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Comparison of maxillary sinus specimens removed during Caldwell-Luc procedures and traditional maxillary sinus antrostomies.

Introduction

Described separately in the late 19th century by George Caldwell and Henri Luc, (1) the Caldwell-Luc (CL) operation was the mainstay of surgical treatment for maxillary sinus disease before the advent of functional endoscopic sinus surgery (FESS), also known as mucosa-preserving surgery. With the rise of FESS in the 1980s, the CL procedure came to be reserved for patients with recalcitrant maxillary sinusitis in whom aggressive medical and surgical management had failed.

Today, many feel the CL operation is of historical value only, to be reserved for tumor resection, trauma, and access for foreign body removal. (2) Others, however, believe that it continues to be effective for patients with persistent maxillary sinus disease after the failure of a previously well-performed FESS. (3) Questions persist, however, regarding what factors identify patients who have done so poorly with standard management techniques as to require this aggressive procedure.

The purpose of this study is to compare histopathologic samples of patients who have undergone CL procedures for chronic rhinosinusitis (CRS) with those of patients who have undergone standard FESS. In so doing, we set out to identify the factors that--on a microscopic level--might determine why some patients will require CL procedures compared with those who can be treated successfully with standard FESS.

Patients and methods

A retrospective study of all patients who underwent a CL procedure for CRS by physicians at the Vanderbilt University Medical Center's Department of Otolaryngology between 2002 and 2007 was performed. After approval from the Human Investigations Committee (Study #071131), medical records were reviewed for data on demographics, comorbidities (e.g., smoking, aspirin triad, asthma, cystic fibrosis, inhalant allergies, and diabetes mellitus), details of surgery, surgical pathology, and histology. Surgical data were reviewed for age at surgery, number of previous maxillary sinus surgeries, side of surgery, and days since last surgery. Detailed data were also collected on pathologic findings, including tissue eosinophilia. The same set of data was then collected on a group of 40 consecutive patients who underwent standard FESS in 2007. Analysis of variance (ANOVA) and the chi-square test were used to determine statistically significant differences. When a significant difference was found (p < 0.05), unpaired t-tests were used for pairwise comparisons between groups.

Results

The study population of 80 patients who underwent CL surgery consisted of 26 males and 54 females; mean age was 55 years (range: 27 to 79 years). The control group included 16 males and 24 females; mean age was 48.4 years (range: 13 to 76 years). Pertinent comorbidities in the CL group included 5 (6.3%) patients with diabetes mellitus, 19 (23.8%) patients with inhalant allergies, and 2 (2.5%) patients with aspirin sensitivity; 22 (27.5%) patients were smokers (table 1).

Pertinent comorbidities in the non-CL group included 3 (7.5%) patients with diabetes mellitus, 15 (37.5%) patients with inhalant allergies, and 4 (10%) patients with aspirin sensitivity; 6 (15%) of these patients were smokers (table 1). Differences between groups in patient age and distribution of sex were statistically significant (p < 0.02).

In the CL group, 24 patients underwent surgery on the right side, 25 patients underwent surgery on the left, and 31 patients underwent bilateral CL surgery. In the non-CL group, 6 patients underwent surgery on the right side, 7 patients underwent surgery on the left, and 27 patients underwent bilateral surgery. In the CL group, the mean number of prior maxillary sinus surgeries was 1.5 (range: 0 to 7), compared with a mean of 0.6 (range: 0 to 3) in the non-CL group. This difference was statistically significant (p < 0.01).

In the CL group, the mean total number of sinuses addressed (including sinuses other than maxillary sinuses) at the time of surgery was 2.5 compared with a mean of 4.3 in the non-CL group. This difference between groups was also statistically significant (p < 0.01). In the CL group, the mean number of days since the last maxillary sinus surgery was 878 (range: 0 to 18,882), compared with a mean of 1,618 (range: 0 to 9,855) in the non-CL group (table 2).

On histologic examination of the surgical sinus tissue specimen from the CL patients, the mean number of eosinophils per high-power field was 5.68 ([+ or -] 7.65 SD). Twenty-nine patients had no eosinophils per high-power field, 16 had 1 or 2 eosinophils, 15 had 3 to 9 eosinophils, 4 had 10 to 14 eosinophils, 12 had 15 to 24 eosinophils, and 4 had more than 25 eosinophils per high-power field (table 3).

Examination of surgical specimens from the non-CL patients demonstrated a mean number of eosinophils per high-power field of 28.33 ([double dagger]41.62 SD). Eight patients had no eosinophils per high-power field, 5 had 1 or 2 eosinophils, 7 had 3 to 9 eosinophils, 3 had 10 to 14 eosinophils, I had 15 to 24 eosinophils, and 16 had more than 25 eosinophils per high-power field (table 3). The differences in eosinophil counts between the two groups were statistically significant (p < 0.01).

Microscopic examination also revealed the presence of "necrotic bone" in 2 CL specimens and "necrotic debris" in 2 other CL specimens. No similar finding was seen in the non-CL group.

Discussion

In the late 19th century, George Caldwell (4) of the United States, Robert Henry Scanes Spice. (5) of England, and Henri Luc (6) of France, working separately, described a procedure to remove the contents and diseased mucosal lining of the maxillary sinus, along with a method to create counter-drainage through an inferior meatus antrostomy. The Caldwell-Luc procedure (Dr. Scanes Spicer's name never gained association with the similar procedure that his colleagues in the United States and France described) involved a sublabial transantral approach to the maxillary sinus, with trephination of the sinus through the antrum near the canine fossa. This procedure was the gold standard for surgical management of chronic maxillary sinus disease until the advent of intranasal surgery in the 1920s.

With the arrival of the sinus endoscope in the mid1980s (1) and the ability to create precise endonasal antrostomies, the CL procedure became a surgeryoflast resort. Since that time it has, for the most part, been replaced by the FESS, which has been proven safe and effective in the treatment of chronic maxillary sinus disease and has much less associated morbidity than the CL approach. The CL procedure, therefore, is reserved for recalcitrant cases not responsive to FESS. While FESS is appropriate and effective for the treatment of almost all chronic maxillary sinusitis, there continues to be a small subset of patients with recalcitrant mucosal disease despite well-performed FESS procedures. In those patients whose disease persists--without any signs of scarring, recirculation, retained uncinate processes, or otherwise incomplete surgery--the CL procedure has proven to be effective. The CL procedure not only allows the removal of the infected sinus contents, but it also allows the removal of the nonfunctional, condemned mucosa when present. (3)

In a previous study by the senior author (I.A.D.), a 92% success rate for the CL procedure in patients with recalcitrant maxillary sinusitis was reported? These patients demonstrated disease-free maxillary sinuses on endoscopic examination or computed tomography. Two of the 3 patients (8%) who demonstrated continued sinus disease and underwent a repeat CL procedure demonstrated clinical improvement during follow-up. Despite this success rate, the CL procedure is appropriately reserved as a surgery of last resort, given its increased morbidity compared with that of more conservative approaches.

DeFreitas and Lucente reported a 19% overall complication rate with the Caldwell-Luc approach. (7) Robinson et al described a 16% rate of persistent adverse effects from canine fossa puncture, most commonly facial pain, facial paresthesia, and numbness. (8)

While the CL procedure is a valuable tool in the management of patients with irreversible mucosal changes in the maxillary sinus, it is unclear why this small group of patients has persistent disease in the face of technically sound maxillary sinus surgery and aggressive medical management. What is well known is that inflammatory disease of the maxillary sinus leads to mucosal changes and impaired ciliary clearance. In addition to the influx of inflammatory white blood cells into the sinus tissue, squamous metaplasia, ciliary disorientation, cilia loss, and compound cilia are just some of the many morphologic abnormalities documented to occur in the chronically inflamed maxillary sinus. (9)

While the mucosa in many patients slowly recovers some of its normal function after surgery, this recovery is often incomplete. (10,11) Moreover, it is well documented that recovery of mucosal function and histology is variable and does not occur in all patients. (12-14) It is in this context that we hypothesize that there is a small subset of patients who, on a microscopic level, demonstrate differences from their counterparts who did not require the CL procedure. We further hypothesize that in these patients, the inflammatory response has essentially "burned out" and given way to more severe, permanent morphologic changes.

The data from our study are consistent with the hypothesis that the mucosal function of the vast majority of patients with maxillary sinusitis recovers after standard FESS. In a small minority of patients, however, mucosal changes are severe and irreversible. It is these patients who fail revision FESS who are selected to undergo the CL procedure. Because this procedure involves mucosal extirpation, the vast majority of this small group does well once their diseased lining is removed.

The data in our study show that in terms of tissue eosinophilia--a marker for chronic sinus inflammation--the non-CL patients had a significantly increased number of eosinophils. This corresponds with our hypothesis that in patients requiring the CL procedure, there are qualitative mucosal and functional changes that have gone beyond basic tissue inflammation and, in fact, are characterized by severe ciliary dysfunction and histologic change. Additionally, it is only in the CL patients that we observed necrotic tissue and necrotic debris--highly unusual findings that further support the hypothesis that the sinus mucosa in these patients is so dysfunctional and diseased that nearly all mucociliary function is gone. While it will fall to future, prospective studies to further characterize the specific ciliary dysfunction, squamous metaplasia, or any other abnormalities beyond standard tissue inflammation that are present in the sinus mucosal lining of these patients, our data do support the hypothesis that there is a continuum in the tissue response of the maxillary sinus. This continuum extends from acute and chronic inflammatory responses to more long-standing tissue responses associated with a decrease in the presence of inflammatory white blood cells. These latter changes can have lasting and permanent effects on maxillary sinus function.

Other findings of statistical and clinical significance include the differences between the groups in terms of the number of sinuses treated and the number of prior surgeries. As expected, the CL patients had a greater number of prior surgeries than those in the non-CL group. This corresponds with our understanding of the CL procedure as a surgery of last resort, used primarily on patients who have failed FESS.

Similarly, the patients in the CL group were also noted to have fewer sinuses treated during their surgical procedure (average of 2.5 vs. 4.3, including sinuses other than maxillary sinuses). Traditionally, the maxillary sinus has been seen as the easiest sinus to open surgically, with the frontal sinus being the most challenging. Over time, however, it has become clear that the maxillary sinus is the sinus that most often requires revision surgery, is most difficult to keep consistently healthy after surgery and, consequently, creates the greatest challenge to those who treat patients with sinusitis. Patients undergoing the CL procedure often have their ethmoid sinuses subsequently removed but have healthy frontal and sphenoid sinuses. Therefore, we can understand how these patients underwent fewer procedures at the time of their CL surgeries.

In conclusion, the CL procedure is a surgery of last resort for patients who have failed aggressive medical and surgical intervention for the treatment of maxillary sinusitis. In this small group of patients, the mucosal lining appears to be fundamentally different from that of patients who respond favorably to FESS. Future studies will be required to further define and characterize the tissue response that occurs in these patients.

Acknowledgment

The authors would like to acknowledge Daniel M. Maggin, MS, for his assistance with the statistical analysis of the data set.

References

(1.) MacBeth R. Caldwell, Luc and their operation. Laryngoscope 1971; 81(10):1652-7.

(2.) Barzilai G, Greenberg E, Uri N. Indications for the Caldwell-Luc approach in the endoscopic era. Otolaryngol Head Neck Surg 2005; 132(2):219-20.

(3.) Cutler JL, Duncavage JA, Matheny K, et al. Results of Caldwell-Luc after failed endoscopic middle meatus antrostomy in patients with chronic sinusitis. Laryngoscope 2003;113(12):2148-50.

(4.) Caldwell GW. Diseases of the accessory sinuses of the nose, and an improved method of treatment for suppuration of the maxillary antrum. N Y State J Med 1893;58:526-8.

(5.) Scanes Spicer RH. The surgical treatment of chronic empyema of the antrum maxillare. Br Med J 1894;2:1359-60.

(6.) Luc H. Une nouvelle methode operatoire pour la cure radicale et rapide de l'empyeme chronique du sinus maxillaire. Archives internationales de laryngologie, d'otologie et de rhinologie 1897: 77-93.

(7.) DeFreitas J, Lucente FE. The Caldwell-Luc procedure: Institutional review of 670 cases: 1975-1985. Laryngoscope 1988;98(12):1297-1300.

(8.) Robinson S, Baird R, Le T, Wormald PJ. The incidence of complications after canine fossa puncture performed during endoscopic sinus surgery. Am J Rhinol 2005; 19(2):203-6.

(9.) Toskala E, Rautiainen M. Electron microscopy assessment of the recovery of sinus mucosa after sinus surgery. Acta Otolaryngol 2003;123(8):954-9.

(10.) Guo Y, Majima Y, Hattori M, et al. Effects of functional endoscopic sinus surgery on maxillary sinus mucosa. Arch Otolaryngol Head Neck Surg 1997;123(10):1097-1100.

(11.) Fang SY. Normalization of maxillary sinus mucosa after FESS. A prospective study of chronic sinusitis with nasal polyps. Rhinology 1994 32(3):137-40.

(12.) Anselmo-Lima WT, Ferreira M, Valera FC, et al. Histological evaluation of maxillary sinus mucosa after functional endoscopic sinus surgery. Am J Rhinol 2007;21(6):719-24.

(13.) Forsgren K, Stierna P, Kumlien J, Carlsoo B. Regeneration of maxillary sinus mucosa following surgical removal. Experimental study in rabbits. Ann Otol Rhinol Laryngol 1993;102(6):459-66.

(14.) Forsgren K, Fukami M, Penttila, et al. Endoscopic and Caldwell-Luc approaches in chronic maxillary sinusitis: A comparative histopathologic study on preoperative and postoperative mucosal morphology. Ann Otol Rhinol Laryngol 1995;104(5):350-7.

Samuel S. Becker, MD; Deanne M. Roberts, MD; Peter A. Beddow, MA; Paul T. Russell, MD; James A. Duncavage, MD

From the Department of Otolaryngology-Head and Neck Surgery, Vanderbilt University Medical Center, Nashville, Tenn.

Corresponding author: Samuel S. Becket, MD, Department of Otolaryngology-Head and Neck Surgery, Vanderbilt University Medical Center, 7209 Medical Center East, South Tower, Nashville, TN 37232-8605. Email: sam.s.becker@gmail.com
Table 1. Patient demographics and comorbidities

                       Caldwell-Luc   Non-Caldwell-Luc
Age
Mean                      55 yr           48.4 yr
Range                  27 to 79 yr      13 to 76 yr

Sex
Male                    26(32.5%)         16(40%)
Female                  54(67.5%)         24(60%)
Comorbidities

Diabetes                 5(6.3%)          3(7.5%)
Aspirin sensitivity      2(2.5%)           4(10%)
Inhalant allergies      19(23.8%)        15(37.5%)
Smoker                  22(27.5%)          6(15%)

Table 2. Surgical sites and prior surgeries

                       Caldwell-Luc   Non-Caldwell-Luc

Surgical site
  Right                     24               6
  Left                      25               7
  Bilateral                 31               27

Prior maxillary
  surgeries
  Mean                     1.5              0.6
  Range                    0-7              0-3

Mean total no.             2.5              4.3
  sinuses addressed

Days since last
  surgery
  Mean                     878             1,618
  Range                  0-18,882         0-9,855

Table 3. Histologic findings: Eosinophils per high-power field

         Caldwell-Luc   Non-Caldwell-Luc

Mean         5.68            28.33
0             29               8
1-2           16               5
3-9           15               7
10-14         4                3
15-24         12               1
>25           4                16
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Title Annotation:ORIGINAL ARTICLE
Author:Becker, Samuel S.; Roberts, Deanne M.; Beddow, Peter A.; Russell, Paul T.; Duncavage, James A.
Publication:Ear, Nose and Throat Journal
Article Type:Report
Geographic Code:1USA
Date:Jun 1, 2011
Words:2632
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