- Email: [email protected]
Prevalence of tympanometric alterations in children with chronic sinusitis
International Journal of Pediatric Otorhinolaryngology (2008) 72, 315—319
www.elsevier.com/locate/ijporl
Prevalence of tympanometric alterations in children with chronic sinusitis Gualtiero Leo a,*, Elena Piacentini a, Cristoforo Incorvaia b, Dario Consonni c, Alessandro Cazzavillan d a
Pediatric Allergy and Respiratory Pathophysiology Unit, Istituti Clinici di Perfezionamento, Via Castelvetro 32, 20154 Milan, Italy b Allergy/Pulmonary Rehabilitation, Istituti Clinici di Perfezionamento, Milan, Italy c Unit of Epidemiology, Fondazione IRCCS Ospedale Maggiore Policlinico, Mangiagalli and Regina Elena, Milan, Italy d Department of Pediatric Otorhinolaryngology, Buzzi Children Hospital, Istituti Clinici di Perfezionamento, Milan, Italy Received 27 October 2006; received in revised form 26 October 2007; accepted 26 October 2007 Available online 19 December 2007
KEYWORDS Sinusitis; Middle ear dysfunction; Tympanogram; Atopy
Summary Objective: Due to its anatomical and functional connections, middle ear disorders frequently occur in sinusitis. Its prevalence, however, is likely to be underestimated. We evaluated the prevalence of middle ear dysfunction, as assessed by tympanometry, in children with chronic sinusitis in a large group of patients with chronic respiratory symptoms, and its possible relationship with respiratory allergy. Methods: From a population of 1810 children with respiratory symptoms referred to our Pediatric Allergy center, subjects with chronic sinusitis diagnosed by clinical criteria were selected. Children underwent testing of middle ear function by tympanometry and of allergy by skin tests with environmental allergens. Patients were divided into three groups according to age. Results: Two hundred and eighty-eight children (15.9%) had clinical diagnosis of chronic sinusitis according to the established criteria. Twenty-four patients were in group 1, 220 in group 2, and 44 in group 3. Altered middle ear pressure was found in 76.4% of patients, with a significantly higher rate of altered tympanograms in younger children ( p < 0.001). A positive skin prick test was found in 29.9% of children, with a significantly higher rate of positivity in older children ( p = 0.01). Conclusions: The decrease with age in the rate of tympanometric alterations is likely to be associated to the anatomic development of the upper airways, while the presence of atopy does not seem to play a role in their occurrence. # 2007 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: +39 02 57995156; fax: +39 02 57995741. E-mail address: [email protected] (G. Leo). 0165-5876/$ — see front matter # 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2007.10.018
316
1. Introduction Intermittent and persistent rhinitis, as defined by the occurrence of nasal symptoms such as sneezing, discharge and blockage for less or more than 4 weeks, respectively [1], is a very common condition in children. Allergies are frequently implicated as a cause of rhinitis [2,3]. Due to the anatomical contiguity of the paranasal sinuses with the nose, it has been suggested that the term rhinosinusitis should be used instead of sinusitis [4]. The middle ear has anatomical and functional connections with the nasopharynx through the Eustachian tube and the pathophysiology of its disorders is considered similar to that of sinusitis [5]. Inflammation of the nasal mucosa may lead to obstruction of the sinuses ostia and to Eustachian tube dysfunction which results in impairment of the middle ear pressure and in fluid exudation with the clinical picture of otitis media with effusion (OME), which is defined as ‘‘the presence of fluid in the middle ear without signs or symptoms of acute ear infections’’ [6]. The prevalence of OME in children has been estimated in the last three decades in a wide range from 15% to 80% [7—10]. According to a number of studies the presence of sinusitis in children with OME ranges from 48% to 62% [11—13], and concerning the role of allergy some Authors reported that from 23% to 90% of children with OME had hypersensitivity to inhalant allergens [14—17], a range too large to help in clinical practice. We sought to evaluate in children with chronic sinusitis, diagnosed by clinical criteria from a large group of patients with chronic respiratory symptoms, the prevalence of middle ear dysfunction, as assessed by tympanometry, and the prevalence of respiratory allergies.
2. Methods 2.1. Patients Between 2001 and 2004, 1810 children with respiratory symptoms referred to our Pediatric Allergy center. Children underwent a medical examination aimed at detecting the involvement of paranasal sinuses and middle ear. The presence of chronic sinusitis was assessed by the criteria of Shapiro and Rachelefsky [18], considering the presence of at least two of the three major criteria — purulent nasal discharge, purulent pharyngeal drainage, and cough — for a period of at least 12 weeks. As suggested by the Position paper of the European Academy of Allergology and Clinical Immunology [4], the mucopurulent discharge, as well as oedema
G. Leo et al. or obstruction of the middle meatus, was assessed by endoscopy–—performed by a ENT specialist. The presence of middle ear tube dysfunction was assessed by performing tympanometry. In addition, allergy testing was done by skin tests with common inhalant allergens and, in children younger than 3 years of age, with common food allergens. Exclusion criteria were: odontogenic causes of sinusitis, malformations of ear and palate, Down syndrome, nasal polyposis, metabolic diseases, previous surgical interventions of nose, ear and throat, history of chronic ear infections, as assessed by diagnosis of ENT specialists, and family history of hear loss. None of the children were receiving medications for at least the 2 weeks prior to the examination. Patients were divided in three groups according to their age: group 1 comprised children aged less than 3 years, group 2 between 3 and 6 years, and group 3 more than 6 years. Evaluation was performed within groups. The study was approved by the institutional board and oral consent was obtained by the parents.
2.2. Endoscopy Nasopharyngeal endoscopy were performed by fiberoptic flexible nasopharyngoscope Storz 11101 SK of 2.5 mm of diameter (Karl Storz GmbH & Co. KG D, Tuttlinghen, Germany); in all cases endoscopic evaluation included nasal turbinates and middle meatus, and the rhinopharynx to evaluate adenoid and Eustachian tube orifice.
2.3. Tympanometry Tympanometry was performed by a middle ear analyzer (Impedance Audiometer AZ 26, Interacoustics A/S, Assens, Denmark). Results were analysed by standard criteria [19]. The tympanogram was classified as type A (normal) when the pressure in the middle ear was higher than 100 daPa, as type B when no peak was detectable on the graphic, and as type C when the pressure ranged from 100 to 200 daPa (C1) and from 200 to 300 daPa (C2). Tympanograms of type B and C were considered abnormal.
2.4. Skin tests Skin prick tests (SPT) were performed according to guidelines from the European Academy of Allergology and Clinical Immunology [20] using standardized extracts (Stallerge ´nes, Antony, France) of the common aeroallergens (grasses, Parietaria, ragweed, Artemisia, olive, birch, alder, Dermatophagoides
Tympanometric alterations in chronic sinusitis pteronyssinus and farinae, Alternaria, Aspergillus, cat and dog epithelia). Children younger than 3 years also underwent food allergen testing using food extracts, namely cow milk, hen’s egg, fish, wheat, and peanut. A 10 mg/ml solution of histamine dihydrochloride served as positive control and a saline solution as negative control. A positive SPT was defined by the appearance of a wheal with an area larger than 7 mm2 with no reaction to negative control.
317
Fig. 1 Altered middle ear pressure and age. TPM: tympanometry.
2.5. Statistical analysis Tables of frequencies were analyzed using the x2test. Data management and statistical analyses were performed using the software Stata (Statacorp, College Station, TX, USA).
3. Results Out of the 1810 children with respiratory symptoms, 288 (15.9%) had a clinical diagnosis of chronic sinusitis according to the inclusion criteria. There were 173 males and 115 females, with a mean age of 5.1 2.0 years, range 1.9—14.0 years. Groups consisted as follows: group 1, 24 children; group 2, 220 children and group 3, 44 children. Altered pressure of middle ear was found in 220 of the 288 subjects (76.4%), in 78.3% of the females and in 75.1% of the males. Forty-six (16.0%) had a type C tympanogram (mono or bilateral), and 174 (60.4%) had a type B tympanogram, in which 56 abnormalities were monolateral (19.4%), and 118 were bilateral (41%). The prevalence of altered tympanograms was significantly higher among the younger children (Fig. 1). A positive reaction to SPTwas found in 86 children (29.9%), with a prevalence of positivity significantly different among age groups ( p = 0.01). The children aged less than 3 years had a prevalence of atopy of 4.2%, while in children aged between 3 and 6 years it was 31.8%, and it was 34.1% for those aged more than 6 years. Fifty-six subjects (19.4%) were sensitized to only one allergen, while 30 (10.4%) were sensitized to two or more. The most frequently found allergens
Fig. 2
Altered middle ear pressure and allergy.
were pollens (20.1%), house dust mites (12.5%), molds (5.2%), and animal epithelia (4.5%). Altered pressure of middle ear was found in 69.8% of allergic (60 subjects) and in 79.2% (160 subjects) of nonallergic children; this difference being not significant. In atopics, there were 26.7% of type C tympanogram subjects and 43% of type B subjects; in nonatopic, there were 11.4% of type C tympanogram subjects and 67.8% of type B subjects. The amount of type C and B tympanogram was significantly higher ( p < 0.001) in nonatopics than in atopics (Fig. 2). According to number of sensitizations, tympanometric dysfunction was present in 67.9% of monosensitized and in 73.3% of polysensitized children, with a not significant difference. Table 1 reports the rates of altered tympanograms according to the presence/absence of atopy among the three age groups, which were not significantly different of each other. According to the kind of sensitization, altered pressure of the middle ear was found in 81.2% of children monosensitized to house dust mites (with a type C tympanogram in 43.7% and a type B in 37.5%)
Table 1 Altered tympanogram in atopic and nonatopic children Group
Altered tympanogram
p
Atopics (%)
Nonatopics (%)
1. <3 year (24 children) 2. 3—6 year (220 children) 3. >6 year (44 children)
1/1 (100%) 52/70 (74.3%) 7/15 (46.7%)
20/23 (87.0%) 123/150 (82.0%) 17/29 (58.6%)
0.69 0.18 0.45
318
Fig. 3 year.
G. Leo et al.
Type of tympanogram in different periods of the
and in 63.6% of children monosensitized to pollen (with a type C tympanogram in 18.2% and type B in 45.4%). Regarding seasonal variations in the kind of tympanograms, there was a significantly higher rate of altered tympanograms ( p = 0.02) during cold months (Fig. 3).
4. Discussion The nose is anatomically and functionally related to the paranasal sinuses and middle ear, and this relationship clearly accounts for the association of rhinitis with sinusitis and pathologies such as OME [4—15]. It is not fully understood why only some subjects with rhinitis develop such disorders, but anatomical characteristics influencing the draining of the sinuses and the patency of the Eustachian tube are likely to play a pivotal role. This seems particularly important in children, whose rhino-sinusal anatomy experiences modifications as they grow up. Mills performed sinus radiographs in 240 children with OME and found abnormalities in 28% of cases, though only in 7% an infection was confirmed by a sinus lavage [21]. The same authors argued that radiograph — which currently is no longer considered a reliable diagnostic tool in the diagnosis of sinusitis [4] — may underestimate sinusitis. On the other hand, Fujita reported in a population of subjects aged 10—20 years with OME resistant to medical treatment that in 49% of cases radiology detected sinusitis, while in children aged 4—9 years the rate of radiologic abnormalities was 78% [22]. In adults, OME may be the presenting symptom of chronic sinusitis, as demonstrated by an endoscopic study which reported that in 23% of subjects with sinus disease — mainly of the ethmoid system — there was evidence of otitis media [23]. Lazo-Sa ´enz et al. extended the investigation to the role of allergy, by evaluating a group of 57 children aged less than 11 years and found that in
a group of 40 children with allergic rhinitis Eustachian tube dysfunction, as demonstrated by a tympanogram of C or B type, was present in 15.5% of subjects, while no subject of the control group had altered tympanogram [24]. Duration of allergic rhinitis and seasonal or perennial presentation did not show different associations with the middle ear pathology, and led the authors to conclude that just the presence of allergic rhinitis is a risk factor for Eustachian tube dysfunction in children. This study confirmed previous observations about allergy and otitis media, in which allergy was detected by means of skin tests, in vitro IgE tests, and assessment of inflammatory cells and cytokine profiles [25—28]. We designed the present study to evaluate the prevalence of middle ear alterations in children with sinusitis diagnosed by generally accepted clinical criteria [4,18]. To do this, all children underwent to tympanogram, which is a validated technique to detect middle ear effusion by measuring altered pressure, as demonstrated by comparison with magnetic resonance imaging [29]. Results demonstrate that Eustachian tube dysfunction is very common in children with chronic sinusitis but that this pathology significantly decreases its frequency with age, showing a rate of 87.5% in children aged less than 3 years, of 79.6% in those from 3 to 6 years, and of 54.5% in those aged more than 6 years, respectively. As suggested before, the anatomic development of the upper airway associated with growth and favouring a correct drainage of mucosal secretion and a normal ventilation of the middle ear can probably explain this change. Of note, in clinically healthy children the prevalence of tympanometric alterations indicating OME is low, with values of 3% in first grade and of 1.5% in second grade primary school students, respectively [30]. We looked for a possible role of allergy in inducing middle ear dysfunction by performing SPT with common environmental allergens. The prevalence of altered tympanograms, however, was not significantly different in nonatopic and atopic subjects. In addition, no difference could be observed between monosensitised and plurisensitised subjects. The significantly higher rate of altered tympanograms during winter is likely to be due to the more frequent upper airway inflammatory disorders in such period, and seems to play down the role of seasonal allergies such as grass, tree, or Parietaria pollenosis. Previous reports on this issue are discordant. The incidence of allergy in OME has been reported to range from 5% to 80%, as reviewed by Bernstein in 1996 [26], but more recent surveys indicate that the prevalence of allergy in OME does not seem to be higher than among the general population [17,27]. In particular, in the most recent study
Tympanometric alterations in chronic sinusitis the prevalence of allergic rhinitis was 28% in children with OME and 24% in controls [17]. Other pathologies such as infectious rhinitis or common cold are important in causing OME, but were not considered in our study which included only children with chronic sinusitis, i.e. present for at least 12 weeks. The cause of sinus inflammation in nonallergic children remains to be determined, possibly requiring the study of inflammatory cells and cytokine profiles obtained from mucosal samples.
319
[14]
[15]
[16]
[17]
References [18] [1] J. Bousquet, P. van Cauwenberge, N. Khaltaev (Eds.), Allergic rhinitis and its impact on asthma, J. Allergy Clin. Immunol. 108 (2001) S147—S334. [2] The International Study of Asthma and Allergies in Childhood (ISAAC), Steering Committee, Worldwide variations in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema, Lancet 351 (1998) 1225—1232. [3] C. Galassi, M. De Sario, A. Biggeri, L. Bisanti, E. Chellini, G. Ciccone, et al., Changes in prevalence of asthma and allergies among children and adolescents in Italy: 1994—2002, Pediatrics 117 (2006) 34—42. [4] W. Fokkens, V. Lund, C. Bachert, P. Clement, P. Hellings, M. Holmstrom, et al., EAACI position paper on rhinosinusitis and nasal polyps executive summary, Allergy 60 (2005) 583—601. [5] D.S. Parsons, E.R. Wald, Otitis media and sinusitis: similar diseases, Otolaryngol. Clin. North Am. 29 (1996) 11—25. [6] R.M. Rosenfeld, L. Culpepper, K.J. Doyle, K.M. Grundfast, A. Hoberman, M.A. Kenna, et al., Clinical practice guidelines: otitis media with effusion, Otolaryngol. Head Neck Surg. 130 (2004) S95—S118. [7] C.H. Sorensen, S.H. Jensen, M. Tos, The post-winter prevalence of middle-ear effusion in four-year-old children, judged by tympanometry, Int. J. Pediatr. Otorhinolaryngol. 3 (1981) 119—128. [8] G.A. Zielhuis, G.H. Rach, A.V. van den Bosch, P.V. van den Broek, The prevalence of otitis media with effusion: a critical review of the literature, Clin. Otolaryngol. Allied Sci. 15 (1990) 283—288. [9] J.L. Paradise, H.E. Rockette, D.K. Colborn, B.S. Bernard, C.G. Smith, M. Kurs-Lasky, et al., Otitis media in 2253 Pittsburgh area infants: prevalence and risk factors during the first two years of life, Pediatrics 99 (1997) 318—333. [10] D. Umapathy, A. Roshini, G.K. Scadding, A community based questionnaire study on the association between symptoms suggestive of otitis media with effusion, rhinitis and asthma in primary school children, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 705—712. [11] T.C. Hoshaw, N.J. Nickman, Sinusitis and otitis in children, Arch. Otolaryngol. 100 (1974) 194—195. [12] J.J. Grote, W. Kuijpers, Middle ear effusion and sinusitis, J. Laryngol. Otol. 94 (1980) 177—183. [13] A. Fujita, I. Honjo, K. Kurata, I. Gan, H. Takahashi, Refractory otitis media with effusion from viewpoints of eustachian tube
[19]
[20]
[21]
[22]
[23]
[24]
[25] [26]
[27]
[28]
[29]
[30]
dysfunction and nasal sinusitis, Am. J. Otolaryngol. 14 (1993) 187—190. B.M. Baker, C.D. Baker, H.T. Le, Vocal quality, articulation and audiological characteristics of children and young adults with diagnosed allergies, Ann. Otol. Rhinol. Laryngol. 91 (1982) 277—280. J.E. Gamble, J.A. Bizal, E.P. Daetwyler, Otitis media and chronic middle ear effusion in the asthmatic pediatric patient, Ear Nose Throat J. 71 (1992) 397—399. J.P. Corey, R.E. Adham, A.H. Abbass, I. Seligman, The role of IgE-mediated hypersensitivity in otitis media with effusion, Am. J. Otolaryngol. 15 (1994) 138—144. S.G. Yeo, D.C. Park, Y.G. Eun, C.I. Che, The role of allergic rhinitis in the development of otitis media with effusion: effect on Eustachian tube function, Am. J. Otolaryngol. 28 (2007) 148—152. G.G. Shapiro, G.S. Rachelesfky, Introduction and definition of sinusitis, J. Allergy Clin. Immunol. 90 (1992) 417—418. T. Finitzo, S. Friel-Patti, K. Chinn, O. Brown, Tympanometry and otoscopy prior to myringotomy: issues in diagnosis of otitis media, Int. J. Pediatr. Otorhinolaryngol. 24 (1992) 101—110. S. Dreborg (Ed.), Skin tests used in type I allergy testing. Position paper of the European Academy of Allergology and Clinical Immunology, Allergy 44 (suppl 10) 1989. R.P. Mills, B.S. Irani, R.J. Vaughan-Jones, N.D. Padgham, Maxillary sinusitis in children with otitis media with effusion, J. Laryngol. Otol. 108 (1994) 842—844. A. Fujita, I. Honjo, K. Kurata, I. Gan, H. Takahashi, Refractory otitis media with effusion from viewpoints of Eustachian tube dysfunction and nasal sinusitis, Am. J. Otolaryngol. 14 (1993) 187—190. Y. Finkelstein, Y.P. Talmi, Y. Rubel, J. Bar-Ziv, Y. Zohar, Otitis media with effusion as a presenting symptom of chronic sinusitis, J. Laryngol. Otol. 103 (1989) 827—832. J.G. Lazo-Sa ´enz, A.A. Galvan-Aguilera, V.A. Martines-Ordaz, V.M. Velasco-Rodriguez, A. Nieves-Renteria, C. Rincon-Castaneda, Eustachian tube dysfunction in allergic rhinitis, Otolaryngol. Head Neck Surg. 132 (2005) 626—631. P. Fireman, Otitis media and nasal disease: a role for allergy, J. Allergy Clin. Immunol. 82 (1988) 917—924. J.M. Bernstein, The role of IgE-mediated hypersensitivity in the development of otitis media with effusion: a review, Otolaryngol. Head Neck Surg. 109 (1993) 611—620. L.H. Nguyen, J.J. Manoukian, S.E. Sobol, T.L. Tewfik, B.D. Mazer, M.D. Schloss, et al., Similar allergic inflammation in the middle ear and the upper airways: evidence linking otitis media with effusion to the united airway concept, J. Allergy Clin. Immunol. 114 (2004) 1110—1115. C. Caffarelli, E. Savini, G. Giordano, G. Gianlupi, G. Cavagni, Atopy in children with otitis media with effusion, Clin. Exp. Allergy 28 (1998) 591—596. C.M. Alper, D.L. Sabo, W. Doyle, Validation by magnetic resonance imaging of tympanometry for diagnosing middle ear effusion, Otolaryngol. Head Neck Surg. 121 (1999) 523— 527. E. Keles, I. Kaygusuz, T. Karlidag, S. Yalc¸in, Y. Ac¸ik, H.C. Alpay, et al., Prevalence of otitis media with effusion in first and second grade primary school students and its correlation with BCG vaccination, Int. J. Pediatr. Otorhinolaryngol. 68 (2004) 1069—1074.
Available online at www.sciencedirect.com
www.elsevier.com/locate/ijporl
Prevalence of tympanometric alterations in children with chronic sinusitis Gualtiero Leo a,*, Elena Piacentini a, Cristoforo Incorvaia b, Dario Consonni c, Alessandro Cazzavillan d a
Pediatric Allergy and Respiratory Pathophysiology Unit, Istituti Clinici di Perfezionamento, Via Castelvetro 32, 20154 Milan, Italy b Allergy/Pulmonary Rehabilitation, Istituti Clinici di Perfezionamento, Milan, Italy c Unit of Epidemiology, Fondazione IRCCS Ospedale Maggiore Policlinico, Mangiagalli and Regina Elena, Milan, Italy d Department of Pediatric Otorhinolaryngology, Buzzi Children Hospital, Istituti Clinici di Perfezionamento, Milan, Italy Received 27 October 2006; received in revised form 26 October 2007; accepted 26 October 2007 Available online 19 December 2007
KEYWORDS Sinusitis; Middle ear dysfunction; Tympanogram; Atopy
Summary Objective: Due to its anatomical and functional connections, middle ear disorders frequently occur in sinusitis. Its prevalence, however, is likely to be underestimated. We evaluated the prevalence of middle ear dysfunction, as assessed by tympanometry, in children with chronic sinusitis in a large group of patients with chronic respiratory symptoms, and its possible relationship with respiratory allergy. Methods: From a population of 1810 children with respiratory symptoms referred to our Pediatric Allergy center, subjects with chronic sinusitis diagnosed by clinical criteria were selected. Children underwent testing of middle ear function by tympanometry and of allergy by skin tests with environmental allergens. Patients were divided into three groups according to age. Results: Two hundred and eighty-eight children (15.9%) had clinical diagnosis of chronic sinusitis according to the established criteria. Twenty-four patients were in group 1, 220 in group 2, and 44 in group 3. Altered middle ear pressure was found in 76.4% of patients, with a significantly higher rate of altered tympanograms in younger children ( p < 0.001). A positive skin prick test was found in 29.9% of children, with a significantly higher rate of positivity in older children ( p = 0.01). Conclusions: The decrease with age in the rate of tympanometric alterations is likely to be associated to the anatomic development of the upper airways, while the presence of atopy does not seem to play a role in their occurrence. # 2007 Elsevier Ireland Ltd. All rights reserved.
* Corresponding author. Tel.: +39 02 57995156; fax: +39 02 57995741. E-mail address: [email protected] (G. Leo). 0165-5876/$ — see front matter # 2007 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.ijporl.2007.10.018
316
1. Introduction Intermittent and persistent rhinitis, as defined by the occurrence of nasal symptoms such as sneezing, discharge and blockage for less or more than 4 weeks, respectively [1], is a very common condition in children. Allergies are frequently implicated as a cause of rhinitis [2,3]. Due to the anatomical contiguity of the paranasal sinuses with the nose, it has been suggested that the term rhinosinusitis should be used instead of sinusitis [4]. The middle ear has anatomical and functional connections with the nasopharynx through the Eustachian tube and the pathophysiology of its disorders is considered similar to that of sinusitis [5]. Inflammation of the nasal mucosa may lead to obstruction of the sinuses ostia and to Eustachian tube dysfunction which results in impairment of the middle ear pressure and in fluid exudation with the clinical picture of otitis media with effusion (OME), which is defined as ‘‘the presence of fluid in the middle ear without signs or symptoms of acute ear infections’’ [6]. The prevalence of OME in children has been estimated in the last three decades in a wide range from 15% to 80% [7—10]. According to a number of studies the presence of sinusitis in children with OME ranges from 48% to 62% [11—13], and concerning the role of allergy some Authors reported that from 23% to 90% of children with OME had hypersensitivity to inhalant allergens [14—17], a range too large to help in clinical practice. We sought to evaluate in children with chronic sinusitis, diagnosed by clinical criteria from a large group of patients with chronic respiratory symptoms, the prevalence of middle ear dysfunction, as assessed by tympanometry, and the prevalence of respiratory allergies.
2. Methods 2.1. Patients Between 2001 and 2004, 1810 children with respiratory symptoms referred to our Pediatric Allergy center. Children underwent a medical examination aimed at detecting the involvement of paranasal sinuses and middle ear. The presence of chronic sinusitis was assessed by the criteria of Shapiro and Rachelefsky [18], considering the presence of at least two of the three major criteria — purulent nasal discharge, purulent pharyngeal drainage, and cough — for a period of at least 12 weeks. As suggested by the Position paper of the European Academy of Allergology and Clinical Immunology [4], the mucopurulent discharge, as well as oedema
G. Leo et al. or obstruction of the middle meatus, was assessed by endoscopy–—performed by a ENT specialist. The presence of middle ear tube dysfunction was assessed by performing tympanometry. In addition, allergy testing was done by skin tests with common inhalant allergens and, in children younger than 3 years of age, with common food allergens. Exclusion criteria were: odontogenic causes of sinusitis, malformations of ear and palate, Down syndrome, nasal polyposis, metabolic diseases, previous surgical interventions of nose, ear and throat, history of chronic ear infections, as assessed by diagnosis of ENT specialists, and family history of hear loss. None of the children were receiving medications for at least the 2 weeks prior to the examination. Patients were divided in three groups according to their age: group 1 comprised children aged less than 3 years, group 2 between 3 and 6 years, and group 3 more than 6 years. Evaluation was performed within groups. The study was approved by the institutional board and oral consent was obtained by the parents.
2.2. Endoscopy Nasopharyngeal endoscopy were performed by fiberoptic flexible nasopharyngoscope Storz 11101 SK of 2.5 mm of diameter (Karl Storz GmbH & Co. KG D, Tuttlinghen, Germany); in all cases endoscopic evaluation included nasal turbinates and middle meatus, and the rhinopharynx to evaluate adenoid and Eustachian tube orifice.
2.3. Tympanometry Tympanometry was performed by a middle ear analyzer (Impedance Audiometer AZ 26, Interacoustics A/S, Assens, Denmark). Results were analysed by standard criteria [19]. The tympanogram was classified as type A (normal) when the pressure in the middle ear was higher than 100 daPa, as type B when no peak was detectable on the graphic, and as type C when the pressure ranged from 100 to 200 daPa (C1) and from 200 to 300 daPa (C2). Tympanograms of type B and C were considered abnormal.
2.4. Skin tests Skin prick tests (SPT) were performed according to guidelines from the European Academy of Allergology and Clinical Immunology [20] using standardized extracts (Stallerge ´nes, Antony, France) of the common aeroallergens (grasses, Parietaria, ragweed, Artemisia, olive, birch, alder, Dermatophagoides
Tympanometric alterations in chronic sinusitis pteronyssinus and farinae, Alternaria, Aspergillus, cat and dog epithelia). Children younger than 3 years also underwent food allergen testing using food extracts, namely cow milk, hen’s egg, fish, wheat, and peanut. A 10 mg/ml solution of histamine dihydrochloride served as positive control and a saline solution as negative control. A positive SPT was defined by the appearance of a wheal with an area larger than 7 mm2 with no reaction to negative control.
317
Fig. 1 Altered middle ear pressure and age. TPM: tympanometry.
2.5. Statistical analysis Tables of frequencies were analyzed using the x2test. Data management and statistical analyses were performed using the software Stata (Statacorp, College Station, TX, USA).
3. Results Out of the 1810 children with respiratory symptoms, 288 (15.9%) had a clinical diagnosis of chronic sinusitis according to the inclusion criteria. There were 173 males and 115 females, with a mean age of 5.1 2.0 years, range 1.9—14.0 years. Groups consisted as follows: group 1, 24 children; group 2, 220 children and group 3, 44 children. Altered pressure of middle ear was found in 220 of the 288 subjects (76.4%), in 78.3% of the females and in 75.1% of the males. Forty-six (16.0%) had a type C tympanogram (mono or bilateral), and 174 (60.4%) had a type B tympanogram, in which 56 abnormalities were monolateral (19.4%), and 118 were bilateral (41%). The prevalence of altered tympanograms was significantly higher among the younger children (Fig. 1). A positive reaction to SPTwas found in 86 children (29.9%), with a prevalence of positivity significantly different among age groups ( p = 0.01). The children aged less than 3 years had a prevalence of atopy of 4.2%, while in children aged between 3 and 6 years it was 31.8%, and it was 34.1% for those aged more than 6 years. Fifty-six subjects (19.4%) were sensitized to only one allergen, while 30 (10.4%) were sensitized to two or more. The most frequently found allergens
Fig. 2
Altered middle ear pressure and allergy.
were pollens (20.1%), house dust mites (12.5%), molds (5.2%), and animal epithelia (4.5%). Altered pressure of middle ear was found in 69.8% of allergic (60 subjects) and in 79.2% (160 subjects) of nonallergic children; this difference being not significant. In atopics, there were 26.7% of type C tympanogram subjects and 43% of type B subjects; in nonatopic, there were 11.4% of type C tympanogram subjects and 67.8% of type B subjects. The amount of type C and B tympanogram was significantly higher ( p < 0.001) in nonatopics than in atopics (Fig. 2). According to number of sensitizations, tympanometric dysfunction was present in 67.9% of monosensitized and in 73.3% of polysensitized children, with a not significant difference. Table 1 reports the rates of altered tympanograms according to the presence/absence of atopy among the three age groups, which were not significantly different of each other. According to the kind of sensitization, altered pressure of the middle ear was found in 81.2% of children monosensitized to house dust mites (with a type C tympanogram in 43.7% and a type B in 37.5%)
Table 1 Altered tympanogram in atopic and nonatopic children Group
Altered tympanogram
p
Atopics (%)
Nonatopics (%)
1. <3 year (24 children) 2. 3—6 year (220 children) 3. >6 year (44 children)
1/1 (100%) 52/70 (74.3%) 7/15 (46.7%)
20/23 (87.0%) 123/150 (82.0%) 17/29 (58.6%)
0.69 0.18 0.45
318
Fig. 3 year.
G. Leo et al.
Type of tympanogram in different periods of the
and in 63.6% of children monosensitized to pollen (with a type C tympanogram in 18.2% and type B in 45.4%). Regarding seasonal variations in the kind of tympanograms, there was a significantly higher rate of altered tympanograms ( p = 0.02) during cold months (Fig. 3).
4. Discussion The nose is anatomically and functionally related to the paranasal sinuses and middle ear, and this relationship clearly accounts for the association of rhinitis with sinusitis and pathologies such as OME [4—15]. It is not fully understood why only some subjects with rhinitis develop such disorders, but anatomical characteristics influencing the draining of the sinuses and the patency of the Eustachian tube are likely to play a pivotal role. This seems particularly important in children, whose rhino-sinusal anatomy experiences modifications as they grow up. Mills performed sinus radiographs in 240 children with OME and found abnormalities in 28% of cases, though only in 7% an infection was confirmed by a sinus lavage [21]. The same authors argued that radiograph — which currently is no longer considered a reliable diagnostic tool in the diagnosis of sinusitis [4] — may underestimate sinusitis. On the other hand, Fujita reported in a population of subjects aged 10—20 years with OME resistant to medical treatment that in 49% of cases radiology detected sinusitis, while in children aged 4—9 years the rate of radiologic abnormalities was 78% [22]. In adults, OME may be the presenting symptom of chronic sinusitis, as demonstrated by an endoscopic study which reported that in 23% of subjects with sinus disease — mainly of the ethmoid system — there was evidence of otitis media [23]. Lazo-Sa ´enz et al. extended the investigation to the role of allergy, by evaluating a group of 57 children aged less than 11 years and found that in
a group of 40 children with allergic rhinitis Eustachian tube dysfunction, as demonstrated by a tympanogram of C or B type, was present in 15.5% of subjects, while no subject of the control group had altered tympanogram [24]. Duration of allergic rhinitis and seasonal or perennial presentation did not show different associations with the middle ear pathology, and led the authors to conclude that just the presence of allergic rhinitis is a risk factor for Eustachian tube dysfunction in children. This study confirmed previous observations about allergy and otitis media, in which allergy was detected by means of skin tests, in vitro IgE tests, and assessment of inflammatory cells and cytokine profiles [25—28]. We designed the present study to evaluate the prevalence of middle ear alterations in children with sinusitis diagnosed by generally accepted clinical criteria [4,18]. To do this, all children underwent to tympanogram, which is a validated technique to detect middle ear effusion by measuring altered pressure, as demonstrated by comparison with magnetic resonance imaging [29]. Results demonstrate that Eustachian tube dysfunction is very common in children with chronic sinusitis but that this pathology significantly decreases its frequency with age, showing a rate of 87.5% in children aged less than 3 years, of 79.6% in those from 3 to 6 years, and of 54.5% in those aged more than 6 years, respectively. As suggested before, the anatomic development of the upper airway associated with growth and favouring a correct drainage of mucosal secretion and a normal ventilation of the middle ear can probably explain this change. Of note, in clinically healthy children the prevalence of tympanometric alterations indicating OME is low, with values of 3% in first grade and of 1.5% in second grade primary school students, respectively [30]. We looked for a possible role of allergy in inducing middle ear dysfunction by performing SPT with common environmental allergens. The prevalence of altered tympanograms, however, was not significantly different in nonatopic and atopic subjects. In addition, no difference could be observed between monosensitised and plurisensitised subjects. The significantly higher rate of altered tympanograms during winter is likely to be due to the more frequent upper airway inflammatory disorders in such period, and seems to play down the role of seasonal allergies such as grass, tree, or Parietaria pollenosis. Previous reports on this issue are discordant. The incidence of allergy in OME has been reported to range from 5% to 80%, as reviewed by Bernstein in 1996 [26], but more recent surveys indicate that the prevalence of allergy in OME does not seem to be higher than among the general population [17,27]. In particular, in the most recent study
Tympanometric alterations in chronic sinusitis the prevalence of allergic rhinitis was 28% in children with OME and 24% in controls [17]. Other pathologies such as infectious rhinitis or common cold are important in causing OME, but were not considered in our study which included only children with chronic sinusitis, i.e. present for at least 12 weeks. The cause of sinus inflammation in nonallergic children remains to be determined, possibly requiring the study of inflammatory cells and cytokine profiles obtained from mucosal samples.
319
[14]
[15]
[16]
[17]
References [18] [1] J. Bousquet, P. van Cauwenberge, N. Khaltaev (Eds.), Allergic rhinitis and its impact on asthma, J. Allergy Clin. Immunol. 108 (2001) S147—S334. [2] The International Study of Asthma and Allergies in Childhood (ISAAC), Steering Committee, Worldwide variations in prevalence of symptoms of asthma, allergic rhinoconjunctivitis, and atopic eczema, Lancet 351 (1998) 1225—1232. [3] C. Galassi, M. De Sario, A. Biggeri, L. Bisanti, E. Chellini, G. Ciccone, et al., Changes in prevalence of asthma and allergies among children and adolescents in Italy: 1994—2002, Pediatrics 117 (2006) 34—42. [4] W. Fokkens, V. Lund, C. Bachert, P. Clement, P. Hellings, M. Holmstrom, et al., EAACI position paper on rhinosinusitis and nasal polyps executive summary, Allergy 60 (2005) 583—601. [5] D.S. Parsons, E.R. Wald, Otitis media and sinusitis: similar diseases, Otolaryngol. Clin. North Am. 29 (1996) 11—25. [6] R.M. Rosenfeld, L. Culpepper, K.J. Doyle, K.M. Grundfast, A. Hoberman, M.A. Kenna, et al., Clinical practice guidelines: otitis media with effusion, Otolaryngol. Head Neck Surg. 130 (2004) S95—S118. [7] C.H. Sorensen, S.H. Jensen, M. Tos, The post-winter prevalence of middle-ear effusion in four-year-old children, judged by tympanometry, Int. J. Pediatr. Otorhinolaryngol. 3 (1981) 119—128. [8] G.A. Zielhuis, G.H. Rach, A.V. van den Bosch, P.V. van den Broek, The prevalence of otitis media with effusion: a critical review of the literature, Clin. Otolaryngol. Allied Sci. 15 (1990) 283—288. [9] J.L. Paradise, H.E. Rockette, D.K. Colborn, B.S. Bernard, C.G. Smith, M. Kurs-Lasky, et al., Otitis media in 2253 Pittsburgh area infants: prevalence and risk factors during the first two years of life, Pediatrics 99 (1997) 318—333. [10] D. Umapathy, A. Roshini, G.K. Scadding, A community based questionnaire study on the association between symptoms suggestive of otitis media with effusion, rhinitis and asthma in primary school children, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 705—712. [11] T.C. Hoshaw, N.J. Nickman, Sinusitis and otitis in children, Arch. Otolaryngol. 100 (1974) 194—195. [12] J.J. Grote, W. Kuijpers, Middle ear effusion and sinusitis, J. Laryngol. Otol. 94 (1980) 177—183. [13] A. Fujita, I. Honjo, K. Kurata, I. Gan, H. Takahashi, Refractory otitis media with effusion from viewpoints of eustachian tube
[19]
[20]
[21]
[22]
[23]
[24]
[25] [26]
[27]
[28]
[29]
[30]
dysfunction and nasal sinusitis, Am. J. Otolaryngol. 14 (1993) 187—190. B.M. Baker, C.D. Baker, H.T. Le, Vocal quality, articulation and audiological characteristics of children and young adults with diagnosed allergies, Ann. Otol. Rhinol. Laryngol. 91 (1982) 277—280. J.E. Gamble, J.A. Bizal, E.P. Daetwyler, Otitis media and chronic middle ear effusion in the asthmatic pediatric patient, Ear Nose Throat J. 71 (1992) 397—399. J.P. Corey, R.E. Adham, A.H. Abbass, I. Seligman, The role of IgE-mediated hypersensitivity in otitis media with effusion, Am. J. Otolaryngol. 15 (1994) 138—144. S.G. Yeo, D.C. Park, Y.G. Eun, C.I. Che, The role of allergic rhinitis in the development of otitis media with effusion: effect on Eustachian tube function, Am. J. Otolaryngol. 28 (2007) 148—152. G.G. Shapiro, G.S. Rachelesfky, Introduction and definition of sinusitis, J. Allergy Clin. Immunol. 90 (1992) 417—418. T. Finitzo, S. Friel-Patti, K. Chinn, O. Brown, Tympanometry and otoscopy prior to myringotomy: issues in diagnosis of otitis media, Int. J. Pediatr. Otorhinolaryngol. 24 (1992) 101—110. S. Dreborg (Ed.), Skin tests used in type I allergy testing. Position paper of the European Academy of Allergology and Clinical Immunology, Allergy 44 (suppl 10) 1989. R.P. Mills, B.S. Irani, R.J. Vaughan-Jones, N.D. Padgham, Maxillary sinusitis in children with otitis media with effusion, J. Laryngol. Otol. 108 (1994) 842—844. A. Fujita, I. Honjo, K. Kurata, I. Gan, H. Takahashi, Refractory otitis media with effusion from viewpoints of Eustachian tube dysfunction and nasal sinusitis, Am. J. Otolaryngol. 14 (1993) 187—190. Y. Finkelstein, Y.P. Talmi, Y. Rubel, J. Bar-Ziv, Y. Zohar, Otitis media with effusion as a presenting symptom of chronic sinusitis, J. Laryngol. Otol. 103 (1989) 827—832. J.G. Lazo-Sa ´enz, A.A. Galvan-Aguilera, V.A. Martines-Ordaz, V.M. Velasco-Rodriguez, A. Nieves-Renteria, C. Rincon-Castaneda, Eustachian tube dysfunction in allergic rhinitis, Otolaryngol. Head Neck Surg. 132 (2005) 626—631. P. Fireman, Otitis media and nasal disease: a role for allergy, J. Allergy Clin. Immunol. 82 (1988) 917—924. J.M. Bernstein, The role of IgE-mediated hypersensitivity in the development of otitis media with effusion: a review, Otolaryngol. Head Neck Surg. 109 (1993) 611—620. L.H. Nguyen, J.J. Manoukian, S.E. Sobol, T.L. Tewfik, B.D. Mazer, M.D. Schloss, et al., Similar allergic inflammation in the middle ear and the upper airways: evidence linking otitis media with effusion to the united airway concept, J. Allergy Clin. Immunol. 114 (2004) 1110—1115. C. Caffarelli, E. Savini, G. Giordano, G. Gianlupi, G. Cavagni, Atopy in children with otitis media with effusion, Clin. Exp. Allergy 28 (1998) 591—596. C.M. Alper, D.L. Sabo, W. Doyle, Validation by magnetic resonance imaging of tympanometry for diagnosing middle ear effusion, Otolaryngol. Head Neck Surg. 121 (1999) 523— 527. E. Keles, I. Kaygusuz, T. Karlidag, S. Yalc¸in, Y. Ac¸ik, H.C. Alpay, et al., Prevalence of otitis media with effusion in first and second grade primary school students and its correlation with BCG vaccination, Int. J. Pediatr. Otorhinolaryngol. 68 (2004) 1069—1074.
Available online at www.sciencedirect.com