The Anatomic Variations of the Nose and Paranasal Sinuses and Their Effect on Chronic Rhinosinusitis in Adult Patients

Abstract

To find out the anatomic variations of nose/paranasal sinuses and how they affect the sinuses in chronic rhinosinusitis (CRS). This observational cross-sectional study included adults with CRS, refractory to optimum medical management, planned for functional endoscopic sinus surgery (FESS). Pre-operative naso-endoscopy and computed tomography (CT) were utilized to estimate the extent of CRS, and to note the anatomic variations of the sinuses. The findings were corroborated within the practical scope of FESS. The anatomic variations were evaluated to establish how they affected the related sinus(es). Most of the 53 patients were young adults presenting with nasal obstruction (77%), discharge (76%) and headache (68%). On diagnostic naso-endoscopy, prominent agger bulge (83% of the nasal sides), prominent uncinate (18%), inferior turbinate hypertrophy (34%), concha bullosa (38%), mucopus and polyp in the middle meatus (51%, 19%; respectively), and gross septal deviation (55%) were noted. The spheno-ethmoid and frontal recesses were predominantly unremarkable. CT revealed inferior turbinate hypertrophy (38% of the nasal sides), agger (100%), and lateralized/collapsed uncinate (8%). Ethmoids and maxillary sinuses were diseased in 50% and 65% respectively, with blocked ostiomeatal complex in 32% and prominent bulla in 48%. Frontal and sphenoid sinuses were least involved (10%, 2%; respectively). Enlarged agger caused maxillary sinusitis (87%), whereas anterior ethmoiditis resulted from enlarged agger (100%), bulla (89%) and frontal cells (51%). Identification of the anatomic variations of the nose/paranasal sinuses through CT and naso-endoscopy (diagnostic, per-operative) is crucial to understand the pattern, extent and severity of the involvement of sinuses in CRS.

Introduction

Chronic rhinosinusitis (CRS) affects at least 11% of the world’s population and is a major cause of concern in health and economic burden [1]. CRS is an inflammation of the mucosal lining of the nose and paranasal sinuses characterized by one or more of the following symptoms lasting for more than 12 weeks, like nasal congestion, rhinorrhea, sneezing and itching along with hyposmia, facial pain and headache and persistent inflammatory changes on imaging and endoscopy without complete resolution of symptoms. Recent advances in computed tomography (CT)-scan protocols and the widespread use of diagnostic naso-endoscopy have made the diagnosis of CRS simpler and universal. With the acceptance of imaging and endoscopic aids in diagnosis and classification of CRS and determining its severity and extent, the importance of anatomic variations of the key landmarks in the nose and paranasal sinuses as one of the primary etiologic factors for CRS are being increasingly realized. Given the fact that CRS is primarily a medical disease, the approach to CRS not responding to optimum medical management (antibiotics, topical and/or systemic steroids) is functional endoscopic sinus surgery (FESS). FESS aims at removing the obstruction of the drainage pathway, and thereby restoring the mucociliary function of the sinonasal mucosa. The endoscopic surgeon must have a detailed knowledge of the endoscopic anatomy of nose, especially of its lateral wall, and subsequently needs to identify the various anatomic variations of the endonasal landmarks, both during the imaging study, and at endoscopy before and during surgery. He/she further needs to realize the potential roles these anatomic variations play in the etiopathogenesis of CRS. For example, the importance of the ostiomeatal complex (OMC), and the uncinate process itself as the key anatomic landmarks in understanding the pathology of the sinus disease is based on the concept that obstruction of the OMC and the condition of the uncinate (prolapsed, edematous, its nature of attachment, etc.) perpetuate the sinus disease, and the severity of the sinus disease further occludes the OMC, initiating a vicious cycle of inflammation and infection. It is understandable that the given anatomic variations and the present diseased state of the sinus(es) might be interlinked through a cause-effect relationship which at a given point of time might not be linear. That is, the disease severity may fluctuate with time (like seasonal changes) for a constant anatomic variation, and there might be other factors as well modulating the severity and extent of the disease. Understanding the relationship of the anatomic variations and the diseased state of the sinuses, and its role in decision-making at FESS is indeed a complex task. But, irrespective of the humoral/mucosal factors responsible for sustaining the disease, it is equally an important challenge to establish the anatomic etiology of CRS. Keeping this in the primary focus, the present study attempts to find out the incidence of the anatomical variations of nose/paranasal sinuses in adult patients with CRS with the help of pre-operative (diagnostic) nasal endoscopy, CT scan and per-operative endoscopy (FESS), and also to determine, where possible, how these variations affected the extent and severity of the involvement of the sinuses in CRS.

Materials and Methods

This observational cross-sectional study was conducted in the department of Otorhinolaryngology and Head-Neck Surgery in Medical College and Hospital, Kolkata, India, during January 2017 to June 2018. The clinical diagnosis of CRS in adult patients (age > 18 years) was made following the European Position Paper on Rhinosinusitis and Polyps (EPOS) criteria 2012 [2]. Both CRSwNP and CRSsNP variants (w = with; s = sans; NP = nasal polyposis) were included in the present study, provided their respective diagnostic criteria were maintained even after optimum medical management, thus making them candidates for surgery. Based on the EPOS 2012 guidelines, the optimum medical management followed in the present institute for CRSwNP included three weeks of systemic steroids (oral prednisolone; 1 mg/kg body weight); oral antibiotics (co-amoxiclav; with amoxycillin 40 mg/kg body weight in three divided doses, for two weeks); and intranasal steroid spray (fluticasone propionate; two puffs in each/affected nose in the morning for one month). Similar regimen, sans the systemic steroid, was followed for CRSsNP.

Pediatric age-group (< 18 years), comorbidities like diabetes mellitus, hypertension and immunocompromization, mucosal and auto-immune disorders (atrophic rhinitis, allergic rhinitis, granulomatous disorders, systemic vasculitis), patients with previous history of sinus surgery, fungal rhinosinusitis, neoplastic lesions, and congenital disorders like cystic fibrosis and primary ciliary dyskinesia were excluded from the study.

Selected patients were prepared for surgery. A further, detailed history on admission was obtained which included their socio-demographic data. Findings from pre-operative naso-endoscopy (4 mm 0º endoscope; Karl Storz SE & Co. KG; Tuttlingen, Germany) and CT scan of the nose/paranasal sinuses were evaluated for estimating the severity and extent of the disease, and to note the related anatomic variations, if any. The CT images (GE Healthcare, Boston, Massachusetts, USA) were of 1 mm slices, and were reconstructed from the primary axial cuts into the coronal and parasagittal views, in bone windows. They were extensively studied through the DICOM software (Digital Imaging and Communications in Medicine; National Electrical Manufacturers Association; Arlington, Virginia, USA) in serial sections in each respective cut. Additional information on anatomic variations and extent of the disease were obtained from per-operative findings during FESS, and were duly noted irrespective of the variations of CRS, i.e., CRSw/sNP. Surgeries were conducted with 0º and 70º 4 mm endoscopes (Karl Storz SE & Co. KG; Tuttlingen, Germany), using a three-chip camera with high-definition monitor system (Stryker EndoVision; Kalamazoo, Michigan, USA).

The final grand chart was prepared compiling multiple tabulation sheets using Windows Excel software (Microsoft Corporation; Redmond, Washington, USA). Data entered were analyzed and presented in tabular and pictorial forms through relevant statistical methods (proportions, percentages, etc.) using SPSS (Statistical Package for Social Sciences) software version 22 (IBM Corporation; Armonk, New York, USA). P values < 0.05 were considered statistically significant, where applicable.

The study was approved by the Institutional Ethical Committee (Reference No. MC/Kol/IEC/Non-spon/385/11-2016; dated: November 19, 2016). Informed consent in writing was obtained from each patient prior to his/her inclusion in the study. Investigations and interventions were strictly according to the principles stated in the declaration of Helsinki 1964 and its subsequent amendments.

A level of evidence of 2b has been assigned to this study, following guidelines provided by the Oxford Centre of Evidence-based Medicine [3].

Results

The age-range of the 53 patients included was 15–65 years; most patients belonged to the 16–30 years age-group [Table 1]. There was no sex predilection (27 women; 26 men; female:male = 1.06). Most patients belonged to the urban areas (28%). Thirty-two patients had seasonal variations; 19 of them (~ 36%) had symptoms more during winter and 12 (~ 23%) during the rainy season [Table 2]. Serum IgE was raised above the normal level in 26 patients (49%) [Table 3].

Table 1.

Age-specific distribution of the chronic rhinosinusitis patients

Age (years)	Frequency	Percentage
16–30	27	51%
31–50	20	38%
51–64	6	11%
Total (n)	53	100%

Table 2.

Distribution of chronic rhinosinusitis according to seasonal variation

Seasonal variation		Frequency	Percentage
	Rainy	12	22.64%
YES	Winter	19	35.85%
	Summer	1	1.89%
NO		21	39.62%
Total (n)		53	100%

Table 3.

Level of IgE in chronic rhinosinusitis patients

Serum IgE levels (IU/mL)	Frequency	Percentage
Normal	27	51%
180–1000	14	26%
1001–2000	10	19%
> 2001	2	4%
Total (n)	53	100%

Serum IgE: 10– 179 IU/mL (Harrison's Manual of Medicine, 17th Edition)

Most patients presented clinically with nasal obstruction (~ 77%), nasal discharge (~ 76%) and headache (~ 68%) [Table 4]. On diagnostic naso-endoscopy, the anatomic variations of the internal nasal structures were enumerated and assessed in 106 nasal sides in 53 patients. Agger nasi bulge was prominent in 83% of the nasal sides, prominent uncinate process in 18%, inferior turbinate hypertrophy in 34%, pneumatized middle turbinate (concha bullosa) in 38%, single accessory maxillary sinus ostium in 98%, and an unremarkable spheno-ethmoid and frontal recess in 99% and 92%, respectively. Mucopus in the middle meatus was present in 51% of the nasal side, with evident polyp in only 19%. Gross septal deviation was noted in 55% patients. Detailed findings of the pre-intervention naso-endoscopy are summarized in Table 5. The patients were subjected to CT of the nose and paranasal sinuses. Inferior turbinate hypertrophy was present in 38% of the sides. Agger nasi had universal presence. The uncinate process was normal in 92% sides, and lateralized/collapsed in 8%. Maxillary sinuses were diseased in 65% of the sides, with the OMC blocked in 32%. Ethmoids were involved in 50% sides, with prominent bulla on 48%. The frontal sinus was normal in 90% of the sides. Details of the CT imaging have been summarized in Table 6. Radiologic and endoscopic evaluations were used to diagnose the extent of sinus involvement in CRS, and the anatomic variations as evident primarily from the radiologic evaluation were assessed to discuss their role in sinus disease process. The details have been presented in Table 7. It could be seen that the maxillary sinus was involved the most, followed by anterior and posterior ethmoids, frontal sinus and sphenoid sinus, in order. Enlarged agger bulge was deemed one of the main reasons (~ 87%) that resulted in maxillary sinusitis by causing obstruction of the OMC. In > 89% of the nasal sides, enlarged bulla ethmoidalis appeared responsible for anterior ethmoiditis. Although enlarged agger nasi and frontal cells were not in direct anatomic relation with the anterior ethmoid cells, they often resulted in obstruction of the OMC that indirectly led to anterior ethmoiditis. Thus, enlarged agger nasi was responsible for anterior ethmoiditis in 100% of the sides, and frontal cells in ~ 51%. These two anatomic variations were found to be the primary cause in all cases of frontal sinusitis as they resulted in mechanical obstruction of the frontal recess/ostium. No anatomic variation could be definitely ascertained for posterior ethmoiditis and sphenoiditis.

Table 4.

Presenting symptoms of the patients with chronic rhinosinusitis (n = 53)

Symptoms	Frequency	Percentage
Nasal obstruction	41	77.36%
Nasal discharge	40	75.47%
Headache	36	67.92%
Facial pain	11	20.75%
Nasal bleeding	5	9.43%
Recurrent sneezing	3	5.66%

Table 5.

Details of the pre-intervention endoscopic findings in the CRS patients (n = 106; for deviated nasal septum, n = 53)

Pre-intervention endoscopic findings	Frequency	Percentage
Agger Nasi bulge
Well-pneumatized/prominent	88	83%
Not well-pneumatized/normal	18	17%
Deviated nasal septum
Towards right	29	55%
Towards left
No gross deviation	24	45%
Uncinate process
Prominent	19	18%
Recessed	0	0%
Normal	87	82%
Inferior turbinate
Hypertrophy	36	34%
Atrophy	0	0%
Normal	70	66%
Middle turbinate
Prominent/pneumatized	40	38%
Paradoxical	2	2%
Medialized	31	29%
Normal	33	31%
Bulla ethmoidalis
Prominent/large	50	47%
Rudimentary	0	0%
Normal	56	53%
Accessory maxillary ostium
0	2	2%
1	104	98%
> 1	0	0%
Polyp
Present	20	19%
Absent	86	81%
Sphenoethmoid recess
Mucopus	1	1%
Polyp/edema	0	0%
Normal	105	99%
Frontal recess
Mucopus	4	4%
Polyps/edema	5	5%
Normal	97	92%
Middle meatus discharge
Present	54	51%
Absent	52	49%

Table 6.

Details of the computed tomogram (CT) findings in chronic rhinosinusitis patients

CT findings	Frequency	Percentage
Deviated nasal septum
Present	29	55%
No gross deviation	24	45%
Inferior turbinate
Hypertrophy	38	36%
Atrophy	0	0%
Normal	68	64%
Maxillary sinus
Opacity/mucosal thickening/polypoid changes	69	65%
Normal	37	35%
Ethmoid sinus
Anterior ethmoid opacity	35	33%
Posterior ethmoid opacity	18	17%
Normal	53	50%
Frontal opacity
Opacity	11	10%
Normal	95	90%
Sphenoid opacity
Opacity	2	2%
Normal	104	98%
Ostiomeatal complex
Patent/normal	72	68%
Block	34	32%
Uncinate process
Lateralized	0	0%
Medialized/collapsed	8	8%
Pneumatized	0	0%
Normal	98	92%
Agger nasi prominence
Present	106	100%
Absent	0	0%
Large bulla ethmoidalis
Prominent	51	48%
Rudimentary	55	52%
Frontal cells
Type I	30	28%
Type II	3	3%
Type III	2	2%
Type IV	0	0%
Absent	71	67%
Concha bullosa
Lamellar	0	0%
Bulbar	42	40%
Complete	0	0%
Absent	64	60%
Onodi cells
Present	25	24%
Absent	81	76%
Paradoxical middle turbinate, turbinate sinus
Present	2	2%
Absent	0	0%
Haller cells
Present	1	1%
Absent	105	99%
Bone destruction
Present	0	0%
Absent	106	100%
Dehiscence/erosion
Lamina papyracea	0	0%
Skull base	0	0%
Sphenoid sinus	0	0%
Absent	106	100%
Crista gali pneumatization
Present	12	11%
Absent	94	89%

Table 7.

Association between the anatomic variations and chronic rhinosinusitis

Paranasal sinus disease (n)	Probable anatomic variations associated with CRS as identified on diagnostic naso-endoscopy, CT scan and FESS*		Frequency	Percentage
Maxillary sinusitis (79)	Large enough to cause obstruction to the OMC	Agger nasi	69	87.34%
		Concha bullosa	36	45.57%
		Haller cells	1	1.27%
		Collapsed uncinate process	8	10.13%
		Frontal cells	29	36.71%
		Bulla ethmoidalis	42	53.16%
Frontal sinusitis (32)	Large enough to cause obstruction to the frontal recess/ostium	Agger nasi	32	100%
		Frontal cells	32	100%
		Bulla ethmoidalis	19	59.38%
Anterior ethmoid sinusitis (57)	Large enough to cause obstruction to the OMC	Bulla ethmoidalis	51	89.47%
		Agger nasi**	57	100%
		Frontal cells**	29	50.88%
Posterior ethmoid sinusitis (35)		–	–	–
Sphenoid sinusitis (2)		–	–	–

CRS = chronic rhinosinusitis; OMC = ostiomeatal complex; FESS = functional endoscopic sinus surgery

^* = The anatomic variations were primarily identified on pre-intervention naso-endoscopy and CT scan, and were later corroborated on FESS within the limits and scope of the surgery. The principle of FESS was to perform minimal surgery as guided by diagnostic naso-endoscopy, CT and overall symptomatology

^* = these cells did not directly cause anterior ethmoiditis, but compromised the OMC so as to prevent anterior ethmoid drainage, resulting in ethmoiditis

Discussion

Stammberger had laid down the foundation of our understanding of the importance of the OMC in maintaining the physiology of the sinonasal mucociliary clearance. We now have the common understanding that as long as the contributing sinus passages are healthy, the OMC remains disease-free, and the mucociliary transport is not impaired [4]. Blockage of OMC results in sinusitis. Poor ventilation in the inflamed sinuses further aggravates mucociliary clearance, mucus stasis, super-added infection, resulting in further blockage and inflammation of the OMC. This vicious cycle is further aggravated by contribution of the anatomic variations of the internal architecture of the nose/paranasal sinuses, which are mostly the migrated ethmoid cells and structures contributing to the OMC.

In this study, all 53 patients with CRS had one or more of such anatomic variations as evident during endoscopy and on CT scan. Of the two, the final verdict was obtained from the CT images as they revealed internal anatomic details most accurately. In our series, the commonest anatomic variation was agger nasi, followed by bulla ethmoidalis and concha bullosa; the most common sinuses involved were maxillary, followed by anterior and posterior ethmoids, frontal, and the sphenoid. Involvement of agger as part of the disease process of the frontal recess and ethmoid infundibulum occurs more commonly than a true isolated agger pathology. Depending upon the anatomic configuration of the sinuses, there may be a connection between the agger nasi and the lateral sinus and consequently, disease may spread between these two areas [5]. In a similar study carried out in the Kathmandu University Hospital from January 2015 to January 2016, the commonest anatomic variation was found to be agger nasi, concha bullosa and significant deviated nasal septum, in that order [6]. In an interesting study by Kaya et al., at least one anatomic variation could be seen in 92.9% of the study population. Agger nasi was also found to be associated with a high rate of sinusitis [7]. In a similar study by Pérez-Piñas et al., anatomic variations in the nose and paranasal sinuses could be observed in 67% of the study population, of which, the agger and the asymmetry of the sphenoid sinus were the commonest [8].

Since bulla ethmoidalis occupies the central location and has multiple intimate anatomic relationships to other key areas of the anterior ethmoid sinus, a normally aerated albeit enlarged bulla may be the principal cause for OMC blockage and resultant maxillary sinusitis, especially when it grows downward extensively. In our study, it was the second most common anatomic variation affecting the anterior ethmoid and maxillary sinus. Studies conducted by Alosowey et al. observed that a large bulla could be detected in 10% of the study subjects, and concluded they can compromise the drainage pathway of the related sinuses, resulting in inflammatory sinus disease [9].

An extensive concha bullosa, the pneumatization of the middle turbinate, may result in OMC obstruction and can result in maxillary sinusitis. In our study, 40% of the nasal sides had large concha bullosa, and they were large enough to cause OMC blockage and resultant maxillary sinusitis in ~ 46% nasal sides. The figures were 51% and 67% respectively in the study by Kaya et al. [7]

In the present study, both CT scan and diagnostic naso-endoscopy were complimentary in identification of the anatomic variations in CRS. However, CT provided the more accurate observations because diagnostic naso-endoscopy has its limitations in not being able to read the posterior group of air cells and the frontal recess/sinus, and the per-operative findings are generally limited to these areas where surgery is actually indicated depending upon the extent of the disease as determined by imaging, pre-operative endoscopy and symptomatology. Opinions, however, might differ. Maru et al. observed that diagnostic naso-endoscopy was a better option than CT scan to detect various sinonasal pathologies as well as anatomical variations [10]. On the other hand, Duarte et al. showed that naso-endoscopic findings were more conclusive in diagnosing anatomic variations of the paranasal sinuses and their diseased state compared to CT [11]. The Lund-Mackay score attempts to correlate the two through a point-based system [12]. However, the study by Hasan et al. showed a weak negative correlation between the Lund-Mackay score and the number of anatomical variations [13]. According to Rathor et al., the relationship between CT scan with symptom severity is not reliable. As CT is the imaging modality of choice for evaluation of CRS, use of the Kennedy staging may be advisable to endoscopic surgeons as it provides insight into the pathophysiology and treatment, and helps to predict outcomes of therapy [14].

The present study has several limitations. The sample size needs to be increased to statistically strengthen the outcome. However, there is a definite trend revealed in this study that can be extrapolated to larger, sample-heavy researches in the future. Moreover, there is lack of statistical association in terms of correlation and cause-effect relationship among the endoscopic, imaging and per-operative findings regarding the anatomic variations of the nose and paranasal sinuses; this aspect has not been discussed upon in this study. However, one of the strengths of this study design is that, apart from looking for the anatomic variations, it explores the various forms of CRS in terms of involvement of paranasal sinuses and associate them with the anatomic variation(s) that could be responsible for the infection.

Conclusion

From the present study it can be concluded that diagnostic naso-endoscopy and CT scan of nose and paranasal sinuses have improved the visualization of the regional anatomy and have allowed greater accuracy in evaluating CRS. Both the modalities are valuable for determining the anatomic variations, along with the per-operative endoscopic findings. Imaging, however, is of especial help as it can access all the paranasal sinuses and their variations irrespective of whether they need to be operated upon or accessible at diagnostic endoscopy. These anatomic variations play a major role in determining the severity and extent of the sinus involvement in CRS, and are vital clues for the endoscopic surgeons to re-establish the sinus physiology during FESS.

Funding

None.

Compliance with ethical standards

Conflict of interest

None.