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REVIEW

Diagnostic Criteria for a Curable Form of Chronic


Rhinosinusitis: The Mucous Recirculation Syndrome
Adesh Patel, MD,a Richard D. deShazo, MD,a,b Scott Stringer, MDc
a
Department of Medicine, bDepartment of Pediatrics, and cDepartment of Otolaryngology, The University of Mississippi Medical Center,
Jackson.

ABSTRACT
In clinical practice, nonallergic rhinosinusitis (rhinopathy) is a common diagnosis of exclusion. The mucous
recirculation syndrome is one incompletely dened condition 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 medical literature to better characterize mucous recirculation syndrome and to establish diagnostic
criteria for it.
2014 Elsevier Inc. All rights reserved.  The American Journal of Medicine (2014) 127, 586-591
KEYWORDS: Accessory ostium; Antrostomy; Mucous; Recirculation

Nonallergic rhinosinusitis (rhinopathy) is a default diagnosis


for chronic rhinosinusitis with no detectable cause. This
heterogeneous syndrome previously has been called vasomotor rhinitis, nonallergic rhinitis, and idiopathic rhinitis.1-3
Our group has worked to dene conditions responsible for
incompletely dened syndromes of rhinopathy and to
establish diagnostic criteria for them.4-6
In this investigation, we studied a form of chronic rhinosinusitis underappreciated in the clinical literature. The mucous recirculation syndrome, rst noted as a phenomenon in
1978 by Messerklinger and reported in 1996 and 1997 to
cause chronic sinusitis, 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
study, we sought to better characterize and develop diagnostic criteria for the mucous recirculation syndrome.

METHODS
We searched the medical literature to construct a study
cohort with adequate clinical data to complement that of 4
Funding: None.
Conict of Interest: None.
Authorship: All authors had access to the data and participated in
writing this manuscript.
Requests for reprints should be addressed to Richard D. deShazo, MD,
Department of Medicine, The University of Mississippi Medical Center,
2500 North State Street, Jackson, MI 39216.
E-mail address: rdeshazo@umc.edu
0002-9343/$ -see front matter 2014 Elsevier Inc. All rights reserved.
http://dx.doi.org/10.1016/j.amjmed.2014.03.007

unreported patients with mucous recirculation syndrome


from our university referral practice. Using the PubMed and
Scopus search engines, we performed separate computerbased 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: a diagnosis of Mucous Recirculation Syndrome in a peer-reviewed journal; data on age
and sex; documentation of one or more symptoms of
chronic rhinosinusitis to include paroxysmal sneezing, rhinorrhea, nasal congestion, or postnasal drainage; and mucous recirculation visualized on nasal endoscopy (Figure 1).

RESULTS
Study Cohort
Computer-assisted searches produced 21 articles from
PubMed and 37 from Scopus that identied 30 distinct
publications (Figure 1). These 30 publications were
reviewed, and reports in 6 articles were identied that
provided information on patients who met inclusion
criteria. In the process of reviewing these 6 articles, we
found 2 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 female, 3 were
male, and the sex was not reported in 2 patients (Table 1).

Patel et al

The Mucous Recirculation Syndrome

587

The patients ranged from 28 to 80 years old, with an average


patients had previous sinus surgeries.10 Seventeen patients
age of 53 years. Our 4 patients were of Caucasian descent,
had recirculation between a middle meatal antrostomy and
but the races of the study subjects were not provided in any
the natural maxillary ostium. Of the remaining 14 patients,
of the case reports. The most common presenting symptoms
12 had recirculation between a middle and inferior meatal
were persistent postnasal drainage and nasal obstruction.
antrostomy. Six patients in a third study all had previous
Five of 12 patients had received antibiotics without
sinus surgeries as well.12 All 6 patients had recirculation
resolution of symptoms.
between middle and inferior meaEleven of the 12 patients
tal antrostomies.
CLINICAL SIGNIFICANCE
had previous sinus surgeries for
maxillary sinusitis, identied as
 Without established diagnostic criteria
7 on the right, 3 on the left. One
DISCUSSION
and an unknown prevalence, the mucous
patient had surgery on the spherecirculation syndrome is an underFrom Phenomenon to
noid sinus. Six of 12 patients had a
diagnosed condition.
Clinical Syndrome
misplaced middle meatal antrosFor many years, inferior surgical
 The possibility of the mucous recirculatomy such that recirculation ocantrostomy to produce nasoantral
curred between the natural ostium
tion syndrome should be considered in
windows was performed with the
of the maxillary sinus and the
patients with chronic rhinosinusitis.
intention to drain chronically inmiddle meatal antrostomy. Recir Unlike many forms of rhinitis, the mufected sinuses by gravity through
culation between the natural ostium
cous recirculation syndrome is curable.
the nose. It was not until the studies
or antrostomy and an accessory
of Messerklinger demonstrated that
(nonsurgical) ostium was the second
secretions in the sinuses were dimost common mechanism and ocrected by cilia around these surgically placed ostia to the
curred in 3 of 12 patients (25%). For the remaining 25% of
natural ostium that the ineffectiveness of inferior antrostomies
patients, recirculation occurred between a middle meatal
became apparent.7
antrostomy and an inferior meatal antrostomy, between the
The clinical signicance of the mucous recirculation was
natural ostium of the maxillary sinus and an iatrogenic
not identied until mucous recirculation was noted to cause
maxillary ostium, or between the natural ostium of sphenoid
symptoms of chronic rhinosinusitis and that recirculation
sinus and a sphenoidotomy.
between 2 prior surgical antrostomies could be the mechanism for it.9,12 Since then, aberrant mucous recirculation has
been noted between surgically or spontaneously occurring
Patients not Included
accessory sinus ostia.13-16
We believed that exclusion of patients in reports where they
did not meet inclusion criteria was important as we sought to
identify only those patients who were symptomatic from
Mechanism
mucous recirculation. This is important, as mucous recirculation could theoretically occur without symptoms.
Mucous recirculation occurs when mucous propelled by
Therefore, we included only 2 of 44 patients from 3 large
respiratory epithelium deviates from normal mucous cirstudies of mucous recirculation syndrome. However, the
culatory pathways. Under normal conditions, mucoid sedata from these 3 studies were carefully reviewed.
cretions from the frontal sinus, maxillary sinus, and the
One of these studies reported 7 patients, of whom 5 were
anterior ethmoidal complex are transported out of the simale and 2 were female (Table 2).11 They ranged from 14
nuses to join in or near the ethmoidal infundibulum and
travel to the nasopharynx to be swallowed (Figure 2).17
to 55 years of age, with an average age of 35 years. Mucous
recirculation occurred between the natural ostium and an
Secretions from the posterior ethmoid and sphenoid sinus
accessory ostium in all 7 patients. In the second study, all 31
also are transported out of their respective ostia by ciliary

Figure 1

Flowchart used to select patients for inclusion in this study.

588

The American Journal of Medicine, Vol 127, No 7, July 2014

Table 1

Demographics and Characteristics of Study Cohort


Where
Recirculation
Occurred

Patient Age,
Symptoms
No.
Years Sex Reported

Previous Symptoms
Refractory
Sinus
Sinus
Surgery to Antibiotics Involved

40

Recurrent sinusitis

N/A

No

28

Otorrhea

Yes

N/A

48

Yes
Recurrent
rhinosinusitis, nasal
congestion, thick
post nasal drainage

Yes

R Maxillary NO to iatrogenic
maxillary ostia

40

Foul-smelling postnasal Yes


drip

N/A

N/A N/A Recurrent postnasal


discharge
N/A N/A Recurrent
sinusitis with
nasal obstruction
36
F
Recurrent nasal
blockage, drainage,
and right-sided
facial pain
70
M Frontal headaches,
nasal stufness,
and discharge

Yes

N/A

N/A

N/A

L Sphenoid Sphenoid sinus


ostium to
sphenoidotomy
L Maxillary NO of the maxillary N/A
sinus to MMA
L Maxillary NO to AO of
N/A
maxillary sinus

Yes

N/A

None

10

Yes

N/A

80

Postnasal drainage

Yes

Yes

10

64

Yes

Yes

11

58

Recurrent sinusitis
with left-sided
facial pain
Recurrent headaches,
postnasal drainage

R Maxillary NO of the maxillary Opacication of


sinus to MMA
frontal sinuses with
obstruction of each
frontal recess
R Maxillary NO of the maxillary Mucosal thickening of
sinus to MMA
the R maxillary sinus
R Maxillary NO of the maxillary Opacication of
sinus to MMA
maxillary sinus

Yes

Yes

12

66

Yes

Yes

Nasal congestion

R Maxillary NO to AO of
maxillary sinus
R Maxillary NO to AO of
maxillary sinus

MMA to IMA

CT Findings
Large, R-sided maxillary
mucous retention cyst
Mucous ring connecting
natural ostium and
accessory ostium
Bilateral soft tissue
obstruction of the
maxillary ostia,
retention cyst in L
and R maxillary sinuses
N/A

Persistent sinusitis

Reference
Number
9

15

16

14

14

10

Our patient
#1
Our patient
#2

L Maxillary NO of the maxillary Mucosal thickening with Our patient


sinus to MMA
partial opacication
#3
of L maxillary sinus
Our patient
R Maxillary NO of the maxillary Mucosal thickening of
#4
sinus to MMA
R maxillary sinus with
polypoid thickening
in the inferior oor
of R maxillary antrum

AO accessory ostium; F female; IMA inferior meatal antrostomy; L left; M male; MMA middle meatal antrostomy; N/A not available;
NO natural ostium; R Right.

transport to gather in the sphenoethmoidal recess, where


they travel to the nasopharynx posteriorly to join the secretions from other sinuses.17 However, in mucous recirculation syndrome, mucous returns to a sinus via an
accessory ostium or iatrogenically misplaced antrostomy
(Figure 3).8-16 At least 5 pathways have been described
(Table 3).
In the presence of mucous recirculation, impaired mucous clearance develops and seems to increase the risk of
recurrent sinusitis. This may result from the repeated presentation of bacteria and viruses contained in the mucous
within the respective sinuses.9

Differentiation from Nonallergic Rhinopathy Is


Difcult by Clinical Criteria Alone
The prevalence of mucous recirculation syndrome is unknown, although it is likely that it is underdiagnosed. One
reason is the difculty of distinguishing mucous recirculation syndrome from nonallergic rhinopathy. As demonstrated in our study, nonallergic rhinopathy and mucous
recirculation present with similar clinical symptoms such as
postnasal 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

Patel et al
Table 2

The Mucous Recirculation Syndrome

589

Reported Mechanisms of Recirculation Studies of Mucous Recirculation

Study Cohort
Kane10,*
This study
Chung et al11
Coleman &
Duncavage12
Total

No. of
Patients

Maxillary
Ostium to
Middle Meatal
Antrostomy

Middle Meatal
Antrostomy to
Inferior Meatal
Antrostomy

31
12
7
6

17
6
0
0

12
1
0
6

56

23

19

Sphenoid Sinus
Ostium and
Sphenoidotomy

Perforated
Uncinate
Process

Maxillary Ostium
and Iatrogenic
Maxillary Ostium

4
3
7
0

0
1
0
0

1
0
0
0

0
1
0
0

14

Maxillary Ostium
or Antrostomy to
Accessory Ostium

*Three patients had bilateral recirculation.

mucous recirculation syndrome appear to have a similar


ratio.3,18,19 Nonallergic rhinopathy has been thought to be
more prevalent in adults between 30 and 60 years of age.19
Our data show similar age ndings with an average age of
53 years. However, patients with mucous recirculation
syndrome have a broad age range and include younger patients, whereas nonallergic rhinopathy typically occurs in
older patients.

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: symptoms of chronic rhinosinusitis that are refractory to oral or topical treatment;
visualization of mucous recirculation between 2 or more
ostia by rhinoscopy; and resolution of symptoms with
surgical treatment. The latter criterion is important for
clinical studies, as we do not know whether it is possible
to have mucous recirculation without symptoms. Two
studies suggest that it is unlikely.20,21 If that suggestion
can be conrmed, the third challenging criterion can be
deleted. Obviously, the development of 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.
The terms idiopathic, nonallergic, or vasomotor rhinitis
were not incorporated into the proposed criteria. Further
study may determine that one of these terms reects more
patients with mucous recirculation than another; that mucous recirculation may occur in some patients with allergic

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). AE
anterior ethmoid sinus; FS frontal sinus; MO maxillary
ostium; PE posterior ethmoid sinus; SS sphenoid sinus.
Adapted from Stammberger.17

Figure 3 Diagram of right lateral nasal wall showing reported pathways of mucous recirculation. IMA and MMA in
this diagram are misplaced antrostomies. AO accessory
ostium; IMA inferior metal antrostomy; MMA middle
meatal antrostomy; MO maxillary sinus ostium; SS
sphenoid sinus. Adapted from Kane.10

Diagnostic Criteria

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The American Journal of Medicine, Vol 127, No 7, July 2014

Table 3 Five Mucous Recirculation Pathways, Identied in


56 Patients Referred for Revision of Sinus Surgery
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%)

rhinitis; or that mucous recirculation can occur 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 syndrome in the differential diagnosis.

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 efcacious for nonallergic
rhinopathy, these treatments are unlikely to disrupt mucous
recirculation.21,22 Thus, failure of medical therapy should
raise suspicion for mucous recirculation.
Nasal endoscopy enables direct visualization and conrmation of a ring of 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, 5).13 Although

Figure 4 Recirculation of thin mucous (white dashed arrow)


between natural maxillary sinus ostium (MO) and a misplaced
middle maxillary meatal antrostomy (MMA).

Figure 5 Recirculation of thick purulent mucous with


microbubbles (white dashed arrow) between natural maxillary
(MO) and a misplaced middle meatal antrostomy (MMA).

mucous recirculation can be visualized as a ring structure on coronal computed tomography (CT), the specicity, and sensitivity of CT scans in the diagnosis of
mucous recirculation is unclear.11 Mucosal swelling and
the uctuating 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. Estimates of their prevalence range from 4%
to 41%.9,14 Accessory ostia are more commonly found in
the posterior and anterior fontanelle along the lateral nasal
wall. The lateral wall has 2 areas of weakness where it
consists of mucosa only, and this facilitates the development
of anterior and posterior fontanelle defects.20 Some have
argued that accessory ostia are the consequence of chronic
rhinosinusitis.20,21 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 identied.
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 behind the natural ostium anteriorly, they
may be an iatrogenic cause for mucous recirculation
(Figures 4, 5). Patients with ongoing symptoms of
rhinosinusitis despite sinus surgery require further evaluation
to determine if mucous recirculation is occurring. Mucous
recirculation may be terminated by removal of the tissue
separating the 2 ostia to make one large ostium.9,10,13,15

CONCLUSIONS
These data clearly establish mucous recirculation syndrome
as a cause for chronic rhinosinusitis. Further studies to
determine the prevalence of this syndrome are required.

Patel et al

The Mucous Recirculation Syndrome

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, 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, endoscopic sinus surgery considered to terminate recirculation and associated
symptoms. Moreover, a rm diagnosis of nonallergic rhinopathy should probably not be made without exclusion of
this syndrome.

ACKNOWLEDGEMENT
The authors 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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