test for categorical\ndata; chi-square with trend for number of previous procedures\nɸThis means that for every tenfold increase in uterine weight, blood loss and\noperative time increased by the stated percentages and odds of complication\nincreased by the stated OR\nSD standard deviation, GSD geometric standard deviation, LH laparoscopic\nhysterectomy, TLH total laparoscopic hysterectomy, SLH supracervical\nlaparoscopic hysterectomy, LAVH laparoscopic-assisted vaginal hysterectomy\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 3 of 9\n\n(7.7) versus 49.5 (11.9), p < .001), had lower uterine\nweight (149.3 (1.8) gram versus 162.5 (2.1), p < .001),\nlower BMI (27.9 (5.5) versus 28.6 (6.4), p = .04), and\nhad had more previous abdominal surgeries (61.6 ver-\nsus 42.9%, p < .001).\nMost of the hysterectomies performed were TLH\n(94.7% in the endometriosis group versus 90.2%). The\nfour stages of endometriosis were almost equally divided\nin the group with endometriosis (stage I: n = 106\n(26.7%); stage II: n = 103 (25.9%); stage III: n =9 3\n(23.4%); stage IV: n = 95 (23.9%)). A total of 199 compli-\ncations occurred in 175 patients (6.6%), including 22\npatients with endometriosis. Regarding the severity of\nthe complications, no difference between the group with\nand without endometriosis was observed ( p = .16). Spe-\ncifically, no increased risk was observed in the endomet-\nriosis group for the different organ injuries (bladder,\nureter, and bowel). No p values were calculated for the\nthree primary surgical outcomes, as these data were used\nin the regression analysis (Table 3).\nAs demonstrated in Table 2, a total of 93 surgeons reg-\nistered on average 33 (30.6) procedures during the study\nperiod, performed yearly 31 (17.5) LH ’s and had on aver-\nage 6 years (4.5) of experience. As the data were entered\nanonymously, it is unknown how many hospitals were\ninvolved. A significant difference was observed for the\noverall surgical experience and LH ’s performed with and\nwithout endometriosis ( p < .001). In 50.1% of the cases\nwith endometriosis, procedures were performed by sur-\ngeons with an experience of at least 200 LH ’s, compared\nto 34.8% in the group without endometriosis. Of\nnote, no significant correla tion was observed between\nthe number of LH ’s registered in the application and\nthe overall experience of the surgeons (Spearman ’s\nrho = 0.145, p = .169, Appendix 2 ).\nTable 3 summarizes the association between the dif-\nferent case-mix variables, the stages of endometriosis,\nand surgical outcomes, using the mixed model regres-\nsion analysis (univariate a nd multivariate analysis).\nFor BMI, uterine weight and previous abdominal pro-\ncedures, significant associations were observed with\nblood loss and operative time. Regarding endometri-\nosis, we demonstrated that for blood loss and opera-\ntive time, no measurable association was found for\nstages I and II endometriosis compared to LH ’sw i t h -\nout endometriosis (geometric mean blood loss: no\nendometriosis: 67 (3.4) mL; stage I: 71.4 (3.2), p = .48;\nstage II: 79.0 (2.8), p = .10; operative time: no endo-\nmetriosis 90.6 (1.5) min; stage I: 88.1 (1.5), p = .23;\nstage II: 81.9 (1.5), p = .68). Compared to LH ’sw i t h -\nout endometriosis, LH ’sw i t hs t a g eI I Ia n dI Ve n d o -\nmetriosis were associated with more intra-operative\nblood loss (stage III: 70 (3.6), p =. 0 1 ) a n d s t a g e I V :\n106.4 (2.9), p = < . 0 0 1 )a n dap r o l o n g e do p e r a t i v et i m e\n(stage III: 95.1 (1.5), p = <.001 and stage IV: 117.6\n(1.6), p = <.001). No significant association was found\nbetween endometriosis (all stages) and complication\nrates ( p = .62).\nFor an index patient with stage IV endometriosis, a\nmean intra-operative blood loss of 140.8 ml (109.4 –\n180.9) was expected compared to a mean of 65.7 ml\n(57.2–75.6) for a patient with the same characteristics\nbut without endometriosis. Also, an additional mean\noperative time of 47 min was demonstrated for an\nTable 2 Surgeon’s characteristics\nSurgeon characteristics* Total n = 93 surgeonsɸ\nNumber of procedures registered in QUSUM 33 (30.6), (1 –130)\nNumber of procedures per year 31 (17.5), (10 –140)\nYears of experience 6 (4.5), (0 –21)\nOverall experience 160 (158.9), (0 –800)\nTotal surgical experience for the LH ’s with and without\nendometriosis**\nTotal\nn =9 3\nsurgeonsɸ\nLH’s with\nendometriosis\nn = 397\nLH’s without\nendometriosis\nn = 2258 LH\np\nvalue\nOverall experience < .001\n0–99 42 (45.2) 125 (31.5) 954 (43.4)\n100–199 21 (22.6) 73 (18.4) 518 (21.8)\n200–299 10 (10.8) 99 (24.9) 347 (15.4)\n≥ 300 19 (20.4) 100 (25.2) 437 (19.4)\n*Data are presented as mean (SD), (minimum-maximum)\n**Data are presented as number (percentage)\nɸFor one surgeon no information on experience was available\nStatistics: chi-square test for trend\nLH laparoscopic hysterectomy\nNumber of procedures per year is the number of LH they perform an average on a yearly basis\nYears of experience is defined as the number of years of experience since they have finished residency\nOverall experience is defined as the total number of LH ’s performed by a gynecologist during his or her career as attending, including the teaching cases\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 4 of 9\n\nTable 3 Influence of each covariate on blood loss, operative time and complications\nCrude analysis Adjusted analysis\nBlood loss (Geometric)\nmean + (G)SD§ or\nnumber (%)\nPercentage\nincrease (95% CI)\np value of\nunivariate analysis\nPercentage\nincrease (95% CI)\nIndex patient*\nData expressed\nin ml (95% CI)\np value of\nmultivariate\nanalysis\nPatient\ncharacteristics\n–\n10LOG uterine weight ɸ 153.6; 2.0 84.8 (74.5 –95.4) < .001\nBMI (increase/1 kg/\nm2)\n28.5 ± 6.2 2.4 (1.8 –3.0) < .001\nPrevious\nprocedures\n-\nYes (versus no) 1213 (45.7) 13.1 (4.3 –22.6) < .001\nStage of endometriosis < .001 < .001\nNo endometriosis 67.3; 3.4 Reference Reference 65.7 (57.2 –75.6)\nStage I 71.4; 3.2 4.9 ( −16.1–31.2) .68 7.6 ( − 12.3–31.9) 70.7 (55.7 –89.7) .48\nStage II 79.0; 2.8 16.0 ( − 7.3–44.9) .20 18.8 ( − 3.2–45.6) 78.0 (61.4 –99.2) .10\nStage III 70.0; 3.6 27.9 (1 –62.1) .04 34.0 (8.0 –66.4) 88.1 (68.7 –113.0) .01\nStage IV 106.4; 2.9 98.8 (56.7 –152.4) < .001 114.3 (72.1 –166.7) 140.8 (109.4 –\n180.9)\n< .001\nOperative\ntime\nNumber (%) Percentage increase\n(95% CI)\nP-value of\nunivariate analysis\nPercentage\nincrease (95% CI)\nIndex patient*\nData expressed in\nmin (95% CI)\np value of\nmultivariate analysis\nPatient\ncharacteristics\n–\n10LOG uterine weight ɸ 20.0 (18.1–21.8) < .001\nBMI (increase/1 kg/\nm2)\n1.0 (0.8–1.2) < .001\nPrevious\nprocedures\n–\nYes (versus no) 3.8 (1.5 –6.1) <.001\nStage of endometriosis < 0.001 < .001\nNo endometriosis 90.6; 1.5 Reference Reference 92.0 (87.4 –96.9)\nStage I 88.1; 1.5 − 4.4 (− 10.1–1.7) .16 − 3.3 (− 8.6–2.1) 88.9 (82.7 –95.7) .23\nStage II 81.9; 1.5 0.3 ( − 5.7–6.7) .93 1.2 ( − 4.3–6.9) 93.1 (86.5 –100.3) .68\nStage III 95.1; 1.5 15.3 (8.0 –23.1) < .001 17.0 (10.3 –24.0) 107.7 (99.8 –116.2) < .001\nStage IV 117.6; 1.6 47.6 (38.0 –57.6) < .001 51.0 (42.3 –60.3) 139.1 (128.8 –\n150.1)\n< .001\nComplications Number (%) Odds ratio (95% CI) p value of\nunivariate analysis\nOdds ratio (95%\nCI)\n– p value of\nmultivariate analysis\nPatient\ncharacteristics\n–\n10LOG uterine weight ɸ 0.69 (0.56–0.82) < .001\nBMI (increase/1 kg/\nm2)\n1.00 (0.98–1.03) .935\nPrevious procedures –\nYes (versus no) 1.17 (0.87 –1.58) .305\nStage of endometriosis .72 .62\nNo endometriosis 153 (6.8) Reference Reference\nStage I (versus no) 5 (2.9) 1.27 (0.55 –2.95) .57 1.27 (0.54 –2.98) .59\nStage II 7 (4.0) 0.69 (0.33 –1.43) .32 0.67 (0.32 –1.36) .26\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 5 of 9\n\nindex patient with stage IV endometriosis compared\nto a patient with the same characteristics but without\nendometriosis (139.1 min (128.8 –150.1) versus 92 min\n(87.4–96.9)).\nDiscussion\nMain findings\nIn this present study, we demonstrated that LH with\nconcomitant stages I or II endometriosis had no\nmeasurable and clinical relevant associations with sur-\ngical outcome measures compared to LH without\nendometriosis. Stages III and IV endometriosis, how-\never, appeared to be of influence for the outcomes\nblood loss and operative time.\nStrengths and limitations\nA limitation of our study was that gynecologists reg-\nistered themselves the procedures and that these data\ncould not be verified as entered anonymously. As a\nresult, we cannot guarantee that the surgeons in-\ncluded all their consecutiv ec a s e s .Y e t ,t h i si ss i m i l a r\nto daily clinical practice where data are also entered\nby the surgeons. Moreover, previous studies have\nshown that these self-reported data are often accurate\nand reliable [ 10, 11].\nAnother limitation is the fact that information\nregarding the setting, the indication of surgery, or\nthe participation of a fellow or resident during the\nprocedure was missing. This might have biased the\noutcomes. Although these data would have been in-\nteresting, the baseline cha racteristics (BMI, uterine\nweight, and previous procedures), known to influence\noutcomes were analyzed and therefore we believe our\ncomparison is reliable. Regarding the participation of\nat r a i n e ew eb e l i e v et h a ti ti st h er e s p o n s i b i l i t yo f\nthe principle surgeon to judge if his or her involve-\nment remains acceptable and therefore, no correction\nfor this factor was applied. Additionally, it would\nhave been interesting to know if surgeons knew pre-\noperatively of the presence of endometriosis as this\nmight be relevant for the choice of the surgeon and\nthe surgical planning.\nAlthough the outcome “previous surgeries ” has\nbeen demonstrated to be associated with worse sur-\ngical outcome [ 2, 10], collecting data on adhesions\nwould have been interesting as well. The advantage\nof the registration we used was that the number of\nprevious procedures was an objective measure,\nwhereas adhesions and their grading would have\nbeen more at risk for intra-observer variations [ 12].\nFinally, in our study, surgery with bowel and bladder\ndissection of endometriosis was excluded. This might\nhave resulted in an underestimation of the impact of\nendometriosis on surgery in general. Our data should\nthus not be generalized to all endometriosis cases\nbut are limited to LH with concomitant endometri-\nosis. Because the aim of our study was to determine\nthe influence of concomitant endometriosis during\nLH, we believe that it would not be correct to com-\npare these advanced cases to hysterectomies for be-\nnign indication or low-grade malignancy. Similar\nstudies should be performed analyzing specifically\nsurgical outcomes of procedures with bladder and/or\nbowel dissections. Strengths of this study included\nthe relatively large database and number of cases\nwith endometriosis. Also, the high number of sur-\ngeons with varying experience adds to the\ngeneralizability of the data.\nInterpretation\nAlthough endometriosis is often mentioned as com-\nplicating factor during LH, the additional surgical\nrisks associated with LH ’s with concomitant endo-\nmetriosis have not been we ll established. Yet, for a\nreliable interpretation and comparison of surgical\noutcome measures between surgeons and/or hospi-\ntals, numeric support of the impact of concomitant\ne n d o m e t r i o s i sd u r i n gL Hi sn e c e s s a r y .T h i si sa l s o\nrelevant for determining if concomitant endometri-\nosis should be considered a case-mix variable. In this\nstudy, we firstly demonstrated that stages III and IV\nTable 3 Influence of each covariate on blood loss, operative time and complications (Continued)\nCrude analysis Adjusted analysis\nStage III 4 (2.3) 1.23 (0.48 –3.10)0.76 .67 1.16 (0.45 –2.96) .76\nStage IV 6 (3.4) (0.34 –1.65) .48 0.67 (0.30 –1.50) .34\n§Interpretation of the geometric standard deviation (GSD): 95% of the data are expected to lie in the range of GM/(GSD) 2 to GM*(GSD) 2\n*Index patient with BMI of 28.5, uterine weight of 161.3 g, and 50% previous procedures\nɸThis means that for every tenfold increase in uterine weight, blood loss, and operative time increased by the stated percentages and odds of complicat ion\nincreased by the stated OR\nStatistics: linear mixed model (for outcome blood loss and operative time) and generalized linear mixed model (with logistic link function) (for\noutcome complications)\n95% CI 95% confidence interval\nBMI body mass index, GM geometric mean, GSD geometric standard deviation\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 6 of 9\n\nendometriosis were associated with more intra-\noperative blood loss compared to the group without\nendometriosis. This finding has, to our knowledge,\nnot been observed in previous studies [ 3–5, 10]. Al-\nthough the amount of blood loss was twice as much\nin the group with stage IV endometriosis compared\nto the group without, the mean blood loss was still\nlow (141 mL for stage IV). The clinical relevancy for\npatients is therefore questionable, yet, for the sur-\ngeons, it is important to be aware of this potentially\nincreased amount of blood loss. Furthermore, our\nfinding demonstrated that concomitant endometriosis\nindependently influence surgical outcome and there-\nfore should be taken into consideration when apply-\ning a case-mix correction.\nIn agreement with previous studies [ 4, 13], stages III\nand IV endometriosis was associated with a prolonged\noperative time, up to 47 min for stage IV endometriosis.\nThis finding is important to consider for pre-operatively\nscheduling but also as prolonged operative time has\nbeen associated with increased morbidity [ 14, 15]. One\nstudy even demonstrated that every additional hour of\nsurgery during LH increases the risk of postoperative\ncomplications by 22% [ 15].\nRegarding complications, previous studies have\ndemonstrated an increased risk for LH ’sw i t he n d o -\nmetriosis compared to LH ’s without endometriosis.\n[3–5, 13]S p e c i f i c a l l yf o rL H’s with moderate-severe\nendometriosis (stages III and IV), one of the studies\nshowed an almost fourfold increase in the risk of\ncomplications compared to controls [ 13]. Interest-\ningly, in our study, no significant difference in\ncomplication risk was observed (5.5% for the endo-\nmetriosis group versus 6.8% for the non-\nendometriosis group). This could be explained by the\nfact that in previous studies, patients undergoing\nbowel and bladder resection were included. Other ex-\nplanations could be related to the overall low num-\nber of complications in our study and hence the lack\nof power to demonstrate a significant difference and/\nor the high surgical experience for LH with endomet-\nriosis [ 16]. Indeed, LH ’sw i t hs t a g e sI I Ia n dI Ve n d o -\nmetriosis were significantly more often performed by\nsurgeons with more experi ence, and this might have\naffected the outcomes. However, we explicitly did not\ncorrect for surgical experience in our model as we\naimed to demonstrate how patient ’s characteristics\nindependently influence su rgical outcomes. In daily\nclinical practice, surgical experience cannot be used\neither to justify worse surgical outcomes. We want to\nunderline that it is the responsibility of the surgeon\nto know his individual limitations when counseling a\npatient. This pre-operative awareness was reflected in\nour study as most severe endometriosis cases were\nperformed by the more experienced surgeons, and\nthis selection most probably has improved overall sur-\ngical outcomes. However, it is important to keep in\nm i n dt h a tah i g hs u r g i c a lv o l u m ed o e sn o tn e c e s s a r i l y\ndirectly stand for better surgical outcomes [ 1]. Al-\nthough high surgical experience is often associated\nwith positive outcomes, it is not a guarantee. As such,\nwe would recommend surgeons to monitor their indi-\nvidual surgical performan ces over time rather than to\nfocus on the number of surgeries T able 4 [1].\nConclusions\nFor a reliable comparison of surgical outcomes between\nhospitals and/or surgeons, it is necessary to correct for the\npatient characteristics that are independently influencing\nthese outcomes. For LH, previous studies have already\ndemonstrated that a case-mix correction for BMI, uterine\nweight, and previous procedures is required [ 1, 2]. The\nfindings of our study have provided numeric support for\nthe influence of concomitant endometriosis on the surgi-\ncal outcomes of LH. We demonstrated that stages III and\nIV endometriosis were associated with a longer operative\ntime and more blood loss. These specific stages should\nthus be considered as case-mix variable for these out-\ncomes in future quality measurement tools.\nAppendix 1\nTable 4 Complication classification according to the NVOG\nMain category Complication\nInfection - Local\n- Organ\n- Systemic\nInjury - Vascular\n- Bowel\n- Bladder\n- Ureter\n- Other\nWound dehiscence –\nHemorrhage - > 1000 mL\n- Post-operative bleeding\nThrombo-embolism –\nDysfunction - Urinary retention\n- Incontinence\n- Ileus\n- Liver\n- Kidney\nSystemic - Medication error\n- Adverse drug event\n- Other\nTechnical - Failed procedure\n- Retained foreign body\nReactive conversion –\nOther –\nSandberg et al. Gynecological Surgery  (2018) 15:8 Page 7 of 9\n\nAppendix 2\nAcknowledgements\nNone\nFunding\nEvelien M. Sandberg has received a research grant from the Bronovo\nResearch Fund (Bronovo Hospital, the Hague, the Netherlands). The funding\nsource had no involvement in the conduct of the study.\nAuthors’ contributions\nAll authors contributed to the work presented in this paper. EMS was\nresponsible for the project development, the acquisition, analysis and\ninterpretation of data, as well as the drafting and finalization of the\nmanuscript. EATB and SRCD were also responsible for the acquisition of data\nand contributed to the analysis and interpretation of the data as well as the\nfinalization of the manuscript. NvG contributed to the analysis and\ninterpretation of data as well as the finalization of the manuscript. JPB,\nMJGHS, and JPTR contributed to the acquisition, the analysis and\ninterpretation of data as well as the finalization of the manuscript. FWJ was\nresponsible for the conception of the study and contributed to the\nacquisition and interpretation of data and the finalization of the manuscript.\nAll authors take responsibility for this study and its findings. All authors read\nand approved the final manuscript.\nEthics approval and consent to participate\nThe Institutional Review Board (IRB) of Leiden University Medical Centre,\nLeiden, the Netherlands reviewed the study and exempted it from IRB\napproval. All procedures performed in studies involving human participants\nwere in accordance with the ethical standards of the institutional and/or\nnational research committee and with the 1964 Helsinki declaration and its\nlater amendments or comparable ethical standards. For this retrospective\nstudy, formal consent is not required. This article does not contain any\nstudies with animals performed by any of the authors.\nCompeting interests\nThe authors declare that they have no competing interests.\nPublisher’sN o t e\nSpringer Nature remains neutral with regard to jurisdictional claims in\npublished maps and institutional affiliations.\nAuthor details\n1Department of Gynecology, Leiden University Medical Centre, Leiden, the\nNetherlands. 2Department of Medical Statistics, Leiden University Medical\nCentre, Leiden, the Netherlands. 3Department of Gynecology, Haaglanden\nMedical Centre, the Hague, the Netherlands. 4Department BioMechanical\nEngineering, Delft University of Technology, Delft, the Netherlands.\n5Department of Gynecology, Minimally Invasive Surgery, Leiden University\nMedical Centre, PO Box 9600, 2300, RC, Leiden, the Netherlands.\nReceived: 10 December 2017 Accepted: 7 February 2018\nReferences\n1. 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