Clinical effects of middle turbinate resection after endoscopic sinus surgery: A systematic review Garret W. Choby, M.D., Candace E. Hobson, M.D., Stella Lee, M.D., and Eric W. Wang, M.D.
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ABSTRACT
Background: The middle turbinate (MT) is a structure that is often carefully preserved during endoscopic sinus surgery (ESS) in an effort to preserve nasal physiology and serve as an anatomic landmark. However, resection is performed in select cases because of involvement of the MT in the inflammatory process, obstruction, or instability. Therefore, significant controversy exists among surgeons regarding the indications for proceeding with MT resection in ESS. This study evaluates clinical outcomes of MT resection after ESS. Methods: An English language search of the PubMed and Ovid databases was conducted for publications examining clinical outcomes of MT resection after ESS performed for chronic rhinosinusitis. Two authors independently examined the articles to identify those meeting inclusion criteria. Any differences over which studies to include were resolved by discussion and consensus. Bias assessment was conducted using the Cochrane Collaboration bias tool for randomized controlled trials and the Newcastle–Ottawa bias tool for cohort and case– control studies. Results: After initial screening, search results revealed 71 articles that warranted detailed evaluation. After applying inclusion criteria, 9 studies were selected. A total of 2123 patients were included among the studies. All studies were controlled. Within the limited available data, olfaction scores may be improved in the MT resection patients compared with MT preservation patients. No difference between the groups was noted for quality of life outcomes, nasal airway resistance, or rates of postoperative frontal sinusitis. In regard to postoperative endoscopic examinations, some studies note greater improvement in the MT resection group compared with the MT preservation group, while others were equivalent. Conclusion: Although some studies show outcome benefit in MT resection patients compared with MT preservation patients, several others show no difference. When MT resection was appropriately indicated, no studies showed detrimental effects compared with MT preservation in their designated outcomes. Additional more stringent studies are warranted. (Am J Rhinol Allergy 28, 502–507, 2014; doi: 10.2500/ajra.2014.28.4097)
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hronic rhinosinusitis (CRS) is a common condition frequently treated by rhinologists and general otolaryngologists. Patient symptoms including nasal congestion, anosmia, facial pressure, and nasal discharge can cause significant reduction in patients’ quality of life (QOL). For patients who have failed maximal medical therapy, endoscopic sinus surgery (ESS) is often the next step in treatment. A variety of techniques are championed by different surgeons, but with a lack of significant evidence, treatment of the diseased middle turbinate (MT) remains a topic of debate. Most surgeons agree that a destabilized or severely diseased MT should be partially resected during ESS. However, there is little agreement regarding the benefits of MT resection in the absence of obvious disease involvement of this structure. Many proponents of diseased MT resection argue that it helps to prevent postoperative lateralization of the MT, thus helping to maintain the patency of the osteomeatal complex. Authors also suggest that MT resection may help to decrease synechiae formation, allow for easier in-office access to the ethmoid labyrinth, and improved nasal airflow.1–3 On the other hand, those favoring MT preservation fear that liberal resection may lead to atrophic rhinitis, stenosis of the frontal recess, and the unnecessary loss of an important anatomic landmark.3 The purpose of this study was to systematically review the published literature to evaluate clinical outcomes of MT resection during ESS.
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From the Department of Otolaryngology–Head and Neck Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania Presented at the Combined Otolaryngology Spring Meeting of the Triological Society, Orlando, Florida, April 10 –14, 2013 The authors have no conflicts of interest to declare pertaining to this article Address correspondence to Eric W. Wang, M.D., Department of Otolaryngology–Head and Neck Surgery, University of Pittsburgh Medical Center, 200 Lothrop Street, EEI 500, Pittsburgh, PA 15213 E-mail address: [email protected] Copyright © 2014, OceanSide Publications, Inc., U.S.A.
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MATERIALS AND METHODS Study Design
A protocol was developed at the outset of the study to define the research question, study population, and inclusion/exclusion criteria. Principles of Preferred Reporting Items of Systematic Reviews and Meta-Analysis (PRISMA) including the PRISMA flow diagram (Fig. 1) served as the model.4 Because of a lack of literature evaluating MT resection, studies were not limited to randomized controlled trials (RCTs). Included studies were required to have a control group for comparison. Case reports and expert opinions were excluded. A meta-analysis was not performed secondary to the heterogeneity of the studies available and lack of homogenous clinical end points. Inclusion criteria included studies of adult patients with CRS who underwent ESS along with MT resection. Studies examining relevant clinical outcomes were included. Studies were excluded in which patients underwent ESS for reasons other than CRS, reporting of only nonclinical outcomes, or lack of a control group.
Selection of Articles On August 1–8, 2012, an English language search of the PubMed and Ovid Medline databases for publications examining clinical outcomes of MT resection during ESS performed for CRS was performed (encompassing the search range from “unlimited” start date to July 2012). Moreover, this search was updated on May 25, 2014, to update the search before publication (encompassing the search range of July 2012 to May 2014). Major and minor search terms and their outcomes are included in Table 1. Furthermore, the citation lists of reviewed articles were also explored for relevant publications. Our initial search resulted in 992 publications. Two reviewers screened the titles and abstracts of these 992 publications for relevance, leaving 71 publications for review (48 articles were from PubMed and 23 articles from Ovid Medline; Fig. 1). In the second level of review, two independent reviewers evaluated the remaining articles in their entirety, to determine if they met inclusion criteria for the systematic review. When a discrepancy arose
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provided by the Cochrane Collaboration.6 Extracted data included the author information, year of publication, study type, number of participants, number of cases, number of controls, follow-up time, CRS definition used in study, MT resection technique used in the study, method of case selection, and selected outcome measures.
Potenally relevant studies idenfied and screened for retrieval (n=992) Studies excluded for clear irrelevance to the study topic (n=921)
RESULTS Studies retrieved for more detailed evaluaon (n=71)
Included Studies
Studies excluded, with reasons (n=49) -
-
Potenally appropriate studies to be included in the systemac review (n=22)
Studies excluded, with reasons (n=13) -
Histology studies without clinical outcomes (n=2) Paents not defined as having CRS (n=3) Literature review without any original data (n=1) Did not report data on MT resecon paents (n=1) Expert opinion without any data (n=1) No control group (n=5)
Studies included in systemac review (n=9)
Table 1 Major and minor key word initial search results
CRS CS CRS CS CRS CS CRS CS CRS CS CRS CS CRS CS Total
PubMed Results
Ovid Medline Results
Middle meatus Middle meatus MT MT Synechiae Synechiae Adhesions Adhesions Pexy Pexy Medialization Medialization Lateralization Lateralization
70 150 125 247 14 25 22 49 0 0 0 4 6 9 721
56 49 39 54 11 12 20 20 0 0 0 1 5 4 271
CRS ⫽ chronic rhinosinusitis; CS ⫽ chronic sinusitis; MT ⫽ middle turbinate.
among the two reviewers, resolution was achieved with consensus of all four authors. After the articles were screened, 22 total articles were consistent with the systematic review protocol. One additional article was identified from the reference list of several included articles and was evaluated. After application of the defined inclusion/exclusion criteria, a total of nine articles met final eligibility criteria and were included in the review (Fig. 1).
Eight of the studies examined endoscopic examination scores as part of their results. Of these, four studies found statistically significant improved postoperative exam scores in MT resection groups compared with MT preservation groups. These four groups had a mean follow-up time of 17.4,8 36,9 50,10 and 36 months,11 respectively. Three of these studies specified that patients were included with both CRS with polyps (CRSwPs) and CRS without polyps (CRSsPs),8–10 whereas one study included CRSwPs only.11 Moreover, three of these studies specified that they performed a partial MT resection aimed at the anterior–inferior portion of the MT,8–10 and the authors of one study performed a complete MT resection.11 Four studies found no statistically significant difference in the postoperative endoscopic appearance between the two groups. The mean follow-up time for these groups was 12,3 12,12 24,13 and 36 months.14 Two studies defined their patient disease definition as “CRS” only3,14 and two studies included CRSwPs only.12,13 All of these studies also specified that they performed a partial MT resection aimed at the anterior–inferior portion of the MT.
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Search Key Word No. 2
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Postoperative Endoscopic Exam Assessments
Figure 1. The Preferred Reporting items of Systematic Reviews and Metaanalysis (PRISMA) flow diagram is shown.
Search Key Word No. 1
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The studies meeting inclusion criteria were quite heterogeneous with a variety of study types and outcomes reported. The nine included articles are summarized in Table 2. A total of 2123 patients were included among the studies. The level of evidence assigned to each article is documented in Table 2. Bias assessment was conducted using the Cochrane Collaboration bias tool for RCTs6 (Table 3) and the Newcastle–Ottawa bias tool for cohort and case–control studies7 (Tables 4 and 5). These bias assessment tools are designed to evaluate the extent to which the differences in outcomes between the two groups can be ascribed to the intervention, rather than some other potential flaw or bias.6,7 Key factors of each article can be viewed in Table 2 including the definition of CRS used in each study, follow-up time, degree of MT resection, and selection of cases to undergo MT resection.
Intervenon was stent or chemical treatment of middle meatus (i.e. stent, mitomycin C, etc) (n= 45) Other (n=4)
Postoperative Rates of Frontal Sinusitis Two studies examined rates of postoperative frontal sinusitis as an outcome measure. A case–control study examined rates of postoperative frontal sinusitis on postoperative computed tomography scan in MT resection patients versus MT preservation patients (case–control study of patients referred from outside institutions for revision surgery).15 Because these patients were referred from outside institutions, the MT resection technique and method for case selection were not known. There was no statistically significant difference in rate of frontal sinusitis between the two groups. Follow-up time from the initial surgery was not specified.15 Another case–control study analyzed the extent of stenosis of the frontal recess postoperatively after MT resection.3 MT resection was performed in a partial manner aimed at the anterior–inferior portion and resection was undertaken for disease involvement of the MT. They found no significant difference in rates of frontal recess stenosis between the two groups (patients with MT resection for disease involvement versus patients with MT preservation).3
Data Extraction The quality of the selected articles was then assessed after assigning a U.S. Preventative Services Task Force (USPTF) ranking to each of the articles.5 Data extraction forms were based on the example forms
Olfaction Outcomes Two studies examined olfaction outcomes. A cohort study had a mean follow-up of 17.4 months, included both CRSwPs and CRSsPs,
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503
504
2000
Havas
2003
2000
Giacchi
Shih
1995
1992
Lamear
Swanson
Year
First Author
Prospective nonrandomized cohort
Prospective RCT
Retrospective case–control
Retrospective case–control
Retrospective; case–control
Study Type
II-1
I
II-2
II-2
II-2
USPSTF ranking
31 Sides
509
39 Patients (50 sides; i.e. 11 bilateral)
69 Total cases
199 Patients (324 sides)
No. of Cases
41 Total controls
107 Patients (162 sides)
No. of Controls
Table 2 Article characteristics and summaries (see separate attachment)
O D NA
36 (3, 6, 12, 18, 24, 36, 48)
Follow-Up (mo)
Not indicated
Concha bullosa, flail turbinate, MT obstructing middle meatus, diseased MT
Technique not specified
Anterior–inferior one-third to one-half removed
CRS or recurrent acute RS (CRSwP and CRSsP)
31 Sides
597
32 Patients (50 sides; i.e. 18 bilateral)
24 (6 mo and 2 yr)
Minimum of 12 mo (mean of 50 mo)
24
Defined only as “CRS”
Defined only as “CRS”
Included both CRSwPs and CRSsPs (no percentage for each group mentioned)
Anterior one-third to one-half removed
Anterior–inferior one-third
Random assignment (based on even/ odd case no. on day of surgery)
Not indicated
Case Selection
Anterior one-third to one-half was resected
MT Resection Technique
Included both CRSwP and CRSsP
CRS Definition
O N T
Right MT was resected in all patients while the left MT was preserved
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Continued
Outcome measures: Postoperative endoscopic exam at 3 mo Partial MT resection improves patency of middle meatotomy and decreases rate of synechiae formation in the long-term follow-up (36 mo) compared with controls (p ⬍ 0.05) Outcome measures: Rates of frontal sinusitis in MT resection groups vs controls (previous ethmoidectomy without MT resection) after surgery from outside surgeon with postoperative CT scan Cases and controls had similar rates of frontal sinus disease on postoperative CT scans Limitation: Were not able to determine the extent of frontal sinus disease before the original outside hospital surgery Outcome measures: Postoperative endoscopic appearance scores and rate of postoperative frontal sinusitis Partial MT resection was not associated with an increased incidence of frontal recess stenosis and secondary frontal sinusitis (obstruction of the frontal recess on endoscopic exam) No difference between groups in regard to synechiae formation Outcome measures: Olfaction; operative complications; synechiae; revision surgery rates Subset of 149 patients with hyposmia complaints: slight smell outcome benefit to MT resection group (p ⫽ 0.0006) MT preservation pts were more likely to require revision surgery (p ⬎ 0.05) and more likely to develop synechiae (p ⬍ 0.05) Outcome measures: Postoperative synechiae formation on endoscopic exam No difference in rate of postoperative synechiae formation in MT resection group compared with MT preservation (no statistical analysis performed) Patients served as self-controls with right MT resection and left MT preservation
Outcome Measures, Conclusions, and Comments
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2012
Byun
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II-1
II-1
II-2
USPSTF ranking
24
47
22
23
No. of Cases
34
25
No. of Controls
36
12 (3 and 12 mo followup)
Follow-Up (mo)
Presence of MT instability, polypoid MT, and MT obstruction of access to frontoethmoidal recess
Based on disease process and intraoperative judgment
Complete MT resection
Anterior–inferior two-thirds was removed
CRSwPs only
129
195
12
Mean 17.4 (minimum, 6 mo)
Outcome measures: Pre- and postoperative nasal resistance; endoscopic score of extent of disease No statistically significant difference in airway rhinometry values, endoscopic visual score or minor/ major postoperative complications (bleeding and synechiae) between the two groups Outcome measures: University of Cologne QOL questionnaire; postoperative endoscopic evaluations Surgical treatment shows a significant improvement in QOL in all patients aside from surgical technique used Patients with MT preservation had hazard ratio of 4.06 to relapse within the follow-up time range compared with MT resection (p ⫽ 0.0102) based on serial endoscopic examinations Outcome measures: Postoperative endoscopic appearance scores, QOL scores and olfaction scores No difference in QOL outcomes in patients with MT preservation vs resection Patients undergoing MT resection have greater improvements in endoscopy and smell identification test scores compared with MT preservation Outcome measures: Sino-Nasal Outcome Test 20 scores, visual analog scale scores Nonrandomized study; baseline disease burden was significantly greater in the MT resection group (p ⬍ 0.001) No statistically significant difference at 12 mo follow-up in Sino-Nasal Outcome Test 20 and visual analog scale scores between resection and preservation groups (p ⫽ 0.273) Nasal endoscopy scores trended towards worse in MT resection group (p ⫽ 0.084), but this was attributed to the worse baseline disease in the MT resection group
Concha bullosa, MT obstructing middle meatus; polypoid MT
Outcome Measures, Conclusions, and Comments
Case Selection
Designated as “partial”
MT Resection Technique
CRSwPs only
CRS Definition
As defined by RS task force criteria (CRSwPs and CRSsPs included)
CRSwPs only
Anterior–inferior two-thirds was removed
Based on intraoperative judgment (severely disease or instable MT’s were resected)
CRS ⫽ chronic rhinosinusitis; CRSsPs ⫽ chronic rhinosinusitis without polyps; CRSwPs ⫽ chronic rhinosinusitis with polyps; CT ⫽ computed tomography; MT ⫽ middle turbinate; QOL ⫽ quality of life; RCT ⫽ randomized controlled trial; RS ⫽ rhinosinusitis; UPSTF ⫽ United States Preventative Task Force.
Prospective nonrandomized cohort
Prospective nonrandomized cohort
2010
Soler
Retrospective case–control
Prospective nonrandomized cohort
2008
Brescia
Study Type
Marchioni 2008
Year
First Author
Table 2 Continued
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compared with preoperative scores (p ⬍ 0.001). No significant differences were found between cases and controls for any of the QOL metrics (p ⬎ 0.05).8 Another cohort study examined QOL outcomes using the University of Cologne questionnaire (nonvalidated questionnaire designed to measure QOL restriction attributable to CRS).11 They examined patients with CRSwPs only and had a follow-up time of 36 months. They undertook a complete MT resection and selected cases based on MT instability or disease involvement. Cases and controls showed statistically significant improvement in postoperative QOL scores that were not significantly different between the two groups.11 A third cohort study examined QOL outcomes using the SinoNasal Outcome test 20 and a visual analog scale.12 They examined patients with CRSwPs only and had a follow-up time of 12 months. They selected patients for MT resection who had severely disease or destabilized MT and undertook a partial resection. As expected, there was significantly great disease burden at baseline in the MT resection group (p ⬍ 0.001). There was no significant difference between the two groups in Sino-Nasal Outcome test 20 or visual analog scale scores at the 12-month follow-up (p ⬎ 0.05).12
Table 3 Newcastle–Ottawa bias risk assessment for cohort studies 8
Soler et al. Marchioni et al.11 Shih et al.12 Byun et al.14
Selection
Comparability
Outcome
**** **** **** ****
*
** *** ** **
** *
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Selection criteria may be assigned up to four stars; comparability criteria may be assigned up to two stars; outcome criteria may be assigned up to three stars (more stars indicate less biased).
Table 4 Newcastle–Ottawa bias risk assessment for case– control studies Giacchi et al.3 Brescia et al.13 Lamear et al.9 Swanson et al.15
Selection
Comparability
Exposure
**** **** **** ****
* * * *
** *** *** ***
Selection criteria may be assigned up to four stars; comparability criteria may be assigned up to two stars; exposure criteria may be assigned up to three stars (more stars indicate less biased).
Random sequence generation Allocation concealment Blinding of participants and personnel Blinding of outcome assessment Incomplete outcome data Selective reporting Other bias
Risk Assessment
O N Low ? High High Low Low Low
RCTs ⫽ randomized controlled trials; Low ⫽ low risk of bias; ? ⫽ unknown risk of bias; High ⫽ high risk of bias.
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used a partial MT resection technique, and selected cases based on disease involvement and intraoperative judgment.8 They found a greater improvement in smell identification test scores in MT resection patients, even after controlling for confounding factors such as asthma, allergies, aspirin intolerance, extent of surgery, and history of nasal polyps (p ⫽ 0.045).8 The prospective RCT had a mean follow-up of 50 months, included both CRSwPs and CRSsPs, used a partial MT resection technique, and selected cases on a predetermined basis without regard to disease involvement.10 They only assessed olfaction outcomes in a subgroup of patients who complained of hyposmia preoperatively. The Olfactolab Smell Test Kit was used from 1987 to 1993 and the University of Pennsylvania Smell Identification Test was used after 1993. In this group, there was a significant olfaction benefit in the MT resection group compared with the MT preservation group (p ⫽ 0.0006), but clinical importance of this was unclear.10
Quality of Life A cohort study used two validated disease-specific QOL instruments (Rhinosinusitis Disability Index and Chronic Sinusitis Survey), in addition to a general health-related QOL instrument (Medical Outcomes Study Short Form 36).8 Both MT resection and MT preservation patients had significant improvements in postoperative scores
506
Several other outcomes were only examined in single studies. A case–control study examined pre- and postoperative nasal resistance.13 They determined nasal airflow resistance using a computerized rhinomanometer with facial mask. The follow-up time was 12 months and only patients with CRSwPs were examined. A partial MT resection was performed based on disease involvement of the MT. There was no significant difference in nasal airflow resistance at the 3or 12 month follow-up between the MT resection group versus the MT preservation group (p ⬍ 0.001).13 The RCT also examined rates of revision surgery and operative complications.10 There were no significant differences in regard to immediate complications. However, the MT resection group was less likely to develop synechiae (8.5% of the MT preservation group versus 0% of the MT resection group; p ⬍ 0.05) and was less likely to require revision surgery (15.6% of the MT preservation group versus 7.1% of the MT resection group; p ⬍ 0.05).10
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Table 5 Cochrane Collaboration bias assessment tool for RCTs Havas et al.10
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Other Outcomes
DISCUSSION MT resection remains controversial among endoscopic sinus surgeons and there is lack of data to support whether preservation or resection improves patient outcomes and which patients would benefit from resection.3 This systematic review of the English literature was conducted to investigate clinical outcomes in patients with CRS undergoing ESS, which included MT resection during their surgery. The purpose of this study was to evaluate the evidence in the literature to better understand clinical outcomes of MT resection. Surgeons in favor of MT resection believe it leads to decreased postoperative synechiae formation and improved sinus outflow tract patency. MT resection may allow for better intraoperative and postoperative visualization of the paranasal sinuses. Those advocating routine MT preservation believe the MT plays an important role in humidification and nasal immune function. Additionally, MT resection may result in an increased risk of atrophic rhinitis, anosmia, and destruction of intraoperative landmarks.1–3,10,11 The anterior MT has been implicated as a key area in regulation of mucosal edema, polyposis, and secretion of vasoactive neuropeptides. Mechanical contact or chemical irritation of this portion of the MT has been shown to reflexively provoke secretion of these inflammatory neuropeptides (substance P, neurokinin A, and calcitonin gene-related peptide), which may play a role in the pathophysiology of CRS.10,16–18 Lacroix has previously shown that patients with chronic nonallergic rhinosinusitis have a twofold increase in calcitonin generelated peptide in their MT mucosa and that concentration of this peptide is related to intensity of CRS symptoms.10,16–18 Thus, they
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advocate that MT resection in patients with chronic inflammation in this area could be helpful based on nasal physiology. One of the interesting findings of this systematic review was the lack of difference in rates of postoperative frontal sinusitis or stenosis between MT resection and MT preservation groups. The risk of an MT stump causing stenosis of the frontal recess has been discussed as a risk to MT resection. However, there was no significant difference in cases versus controls in the two studies that examined this factor. This has not been a frequently studied topic in the literature. In a related study, Fortune noted a 10% rate of frontal sinusitis in patients treated with ESS and MT resection, which they felt was comparable with MT preservation patients in other studies (excluded from this systematic review because of lack of control group).19 On the other hand, there were mixed results in regard to the eight studies in this review that examined postoperative endoscopic examinations as an outcome measure. Moreover, patient QOL outcomes, which were measured in three studies, showed no statistically significant differences between MT resection and MT preservation groups. The common finding in the three studies examining QOL variables was that both groups established statistically significantly improved QOL scores postoperatively, but there was no significant difference among the two groups.8,11,12 It is also quite interesting that both studies included in this study that examined olfaction showed that the MT resection group had significantly better outcomes than the MT preservation group. It has traditionally been held that MT resection may be detrimental to olfaction because some olfactory fibers located on the superior aspect of the MT may be damaged. It should be noted that the technique used in both of these studies involved resection of the anterior– inferior portion of the MT, which would theoretically leave the superior olfactory fibers unaffected. In this case, airflow to the olfactory cleft may actually be improved and thus result in the improvement on olfaction scores seen in these studies.8,20 In a related study, MT suture conchopexy during ESS was also shown to not impair olfaction.21 As with any systematic review, the quality of the review is limited by the quality of the available published literature. With only a single RCT available for review, there is not a plethora of high-level evidence available for review. Moreover, the definition of CRS in the included studies, MT resection technique, and outcomes evaluated are somewhat heterogeneous in the included studies, which limits the strength of aggregated recommendations. Strengths of this study include an exhaustive literature review of the English language published literature and close adherence to recommended PRISMA guidelines for publication of systematic reviews.
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REFERENCES 1.
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CONCLUSIONS
This systematic review of the English literature was conducted to investigate clinical outcomes in patients with CRS undergoing ESS, which included MT resection during their surgery. Although no evaluated studies showed detrimental effects of MT resection compared with MT preservation in their designated outcomes, this systematic review is limited by a lack of high-level evidence. The addition of more level I evidence would help to further clarify these issues. Additional more stringent study is warranted.
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ABSTRACT
Background: The middle turbinate (MT) is a structure that is often carefully preserved during endoscopic sinus surgery (ESS) in an effort to preserve nasal physiology and serve as an anatomic landmark. However, resection is performed in select cases because of involvement of the MT in the inflammatory process, obstruction, or instability. Therefore, significant controversy exists among surgeons regarding the indications for proceeding with MT resection in ESS. This study evaluates clinical outcomes of MT resection after ESS. Methods: An English language search of the PubMed and Ovid databases was conducted for publications examining clinical outcomes of MT resection after ESS performed for chronic rhinosinusitis. Two authors independently examined the articles to identify those meeting inclusion criteria. Any differences over which studies to include were resolved by discussion and consensus. Bias assessment was conducted using the Cochrane Collaboration bias tool for randomized controlled trials and the Newcastle–Ottawa bias tool for cohort and case– control studies. Results: After initial screening, search results revealed 71 articles that warranted detailed evaluation. After applying inclusion criteria, 9 studies were selected. A total of 2123 patients were included among the studies. All studies were controlled. Within the limited available data, olfaction scores may be improved in the MT resection patients compared with MT preservation patients. No difference between the groups was noted for quality of life outcomes, nasal airway resistance, or rates of postoperative frontal sinusitis. In regard to postoperative endoscopic examinations, some studies note greater improvement in the MT resection group compared with the MT preservation group, while others were equivalent. Conclusion: Although some studies show outcome benefit in MT resection patients compared with MT preservation patients, several others show no difference. When MT resection was appropriately indicated, no studies showed detrimental effects compared with MT preservation in their designated outcomes. Additional more stringent studies are warranted. (Am J Rhinol Allergy 28, 502–507, 2014; doi: 10.2500/ajra.2014.28.4097)
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hronic rhinosinusitis (CRS) is a common condition frequently treated by rhinologists and general otolaryngologists. Patient symptoms including nasal congestion, anosmia, facial pressure, and nasal discharge can cause significant reduction in patients’ quality of life (QOL). For patients who have failed maximal medical therapy, endoscopic sinus surgery (ESS) is often the next step in treatment. A variety of techniques are championed by different surgeons, but with a lack of significant evidence, treatment of the diseased middle turbinate (MT) remains a topic of debate. Most surgeons agree that a destabilized or severely diseased MT should be partially resected during ESS. However, there is little agreement regarding the benefits of MT resection in the absence of obvious disease involvement of this structure. Many proponents of diseased MT resection argue that it helps to prevent postoperative lateralization of the MT, thus helping to maintain the patency of the osteomeatal complex. Authors also suggest that MT resection may help to decrease synechiae formation, allow for easier in-office access to the ethmoid labyrinth, and improved nasal airflow.1–3 On the other hand, those favoring MT preservation fear that liberal resection may lead to atrophic rhinitis, stenosis of the frontal recess, and the unnecessary loss of an important anatomic landmark.3 The purpose of this study was to systematically review the published literature to evaluate clinical outcomes of MT resection during ESS.
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From the Department of Otolaryngology–Head and Neck Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania Presented at the Combined Otolaryngology Spring Meeting of the Triological Society, Orlando, Florida, April 10 –14, 2013 The authors have no conflicts of interest to declare pertaining to this article Address correspondence to Eric W. Wang, M.D., Department of Otolaryngology–Head and Neck Surgery, University of Pittsburgh Medical Center, 200 Lothrop Street, EEI 500, Pittsburgh, PA 15213 E-mail address: [email protected] Copyright © 2014, OceanSide Publications, Inc., U.S.A.
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MATERIALS AND METHODS Study Design
A protocol was developed at the outset of the study to define the research question, study population, and inclusion/exclusion criteria. Principles of Preferred Reporting Items of Systematic Reviews and Meta-Analysis (PRISMA) including the PRISMA flow diagram (Fig. 1) served as the model.4 Because of a lack of literature evaluating MT resection, studies were not limited to randomized controlled trials (RCTs). Included studies were required to have a control group for comparison. Case reports and expert opinions were excluded. A meta-analysis was not performed secondary to the heterogeneity of the studies available and lack of homogenous clinical end points. Inclusion criteria included studies of adult patients with CRS who underwent ESS along with MT resection. Studies examining relevant clinical outcomes were included. Studies were excluded in which patients underwent ESS for reasons other than CRS, reporting of only nonclinical outcomes, or lack of a control group.
Selection of Articles On August 1–8, 2012, an English language search of the PubMed and Ovid Medline databases for publications examining clinical outcomes of MT resection during ESS performed for CRS was performed (encompassing the search range from “unlimited” start date to July 2012). Moreover, this search was updated on May 25, 2014, to update the search before publication (encompassing the search range of July 2012 to May 2014). Major and minor search terms and their outcomes are included in Table 1. Furthermore, the citation lists of reviewed articles were also explored for relevant publications. Our initial search resulted in 992 publications. Two reviewers screened the titles and abstracts of these 992 publications for relevance, leaving 71 publications for review (48 articles were from PubMed and 23 articles from Ovid Medline; Fig. 1). In the second level of review, two independent reviewers evaluated the remaining articles in their entirety, to determine if they met inclusion criteria for the systematic review. When a discrepancy arose
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provided by the Cochrane Collaboration.6 Extracted data included the author information, year of publication, study type, number of participants, number of cases, number of controls, follow-up time, CRS definition used in study, MT resection technique used in the study, method of case selection, and selected outcome measures.
Potenally relevant studies idenfied and screened for retrieval (n=992) Studies excluded for clear irrelevance to the study topic (n=921)
RESULTS Studies retrieved for more detailed evaluaon (n=71)
Included Studies
Studies excluded, with reasons (n=49) -
-
Potenally appropriate studies to be included in the systemac review (n=22)
Studies excluded, with reasons (n=13) -
Histology studies without clinical outcomes (n=2) Paents not defined as having CRS (n=3) Literature review without any original data (n=1) Did not report data on MT resecon paents (n=1) Expert opinion without any data (n=1) No control group (n=5)
Studies included in systemac review (n=9)
Table 1 Major and minor key word initial search results
CRS CS CRS CS CRS CS CRS CS CRS CS CRS CS CRS CS Total
PubMed Results
Ovid Medline Results
Middle meatus Middle meatus MT MT Synechiae Synechiae Adhesions Adhesions Pexy Pexy Medialization Medialization Lateralization Lateralization
70 150 125 247 14 25 22 49 0 0 0 4 6 9 721
56 49 39 54 11 12 20 20 0 0 0 1 5 4 271
CRS ⫽ chronic rhinosinusitis; CS ⫽ chronic sinusitis; MT ⫽ middle turbinate.
among the two reviewers, resolution was achieved with consensus of all four authors. After the articles were screened, 22 total articles were consistent with the systematic review protocol. One additional article was identified from the reference list of several included articles and was evaluated. After application of the defined inclusion/exclusion criteria, a total of nine articles met final eligibility criteria and were included in the review (Fig. 1).
Eight of the studies examined endoscopic examination scores as part of their results. Of these, four studies found statistically significant improved postoperative exam scores in MT resection groups compared with MT preservation groups. These four groups had a mean follow-up time of 17.4,8 36,9 50,10 and 36 months,11 respectively. Three of these studies specified that patients were included with both CRS with polyps (CRSwPs) and CRS without polyps (CRSsPs),8–10 whereas one study included CRSwPs only.11 Moreover, three of these studies specified that they performed a partial MT resection aimed at the anterior–inferior portion of the MT,8–10 and the authors of one study performed a complete MT resection.11 Four studies found no statistically significant difference in the postoperative endoscopic appearance between the two groups. The mean follow-up time for these groups was 12,3 12,12 24,13 and 36 months.14 Two studies defined their patient disease definition as “CRS” only3,14 and two studies included CRSwPs only.12,13 All of these studies also specified that they performed a partial MT resection aimed at the anterior–inferior portion of the MT.
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Search Key Word No. 2
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Postoperative Endoscopic Exam Assessments
Figure 1. The Preferred Reporting items of Systematic Reviews and Metaanalysis (PRISMA) flow diagram is shown.
Search Key Word No. 1
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The studies meeting inclusion criteria were quite heterogeneous with a variety of study types and outcomes reported. The nine included articles are summarized in Table 2. A total of 2123 patients were included among the studies. The level of evidence assigned to each article is documented in Table 2. Bias assessment was conducted using the Cochrane Collaboration bias tool for RCTs6 (Table 3) and the Newcastle–Ottawa bias tool for cohort and case–control studies7 (Tables 4 and 5). These bias assessment tools are designed to evaluate the extent to which the differences in outcomes between the two groups can be ascribed to the intervention, rather than some other potential flaw or bias.6,7 Key factors of each article can be viewed in Table 2 including the definition of CRS used in each study, follow-up time, degree of MT resection, and selection of cases to undergo MT resection.
Intervenon was stent or chemical treatment of middle meatus (i.e. stent, mitomycin C, etc) (n= 45) Other (n=4)
Postoperative Rates of Frontal Sinusitis Two studies examined rates of postoperative frontal sinusitis as an outcome measure. A case–control study examined rates of postoperative frontal sinusitis on postoperative computed tomography scan in MT resection patients versus MT preservation patients (case–control study of patients referred from outside institutions for revision surgery).15 Because these patients were referred from outside institutions, the MT resection technique and method for case selection were not known. There was no statistically significant difference in rate of frontal sinusitis between the two groups. Follow-up time from the initial surgery was not specified.15 Another case–control study analyzed the extent of stenosis of the frontal recess postoperatively after MT resection.3 MT resection was performed in a partial manner aimed at the anterior–inferior portion and resection was undertaken for disease involvement of the MT. They found no significant difference in rates of frontal recess stenosis between the two groups (patients with MT resection for disease involvement versus patients with MT preservation).3
Data Extraction The quality of the selected articles was then assessed after assigning a U.S. Preventative Services Task Force (USPTF) ranking to each of the articles.5 Data extraction forms were based on the example forms
Olfaction Outcomes Two studies examined olfaction outcomes. A cohort study had a mean follow-up of 17.4 months, included both CRSwPs and CRSsPs,
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503
504
2000
Havas
2003
2000
Giacchi
Shih
1995
1992
Lamear
Swanson
Year
First Author
Prospective nonrandomized cohort
Prospective RCT
Retrospective case–control
Retrospective case–control
Retrospective; case–control
Study Type
II-1
I
II-2
II-2
II-2
USPSTF ranking
31 Sides
509
39 Patients (50 sides; i.e. 11 bilateral)
69 Total cases
199 Patients (324 sides)
No. of Cases
41 Total controls
107 Patients (162 sides)
No. of Controls
Table 2 Article characteristics and summaries (see separate attachment)
O D NA
36 (3, 6, 12, 18, 24, 36, 48)
Follow-Up (mo)
Not indicated
Concha bullosa, flail turbinate, MT obstructing middle meatus, diseased MT
Technique not specified
Anterior–inferior one-third to one-half removed
CRS or recurrent acute RS (CRSwP and CRSsP)
31 Sides
597
32 Patients (50 sides; i.e. 18 bilateral)
24 (6 mo and 2 yr)
Minimum of 12 mo (mean of 50 mo)
24
Defined only as “CRS”
Defined only as “CRS”
Included both CRSwPs and CRSsPs (no percentage for each group mentioned)
Anterior one-third to one-half removed
Anterior–inferior one-third
Random assignment (based on even/ odd case no. on day of surgery)
Not indicated
Case Selection
Anterior one-third to one-half was resected
MT Resection Technique
Included both CRSwP and CRSsP
CRS Definition
O N T
Right MT was resected in all patients while the left MT was preserved
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Continued
Outcome measures: Postoperative endoscopic exam at 3 mo Partial MT resection improves patency of middle meatotomy and decreases rate of synechiae formation in the long-term follow-up (36 mo) compared with controls (p ⬍ 0.05) Outcome measures: Rates of frontal sinusitis in MT resection groups vs controls (previous ethmoidectomy without MT resection) after surgery from outside surgeon with postoperative CT scan Cases and controls had similar rates of frontal sinus disease on postoperative CT scans Limitation: Were not able to determine the extent of frontal sinus disease before the original outside hospital surgery Outcome measures: Postoperative endoscopic appearance scores and rate of postoperative frontal sinusitis Partial MT resection was not associated with an increased incidence of frontal recess stenosis and secondary frontal sinusitis (obstruction of the frontal recess on endoscopic exam) No difference between groups in regard to synechiae formation Outcome measures: Olfaction; operative complications; synechiae; revision surgery rates Subset of 149 patients with hyposmia complaints: slight smell outcome benefit to MT resection group (p ⫽ 0.0006) MT preservation pts were more likely to require revision surgery (p ⬎ 0.05) and more likely to develop synechiae (p ⬍ 0.05) Outcome measures: Postoperative synechiae formation on endoscopic exam No difference in rate of postoperative synechiae formation in MT resection group compared with MT preservation (no statistical analysis performed) Patients served as self-controls with right MT resection and left MT preservation
Outcome Measures, Conclusions, and Comments
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2012
Byun
American Journal of Rhinology & Allergy
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II-1
II-1
II-2
USPSTF ranking
24
47
22
23
No. of Cases
34
25
No. of Controls
36
12 (3 and 12 mo followup)
Follow-Up (mo)
Presence of MT instability, polypoid MT, and MT obstruction of access to frontoethmoidal recess
Based on disease process and intraoperative judgment
Complete MT resection
Anterior–inferior two-thirds was removed
CRSwPs only
129
195
12
Mean 17.4 (minimum, 6 mo)
Outcome measures: Pre- and postoperative nasal resistance; endoscopic score of extent of disease No statistically significant difference in airway rhinometry values, endoscopic visual score or minor/ major postoperative complications (bleeding and synechiae) between the two groups Outcome measures: University of Cologne QOL questionnaire; postoperative endoscopic evaluations Surgical treatment shows a significant improvement in QOL in all patients aside from surgical technique used Patients with MT preservation had hazard ratio of 4.06 to relapse within the follow-up time range compared with MT resection (p ⫽ 0.0102) based on serial endoscopic examinations Outcome measures: Postoperative endoscopic appearance scores, QOL scores and olfaction scores No difference in QOL outcomes in patients with MT preservation vs resection Patients undergoing MT resection have greater improvements in endoscopy and smell identification test scores compared with MT preservation Outcome measures: Sino-Nasal Outcome Test 20 scores, visual analog scale scores Nonrandomized study; baseline disease burden was significantly greater in the MT resection group (p ⬍ 0.001) No statistically significant difference at 12 mo follow-up in Sino-Nasal Outcome Test 20 and visual analog scale scores between resection and preservation groups (p ⫽ 0.273) Nasal endoscopy scores trended towards worse in MT resection group (p ⫽ 0.084), but this was attributed to the worse baseline disease in the MT resection group
Concha bullosa, MT obstructing middle meatus; polypoid MT
Outcome Measures, Conclusions, and Comments
Case Selection
Designated as “partial”
MT Resection Technique
CRSwPs only
CRS Definition
As defined by RS task force criteria (CRSwPs and CRSsPs included)
CRSwPs only
Anterior–inferior two-thirds was removed
Based on intraoperative judgment (severely disease or instable MT’s were resected)
CRS ⫽ chronic rhinosinusitis; CRSsPs ⫽ chronic rhinosinusitis without polyps; CRSwPs ⫽ chronic rhinosinusitis with polyps; CT ⫽ computed tomography; MT ⫽ middle turbinate; QOL ⫽ quality of life; RCT ⫽ randomized controlled trial; RS ⫽ rhinosinusitis; UPSTF ⫽ United States Preventative Task Force.
Prospective nonrandomized cohort
Prospective nonrandomized cohort
2010
Soler
Retrospective case–control
Prospective nonrandomized cohort
2008
Brescia
Study Type
Marchioni 2008
Year
First Author
Table 2 Continued
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505
compared with preoperative scores (p ⬍ 0.001). No significant differences were found between cases and controls for any of the QOL metrics (p ⬎ 0.05).8 Another cohort study examined QOL outcomes using the University of Cologne questionnaire (nonvalidated questionnaire designed to measure QOL restriction attributable to CRS).11 They examined patients with CRSwPs only and had a follow-up time of 36 months. They undertook a complete MT resection and selected cases based on MT instability or disease involvement. Cases and controls showed statistically significant improvement in postoperative QOL scores that were not significantly different between the two groups.11 A third cohort study examined QOL outcomes using the SinoNasal Outcome test 20 and a visual analog scale.12 They examined patients with CRSwPs only and had a follow-up time of 12 months. They selected patients for MT resection who had severely disease or destabilized MT and undertook a partial resection. As expected, there was significantly great disease burden at baseline in the MT resection group (p ⬍ 0.001). There was no significant difference between the two groups in Sino-Nasal Outcome test 20 or visual analog scale scores at the 12-month follow-up (p ⬎ 0.05).12
Table 3 Newcastle–Ottawa bias risk assessment for cohort studies 8
Soler et al. Marchioni et al.11 Shih et al.12 Byun et al.14
Selection
Comparability
Outcome
**** **** **** ****
*
** *** ** **
** *
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Selection criteria may be assigned up to four stars; comparability criteria may be assigned up to two stars; outcome criteria may be assigned up to three stars (more stars indicate less biased).
Table 4 Newcastle–Ottawa bias risk assessment for case– control studies Giacchi et al.3 Brescia et al.13 Lamear et al.9 Swanson et al.15
Selection
Comparability
Exposure
**** **** **** ****
* * * *
** *** *** ***
Selection criteria may be assigned up to four stars; comparability criteria may be assigned up to two stars; exposure criteria may be assigned up to three stars (more stars indicate less biased).
Random sequence generation Allocation concealment Blinding of participants and personnel Blinding of outcome assessment Incomplete outcome data Selective reporting Other bias
Risk Assessment
O N Low ? High High Low Low Low
RCTs ⫽ randomized controlled trials; Low ⫽ low risk of bias; ? ⫽ unknown risk of bias; High ⫽ high risk of bias.
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used a partial MT resection technique, and selected cases based on disease involvement and intraoperative judgment.8 They found a greater improvement in smell identification test scores in MT resection patients, even after controlling for confounding factors such as asthma, allergies, aspirin intolerance, extent of surgery, and history of nasal polyps (p ⫽ 0.045).8 The prospective RCT had a mean follow-up of 50 months, included both CRSwPs and CRSsPs, used a partial MT resection technique, and selected cases on a predetermined basis without regard to disease involvement.10 They only assessed olfaction outcomes in a subgroup of patients who complained of hyposmia preoperatively. The Olfactolab Smell Test Kit was used from 1987 to 1993 and the University of Pennsylvania Smell Identification Test was used after 1993. In this group, there was a significant olfaction benefit in the MT resection group compared with the MT preservation group (p ⫽ 0.0006), but clinical importance of this was unclear.10
Quality of Life A cohort study used two validated disease-specific QOL instruments (Rhinosinusitis Disability Index and Chronic Sinusitis Survey), in addition to a general health-related QOL instrument (Medical Outcomes Study Short Form 36).8 Both MT resection and MT preservation patients had significant improvements in postoperative scores
506
Several other outcomes were only examined in single studies. A case–control study examined pre- and postoperative nasal resistance.13 They determined nasal airflow resistance using a computerized rhinomanometer with facial mask. The follow-up time was 12 months and only patients with CRSwPs were examined. A partial MT resection was performed based on disease involvement of the MT. There was no significant difference in nasal airflow resistance at the 3or 12 month follow-up between the MT resection group versus the MT preservation group (p ⬍ 0.001).13 The RCT also examined rates of revision surgery and operative complications.10 There were no significant differences in regard to immediate complications. However, the MT resection group was less likely to develop synechiae (8.5% of the MT preservation group versus 0% of the MT resection group; p ⬍ 0.05) and was less likely to require revision surgery (15.6% of the MT preservation group versus 7.1% of the MT resection group; p ⬍ 0.05).10
T
Table 5 Cochrane Collaboration bias assessment tool for RCTs Havas et al.10
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Other Outcomes
DISCUSSION MT resection remains controversial among endoscopic sinus surgeons and there is lack of data to support whether preservation or resection improves patient outcomes and which patients would benefit from resection.3 This systematic review of the English literature was conducted to investigate clinical outcomes in patients with CRS undergoing ESS, which included MT resection during their surgery. The purpose of this study was to evaluate the evidence in the literature to better understand clinical outcomes of MT resection. Surgeons in favor of MT resection believe it leads to decreased postoperative synechiae formation and improved sinus outflow tract patency. MT resection may allow for better intraoperative and postoperative visualization of the paranasal sinuses. Those advocating routine MT preservation believe the MT plays an important role in humidification and nasal immune function. Additionally, MT resection may result in an increased risk of atrophic rhinitis, anosmia, and destruction of intraoperative landmarks.1–3,10,11 The anterior MT has been implicated as a key area in regulation of mucosal edema, polyposis, and secretion of vasoactive neuropeptides. Mechanical contact or chemical irritation of this portion of the MT has been shown to reflexively provoke secretion of these inflammatory neuropeptides (substance P, neurokinin A, and calcitonin gene-related peptide), which may play a role in the pathophysiology of CRS.10,16–18 Lacroix has previously shown that patients with chronic nonallergic rhinosinusitis have a twofold increase in calcitonin generelated peptide in their MT mucosa and that concentration of this peptide is related to intensity of CRS symptoms.10,16–18 Thus, they
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advocate that MT resection in patients with chronic inflammation in this area could be helpful based on nasal physiology. One of the interesting findings of this systematic review was the lack of difference in rates of postoperative frontal sinusitis or stenosis between MT resection and MT preservation groups. The risk of an MT stump causing stenosis of the frontal recess has been discussed as a risk to MT resection. However, there was no significant difference in cases versus controls in the two studies that examined this factor. This has not been a frequently studied topic in the literature. In a related study, Fortune noted a 10% rate of frontal sinusitis in patients treated with ESS and MT resection, which they felt was comparable with MT preservation patients in other studies (excluded from this systematic review because of lack of control group).19 On the other hand, there were mixed results in regard to the eight studies in this review that examined postoperative endoscopic examinations as an outcome measure. Moreover, patient QOL outcomes, which were measured in three studies, showed no statistically significant differences between MT resection and MT preservation groups. The common finding in the three studies examining QOL variables was that both groups established statistically significantly improved QOL scores postoperatively, but there was no significant difference among the two groups.8,11,12 It is also quite interesting that both studies included in this study that examined olfaction showed that the MT resection group had significantly better outcomes than the MT preservation group. It has traditionally been held that MT resection may be detrimental to olfaction because some olfactory fibers located on the superior aspect of the MT may be damaged. It should be noted that the technique used in both of these studies involved resection of the anterior– inferior portion of the MT, which would theoretically leave the superior olfactory fibers unaffected. In this case, airflow to the olfactory cleft may actually be improved and thus result in the improvement on olfaction scores seen in these studies.8,20 In a related study, MT suture conchopexy during ESS was also shown to not impair olfaction.21 As with any systematic review, the quality of the review is limited by the quality of the available published literature. With only a single RCT available for review, there is not a plethora of high-level evidence available for review. Moreover, the definition of CRS in the included studies, MT resection technique, and outcomes evaluated are somewhat heterogeneous in the included studies, which limits the strength of aggregated recommendations. Strengths of this study include an exhaustive literature review of the English language published literature and close adherence to recommended PRISMA guidelines for publication of systematic reviews.
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10.
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CONCLUSIONS
This systematic review of the English literature was conducted to investigate clinical outcomes in patients with CRS undergoing ESS, which included MT resection during their surgery. Although no evaluated studies showed detrimental effects of MT resection compared with MT preservation in their designated outcomes, this systematic review is limited by a lack of high-level evidence. The addition of more level I evidence would help to further clarify these issues. Additional more stringent study is warranted.
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