Accepted Manuscript Diagnostic Criteria for A Curable Form of Chronic Rhinosinusitis. The Mucous Recirculation Syndrome Adesh Patel, MD Richard D. deShazo, MD Scott Stringer, MD PII:
S0002-9343(14)00234-4
DOI:
10.1016/j.amjmed.2014.03.007
Reference:
AJM 12445
To appear in:
The American Journal of Medicine
Received Date: 7 January 2014 Revised Date:
6 March 2014
Accepted Date: 6 March 2014
Please cite this article as: Patel A, deShazo RD, Stringer S, Diagnostic Criteria for A Curable Form of Chronic Rhinosinusitis. The Mucous Recirculation Syndrome, The American Journal of Medicine (2014), doi: 10.1016/j.amjmed.2014.03.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Running Head: MUCOUS RECIRCULATION SYNDROME
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Diagnostic Criteria for A Curable Form of Chronic Rhinosinusitis. The Mucous Recirculation Syndrome. Adesh Patel, MD,1 Richard D. deShazo, MD,1,2 and Scott Stringer, MD3
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From the Departments of Medicine,1 Pediatrics,2 and Otolaryngology The University of Mississippi Medical Center
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Jackson, Mississippi
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2500 North State Street
Corresponding author:
Richard D. deShazo, MD
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[email protected]
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601.984.5600
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Funding: None. Conflict of Interest: None. Authorship: All authors had access to the data and participated in writing this manuscript
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ABSTRACT In clinical practice, nonallergic rhinosinusitis (rhinopathy) is a common diagnosis of exclusion. The Mucous Recirculation Syndrome is one incompletely defined condition
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that masquerades as nonallergic rhinopathy. Mucous recirculation syndrome, a curable condition, should be differentiated from nonallergic rhinopathy. The underdiagnosis of this condition is due in part to a lack of diagnostic criteria. In this article, we review the
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medical literature to better characterize mucus recirculation syndrome and to establish
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diagnostic criteria for it.
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Keywords: mucous, recirculation, accessory ostium, antrostomy
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Introduction Nonallergic rhinosinusitis (rhinopathy) is a default diagnosis for chronic rhinosinusitis with no detectable cause. This heterogeneous syndrome has previously
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been called vasomotor rhinitis, nonallergic rhinitis, and idiopathic rhinitis.1-3 Our group has worked to define conditions responsible for incompletely defined syndromes of rhinopathy and to establish diagnostic criteria for them.4-6
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In this investigation, we studied a form of chronic rhinosinusitis underappreciated in the clinical literature. The mucous recirculation syndrome, first noted as a
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phenomenon in 1978 by Messerklinger and reported to cause chronic sinusitis in 1996 and 1997, can be a confounder if not excluded in clinical studies of chronic rhinosinusitis. 7-10 Unlike many other forms of chronic rhinosinusitis, it is curable. In this paper, we sought to better characterize and develop diagnostic criteria for the mucous
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recirculation syndrome. Methods
We searched the medical literature to construct a study cohort with adequate
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clinical data to complement that of 4 unreported patients with mucous recirculation syndrome from our university referral practice. Using the PubMed and Scopus search
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engines, we performed separate computer-based searches on “mucous OR mucous AND recirculation” and “mucoid AND rhinitis”. We used MeSH terms limited to the English language only. Inclusion criteria for patients in this cohort were (1) a diagnosis of mucous recirculation syndrome in a peer reviewed journal, (2) Data on age and sex, (3) Documentation of one or more symptoms of chronic rhinosinusitis to include
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paroxysmal sneezing, rhinorrhea, nasal congestion, or post nasal drainage, and (4) Mucous recirculation visualized on nasal endoscopy (Figure 1). Results
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Study Cohort
Computer assisted searches produced 21 articles from PubMed and 37 from Scopus that identified 30 distinct publications (Figure 1). These 30 publications were
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reviewed and reports in 6 articles were identified that provided information on patients who met inclusion criteria. In the process of reviewing these 6 articles, we found 2
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additional reports with 2 more patients who were included in our analysis. With the addition of our 4 patients, 12 patients with mucous recirculation formed the study group (Table 1).
Of the 12 patients in our cohort, 7 were females, 3 were males and the sex was
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not reported in 2 patients (Table 1). The patients ranged from 28 to 80 years old with an average age of 53. Our 4 patients were of Caucasian decent, but the races of the study subjects were not provided in any of the case reports. The most common
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presenting symptoms were persistent post nasal drainage and nasal obstruction. Five of 12 patients had received antibiotics without resolution of symptoms.
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Eleven out of the 12 patients had previous sinus surgeries for “maxillary sinusitis,” identified as 7 on the right, 3 on the left. One patient had surgery on the sphenoid sinus. Six of 12 patients had a “misplaced middle meatal antrostomy” such that recirculation occurred between the natural ostium of the maxillary sinus and the middle meatal antrostomy. Recirculation between the natural ostium or antrostomy and an accessory (nonsurgical) ostium was the second most common mechanism and
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occurred in 3 out of 12 patients (25%). For the remaining 25% of patients, recirculation occurred between a middle meatal antrostomy and an inferior meatal antrostomy, between the natural ostium of the maxillary sinus and an iatrogenic maxillary ostium, or
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between the natural ostium of sphenoid sinus and a sphenoidotomy. Patients Not Included
We felt exclusion of patients in reports where they did not meet inclusion criteria
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was important as we sought to identify only those patients who were symptomatic from mucous recirculation. This is important as mucous recirculation could theoretically
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occur without symptoms. Therefore, we included only 2 of 44 patients from 3 large studies of mucous recirculation syndrome. However, the data from these 3 studies were carefully reviewed.
One of these studies reported 7 patients of whom 5 were males and 2 were
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females (Table 2).11 They ranged from 14 to 55 years of age with an average age of 35. Mucous recirculation occurred between the natural ostium and an accessory ostium in all 7 patients. In the second study, all 31 patients had previous sinus surgeries.12
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Seventeen patients had recirculation between a middle meatal antrostomy and the natural maxillary ostium. Of the remaining 14 patients, 12 had recirculation between a
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middle and inferior meatal antrostomy. Six patients in a third study all had previous sinus surgeries as well.13 All 6 patients had recirculation between middle and inferior meatal antrostomies. Discussion
From Phenomenon to Clinical Syndrome
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For many years, inferior surgical antrostomy to produce nasoantral windows was performed with the intention to “drain” chronically infected sinuses by gravity through the nose. It was not until the studies of Messerklinger demonstrated that secretions in the
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sinuses were directed by cilia around these surgically placed ostia to the natural ostium that the ineffectiveness of inferior anstrostomies became apparent.7
The clinical significance of the mucous recirculation was not identified until
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mucous recirculation was noted to cause symptoms of chronic rhinosinusitis and that recirculation between 2 prior surgical antrostomies could be the mechanism for it .9,13
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Since then, aberrant mucous recirculation has been noted between surgically or spontaneously occurring accessory sinus ostia.14-17 Mechanism
Mucous recirculation occurs when mucous propelled by respiratory epithelium
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deviates from normal mucous circulatory pathways. Under normal conditions, mucoid secretions from the frontal sinus, maxillary sinus, and the anterior ethmoidal complex are transported out of the sinuses to join in or near the ethmoidal infundibulum and
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travels to the nasopharynx to be swallowed (Figure 2).18 Secretions from the posterior ethmoid and sphenoid sinus are also transported out of their respective ostia by ciliary
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transport to gather in the sphenoethmoidal recess where they travel to the nasopharynx posteriorly to join the secretions from other sinuses.18 However, in mucous recirculation syndrome, mucous returns to a sinus via an accessory ostium or iatrogenically misplaced antrostomy (Figure 3).8-17 At least 5 pathways have been described (Table 3).
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In the presence of mucous recirculation, impaired mucous clearance develops and appears to increase the risk of recurrent sinusitis. This may result from the repeated presentation of bacteria and viruses contained in the mucous within the
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respective sinuses.9
Differentiation from Nonallergic Rhinopathy is Difficult by Clinical Criteria Alone
The prevalence of mucous recirculation syndrome is unknown, although it is
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likely that it is underdiagnosed. One reason is the difficulty to distinguish mucous
recirculation syndrome from nonallergic rhinopathy. As demonstrated in our study,
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nonallergic rhinopathy and mucous recirculation present with similar clinical symptoms such as post nasal drip, nasal congestion, and rhinorrhea (Table 1). Nonallergic rhinopathy has been reported to have a female predominance with a ratio of 2:1 to 3:1 and patients with mucous recirculation syndrome appear to have a similar ratio.3,20
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Nonallergic rhinopathy has been thought to be more prevalent in adults between 30 and 60 years of age.20 Our data show similar age findings with an average age of 53. However, patients with mucous recirculation syndrome have a broad age range and
patients.
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Diagnostic Criteria
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include younger patients; whereas nonallergic rhinopathy typically occurs in older
Another reason for the probable underdiagnosis of mucous recirculation syndrome is a lack of diagnostic criteria. Formal criteria for the diagnosis of mucous recirculation could facilitate diagnosis, future investigation of this syndrome, and assure homogeneity of study groups in therapeutic trials. On the basis of our clinical experience and a review of published literature, we propose the following diagnostic criteria: (1)
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Symptoms of chronic rhinosinusitis that are refractory to oral or topical treatment; (2) Visualization of mucous recirculation between 2 or more ostia by rhinoscopy and (3) Resolution of symptoms with surgical treatment. The later criterion is important for
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clinical studies as we do not know whether it is possible to have mucous recirculation without symptoms. Two studies suggest that it is unlikely.21,22 If that suggestion can be confirmed, the third challenging criterion can be deleted. Obviously, the development of
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symptoms of rhinosinusitis after sinus surgery or persistence or the intractable nature of the symptoms should be an important clue that this syndrome may be present.
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The terms idiopathic, nonallergic or vasomotor rhinitis were not been incorporated into the proposed criteria. Further study may determine that one of these terms reflects more patients with mucous recirculation than another, that mucous recirculation may occur in some patients with allergic rhinitis, or that mucous
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recirculation can occupy in individuals with otherwise normal nasal mucosa. Regardless, under these circumstances, it seems imprudent to offer the diagnosis of vasomotor or idiopathic rhinopathy without consideration of mucous recirculation
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Diagnosis
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syndrome in the differential diagnosis.
Mucous recirculation should be suspected when patients are refractory to medical therapy, especially if they have had surgical antrostomy or accessory ostia are present. Although topical nasal corticosteroids and topical antihistamines have been shown to be somewhat efficacious for nonallergic rhinopathy, these treatments are
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unlikely to disrupt mucous recirculation23,24. Thus, failure of medical therapy should raise suspicion for mucous recirculation. Nasal endoscopy enables direct visualization and confirmation of a ring of
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recirculating mucous between natural ostia, accessory ostia or iatrogenic ostia. The appearance of mucous may vary in color and consistency, either as a clear stream of mucous with microbubbles or as a purulent thick yellowish discharge (Figures 4 and 5). Although mucous recirculation can be visualized as a “ring structure” on coronal
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computed tomography (CT) , the specificity, and sensitivity of CT scans in the diagnosis
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of mucous recirculation is unclear.11 Mucosal swelling and the fluctuating volume of mucous complicate the use of CT in this setting. However, CT is useful in demonstrating larger ostia.
Accessory (nonsurgical) ostia may be either spontaneous or congenital.
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Estimates of their prevalence range from 4-41%.9,15 Accessory ostia are more commonly found in the posterior and anterior fontanelle along the lateral nasal wall. The lateral wall has two areas of weakness where it consists of mucosa only and this
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facilitates the development of anterior and posterior fontanelle defects. 21 Some have argued that accessory ostia are the consequence of chronic rhinosinusitis .21,22
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Therefore, mucous recirculation should be suspected not only after antrostomy, but in any patient with an accessory ostium who complains of chronic rhinosinusitis where other causes of rhinitis cannot be identified. Antrostomies are routinely created at the time of endoscopic sinus surgery to improve the drainage of the sinuses when medical treatment is refractory. However, when these antrostomies are misplaced, for instance a right meatal antrostomy placed
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behind the natural ostium anteriorly, they may be an iatrogenic cause for mucous recirculation (Figures 4 and 5). Patients with ongoing symptoms of rhinosinusitis despite sinus surgery, require further evaluation to determine if mucous recirculation is
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occurring. Mucous recirculation may be terminated by removal of the tissue separating the two ostia to make one large ostium.9,12,14,16 Conclusions
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These data clearly establish mucous recirculation syndrome as a cause for
chronic rhinosinusitis. Further studies to determine the prevalence of this syndrome are
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required. Rhinoscopy of a large number of patients without rhinosinusitis to observe for mucous recirculation will be necessary to determine if mucous recirculation without symptoms occurs.
The diagnostic criteria proposed here should facilitate diagnosis, future studies
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and awareness of this little known condition. This condition should be considered when patients have chronic rhinosinusitis despite medical or surgical treatment. Nasal endoscopy should be performed to identify mucous recirculation and, if present,
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endoscopic sinus surgery considered to terminate recirculation and associated symptoms. Moreover, a firm diagnosis of nonallergic rhinopathy should probably not be
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made without exclusion of this syndrome.
Acknowledgement. The authors would like to thank Mr. Walter Cunningham in the Department of Medical Illustration, Mrs. Helvi McCall, Research Librarian, and Mrs. Leigh Baldwin Skipworth, all at the University of Mississippi Medical Center, for their assistance in preparation of this manuscript.
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References 1. Kaliner MA, Baraniuk JN, Benninger M, et al. Consensus definition of nonallergic rhinopathy (NAR), previously referred to as vasomotor rhinitis (VMR), nonallergicrhinitis, and/or idiopathic rhinitis. WAO J 2009;2(6):119–20.
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2. Settipane RA. Other causes of rhinitis: mixed rhinitis, rhinitis medicamentosa, hormonal rhinitis, rhinitis of elderly, and gustatory rhinitis. Immunol Allergy Clin North Am.2011;31(3):457–467.
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3. Kaliner MA: Nonallergic rhinopathy (formerly known as vasomotor rhinitis). Immunol Allergy Clin North Am 2011, 31:441-455.
4. Reed JS, deShazo RD, Houle TT, Stringer S, Wright LB, Moak SJ. Clinical Features of Sarcoid Rhinosinusitis. AJM 123(9): 856-62; 2010.
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5. Ly T, deShazo RD, Oliver J, Stringer S, Daley W, Stodard C. Diagnostic criteria for atrophic rhinosinusitis. AJM 122(8):747-753, 2009 6. deShazo RD, Swain RE. Diagnostic criteria for allergic fungal sinusitis. J Allergy Clin Immunol 96(1):24-35, 1995. 7. Messerklinger W. Endoscopy of the Nose. Urban Schwartzenberg, Baltimore, Maryland. 1978, page 123.
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8. Yanagisawa E, Weaver EM. Endoscopic view of recirculation phenomena of sphenoid sinus drainage. Ear Nose Throat J 1996; 75: 68-70.
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9. Matthews, B. L., Burke, A. J. C. (1997) Recirculation of mucus via accessory ostia causing chronic maxillary sinus disease. Otolaryngology - Head and Neck Surgery 117: 422-423.
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10. Kane KJ. Recirculation as a cause of persistent sinusitis Am J Rhinol 1997; 11: 361-369. 11. Chung SK, Cho DY, Dhong HJ. Computed tomogram findings of mucous recirculation between the natural and accessory ostia of the maxillary sinus. Am J Rhinol. 2002 Sep-Oct;16(5):265-8. 12. K.J. Kane, Recirculation of mucus as a cause of persistent sinusitis, Am. J. Rhinol. 11 (5) (1997) 361– 369. 13. Coleman, J. R., Duncavage, J. A. Extended middle meatal antrostomy: the treatment of circular flow. Laryngoscope 1996 106:1214-1217.
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14. Yanagisawa, E., Yanagisawa, K. (1997) Endoscopic view of recirculation phenomenon of the maxillary sinus. Ear, Nose and Throat Journal 76: 196-198. 15. Chung SK, Dhong HJ, Na DG. Mucus circulation between accessory ostium and natural ostium of maxillary sinus. J Laryngol Otol 1999;113:865-7.
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16. Gutman M, Houser S. Iatrogenic maxillary sinus recirculation and beyond. Ear Nose Throat J 2003; 82: 61-63 17. Kane, K.J. Persistent sinusitis from recirculating mucus after inferior turbinectomy. International Congress Series vol. 1240 October, 2003. p. 463-467
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18. Stammberger HR. Functional Endoscopic Sinus Surgery. The Messerklinger Technique. Philadelphia: B.C. Decker, 1991:17-37
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19. Settipane RA, Charnock DR. Epidemiology of rhinitis: allergic and nonallergic. In: Baraniuk JN, Shusterman D, editors. Nonallergic Rhinitis. New York: Informa; 2007:23Y34. 20. Mladina R et al. The two holes syndrome. Am J Rhinol " Allergy 2009 23(6):602-4 21. Mladina R, Skitarelić N, Casale M. Two holes syndrome (THS) is present in more than half of the postnasal drip patients? Acta Oto Laryngol 2010;130(11):1274.
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22. Webb DR, Meltzer EO, Finn AF, et al. Intranasal fluticasone is effective for perennial nonallergic rhinitis with or without eosinophilia. Ann Allergy Asthma Immunol 2002;88:385–90.
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23. Banov CH, Lieberman P, Vasomotor Rhinitis Study Groups. Efficacy of azelastine nasal spray in the treatment of vasomotor (perennial nonallergic) rhinitis. Ann Allergy Asthma Immunol 2001;86(1):28–35.
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Figure Legends
Figure 1. Flowchart used to select patients for inclusion in this study
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Figure 2. Diagram of right lateral nasal wall showing normal mucous secretion pathways from frontal, anterior ethmoid, and maxillary sinuses (black arrow) and secretion pathways from sphenoid and posterior ethmoid sinus (white arrow). (FS = frontal sinus, AE = anterior ethmoid sinus, MO = maxillary ostium, PE = posterior ethmoid sinus, SS = sphenoid sinus). Adapted from Stammberger (Reference 18).
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Figure 3. Diagram of right lateral nasal wall showing reported pathways of mucous recirculation. IMA and MMA in this diagram are misplaced antrostomies. (SS = sphenoid sinus, MO = maxillary sinus ostium, AO = accessory ostium, MMA = middle meatal antrostomy, IMA = inferior metal antrostomy). Adapted from Kane (Reference 10).
Figure 4. Recirculation of thin mucous (white dashed arrow) between natural maxillary sinus ostium (MO) and a misplaced middle maxillary meatal antrostomy (MMA).
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Figure 5. Recirculation of thick purulent mucous with microbubbles (white dashed arrow) between natural maxillary (MO) and a misplaced middle meatal antrostomy (MMA).
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Table 1. Demographics and Characteristics of Study Cohort
1
40
F
Recurrent sinusitis
28
Where Recirculation occurred
CT Findings
Reference Number
N/A
No
R Maxillary
NO to AO of maxillary sinus
Large, R sided maxillary mucous retention cyst
9
N/A
R Maxillary
NO to AO of maxillary sinus
Mucous ring connecting natural ostium and accessory ostium
15
16
M
Otorrhea
Yes
Yes
Yes
R Maxillary
NO to iatrogenic maxillary ostia
Bilateral soft tissue obstruction of the maxillary ostia, retention cyst in L and R maxillary sinuses
48
M
4
40
F
Foul smelling postnasal drip
Yes
N/A
L Sphenoid
Sphenoid sinus ostium to sphenoidotomy
N/A
8
5
N/A
N/A
Recurrent postnasal discharge
Yes
N/A
L Maxillary
NO of the maxillary sinus to MMA
N/A
14
6
N/A
N/A
Recurrent sinusitis with nasal obstruction
N/A
N/A
L Maxillary
NO to AO of maxillary sinus
N/A
14
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Recurrent Rhinosinusitis, Nasal congestion, thick post nasal drainage
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2
Sinus Involved
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Sex
Symptoms Refractory to Antibiotics
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Age
Symptoms Reported
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Patient No.
Previ ous Sinus Surg ery
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F
Yes
N/A
None
MMA to IMA
Yes
N/A
R Maxillary
NO of the maxillary sinus to MMA
NO of the maxillary sinus to MMA
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36
70
M
9
80
F
Postnasal drainage
Yes
Yes
R Maxillary
10
64
F
Recurrent sinusitis with left sided facial pain
Yes
Yes
R Maxillary
NO of the maxillary sinus to MMA
Yes
Yes
L Maxillary
NO of the maxillary sinus to MMA
Yes
R Maxillary
NO of the maxillary sinus to MMA
F
12
66
F
Nasal congestion
Yes
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58
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Recurrent headaches, post nasal drainage
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8
Frontal headaches, nasal stuffiness and discharge
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7
Recurrent nasal blockage, drainage and right sided facial pain
Persistent sinusitis
10
Opacification of frontal sinuses with obstruction of each frontal recess
10
Mucosal thickening of the R maxillary sinus
Our patient #1
Opacification of maxillary sinus
Our patient #2
Mucosal thickening with partial opacification of L maxillary sinus Mucosal thickening of R maxillary sinus with polypoid thickening in the inferior floor of R maxillary antrum
Our patient #3
Our patient #4
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N/A = not available, M = Male, F = Female, R = Right, L = Left, NO = Natural Ostium, AO = Accessory Ostium , MMA = Middle Meatal Antrostomy, IMA = Inferior Meatal Antrostomy
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Table 2. Reported Mechanisms of Recirculation Studies of Mucous Recirculation Maxillary Ostium or Antrostomy to Accessory Ostium
Sphenoid sinus ostium and sphenoidotomy
Perforated uncinate process
Maxillary Ostium and Iatrogenic Maxillary Ostium
0
1
0
1
0
1
0
0
0
0
0
0
0
14
1
1
1
Kane*
31
17
12
4
This Study
12
6
1
3
Chung
7
0
0
7
Coleman and Duncavage
6
0
6
Total
56
23
19
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*3 patients had bilateral recirculation
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No. of Patients
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Study Cohort
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Middle Meatal Antrostomy to Inferior Meatal Antrostomy
Maxillary Ostium to Middle Meatal Antrostomy
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Table 3. Five Mucous Recirculation Pathways, Identified in 56 Patients Referred for Revision of Sinus Surgery
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1. Between the natural ostium of the maxillary and either a middle meatal antrostomy or an accessory ostium (62%) 2. Between a middle meatal antrostomy and an inferior meatal antrostomy (32%) 3. Between nonsurgical perforations in the uncinate process with or without circulation through the natural ostium (2%) 4. Between sphenoid sinus natural ostium and sphenoidotomy (2%) 5. Between the natural ostium of the maxillary sinus and an iatrogenic maxillary ostium (2%)
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1. Without established diagnostic criteria and an unknown prevalence, the Mucous Recirculation Syndrome is an underdiagnosed condition.
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3. Unlike many forms of rhinitis, the Mucous Recirculation Syndrome is curable.
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2. The possibility of the Mucous Recirculation Syndrome should be considered in patients with chronic rhinosinusitis.
S0002-9343(14)00234-4
DOI:
10.1016/j.amjmed.2014.03.007
Reference:
AJM 12445
To appear in:
The American Journal of Medicine
Received Date: 7 January 2014 Revised Date:
6 March 2014
Accepted Date: 6 March 2014
Please cite this article as: Patel A, deShazo RD, Stringer S, Diagnostic Criteria for A Curable Form of Chronic Rhinosinusitis. The Mucous Recirculation Syndrome, The American Journal of Medicine (2014), doi: 10.1016/j.amjmed.2014.03.007. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Running Head: MUCOUS RECIRCULATION SYNDROME
1
Diagnostic Criteria for A Curable Form of Chronic Rhinosinusitis. The Mucous Recirculation Syndrome. Adesh Patel, MD,1 Richard D. deShazo, MD,1,2 and Scott Stringer, MD3
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From the Departments of Medicine,1 Pediatrics,2 and Otolaryngology The University of Mississippi Medical Center
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Jackson, Mississippi
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2500 North State Street
Corresponding author:
Richard D. deShazo, MD
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[email protected]
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601.984.5600
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Funding: None. Conflict of Interest: None. Authorship: All authors had access to the data and participated in writing this manuscript
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ABSTRACT In clinical practice, nonallergic rhinosinusitis (rhinopathy) is a common diagnosis of exclusion. The Mucous Recirculation Syndrome is one incompletely defined condition
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that masquerades as nonallergic rhinopathy. Mucous recirculation syndrome, a curable condition, should be differentiated from nonallergic rhinopathy. The underdiagnosis of this condition is due in part to a lack of diagnostic criteria. In this article, we review the
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medical literature to better characterize mucus recirculation syndrome and to establish
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diagnostic criteria for it.
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Keywords: mucous, recirculation, accessory ostium, antrostomy
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Introduction Nonallergic rhinosinusitis (rhinopathy) is a default diagnosis for chronic rhinosinusitis with no detectable cause. This heterogeneous syndrome has previously
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been called vasomotor rhinitis, nonallergic rhinitis, and idiopathic rhinitis.1-3 Our group has worked to define conditions responsible for incompletely defined syndromes of rhinopathy and to establish diagnostic criteria for them.4-6
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In this investigation, we studied a form of chronic rhinosinusitis underappreciated in the clinical literature. The mucous recirculation syndrome, first noted as a
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phenomenon in 1978 by Messerklinger and reported to cause chronic sinusitis in 1996 and 1997, can be a confounder if not excluded in clinical studies of chronic rhinosinusitis. 7-10 Unlike many other forms of chronic rhinosinusitis, it is curable. In this paper, we sought to better characterize and develop diagnostic criteria for the mucous
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recirculation syndrome. Methods
We searched the medical literature to construct a study cohort with adequate
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clinical data to complement that of 4 unreported patients with mucous recirculation syndrome from our university referral practice. Using the PubMed and Scopus search
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engines, we performed separate computer-based searches on “mucous OR mucous AND recirculation” and “mucoid AND rhinitis”. We used MeSH terms limited to the English language only. Inclusion criteria for patients in this cohort were (1) a diagnosis of mucous recirculation syndrome in a peer reviewed journal, (2) Data on age and sex, (3) Documentation of one or more symptoms of chronic rhinosinusitis to include
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paroxysmal sneezing, rhinorrhea, nasal congestion, or post nasal drainage, and (4) Mucous recirculation visualized on nasal endoscopy (Figure 1). Results
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Study Cohort
Computer assisted searches produced 21 articles from PubMed and 37 from Scopus that identified 30 distinct publications (Figure 1). These 30 publications were
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reviewed and reports in 6 articles were identified that provided information on patients who met inclusion criteria. In the process of reviewing these 6 articles, we found 2
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additional reports with 2 more patients who were included in our analysis. With the addition of our 4 patients, 12 patients with mucous recirculation formed the study group (Table 1).
Of the 12 patients in our cohort, 7 were females, 3 were males and the sex was
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not reported in 2 patients (Table 1). The patients ranged from 28 to 80 years old with an average age of 53. Our 4 patients were of Caucasian decent, but the races of the study subjects were not provided in any of the case reports. The most common
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presenting symptoms were persistent post nasal drainage and nasal obstruction. Five of 12 patients had received antibiotics without resolution of symptoms.
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Eleven out of the 12 patients had previous sinus surgeries for “maxillary sinusitis,” identified as 7 on the right, 3 on the left. One patient had surgery on the sphenoid sinus. Six of 12 patients had a “misplaced middle meatal antrostomy” such that recirculation occurred between the natural ostium of the maxillary sinus and the middle meatal antrostomy. Recirculation between the natural ostium or antrostomy and an accessory (nonsurgical) ostium was the second most common mechanism and
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occurred in 3 out of 12 patients (25%). For the remaining 25% of patients, recirculation occurred between a middle meatal antrostomy and an inferior meatal antrostomy, between the natural ostium of the maxillary sinus and an iatrogenic maxillary ostium, or
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between the natural ostium of sphenoid sinus and a sphenoidotomy. Patients Not Included
We felt exclusion of patients in reports where they did not meet inclusion criteria
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was important as we sought to identify only those patients who were symptomatic from mucous recirculation. This is important as mucous recirculation could theoretically
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occur without symptoms. Therefore, we included only 2 of 44 patients from 3 large studies of mucous recirculation syndrome. However, the data from these 3 studies were carefully reviewed.
One of these studies reported 7 patients of whom 5 were males and 2 were
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females (Table 2).11 They ranged from 14 to 55 years of age with an average age of 35. Mucous recirculation occurred between the natural ostium and an accessory ostium in all 7 patients. In the second study, all 31 patients had previous sinus surgeries.12
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Seventeen patients had recirculation between a middle meatal antrostomy and the natural maxillary ostium. Of the remaining 14 patients, 12 had recirculation between a
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middle and inferior meatal antrostomy. Six patients in a third study all had previous sinus surgeries as well.13 All 6 patients had recirculation between middle and inferior meatal antrostomies. Discussion
From Phenomenon to Clinical Syndrome
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For many years, inferior surgical antrostomy to produce nasoantral windows was performed with the intention to “drain” chronically infected sinuses by gravity through the nose. It was not until the studies of Messerklinger demonstrated that secretions in the
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sinuses were directed by cilia around these surgically placed ostia to the natural ostium that the ineffectiveness of inferior anstrostomies became apparent.7
The clinical significance of the mucous recirculation was not identified until
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mucous recirculation was noted to cause symptoms of chronic rhinosinusitis and that recirculation between 2 prior surgical antrostomies could be the mechanism for it .9,13
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Since then, aberrant mucous recirculation has been noted between surgically or spontaneously occurring accessory sinus ostia.14-17 Mechanism
Mucous recirculation occurs when mucous propelled by respiratory epithelium
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deviates from normal mucous circulatory pathways. Under normal conditions, mucoid secretions from the frontal sinus, maxillary sinus, and the anterior ethmoidal complex are transported out of the sinuses to join in or near the ethmoidal infundibulum and
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travels to the nasopharynx to be swallowed (Figure 2).18 Secretions from the posterior ethmoid and sphenoid sinus are also transported out of their respective ostia by ciliary
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transport to gather in the sphenoethmoidal recess where they travel to the nasopharynx posteriorly to join the secretions from other sinuses.18 However, in mucous recirculation syndrome, mucous returns to a sinus via an accessory ostium or iatrogenically misplaced antrostomy (Figure 3).8-17 At least 5 pathways have been described (Table 3).
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In the presence of mucous recirculation, impaired mucous clearance develops and appears to increase the risk of recurrent sinusitis. This may result from the repeated presentation of bacteria and viruses contained in the mucous within the
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respective sinuses.9
Differentiation from Nonallergic Rhinopathy is Difficult by Clinical Criteria Alone
The prevalence of mucous recirculation syndrome is unknown, although it is
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likely that it is underdiagnosed. One reason is the difficulty to distinguish mucous
recirculation syndrome from nonallergic rhinopathy. As demonstrated in our study,
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nonallergic rhinopathy and mucous recirculation present with similar clinical symptoms such as post nasal drip, nasal congestion, and rhinorrhea (Table 1). Nonallergic rhinopathy has been reported to have a female predominance with a ratio of 2:1 to 3:1 and patients with mucous recirculation syndrome appear to have a similar ratio.3,20
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Nonallergic rhinopathy has been thought to be more prevalent in adults between 30 and 60 years of age.20 Our data show similar age findings with an average age of 53. However, patients with mucous recirculation syndrome have a broad age range and
patients.
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Diagnostic Criteria
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include younger patients; whereas nonallergic rhinopathy typically occurs in older
Another reason for the probable underdiagnosis of mucous recirculation syndrome is a lack of diagnostic criteria. Formal criteria for the diagnosis of mucous recirculation could facilitate diagnosis, future investigation of this syndrome, and assure homogeneity of study groups in therapeutic trials. On the basis of our clinical experience and a review of published literature, we propose the following diagnostic criteria: (1)
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Symptoms of chronic rhinosinusitis that are refractory to oral or topical treatment; (2) Visualization of mucous recirculation between 2 or more ostia by rhinoscopy and (3) Resolution of symptoms with surgical treatment. The later criterion is important for
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clinical studies as we do not know whether it is possible to have mucous recirculation without symptoms. Two studies suggest that it is unlikely.21,22 If that suggestion can be confirmed, the third challenging criterion can be deleted. Obviously, the development of
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symptoms of rhinosinusitis after sinus surgery or persistence or the intractable nature of the symptoms should be an important clue that this syndrome may be present.
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The terms idiopathic, nonallergic or vasomotor rhinitis were not been incorporated into the proposed criteria. Further study may determine that one of these terms reflects more patients with mucous recirculation than another, that mucous recirculation may occur in some patients with allergic rhinitis, or that mucous
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recirculation can occupy in individuals with otherwise normal nasal mucosa. Regardless, under these circumstances, it seems imprudent to offer the diagnosis of vasomotor or idiopathic rhinopathy without consideration of mucous recirculation
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Diagnosis
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syndrome in the differential diagnosis.
Mucous recirculation should be suspected when patients are refractory to medical therapy, especially if they have had surgical antrostomy or accessory ostia are present. Although topical nasal corticosteroids and topical antihistamines have been shown to be somewhat efficacious for nonallergic rhinopathy, these treatments are
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unlikely to disrupt mucous recirculation23,24. Thus, failure of medical therapy should raise suspicion for mucous recirculation. Nasal endoscopy enables direct visualization and confirmation of a ring of
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recirculating mucous between natural ostia, accessory ostia or iatrogenic ostia. The appearance of mucous may vary in color and consistency, either as a clear stream of mucous with microbubbles or as a purulent thick yellowish discharge (Figures 4 and 5). Although mucous recirculation can be visualized as a “ring structure” on coronal
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computed tomography (CT) , the specificity, and sensitivity of CT scans in the diagnosis
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of mucous recirculation is unclear.11 Mucosal swelling and the fluctuating volume of mucous complicate the use of CT in this setting. However, CT is useful in demonstrating larger ostia.
Accessory (nonsurgical) ostia may be either spontaneous or congenital.
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Estimates of their prevalence range from 4-41%.9,15 Accessory ostia are more commonly found in the posterior and anterior fontanelle along the lateral nasal wall. The lateral wall has two areas of weakness where it consists of mucosa only and this
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facilitates the development of anterior and posterior fontanelle defects. 21 Some have argued that accessory ostia are the consequence of chronic rhinosinusitis .21,22
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Therefore, mucous recirculation should be suspected not only after antrostomy, but in any patient with an accessory ostium who complains of chronic rhinosinusitis where other causes of rhinitis cannot be identified. Antrostomies are routinely created at the time of endoscopic sinus surgery to improve the drainage of the sinuses when medical treatment is refractory. However, when these antrostomies are misplaced, for instance a right meatal antrostomy placed
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behind the natural ostium anteriorly, they may be an iatrogenic cause for mucous recirculation (Figures 4 and 5). Patients with ongoing symptoms of rhinosinusitis despite sinus surgery, require further evaluation to determine if mucous recirculation is
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occurring. Mucous recirculation may be terminated by removal of the tissue separating the two ostia to make one large ostium.9,12,14,16 Conclusions
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These data clearly establish mucous recirculation syndrome as a cause for
chronic rhinosinusitis. Further studies to determine the prevalence of this syndrome are
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required. Rhinoscopy of a large number of patients without rhinosinusitis to observe for mucous recirculation will be necessary to determine if mucous recirculation without symptoms occurs.
The diagnostic criteria proposed here should facilitate diagnosis, future studies
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and awareness of this little known condition. This condition should be considered when patients have chronic rhinosinusitis despite medical or surgical treatment. Nasal endoscopy should be performed to identify mucous recirculation and, if present,
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endoscopic sinus surgery considered to terminate recirculation and associated symptoms. Moreover, a firm diagnosis of nonallergic rhinopathy should probably not be
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made without exclusion of this syndrome.
Acknowledgement. The authors would like to thank Mr. Walter Cunningham in the Department of Medical Illustration, Mrs. Helvi McCall, Research Librarian, and Mrs. Leigh Baldwin Skipworth, all at the University of Mississippi Medical Center, for their assistance in preparation of this manuscript.
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References 1. Kaliner MA, Baraniuk JN, Benninger M, et al. Consensus definition of nonallergic rhinopathy (NAR), previously referred to as vasomotor rhinitis (VMR), nonallergicrhinitis, and/or idiopathic rhinitis. WAO J 2009;2(6):119–20.
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2. Settipane RA. Other causes of rhinitis: mixed rhinitis, rhinitis medicamentosa, hormonal rhinitis, rhinitis of elderly, and gustatory rhinitis. Immunol Allergy Clin North Am.2011;31(3):457–467.
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3. Kaliner MA: Nonallergic rhinopathy (formerly known as vasomotor rhinitis). Immunol Allergy Clin North Am 2011, 31:441-455.
4. Reed JS, deShazo RD, Houle TT, Stringer S, Wright LB, Moak SJ. Clinical Features of Sarcoid Rhinosinusitis. AJM 123(9): 856-62; 2010.
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5. Ly T, deShazo RD, Oliver J, Stringer S, Daley W, Stodard C. Diagnostic criteria for atrophic rhinosinusitis. AJM 122(8):747-753, 2009 6. deShazo RD, Swain RE. Diagnostic criteria for allergic fungal sinusitis. J Allergy Clin Immunol 96(1):24-35, 1995. 7. Messerklinger W. Endoscopy of the Nose. Urban Schwartzenberg, Baltimore, Maryland. 1978, page 123.
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8. Yanagisawa E, Weaver EM. Endoscopic view of recirculation phenomena of sphenoid sinus drainage. Ear Nose Throat J 1996; 75: 68-70.
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9. Matthews, B. L., Burke, A. J. C. (1997) Recirculation of mucus via accessory ostia causing chronic maxillary sinus disease. Otolaryngology - Head and Neck Surgery 117: 422-423.
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10. Kane KJ. Recirculation as a cause of persistent sinusitis Am J Rhinol 1997; 11: 361-369. 11. Chung SK, Cho DY, Dhong HJ. Computed tomogram findings of mucous recirculation between the natural and accessory ostia of the maxillary sinus. Am J Rhinol. 2002 Sep-Oct;16(5):265-8. 12. K.J. Kane, Recirculation of mucus as a cause of persistent sinusitis, Am. J. Rhinol. 11 (5) (1997) 361– 369. 13. Coleman, J. R., Duncavage, J. A. Extended middle meatal antrostomy: the treatment of circular flow. Laryngoscope 1996 106:1214-1217.
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14. Yanagisawa, E., Yanagisawa, K. (1997) Endoscopic view of recirculation phenomenon of the maxillary sinus. Ear, Nose and Throat Journal 76: 196-198. 15. Chung SK, Dhong HJ, Na DG. Mucus circulation between accessory ostium and natural ostium of maxillary sinus. J Laryngol Otol 1999;113:865-7.
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16. Gutman M, Houser S. Iatrogenic maxillary sinus recirculation and beyond. Ear Nose Throat J 2003; 82: 61-63 17. Kane, K.J. Persistent sinusitis from recirculating mucus after inferior turbinectomy. International Congress Series vol. 1240 October, 2003. p. 463-467
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18. Stammberger HR. Functional Endoscopic Sinus Surgery. The Messerklinger Technique. Philadelphia: B.C. Decker, 1991:17-37
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19. Settipane RA, Charnock DR. Epidemiology of rhinitis: allergic and nonallergic. In: Baraniuk JN, Shusterman D, editors. Nonallergic Rhinitis. New York: Informa; 2007:23Y34. 20. Mladina R et al. The two holes syndrome. Am J Rhinol " Allergy 2009 23(6):602-4 21. Mladina R, Skitarelić N, Casale M. Two holes syndrome (THS) is present in more than half of the postnasal drip patients? Acta Oto Laryngol 2010;130(11):1274.
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22. Webb DR, Meltzer EO, Finn AF, et al. Intranasal fluticasone is effective for perennial nonallergic rhinitis with or without eosinophilia. Ann Allergy Asthma Immunol 2002;88:385–90.
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23. Banov CH, Lieberman P, Vasomotor Rhinitis Study Groups. Efficacy of azelastine nasal spray in the treatment of vasomotor (perennial nonallergic) rhinitis. Ann Allergy Asthma Immunol 2001;86(1):28–35.
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Figure Legends
Figure 1. Flowchart used to select patients for inclusion in this study
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Figure 2. Diagram of right lateral nasal wall showing normal mucous secretion pathways from frontal, anterior ethmoid, and maxillary sinuses (black arrow) and secretion pathways from sphenoid and posterior ethmoid sinus (white arrow). (FS = frontal sinus, AE = anterior ethmoid sinus, MO = maxillary ostium, PE = posterior ethmoid sinus, SS = sphenoid sinus). Adapted from Stammberger (Reference 18).
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Figure 3. Diagram of right lateral nasal wall showing reported pathways of mucous recirculation. IMA and MMA in this diagram are misplaced antrostomies. (SS = sphenoid sinus, MO = maxillary sinus ostium, AO = accessory ostium, MMA = middle meatal antrostomy, IMA = inferior metal antrostomy). Adapted from Kane (Reference 10).
Figure 4. Recirculation of thin mucous (white dashed arrow) between natural maxillary sinus ostium (MO) and a misplaced middle maxillary meatal antrostomy (MMA).
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Figure 5. Recirculation of thick purulent mucous with microbubbles (white dashed arrow) between natural maxillary (MO) and a misplaced middle meatal antrostomy (MMA).
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Table 1. Demographics and Characteristics of Study Cohort
1
40
F
Recurrent sinusitis
28
Where Recirculation occurred
CT Findings
Reference Number
N/A
No
R Maxillary
NO to AO of maxillary sinus
Large, R sided maxillary mucous retention cyst
9
N/A
R Maxillary
NO to AO of maxillary sinus
Mucous ring connecting natural ostium and accessory ostium
15
16
M
Otorrhea
Yes
Yes
Yes
R Maxillary
NO to iatrogenic maxillary ostia
Bilateral soft tissue obstruction of the maxillary ostia, retention cyst in L and R maxillary sinuses
48
M
4
40
F
Foul smelling postnasal drip
Yes
N/A
L Sphenoid
Sphenoid sinus ostium to sphenoidotomy
N/A
8
5
N/A
N/A
Recurrent postnasal discharge
Yes
N/A
L Maxillary
NO of the maxillary sinus to MMA
N/A
14
6
N/A
N/A
Recurrent sinusitis with nasal obstruction
N/A
N/A
L Maxillary
NO to AO of maxillary sinus
N/A
14
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Recurrent Rhinosinusitis, Nasal congestion, thick post nasal drainage
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2
Sinus Involved
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Sex
Symptoms Refractory to Antibiotics
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Age
Symptoms Reported
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Patient No.
Previ ous Sinus Surg ery
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Yes
N/A
None
MMA to IMA
Yes
N/A
R Maxillary
NO of the maxillary sinus to MMA
NO of the maxillary sinus to MMA
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36
70
M
9
80
F
Postnasal drainage
Yes
Yes
R Maxillary
10
64
F
Recurrent sinusitis with left sided facial pain
Yes
Yes
R Maxillary
NO of the maxillary sinus to MMA
Yes
Yes
L Maxillary
NO of the maxillary sinus to MMA
Yes
R Maxillary
NO of the maxillary sinus to MMA
F
12
66
F
Nasal congestion
Yes
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58
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11
Recurrent headaches, post nasal drainage
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8
Frontal headaches, nasal stuffiness and discharge
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7
Recurrent nasal blockage, drainage and right sided facial pain
Persistent sinusitis
10
Opacification of frontal sinuses with obstruction of each frontal recess
10
Mucosal thickening of the R maxillary sinus
Our patient #1
Opacification of maxillary sinus
Our patient #2
Mucosal thickening with partial opacification of L maxillary sinus Mucosal thickening of R maxillary sinus with polypoid thickening in the inferior floor of R maxillary antrum
Our patient #3
Our patient #4
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N/A = not available, M = Male, F = Female, R = Right, L = Left, NO = Natural Ostium, AO = Accessory Ostium , MMA = Middle Meatal Antrostomy, IMA = Inferior Meatal Antrostomy
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Table 2. Reported Mechanisms of Recirculation Studies of Mucous Recirculation Maxillary Ostium or Antrostomy to Accessory Ostium
Sphenoid sinus ostium and sphenoidotomy
Perforated uncinate process
Maxillary Ostium and Iatrogenic Maxillary Ostium
0
1
0
1
0
1
0
0
0
0
0
0
0
14
1
1
1
Kane*
31
17
12
4
This Study
12
6
1
3
Chung
7
0
0
7
Coleman and Duncavage
6
0
6
Total
56
23
19
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*3 patients had bilateral recirculation
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No. of Patients
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Study Cohort
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Middle Meatal Antrostomy to Inferior Meatal Antrostomy
Maxillary Ostium to Middle Meatal Antrostomy
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Table 3. Five Mucous Recirculation Pathways, Identified in 56 Patients Referred for Revision of Sinus Surgery
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1. Between the natural ostium of the maxillary and either a middle meatal antrostomy or an accessory ostium (62%) 2. Between a middle meatal antrostomy and an inferior meatal antrostomy (32%) 3. Between nonsurgical perforations in the uncinate process with or without circulation through the natural ostium (2%) 4. Between sphenoid sinus natural ostium and sphenoidotomy (2%) 5. Between the natural ostium of the maxillary sinus and an iatrogenic maxillary ostium (2%)
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1. Without established diagnostic criteria and an unknown prevalence, the Mucous Recirculation Syndrome is an underdiagnosed condition.
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3. Unlike many forms of rhinitis, the Mucous Recirculation Syndrome is curable.
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2. The possibility of the Mucous Recirculation Syndrome should be considered in patients with chronic rhinosinusitis.
