Recurrence of Sinonasal Inverted Papilloma Following Surgical Approach: A Meta-analysis

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1 The Laryngoscope VC 2016 The American Laryngological, Rhinological and Otological Society, Inc. Recurrence of Sinonasal Inverted Papilloma Following Surgical Approach: A Meta-analysis Jong Seung Kim, MD; Sam Hyun Kwon, MD, PhD Objectives/Hypothesis: Inverted papilloma (IP) is a rare benign tumor, which is found in the sinonasal area. It is characterized by recurrence, local destruction, and malignant change. Of these, recurrence is a challenging problem to many otolaryngologists. In this study, we evaluated recurrence based on the type of surgical approach using a meta-analysis. Study Design: MEDLINE, Embase, and Cochrane database. Methods: Relevant studies were identified by searching the following databases: MEDLINE, Embase, and Cochrane through February Random-effects models were used to estimate risk ratio (RR) and 95% confidence interval (CI). The Newcastle-Ottawa scale was used to assess the quality of cohort studies. Results: Our search yielded 14 retrospective cohort studies involving a total of 696 endoscopic approaches and 444 nonendoscopic approaches. The pooled RR for IP recurrence (endoscopic vs. external approach) was 0.56 [95% CI: , I %]. A subgroup analysis was also performed. Conclusions: Surgical management of IP via an endoscopic approach reduces the risk of recurrence compared to an external approach. Although further data are needed, early- stage IP requires endoscopic or endoscopic-assisted surgery to reduce the risk of tumor recurrence. Key Words: Inverted papilloma, recurrence. Level of Evidence: NA Laryngoscope, 127:52 58, 2017 INTRODUCTION Inverted papilloma (IP) is a rare benign tumor that is located in the sinonasal area. 1 IP arises in the Schneiderian epithelium and is characterized by local destruction, recurrence, and possible malignant change. IP is distinguished from malignancy by computed tomography (CT) and magnetic resonance imaging (MRI), and is confirmed by histopathology. The origin of IP is detected by identifying the point of bony thickening on CT scan. 2,3 MRI also provides useful information to find the origin of IP and to discriminate inflammatory changes from the tumor. 4 In addition to these radiologic methods, endoscopy and advanced optical instruments allow surgeons to predict the origin and visualize the tumor, which is distinguished from other inflammatory diseases. 5 With these technological developments, Krouse proposed a staging system to evaluate the extensiveness From the Department of Otorhinolaryngology Head and Neck Surgery, College of Medicine, Chonbuk National University, Jeonju, Korea; and the Research Institute of Clinical Medicine of Chonbuk National University Biomedical Research Institute, Chonbuk National University Hospital, Jeonju, Korea. Editor s Note: This Manuscript was accepted for publication July 5, This work was supported by funding from the Biomedical Research Institute, Chonbuk National University Hospital. The authors have no other funding, financial relationships, or conflicts of interest to disclose. Send correspondence to Sam Hyun Kwon, MD, Department of Otorhinolaryngology Head and Neck Surgery, 2-20 Keum-Am-Dong, Chonbuk National University Medical School, Jeonju , Korea. shkwon@jbnu.ac.kr DOI: /lary of IPs. 6 Surgeons select the appropriate surgical procedure (endoscopic or external approach) according to this staging system and origin of the tumor. Recurrence is a characteristic of IPs that can be modified depending on the surgical technique. The use of an endoscope provides a clear and exact vision of the tumor and lowers the recurrence rate of IPs. 7 However, a large tumor extending to the paranasal sinuses demands a wide surgical field by lateral rhinotomy or midfacial degloving approach or medial maxillectomy. 8,9 Although there has been only one systematic review about endoscopic resection of IP, there are many reports about the comparison of resection of IPs according to surgical approach It is also meaningful to investigate the recurrence rate according to a combination of the Krouse staging system and surgical approaches, which was not performed in the previous systematic review. In this regard, it is interesting to compare the recurrence rate between endoscopic sinus surgery and nonendoscopic surgery. MATERIALS AND METHODS Literature Search Strategy An electronic database search (MEDLINE, Embase, Cochrane databases) using the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines was conducted with the goal of identifying all available studies using an endoscopic or external approach up to February The following search term was used: inverted papilloma, recurrence. Two authors (J.S.K., S.H.K) independently conducted the literature search. Institutional review board approval was

2 TABLE I. Summary of Included Studies. Author Publication Year Endoscopic Recurrence Endoscopic Total External Recurrence External Total Follow-up (Years) Newcastle-Ottawa Scale Gu FM Xiao-Ting W Diaz Molina JP Kim WS Kim YM Woodworth BA Sautter NB Mirza S Thorp MA Han JK Pasquini E Lawson W Giotakis E Klimek T not required due to the nature of this study. The following search detail was used for MEDLINE: (inverting[all Fields] OR inverted[all Fields]) AND ( papilloma [MeSH Terms] OR papilloma [All Fields]) AND ( recurrence [MeSH Terms] OR recurrence [All Fields]). We used analogous search words for other databases. Selection of Studies The two authors were responsible for screening all abstracts and titles for candidate studies and evaluating the complete text of relevant articles. Studies that were not related to surgical management of inverted papilloma were discarded. Reasons for exclusion were noted. Eligible studies met the following inclusion criteria: 1) includes patients with IP, 2) retrospective or prospective studies, 3) data including endoscopic approach and external approach, 4) data including recurrence cases or rates, and 5) postoperative follow-up for more than 1 year. Studies excluded from the analysis were 1) case reports or case series, 2) studies about either endoscopic or external approach, but not both, 3) languages other than English, 4) review articles that that did not include original data, 5) IP from other areas not including the sinonasal area, and 6) postoperative follow-up for less than 1 year. Data Extraction Relevant data from the included studies were extracted using standardized forms and checked by the two authors (J.S.K., S.H.K) independently. The following information was extracted from each included study: author name, publication year, number of cases/recurrences, and number of follow-up years. The primary outcomes were recurrences after surgery by endoscopic or nonendoscopic method. The endoscopic group included pure endoscopic sinus surgery and endoscopic-assisted surgery, and was classified as the experimental group. The nonendoscopic group included surgeries performed by a lateral rhinotomy or midfacial degloving approach or medial maxillectomy using a nonendoscopic classic approach. This group was classified as the control group. Additionally, recurrences according to the Krouse staging system were recorded. STATISTICAL ANALYSIS Meta-analysis of the selected studies with a continuous measure was performed with R statistical software (R Foundation for Statistical Computing, Vienna, Austria). The proportion of recurrences in the experimental group was calculated by dividing the number of recurrent cases by the total number of patients who received endoscopic surgery. The ratio of recurrent cases in the control group who underwent surgery with a nonendoscopic approach was also obtained using the same method. Summarized relative risks (RR) with 95% CIs were estimated by summarizing the risk estimates of each study using random effect models that considered both within- and between-study variations. 22 Hedges g and standard error were determined for each primary outcome measure. 23 The I 2 metric was used to evaluate between-study heterogeneity. I 2 value between 0% and 100% was used to represent the ratio of between-study variance divided by the sum of the within-study and between-study variances. 24 P values under.10 and I 2 > 50% indicated heterogeneity. 25 Egger s test and funnel plots were applied as a visual aid to detect publication bias. 26 Duval and Tweedie trim and fill to compensate for missing studies and to correct for overall effect size regarding publication bias were also used. 27,28 We suggested a forest plot using the random-effects model, which contains both the random variation within the studies and the variation between the different studies. RESULTS Search Results The initial screening process of the title and abstracts for relevance excluded 1,034 studies that did not meet our inclusion criteria. Duplicate records of 12 articles were also excluded. Out of 1,065 articles examined in detail, 24 articles were identified that reported results of recurrences after removal of IPs. After reviewing the full text, 10 53

3 Fig. 1. Flowchart of the study literature search (n 5 number of studies). [Color figure can be viewed in the online issue, which is available at publications were excluded because they failed to meet our eligibility criteria. These articles were excluded due to the lack of a control group (N 5 1), lack of data or statistics that precluded meta-analysis (N 5 2), languages other than English (N 5 4), review article (N52), and duplicated data (N 5 1). Thus, 14 articles were included in our quantitative analysis (Table I) ,29 32 APRISMAdiagramof the study selection progress and main reasons for exclusion can be found in Figure 1. Overall Meta-analysis Results We used a random effect model considering the variation between and within the studies. Analysis of the recurrence across the surgical approaches revealed a risk ratio of 0.56 (95% CI: , P 5.007) with moderate heterogeneity (I %) in a weighted average follow-up time of 44 months (3.7 years) (Fig. 2). Publication Bias In a funnel plot of recurrence after surgery, the studies were spread to the top and center of the plot, which suggests little publication bias (Fig. 3A). Using Duval and Tweedie s trim and fill to adjust the 54 potentially unpublished report revealed no significant change of the pooled RR (Fig. 3B) (RR: , 95% CI: , P ). Egger s regression test detected no significant evidence of publication bias (P ). Cumulative and Sensitivity Meta-analysis Cumulative meta-analysis showed the pooled risk ratio was stable after the early 2000s (Fig. 4A). A sensitivity analysis was conducted by deleting each study in turn to examine the influence of individual data on the overall estimate. The pooled risk ratio in the overall comparison and the stratified analyses were not significantly changed, indicating a stable and robust outcome (Fig. 4B). We also inserted the Baujat plot, which shows heterogeneity and standardized differences simultaneously in the scatter plot (Fig. 4C). 33 Subgroup Analysis Only four articles supplied data regarding recurrences according to Krouse stage (Table II). A subgroup analysis following Krouse stage was performed (Fig. 4D). 6 Stage 1 had a risk ratio of 0.55 (95% CI: ), and stage 4 had a risk ratio of 1.92 (95% CI: 0.13-

4 Fig. 2. Forest plot of recurrence according to surgical approaches. Experimental group contains endoscopic and endoscopic assisted approach. Control group means non-endoscopic approach including external and open approach. CI 5 confidence interval; RR 5 risk ratio. [Color figure can be viewed in the online issue, which is available at ). The overall RR integrated stage was 1.05 (95% CI: ). DISCUSSION Sinonasal IP is a rare benign tumor representing 0.5% to 4% of all nasal tumors; its etiology is unknown, although an association with human papillomavirus (HPV) has been reported. 8,34 Although it is histologically classified as a benign tumor, it causes clinical problems due to aggressive growth and an association with malignancy. 29,35 IP is known for its association with a 10% risk of malignancy or malignant transformation. 36 HPV infection plays an influential role in the progression, recurrence, and malignant transformation of inverted papilloma. 37 For these reasons, it is viewed as an important disease; regular follow-up with CT and endoscopy is crucial for detecting recurrence. 15,37 IP is a challenging disease for many otolaryngologists. There is unanimous agreement that surgery is the gold standard to treat IP. However, there is broad variation in selecting the surgical approach based on operating year, surgeon s experience, and tumor origin. An external approach is the traditional method, and it has been regarded as standard treatment after its superiority was reported by Kristensen et al. 38 This method was regarded as the best way to operate on extrasinus extension of the IP by providing wide exposure and the potential for en bloc resection. Lateral rhinotomy with medial maxillectomy has been regarded as the gold standard for an external approach. 8,39,40 However, this approach leads to significant bleeding, permanent scarring, and facial disfigurement. A midfacial degloving approach is a good alternative; however, it can also result in saddle nose or chronic crusting and nasal obstruction due to alteration of normal nasal airflow. 41 Although these two methods show a lower recurrence rate than intranasal piecemeal ethmoidectomy, 40,42,43 there are limitations to Fig. 3. Funnel plot. (A) In the funnel plot, the studies were spread almost from the top of the pyramid. (B) Duval s trim and fill method estimated the presence of one potentially unreported cohort. After this one cohort was filled, the pooled risk ratio improved to 0.58 (95% confidence interval: , P ). 55

5 Fig. 4. (A) Cumulative meta-analysis. The risk ratio of the recurrence in the endoscopic group was not changed largely after the early 2000s. (B) Sensitivity analysis. The pooled risk ratio (RR) in the overall comparison and the stratified analyses were not significantly changed, indicating a stable and robust outcome. (C) A Baujat plot showed Kim et al. s study (2010) as an outlier study. (D) Subgroup analysis by Krouse staging revealed endoscopic surgery has an advantage over external approach in early stage, not in advanced stage. CI 5 confidence interval. [Color figure can be viewed in the online issue, which is available at visualization of the frontal sinus, sphenoid sinus, and orbital apex. 16 Since the early 1990s, the advent of endoscopy has enabled surgeons to operate with clear vision, less bleeding, and more delicate handling. Over the past 30 years, refinement of endoscopic skills has changed the concept of IP removal from more aggressive surgery to pedicleoriented endoscopic surgery. 44 Endoscopic sinus surgery (ESS) allows better visualization of the frontal sinus and sphenoid sinus than open approaches and results in less bleeding, pain, morbidity, and postoperative complications. Moreover, ESS allows better magnification of the tumor and its border with the consequent avoidance of unnecessary removal of the healthy mucosa and structures. In spite of the benefits of ESS over external open approaches, there is still controversy regarding the recurrence rate of IP according to surgical approach. 13,16 This study aimed to evaluate IP recurrence based on the type of surgical approach. The findings from this metaanalysis of prospective studies suggest that endoscopic or endoscopic-assisted surgery reduces the risk of recurrence by approximately 44%. The publication bias in the funnel plot shows little asymmetry (Fig. 3A). The compensated potential publication bias did not significantly affect the results. Egger s regression test also supports this finding. Although the method of approach is affected by the surgeon s experience and skill, the operating year is also important. Before the 1990s, endoscopy was not used; Author TABLE II. Recurrences According to Krouse Stage. Approach/Krouse Stage Stage 1 Stage 2 Stage 3 Stage 4 Gu FM 10 Endosopic 0/1 1/6 0 0 External 0 2/12 1/2 0 Kim WS 13 Endosopic 2/11 12/46 9/27 0 External 0 0/4 4/26 0 Kim YM 14 Endosopic 0/14 1/43 2/36 1/1 External 1/9 2/28 1/5 0 Sautter NB 16 Endosopic 0/14 1/11 9/19 1/5 External 0/2 2/5 3/4 0/2 Total Endosopic 2/40 15/106 20/82 2/6 External 1/11 6/49 9/37 0/2 All numbers are recurrences/total cases. 56

6 thus, otolaryngologists were compelled to use an external approach. Since the endoscope was invented, surgeons could choose their surgical approach. Our study has several strengths in that the follow-up period includes cases from both the pre- and postendoscopic era. The cumulative meta-analysis revealed that the risk ratio has been stable since the early 2000s (Fig. 4A). The Baujat plot revealed that Kim et al. had the most considerable influence and contribution to the overall heterogeneity 13 (Fig. 4C). Sensitivity analysis also showed that Kim et al. s study is an outlier (Fig. 4B). This outlier study had a high recurrence rate in the endoscopic group (RR ). However, the authors admitted to better visualization and localization of the tumors in the endoscopic approach. They used the midfacial degloving approach for an external approach, which enables en bloc resection and little scarring. The authors also recognized that results could be biased due to differing tumor location and extent of disease as well as different surgeons with diverse levels of experience. Our subgroup analysis revealed that an endoscopic approach reduced the risk of IP recurrence by 45% for Krouse stage 1 disease (Fig. 4D). However, in the Krouse stage 4 group, an endoscopic approach raised the risk of recurrence by 92%. Although there are limited data following Krouse stage and risk of recurrence, this finding suggests that recurrence depends not only on operative approach but also on the tumor s site, origin, and size. For example, if the IP involves the lateral frontal sinus, endonasal endoscopic surgery will be less effective. Transorbital neuroendoscopic surgery enables efficacious access and visualization of the entire frontal sinus including the lateral aspect. 45 To the best of our knowledge, this is the most comprehensive and quantitative assessment of the risk of recurrence based on endoscopic approach or external approach. Our current meta-analysis included results from 14 retrospective studies that enrolled a total of 696 endoscopic approaches and 444 nonendoscopic approaches, and thus had sufficient statistical power to differentiate between the two groups. One limitation of the current meta-analysis is that non randomized controlled trial (RCT) studies were included in this design. Effect sizes in non-rct studies are generally affected by variable confounders; thus, some authors suggest that RCTs and non-rcts should be analyzed separately. 46 Fortunately, we included all observational studies but no RCT studies. These rare outcomes (recurrence according to surgical approach) almost cannot be studied in randomized trials. Moreover, a prospective study that randomly assigns patients to a surgical approach irrespective of tumor condition seems to involve ethical problems. Although meta-analysis with non-rct studies is less powerful, it has been widely accepted in recent studies. 47 Another limitation of this analysis is the limited data in the subgroup analysis. Future statistical data regarding Krouse staging system and recurrences will enrich and strengthen our results. CONCLUSION Surgical management of IP via an endoscopic approach reduces the risk of recurrence by 44% compared to an external approach. Although additional data are needed, endoscopic or endoscopy-assisted endonasal surgery reduces the risk of tumor recurrence by 45% at Krouse stage 1 but increases the risk of recurrence by 92% at Krouse stage 4. BIBLIOGRAPHY 1. Buchwald C, Nielsen LH, Nielsen PL, Ahlgren P, Tos M. 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