Identification of adenoid biofilms in chronic rhinosinusitis

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Summary

Objective

To compare the percent mucosal surface area of adenoids removed from children with chronic rhinosinusitis (CRS) and those with obstructive sleep apnea (OSA) infected with biofilms.

Design

Comparative micro-anatomic investigation of adenoid mucosa using scanning electron microscopy from patients with CRS and OSA.

Subjects

4 females and 12 males ranging from 3 months to 10 years of age.

Results

Adenoids removed from patients with CRS had dense mature biofilms covering the mucosal surface. More specifically, adenoids removed from patients with CRS had an average of 94.9% of their mucosal surface covered with mature biofilms vs. an average of 1.9% coverage on the adenoids removed from patients with OSA. These differences were statistically significant at the p < 0.001 level.

Conclusions

It is well established that adenoidectomy is useful in the treatment of CRS resistant to antibiotics. Adenoids removed from patients with CRS had almost their entire mucosal surface covered with biofilms vs. scant coverage for patients with OSA (p < 0.001). Decreased metabolic activity, decreased growth rate, and transmission of resistance genes all contribute to the antibiotic resistant nature of the biofilms. These metabolically sessile communities shed planktonic microorganisms on an intermittent basis. Therefore biofilms in the nasopharynx of children with CRS may act as a chronic reservoir for bacterial pathogens resistant to standard antibiotics. Also, the mechanical debridement of the nasopharyngeal biofilms may explain the observed clinical benefit associated with adenoidectomy in this subset of pediatric patients.

Introduction

Chronic rhinosinusitis (CRS) in the pediatric population is a complex disease with a considerable impact upon the United States economy. Most otolaryngologists agree that the cornerstone of treating CRS is a prolonged course of a broad-spectrum, beta lactamase stable oral antibiotic. Although the direct cost of pediatric chronic sinusitis is unknown, it is estimated that more than $2 billion is spent annually on the purchase of over-the-counter medications for the treatment of CRS [1]. When combined with the cost of antibiotic therapy, the public health impact is enormous.

Chronic sinusitis is defined as an infectious process of the paranasal sinuses lasting for longer than 3 months. Nasal discharge is most often purulent, but may be minimal or absent in CRS. Throat clearing may be more prominent secondary to discharge from the posterior ethmoid sinuses. A cough may be present in the daytime and worsen at night. The child may suffer from sleep impairment, poor appetite and poor school performance.

The pathogens observed in CRS are not the same well defined set of organisms which cause acute sinusitis. Studies have shown that anaerobes are cultured from the paranasal sinuses at rates ranging from 2% to 100% [2]. Overall, bacteriology is difficult to ascertain in CRS as many organisms are recovered in low densities. As no concrete subset of organisms exists to target with oral antibiotics, CRS is a difficult disease to treat. Although broad spectrum, beta lactamase stable oral antibiotics are often used to target pathogens, CRS typically does not respond with permanent or sustained improvement to antibiotic therapy. Due to the wide variety of both aerobic and anaerobic organisms cultured from the paranasal sinuses, there is no current consensus as to treatment length, organism coverage, or antibiotics that are most effective [3]. It is generally believed that high dose antibiotics should be given for a minimum of 3 weeks in the treatment of CRS.

Alternatives to oral antibiotic therapy include functional endoscopic sinus surgery (FESS) and adenoidectomies. Although pediatric FESS is widely used for the treatment of refractory CRS, with success rates ranging from 80% to 93% [4], concerns exist over possible interference with facial skeletal growth and further scarring of the drainage pathways [5], [6], [7]. Recent literature suggests that adenoidectomies may be beneficial to patients with a diagnosis of CRS. In a study by Vandenberg and Heatley, 58% of patients demonstrated a near or complete resolution of the symptoms of CRS [8]. The adenoidectomy both eliminates nasal airway obstruction, and removes a nidus for chronic bacterial infection.

The presence of bacterial biofilms has been identified in our lab on adenoidal tissue removed from children with a diagnosis of recurrent acute otitis media (RAOM) [9]. Outside the human body, biofilms are found on mineral surfaces, living and dead plant or animal matter, polymers, ceramics and metal alloys. The process of biofilm formation occurs when individual cells adhere and coalesce to various surfaces. Exopolysaccharides (EPS) are produced, resulting in an EPS matrix which forms much of the volume of a biofilm community. Microchannels form through the hydrated EPS matrix, resulting in connections between microbes and periodic shedding of planktonic cells [10], [11]. The individual planktonic cells may then multiply, disperse and infect the host.

Scanning electron microscopy was used to identify the biofilms in this study and in previous studies by our laboratory. Using techniques gathered from previous authors and from the industrial waste industry, it was easy to distinguish those surfaces coated with biofilms from those of a barren adenoid mucosa. Individual planktonic cocci and bacilli could be observed in the background EPS matrix with these techniques.

We feel that the identification of adenoid biofilms in patients with chronic rhinosinusitis might provide new information regarding the pathogenesis of CRS. This article reflects qualitative data gathered from the adenoids removed from children with CRS. The patients chosen for this study only represent an initial sampling of pediatric patients. As such, this paper is intended only as a descriptive study and is not intended to be statistical in nature.

Section snippets

Sample collection

IRB approval for the study was obtained from Wayne State University. All samples were obtained from adenoidectomies performed for chronic rhinosinusitis by the authors at Children's Hospital of Michigan, St. Joseph Mercy's Hospital and Lahser Ambulatory Surgery Center. In some cases of OSA, both the adenoids and tonsils were removed. The ages of the patients ranged from 3 months to 10 years. There were 4 male patients and 12 female patients. Seven samples were collected from patients with

Results

Table 1 displays patient demographics and diagnoses along with their respective presence of biofilms. The presence of biofilms is defined as a dense covering of nearly the entire mucosal surface of the adenoid with the cellular microarchitecture previously mentioned. The absence of biofilms was defined as no discernable accumulations of bacteria in an amorphous matrix on the adenoid.

Adenoids removed from patients with OSA served as controls in this study. Fig. 1 is a high power (2000×) SEM

Discussion

Biofilms have a profound impact on human pathogenesis. For example, Streptococci in dental plaque biofilms are associated with cavity formation and periodontal disease. If given access to the bloodstream, the organisms may weak havoc on a variety of indwelling medical devices such as catheters, synthetic joints, artificial heart valves and pacemakers. Once an infection is present, it usually persists until the biofilm-colonized surface is removed from the body. The EPS matrix affords the

Conclusion

Our identification of dense biofilm structures on adenoids of children with CRS suggests that biofilm production may be a virulence factor for organisms that are responsible for the development of CRS. This is an important step in supporting the notion of an adenoidectomy's role in mechanical debridement of sinus pathogens. The differences found on SEM examination are extremely interesting. Additional investigation comparing surface density analysis of adenoids removed for OSA and CRS is

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