Chronic Rhinosinusitis and Adenoid Hypertrophy in Children

Ulku Tuncer, MD,* Barlas Aydogan, MD,* Levent Soylu, MD,* Mustafa Simsek, MD,* Cagatay Akcali, MD,* and Akif Kucukcan, MD
Purpose: The purpose of this study was to investigate the relationship between adenoid microbiology, adenoid size, and maxillary sinus microbiology in children with both chronic rhinosinusitis and adenoid hypertrophy. Methods: The children with both chronic rhinosinusitis and adenoid hypertrophy were admitted to this prospective study. The study included 30 children. The diagnosis of chronic rhinosinusitis was based on clinical and radiologic examinations. Adenoid hypertrophy was classied as medium and large based on the preoperative exible beroptic endoscopy and nasal endoscopy during surgery. Maxillary sinus aspiration and adenoidectomy was performed in all patients. Sinus aspirate and adenoid tissue specimens were cultured. The correlation of culture results was investigated. The relationship between adenoid size and maxillary sinus culture results was analyzed by using chi-square test. Results: Adenoid sizes were medium in 12 (40%) and large in 18 (60%) cases. Bacterial growth was found on 14 of 30 (47%) sinus aspirate, and all adenoid specimen cultures showed bacterial growth (100%). There was no statistical correlation between cultures obtained from the adenoid tissue with those from the maxillary sinus. The relationship between adenoid size and maxillary sinus culture results was not found statistically significant (2 0.96, P 1.0). Conclusion: The reason that there was no correlation between cultures obtained from the adenoid tissue with those from the maxillary sinus is that it seems possible that the adenoids act as a barrier causing mechanical obstruction rather than a nidus for chronic sinus infection. However, there is no relationship between adenoid size and maxillary sinus culture positivity. Medium adenoids causing partial obstruction may lead to changes in the microenvironment and may start bacterial growth in children with positive maxillary culture. Further investigation is needed to explain the association between adenoid hypertrophy and rhinosinusitis. Adenoidectomy helps to resolve the symptoms of chronic rhinosinusitis in the children with both chronic rhinosinusitis and adenoid hypertrophy. (Am J Otolaryngol 2004;25:5-10. 2004 Elsevier Inc. All rights reserved.)

Adenoid hypertrophy and sinus infection are common diseases seen in the otolaryngological practice, and the symptoms and clinical ndings in each of these conditions are similar. There is a known association between adenoid hypertrophy or chronic adenoid infection and rhinosinusitis.1 The adenoids may predispose to sinus infections via mechanical blockage of nasal breathing or by harboring pathogenic bacteria.2 Although the maxillary sinus microbiology in adults was adequately

investigated in many reports, there are few studies in children.3-8 Furthermore, despite many reports stating a considerable efcacy of adenoidectomy in managing of chronic rhinosinusitis in children, to our knowledge, there is no report in the literature comparing adenoid microbiology and adenoid size with maxillary sinus microbiology.9-11 The purpose of this study was to investigate the relationship between adenoid microbiology, adenoid size, and maxillary sinus microbiology in children with both chronic rhinosinusitis and adenoid hypertrophy. PATIENTS AND METHODS
The children with both chronic rhinosinusitis and adenoid hypertrophy were admitted to this prospective study. The study included 30 children, 22 male and 8 female. Their ages ranged from 4 to 12 years, with a median age of 6 years.
5

From the Departments of *Otorhinolaryngology; and Microbiology, C ukurova University, Adana, Turkey. lku Tuncer, MD, DeAddress correspondence to: U partment of Otorhinolaryngology, C ukurova University, 01330 Balcal, Adana, Turkey. E-mail: ulkutuncer@ ixir.com 0196-0709/$ - see front matter 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.amjoto.2003.10.003

American Journal of Otolaryngology, Vol 25, No 1 (JanuaryFebruary), 2004: pp 5-10

TUNCER ET AL

The diagnosis of chronic rhinosinusitis was based on clinical and radiologic examinations. Patients presenting with recurrent (4 acute episodes per year) or persistent (12 weeks) sinusitis complaints, including rhinorrhea, nasal obstruction, cough, headache, and postnasal drainage, were evaluated for chronic rhinosinusitis. Patients with these complaints and mucoperiosteal thickening of more than 5 mm or complete opacication in 1 or both maxillary sinuses on computed tomography scans were diagnosed as chronic rhinosinusitis. All of the patients also had adenoid hypertrophy signs (mouth breathing, snoring, and nasal airway obstruction). Adenoid hypertrophy was classied as medium (adenoids causing the partial obstruction of the posterior nares), and large (adenoids causing complete obstruction of the posterior nares) based on the preoperative exible beroptic endoscopy and nasal endoscopy during surgery. The patients and parents were asked for allergic history. In children with a suggestive history including itching mucous membranes of the upper aerodigestive tracts; eczema; food intolerance; sensitivity to house dust mites, animal danders, and molds; and seasonal allergic symptoms, nasal smear and serum total immunoglobulin E level testing were performed. When serum total immunoglobulin E level was elevated, patients were consulted to the pediatric allergy department to investigate specic allergens. None of the patients received antibiotic treatment for at least 2 weeks before the operation. After informed parental consent was obtained, maxillary sinus aspiration and adenoidectomy was performed in all patients. Maxillary sinus aspiration was performed with the patient under general anesthesia. After orotracheal intubation procedure, patients were kept in a supine position with hyperextension of the head. The nasal mucosa was cleaned with a sterile saline solution and then a sterile gauze was embedded with 1% povidone-iodine solution and applied to the nasal mucosa and removed. The area was allowed to dry. After disinfection and before aspiration, puncture site culture was taken with a swab. A 16-gauge needle was introduced beneath the inferior turbinate through the nasal lateral wall, inside the maxillary sinus; any uid present in the sinus was aspirated with a syringe. If no uid was obtained, 3 mL of sterile saline was instilled into the maxillary antrum and then aspirated back into the syringe. All the aspirated material was transported to the microbiology laboratory. After the aspiration procedure, the adenoids were removed with a curette. Adenoid specimens were placed into aerobic and anaerobic transport medium and sent to the microbiology laboratory. All specimens were inoculated into media supportive for aerobic and anaerobic organisms. The time between specimen collection and inoculation never exceeded 30 minutes. The adenoid tissue was homogenized in a small amount of brain-heart infusion broth or sterile

physiologic nonbacteriostatic saline. An aliquot of the homogenized tissue was then inoculated on a Trypticase soy agar medium (Acumedia, Baltimore, MD) that contained 5% sheep blood, a chocolate agar plate, and a MacConkey agar plate. The plates were then incubated in 5% to 10% CO2 at 37C for 24 to 48 hours. For maxillary sinus aspirate, several drops were inoculated on same types of media and incubated under same conditions. For anaerobes, the materials were plated onto prereduced vitamin K1-enriched Brucella blood agar, anaerobic blood agar plate containing phenylethyl alcohol, and enriched thioglycolate broth (containing hemin, sodium bicarbonate, and vitamin K1). The plates were incubated in anaerobic jars and examined at 48 and 96 hours. The thioglycolate broth was incubated for 14 days. The organisms were isolated and identied by the standard methods described in the Bailey and Scotts Diagnostic Microbiology.12 Results of cultures were correlated between maxillary sinus aspirate and adenoid tissues. If the same pathogen was isolated from both sides, this implied a positive correlation. If a pathogen isolated from maxillary sinus was not isolated from the adenoid, then a negative correlation was considered. In the comparison of the relationship between adenoid size and maxillary sinus culture results, a chi-square test was used. Postoperatively, oral antibiotics were administered empirically; however, based on culture and susceptibility studies, the antibiotic agents were altered accordingly. The complaints of patients were assessed at a visit 4 weeks after surgery. An estimate of overall improvement was also made by the investigator. Long-term symptom control and overall improvement were assessed during a telephone interview 3 to 18 months after surgery (mean, 9 months). Three patients were lost to follow-up.

RESULTS The most frequently presenting symptoms were nasal obstruction (100%), mouth breathing (100%), and snoring (100%), followed by cough (83%), rhinorrhea (80%), and postnasal drainage (80%) (Table 1). Allergy was recorded in 8 patients (27 %): 2 house dust mite, 2 animal dander, 1 food allergy (egg), and 3 more than 1 allergen (grass, animal dander, and mold). Preoperative computed tomography scans showed varying degrees of maxillary, ethmoid, frontal, and sphenoid sinus mucosal thickening. The sinuses involved were the maxillary (30 cases), ethmoid (15 cases), frontal (12 cases), and sphenoid (17 cases). Pansinusitis was present in 5 instances (Table 2).

CHRONIC RHINSINUSITIS

TABLE 1. The Presenting Symptoms in 30 Children on Initial Evaluation Patients (No.) 30/30 24/30 25/30 20/30 24/30 30/30 30/30

Symptom Nasal obstruction Rhinorrhea Cough Headache Postnasal drainage Mouth breathing Snoring

(%) 100 80 83 67 80 100 100

were better after surgery and their symptoms severity were reduced, some patients had reduced symptoms of rhinorrhea (27%), cough (17%), postnasal drainage (20%), headache (7%), and nasal obstruction (7%) (Table 4). Long-term symptom control and overall improvement assessment by telephone interview could be made on 27 patients. Of these 27 patients, 5 (11.2%) still had rhinosinusitisrelated symptoms. DISCUSSION

Adenoid sizes were medium in 12 (40%) and large in 18 (60%). All nasal mucosa cultures obtained after disinfection and before aspiration of the maxillary sinus showed no bacterial growth. Whereas among the maxillary sinus aspirate, bacteria were cultured from 14 of 30 (47%), all adenoid specimen cultures showed bacterial growth (100%). The types of bacterial growth of the maxillary sinus aspirate and adenoid specimens are shown in Table 3. From 14 culture-positive maxillary sinus aspirates, a total of 20 aerobic bacterial isolates were recovered. The most frequently isolated bacteria were Staphylococcus aureus and Streptococcus pneumoniae. From the 30 culture-positive adenoid specimens, a total of 57 aerobic and 1 anaerobic bacterial isolates were recovered. The most frequently isolated bacteria, in descending order, were -hemolytic streptococcus, neisseria, and -hemolytic streptococcus. Maxillary sinus culture sets yielded a single organism in 10 aspirate and polymicrobial growth in 4. One isolated microorganism was the same in both 9 maxillary sinus and adenoid tissue specimens. Although the same pathogen was yielded in 9 cases bilaterally, the correlation between cultures obtained from the adenoid tissue with those from the maxillary sinus was not shown statistically. Adenoid size was large in 18 children and medium in 12. Of 14 maxillary sinus culturepositive children, 9 had large adenoid and 5 medium. The relationship between adenoid size and maxillary sinus culture results was not found statistically signicant (2 0.96, P 1.0). The symptoms of mouth breathing and snoring were improved in all patients four weeks after surgery. Although the patients

Pediatric chronic rhinosinusitis is a complex disease whose pathogenesis is poorly understood. There is a known association between adenoid hypertrophy or chronic adenoid infection and rhinosinusitis.1 Various investigators have reported incidence of rhinosinusitis in 22% and 69% cases of tonsillitis and adenoid hypertrophy.13 Adenoidectomy is recommended as a treatment option for refractory chronic rhinosinusitis in children.9,14 To explain the relationship between adenoids and symptoms of chronic rhinosinusitis, a theory describes the adenoids as a bacterial reservoir that serves as a nidus for chronic infection.1 This relationship is really unknown. Also, to our knowledge, there are no adequate reports in the literature that compare adenoid microbiology with maxillary sinus microbiology. In the present study, maxillary sinus cultures were compared with adenoid tissue cultures. Whereas all adenoid specimen cultures showed bacterial growth (100%), bacteria were cultured from 14 of 30 maxillary sinus aspirate (47%). Moreover, there was no statistically correlation between cultures obtained from the adenoid tissue with those from the maxillary sinus. These ndings suggest that the adenoid tissue does not seem to be a bacterial reservoir that serves as a nidus for

TABLE 2.

Preoperative CT Scan Findings in 30 Children Patients (No.) 30 15 12 17

Sinusitis Involvement Maxillary Ethmoid Frontal Sphenoid

(%) 100 50 40 57

TUNCER ET AL

TABLE 3. The Culture Results of the Maxillary Sinus Aspirate and Adenoid Tissue Specimens Patient No. 1 Sinus Aspirate Adenoid Specimen

-hemolytic streptococcus -hemolytic streptococcus -hemolytic streptococcus S pneumoniae No growth No growth

-hemolytic streptococcus Neisseria Diphtheroid -hemolytic streptococcus

S pneumoniae -hemolytic streptococcus S pneumoniae Neisseria Diphtheroid S. pneumoniae H inuenzae Neisseria -hemolytic streptococcus Neisseria H inuenzae -hemolytic streptococcus -hemolytic streptococcus -hemolytic streptococcus -hemolytic streptococcus Neisseria -hemolytic streptococcus S pneumoniae -hemolytic streptococcus S epidermidis H inuenzae S epidermidis -hemolytic streptococcus H inuenzae -hemolytic streptococcus Diphtheroid Neisseria Peptostreptococcus S aureus S pneumoniae Neisseria -hemolytic streptococcus -hemolytic streptococcus S pneumoniae S pneumoniae Neisseria S aureus -hemolytic streptococcus -hemolytic streptococcus S pneumoniae -hemolytic streptococcus Neisseria -hemolytic streptococcus S pneumoniae -hemolytic streptococcus S aureus -hemolytic streptococcus -hemolytic streptococcus S aureus -hemolytic streptococcus S pneumoniae H inuenzae Neisseria S aureus

3 4

S pneumoniae

6 7 8 9 10 11 12 13 14 15 16 17 18 19 20

No growth No No No No No growth growth growth growth growth

No growth S aureus No growth S. epidermidis H inuenzae No growth No growth Diphtheroid M catarrhalis Neisseria S aureus Diphtheroid No growth

21

22 23

No growth S aureus

24 25 26 27

No growth S pneumoniae S aureus No growth

28

S aureus

29 30

H inuenzae S aureus

CHRONIC RHINSINUSITIS

TABLE 4. The Symptoms of the Patients on the Evaluation 4 Weeks After Surgery Patients (No.) 2/30 8/30 5/30 2/30 6/30 0/30 0/30

Symptom Nasal obstruction Rhinorrhea Cough Headache Postnasal drainage Mouth breathing Snoring

(%) 7 27 17 7 20 0 0

pediatric chronic maxillary sinusitis. Another theory is based on adenoid hypertrophy causing mechanical obstruction, stasis of nasal secretions, and a cycle of inammation and infection.15 According to our results, it seems that the adenoids act as a barrier causing mechanical obstruction rather than a nidus for chronic sinus infection. Adenoid hypertrophy causes mechanical obstruction, but the relationship between adenoid sizes and sinus infection is not dened clearly. The nasopharyngeal space and the size of the adenoids have been evaluated by using different methods of assessment such as determination of the roentgenographic adenoid/nasopharyngeal ratio, exible beroptic endoscopy, and direct measurements during surgery.16 We evaluated the size of the adenoids by using exible beroptic endoscopy preoperatively and nasal endoscopy during surgery. Although it is suggested that the presence of adenoid tissue in a small postnasal space rather than adenoidal hypertrophy itself is the main cause of symptoms, Cassellbrant16 states that adenoid hyperplasia, rather than a decreased nasopharyngeal space, is the main cause of nasopharyngeal obstruction in young children.17 In our study, all children had adenoid hyperplasia and adenoid hypertrophy signs. The relationship between adenoid size and maxillary sinus culture results was not found statistically signicant. In other words, the children with medium-size adenoids had maxillary sinusitis. These ndings suggest that medium adenoids causing partial obstruction may lead to changes in the microenvironment and may foster bacterial growth in children with positive maxillary culture. Studies using maxillary sinus lavage have consistently shown that the predominant or-

ganisms of acute and subacute pediatric rhinosinusitis are Streptococcus pneumoniae, nontypeable Hemophilus inuenzae, and Moraxella (Branhamella) catarrhalis.18,19 Studies of pediatric patients with chronic rhinosinusitis have sometimes shown an increased importance of anaerobic bacteria and staphylococcal species.8 Muntz and Lusk20 studied the microbiology of tissues taken at the time of surgery for chronic rhinosinusitis. Their results showed very different bacteria from those present in acute rhinosinusitis including -hemolytic streptococcus, S aureus, M catarrhalis, S pneumoniae, and H inuenzae. In our study, the most frequently isolated bacteriawere S aureus and S pneumoniae, and no aerobic and/or anaerobic microorganism was yielded in 53% of the patients. Wald et al18 were found bacterial growth in 58% of sinus aspirates obtained from children with subacute sinusitis. One study reported that 20% to 35% of maxillary sinus aspirates were sterile in pediatric rhinosinusitis.14 Sterile conditions in sinusitis are partially explained by the potential involvement of chronic catarrhal sinusitis or edematous allergic sinusitis, which are reported to have increased in recent years.21 In chronic rhinosinusitis, underlying conditions such as allergy, immunodeciency, cystic brosis, ciliary dyskinesia, and gastro-oesophageal reux may be present. Of these, respiratory allergy is perhaps the most frequent.22 Therefore, in children with chronic rhinosinusitis with a suggestive history and/or physical examination, performing allergic assessment is recommended. Infantile eczema, asthma, food allergy in infancy, and previous good response to antihistamine treatment or intranasal anti-inammatory drugs are also very suggestive for allergic disease, as well as positive family history in the rstdegree relative. Children with allergic problems often show adenoidal hypertrophy and often present with the symptoms of chronic rhinosinusitis.23 Among our culture-negative patients, only 3 had allergy. In the remaining 13, we could not nd any obvious factor to cause rhinosinusitis. If we had performed allergic assessment for all children, the number of allergic patients would have been higher. Further investigation is needed to explain the sterile conditions in rhinosinusitis.

10

TUNCER ET AL

In conclusion, the reason that there was no correlation between cultures obtained from the adenoid tissue with those from the maxillary sinus is that it seems possible that the adenoids act as a barrier causing mechanical obstruction rather than a nidus for chronic sinus infection. However, there is no relationship between adenoid size and maxillary sinus culture positivity. Medium adenoids causing partial obstruction may lead to changes in the microenvironment and may start bacterial growth in children with positive maxillary culture. Further investigation is needed to explain the association between adenoid hypertrophy and rhinosinusitis. Adenoidectomy helps to resolve the symptoms of chronic rhinosinusitis in the children with both chronic rhinosinusitis and adenoid hypertrophy. REFERENCES
1. Lee D, Rosenfeld RM: Adenoid bacteriology and sinonasal symptoms in children. Otolaryngol Head Neck Surg 116:301-07, 1997 2. Manning SC: Pediatric sinusitis. Otolaryngol Clin North Am 26:623-638, 1993 nerci M, et al: Evaluation of 3. S ener B, Hasc elik G, O the microbiology of chronic sinusitis. J Laryngol Otol 110:547-550, 1996 4. Cook HE, Haber J: Bacteriology of the maxillary sinus. J Oral Maxillofac Surg 45:1011-1014, 1987 5. Jiang RS, Hsu CY, Jang JW: Bacteriology of the maxillary and ethmoid sinuses in chronic sinusitis. J Laryngol Otol 112:845-848, 1998 6. Don DM, Yellon RF, Casselbrant ML, et al: Efcacy of a stepwise protocol that includes intravenous antibiotic therapy for the management of chronic sinusitis in children and adolescents. Arch Otolaryngol Head Neck Surg 127:1093-1098, 2001

7. Brook I: Aerobic and anaerobic bacterial ora of normal maxillary sinuses. Laryngoscope 91:372-376, 1981 8. Brook I: Bacteriologic features of chronic sinusitis in children. JAMA 246:967-969, 1981 9. Vanderberg SJ, Heatley DG: Efcacy of adenoidectomy in relieving symptoms of chronic sinusitis in children. Arch Otolaryngol Head Neck Surg 123:675-678, 1997 10. Jones NS: Current concepts in the management of pediatric rhinosinusitis. J Laryngol Otol 113:1-9, 1999 11. Ramadan HH: Adenoidectomy vs endoscopic sinus surgery for the treatment of pediatric sinusitis. Arch Otolaryngol Head Neck Surg 125:1208-1211, 1999 12. Finegold SM, Baron EJ (eds): Bailey and Scotts diagnostic microbiology). St. Louis, CV Mosby, 1986 13. Paul D: Sinus infection and adenotonsillitis in pediatric patients. Laryngoscope 91:997-1000, 1981 14. Isaacson G: Sinusitis in childhood. Pediatr Clin North Am 43:1297-1317, 1996 15. Lusk RP, Lazar RH, Muntz HR: The diagnosis and treatment of recurrent and chronic sinusitis in children. Pediatr Clin North Am 36:1411-1421, 1989 16. Casselbrant ML: What is wrong in chronic adenoditis/tonsillitis anatomical considerations. Int J Pediatr Otolaryngol 49:133-135, 1999 17. Tankel JW, Cheesman AD: Symptom relief by adenoidectomy and relationship to adenoid and post-nasal airway size. J Otol Laryngol 100:637-640, 1986 18. Wald ER, Byers C, Guerra N, et al: Subacute sinusitis in children. J Pediatr 115:28-32, 1989 19. Wald ER, Reilly JS, Casselbrant M, et al: Treatment of acute maxillary sinusitis in childhood: A comparative study of amoxicillin and cefaclor. J Pediatr 104:297-302, 1984 20. Muntz HR, Lusk RP: Bacteriology of the ethmoid bullae in children with chronic sinusitis. Arch Otolaryngol Head Neck Surg 117:179-181, 1991 21. Suzuki K, Nishiyama Y, Sugiyama K, et al: Recent trends in clinical isolates from paranasal sinusitis. Acta Otolaryngol 525:51-55, 1996 22. Clement PAR, Bluestone CD, Gordts F, et al: Management of rhinosinusitis in children. Int J Pediatr Otorhinolaryngol 49:95-100, 1999 23. Cook PR, Nishioka GJ: Allergic rhinosinusitis in the pediatric population. Otolaryngol Clin North Am 29:3956, 1996