EGYPT. J. Med. Lab. Sci., (ESIC), Vol. 13, No. 2, Sept.

, 2004

BACTERIOLOGY OF TONSIL SURFACE AND CORE IN CHILDREN WITH CHRONIC TONSILLITIS AND INCIDENCE OF BACTERAEMIA DURING TONSILLECTOMY
Afaf S. Abdulrahman, Laila A. Kholeif, Yasser M. El-Beltagy *and Abeer A Eldesouky Microbilology and immunology and E. N. T departments, faculty of medicine, Ain shams university

ABSTRACT
This study included 27 children with age ranges from 2 to 9 years with chronic tonsillitis. They underwent elective tonsillectomy in the E.N.T. department of Ain Shams University hospitals. The following specimens were taken from each patient; throat swab after positioning the patient under general anesthesia, core swab specimen after removal of tonsils and blood sample early post operative (within two minutes after tonsillectomy) for bacteriological examination. Pathogens were detected in 81.5% of core specimens versus 44.4% in surface swab culture. Throat swab was found to have 38.9% sensitivity, 33.3% specificity and 63.6% positive predictive value in detecting pathogens in cases of chronic tonsillitis. Staphylococcus aureus was the most commonly grown organism in the core of the tonsils and/or surface culture (21 patients out of 27(77.7%)), 2 in throat swab only 10 in tonsil core only and 9 in both throat swab and tonsil core, Group A hemolytic streptococci was isolated from 5 patients (18.5%), only one case yielded the organism in throat swab and 4 cases yielded the organism in the tonsil core, E.coli was detected in tonsil core of one patient (3.7%), and Klebsiella pneumoniae was detected in both throat swab and tonsil core of one patient (3.7%). Regarding antibiotic sensitivity, commonly used antibiotics yielded unsatisfactory results for isolated pathogens. The incidence of post tonsillectomy bacteraemia in the current study was 7.4% (2/27). Staph aureus was isolated from the two cases. In conclusion, there is discrepancy between tonsillar surface and tonsillar core culture results in cases of chronic tonsillitis. Staph aureus was the commonest isolated organism in throat swab or core culture. The problem of bacterial resistance to commonly used antibiotics is apparent but further studies on larger scales are needed to determine the magnitude of the problem. Post-tonsillectomy bacteraemia occurs in low percent of patients.

INTRODUCTION
Chronic tonsillitis is the most common disease in throat that occurs predominantly in the younger age group (Wiatrak and Woolley, 1998). The disease is diagnosed mainly by history and clinical examinations. Superficial tonsillar swabs are often used as a guide in identifying the offending organism and the proper selection of therapy in acute and recurrent tonsillitis. However, their use may lead to incorrect conclusions. Several studies indicate a marked discrepancy in the external and the core tonsillar pathogenic flora (Kurien et al., 2000 and Timon et al., 1991). Surow et al., (1989) noted that tonsillar disease may arise from the bacteria within the substance of the tonsil rather than bacteria identified on the surface. They added that the surface of the tonsils is consistently exposed to oral secretions with their attendant flora. Tonsillar surface culture is likely to grow these organisms. Several studies concluded that determination of the surface flora was not useful in predicting core bacteria (Brook et al., 1980, Rosen et al., 1977 and Timon et al.,

1991). However Almadori et al. (1988) stated that surface swab cultures did reflect organisms present in the core. Tonsillectomy is indicated in recurrent acute tonsillitis for at least two years with five or more acute attacks per year, the procedure may be associated with transient bacteraemia in some cases which may or may not be associated with any enhanced post-operative morbidity (Yildirim et al., 2003). The incidence of bacteraemia associated with tonsillectomy varies among different investigators. (Yildirim et al., 2003, Kaygusuz et al, 2001 and Anand et al, 1999) The aim of this work is to compare between throat swab and tonsil core culture results in chronic tonsillitis and determine the incidence of bacteraemia following tonsillectomy.

SUBJECTS AND METHODS

The present study was conducted on 27 children (14 females and 13 males) suffering from chronic tonsillitis. They had been admitted to the ENT department of Ain Shams University Hospitals for elective tonsillectomy. Their age ranged from 2 to 9 years. All patients had a history of recurrent sore throat for at least 2 years, with a frequency of five or more significant acute attacks per year. Over this period, treatment by the primary care physician involved numerous courses of oral antibiotics. The antibiotics most commonly prescribed were, Amoxycillin, Amoxycillinclavulanic acid, Erythromycin and Trimethoprim-sulfamethoxazole. All patients had slightly enlarged or normal size tonsils, peritonsillar erythema, tonsilloliths, and tender cervical lymph nodes. A) Collection of specimens: 1) Tonsillar surface swab: After positioning the patient under general anesthesia and oropharyngeal suction, the tonsil surface was swabbed and the swabs were collected in a sterile tube. 2) Core specimen: The tonsils were removed by dissection, placed in a sterile container, and dispatched immediately with the swabs to the microbiology laboratory. 3) Blood samples: Two mililiters of blood were taken from every patient aseptically by venipuncture early post operative (within two minutes after tonsillectomy) B) Preparation of the core specimens: An aseptic, non touch technique was used to prepare the tonsils for culture. The tonsils were washed in sterile saline and placed in a sterile Petri dish, and the deep surface of the tonsils was cut using a flamed scalpel and the core was sampled using a sterile swab. C) Culture of tonsillar surface and core swabs: Tonsil surface swabs and tonsil core specimens were cultured on the following media: - Sheep blood agar: to show the hemolytic properties of micro-organisms. - MacConkeys agar for isolation of Enterobacteriacea. - Chocolate agar, containing 0.5 unit /ml. penicillin as a selective media for inhibiting growth of Streptococci, Neisseriae diphetheroid bacilli and coagulase negative Staphylococci and allow growth of Haemophilus influenzae. The paired samples (Tonsil surface swab and tonsil core swab) cultured on these three media were then incubated overnight aerobically at 37oC.The organisms were identified according to Collee et al. (1996). D) Blood culture: Two milliliters of blood were added to 20 ml N. broth and incubated at 37oC aerobically and then sub cultured on blood agar and MaCconckeys agar every 48h. Incubation continued for a week before discarding as negative. Any isolate was identified according to Collee et al. (1996)

E) Antibiotic sensitivity tests were carried for pathogenic isolates by disc diffusion technique according to the recommendations of National Committee of clinical laboratory standard (1990) Antibiotic discs used: Oxacillin, Bacitacin, Ampicillin, Amoxycillin, Amoxacillin-clavulanic acid, Erythromycin, Dalacin,-Cefpodoxim-and Sulphamethoxazoletrimethoprim. Reading of the plates was done according to WHO (2002) by measuring the size of inhibition zone in mm. F) Statistical Analysis: Statistical analysis of the results was carried out using SPSS (statistical package for social science), version 8. The following were done: Chisquare test, kappa (agreement test), sensitivity, and specificity using standardized formula. Level of significance is considered < 0.05.

RESULTS
On comparing the culture results of throat swab and tonsil core regarding the type of isolated organisms, core culture revealed pathogenic organisms in 81.5% (22 cases) of the studied cases while throat swab detected pathogenic organisms in 44.4%(12 cases). Throat swab revealed growth of normal flora only in 55.6% (15 cases) of cases versus 18.5% (5 cases) in tonsil cores Both tonsil surface and core culture yielded commensal growth in three cases. Table (1) compares between throat swab and tonsil core as regards similarity in detected pathogens. It revealed that out of 24 patients yielding pathogens, 7 cases (29.2%) had the same pathogens in both throat swab and tonsil core cultures, 2 cases (8.3%) had same the pathogens in addition to different pathogen in the tonsil core culture, only one case (4.2%) had different pathogens in both cultures, 12 cases (50%) had pathogens in tonsil core culture with no pathogens in the corresponding throat swab culture. No cases revealed additional pathogens in throat swab culture and 2 cases (8.3%) revealed pathogenic growth in the throat swab with no pathogens in tonsil core. No agreement between the results of throat swab and tonsillar core culture was detected by kappa test (P = 0.2). Table (1): Comparison between throat swab and tonsil core as regards similarity in detected pathogens: Throat Swab Tonsil Core No of patient % Same Path. Same Path. 7 29.2 Same path. Same Path + Diff. path 2 8.3 Diff. path Different path 1 4.2 Diff. Path.+ Same path Same path Pathogen No path. 2 8.3 No path. Pathogen 12 50.0 Total 24 100 Kappa = (0.21) P (0.2) Sensitivity = (38.9%) Specificity = (33.3%) Positive predictive value = (63.6)

Table (2): Organisms isolated from throat swab and tonsil core:. Throat Throat swab& Tonsil core swab Organism and tonsil core only only No No No Pathogenic: 2 9 10 Staph aureus 1 4 .hemolytic strept.(A) 1 E.coli 1 Klebsiella pneumoniae Commensals: 4 13 3 Neisseria catarrhalis 6 6 2 Viridans strepococci. 2 Stept. pneumoniae 2 Coagulase negative staphylococci 1 Lactobacillus 1 Micrococcus 1 Diphetheroid

Cases yielding that organism No 21 5 1 1 20 14 2 2 1 1 1 % 77.7% 18.5% 3.7% 3.7% 74.1% 51.8% 7.4% 7.4% 3.7% 3.7% 3.7%

Table (2) revealed the organisms isolated from the tonsil surface swabs and core specimens, Regarding pathogens Staphylococcus aureus was the most commonly grown organism in the core of the tonsils and/or surface culture (21 patients out of 27(77.7%)), 2 in throat swab only, 10 in tonsil core only and 9 in both throat swab and tonsil core, Group A hemolytic streptococci was isolated from 5 patients (18.5%), one case yielded the organism in throat swab and 4 in the tonsil core, E.coli was detected in tonsil core of one patient (3.7%), and Klebsiella pneumoniae was detected in both throat swab and tonsil core of only one patient (3.7%).Regarding commensals Neisseria catarrhalis was isolated from 20 cases (74.1%), 4 cases yielded Neisseria in throat swab, 13 in both throat swab and tonsillar core and 3 in tonsillar core only. Viridans streptococci was isolated from 14 cases, 6 revealed the organism in throat swab, 6 from both throat swab and tonsil core and 2 from tonsil core only. Strept pneumoniae, coagulase negative Staphylococci and lactobacillus were isolated from 2 (7.4%), 2 (7.4%) and 1 (3.7%) of patients respectively. One case (3.7%) yielded Micrococcus in throat swab only and one case yielded Diphetheroid in both throat swab and tonsil core.

Table (3): Antibiotic sensitivity results of pathogenic isolates in the current study Group A Gram negative Staph. aureus hemolytic bacilli N=21 streptococci N=2 N=5 S I R S I R S I R Oxacillin 12 2 7 Ampicillin 1 2 18 5 2 Erythromycin 2 17 2 1 4 Amoxycillin 4 2 15 1 4 2 Amoxacillin clavulanic acid 4 17 1 1 3 2 -

Cefpodoxim Dalacin Sulphamethoxazole-Trimethoprim S= Sensitive I= Intermediate

8 4 7

2 6 1

11 1 11 13 2 R= Resistant

4 5 3

2 2

2 -

Table (3) shows antibiotic sensitivity results of the isolated strains. Regarding Staph. aureus; 14 out of 21 isolates were Methicillin sensitive and 7 were Methicillin resistant. Eight strains were sensitive to Cefpodoxim and 4 strains were sensitive to Dalacin Most isolated Staph aureus strains were resistant to Ampicillin (18 out of 21) followed by Amoxacillin Clavulanic Acid (17 out of 21) and Trimethoprimsulfamethoxazole (13 out of 21). Regarding Group A hemolytic Streptococci strains; only one strain was sensitive to Amoxycillin-clavulanic acid (20%) while all are resistant to Dalacin and Ampicillin (100%) followed by Erythromycin, Amoxycillin and Cefpodoxim (80%). The two Gram negative isolates were sensitive to Cefpodoxim, and Trimethoprim sulphamethoxazol and resistant to Amoxycillin-clavulanic acid, Amoxycillin, Dalacin and Ampicillin. The results of blood culture obtained during tonsillectomy revealed that the incidence of bacteraemia was 7.4% (2 cases out of 27). Both cases yielded Staph aureus.

DISCUSSION
Chronic tonsillitis is the commonest disease occurring in younger age group (Wiatrak and Woolley, 1998). It is due to chronic inflammation within the tonsils because of insufficient penetration of antibiotics into the core or inappropriate antibiotic therapy (Kurien et al., 2000). If the surface culture was representative of the bacteriology of the core then rational therapy could be directed at organisms cultured by surface swab. This study was done primarily to compare between throat swab and tonsil core culture results in chronic tonsillitis. Pathogens were detected in 44.4%in throat swabs versus 81.5% in tonsil cores. These results were near to those of Kurien et al. (2000) which revealed pathogens in 55% of throat swabs and in 72.5% of core culture. Organisms isolated from the tonsil surface in the current study did not always correspond with the organisms isolated from the deep tissue specimens. While the surface cultures commonly showed entirely normal flora, the tonsil core cultures yielded pathogenic microorganisms. In this study one case showed a pathogen in the surface and different pathogen in the core. This was in agreement with Surow et al. (1989) who noted that a small group of patients showed pathogen on the surface and a different pathogen in the core. On statistical analysis of surface swab and core culture results for similar organisms, throat swab was found to have 38.9% Sensitivity, 33.3% specificity and 63.6% positive predictive value in diagnosis of chronic tonsillitis Kurien et al. (2000) noted higher sensitivity and specificity for throat swab than that recorded in the current study being 42%and 50% respectively. The current study results show non reliability of the throat swab in diagnosis of chronic bacterial infection of the tonsils. This was in agreement with Kurien et al. (2000), Abbas et al (1997) and Timon et al. (1991) who noted that throat swab is neither a reliable nor valid diagnostic test for representing the growth of the same bacterial flora as the tonsil core.

However Almadori et al, (1988) did not agree that there is discrepancy between surface and core cultures. They relied on the assumption that there is a certain degree of homogeneity in the bacterial flora of the tonsils so sampling of any single area may be reflective of the entire tonsil. Microbiological study of both surface and core of the tonsils in the current study revealed that Staph aureus was the commonest isolate This was in agreement with the finding of Surow et al. (1989), Endo et al. (1996), Abbas et al., (1997) and Yildirim et al., (2003) Mitchelmore et al. (1994) noted that Staph. aureus could be a direct pathogen or indirect pathogens by releasing -lactamase protecting susceptible pathogens from the effect of lactam antibiotics. Out of the 21 Staph. aureus isolates in the current study, 7 were methicillin resistant. Community acquired methicillin resistant Staph. aureus (MRSA) were reported in many studies (Gorak et al., 1999). Risk factors for community acquired MRSA infection include age more than 1 year and prior antimicrobial use (Morino et al. 1995, Layton et al. 1995 and Marcinak and Frank, 2003) All patients in the current study were above 1 year old and gave a history of antibiotic intake for many courses. Gorak et al. (1999) also demonstrated community acquired MRSA infection in previously healthy young children without known risk factors for MRSA. Group A hemolytic streptococci was the second most frequent organism encountered in the current study. This was in agreement with Yildirim et al. (2003) and Surow et al. (1989). Abbas et al (1997) stated that the incidence of hemolytic Streptococus as the organism responsible for chronic tonsillitis is steadily decreasing over years, whereas that of Staphylococcus aureus is on gradual increase. However several studies noted that Group A hemolytic streptococci was the commonest organism isolated from tonsils (Kurien et al., 2000). E-coli and Klebsiella species were isolated in low percent in the current study. Several studies isolated enterobacteriaceae from the surface or the core of tonsils (Abbas et al, 1997, Kurien et al., 2000 and Brook and Kiran 2001). The problem of bacterial resistance to commonly used antibiotics was apparent among Gram positive isolates of the current study The problem of bacterial resistance to commonly used antibiotics is world wide and individual institutions need constant monitoring of their isolates and perhaps establishment of some from of regulatory measures to combat it. Farid and Saffar (2000) and Stein et al. (2003) noted that decrease resistance rates to antibiotics could be achieved through judicious antibiotic use. Arason et al. (1996) and Trepeka et al. (2001) noted that not only regional trends in antibiotic resistance have been linked to antibiotic use but decreasing antibiotic use has resulted in declining levels of resistance. Other approaches to decrease resistance are to rotate antibiotics used for empiric therapy and use combinations of drugs from different classes (David and Bowton, 1999). We cant comment on Gram negative isolates resistance because the current study detected only 2 Gram negative strains. Tonsillectomy in children remains a very common procedure performed for a variety of indications including recurrent tonsillitis (Surow et al., 1989). One of the known complications in tonsillectomy is bacteraemia (Blumerthol, 1997). The incidence of bacteraemia in the present study was 7.4% (2/27).

Anand et al. (1999) and Yildirim et al. (2003) noted a higher incidence of bacteraemia in their studies being 27.3% and 22% respectively. Several theories tried to explain the cause of bacteraemia during tonsillectomy. Yildirim et al (2003) noted that during tonsillectomy the oropharyngeal mucosa is torn with the resultant fresh wound in a field full of bacteria and rich in vascular supply. They noted that any surgical procedure in such a heavily colonized site and tissue such as tonsils may lead to bacteraemia by the venous rout However it has been noted that the incidence of bacteraemia is close to zero during septoplasty and rhinoplasty and it rarely occurs during endoscopic sinus surgery although there is bacterial colonization in these sites as well (Silk et al, 1991 and Slavin et al, 1983) Yildirim et al. (2003) and Icacson and Parke (1996) concluded that the occurrence of bacteraemia is not related to the presence of colonization in the operative site. Bacteraemia may be related to the traction and handling by forceps of the tonsils before or during dissection, application of gauze tamponade or suture ligation for treatment of hemorrhage during the operation or over pressure to tonsillar fossa with suction rather than direct spread of bacteria into the exposed and traumatized vessels. Walsh et al, (1997) noted that the incidence of bacteraemia depends upon the type of tonsillectomy operation. They noted that bacteraemia rate following guillotine tonsillectomy is lower than that following dissection tonsillectomy due to intraoperative compression of tonsillar blood vessels by the guillotine. Patients in the current study underwent guillotine tonsillectomy Nosocomial infections might be a frequent cause of bacteraemia after tonsillectomy (Yildirim et al, 2003). Anand et al. (1999) and Yildirim et al. (2003) noted that blood culture findings after tonsillectomy didnt always correlate with the bacteriology of tonsillar surface or core. The 2 bacteraemic cases in the current study revealed Staph aureus. Staph aureus was also isolated from tonsils of these 2 patients but we didnt do strain typing Yildirim et al, (2003) noted that Staph aureus is an important pathogen in nosocomial infections. They added that Staph aureus is a frequent cause of bacteraemia in post operative patients. None of the two patients yielding positive blood culture patients included in the current study develop any postoperative complications. Yildirim et al, (2003) noted that transient bacteraemia is generally harmless in healthy subjects and resolve spontaneously without complications however it might lead to dramatic results in patients carrying a high risk of cardiovascular infection. Also any weakness or failure of the host defense mechanism due to leukemia, acquired immune deficiency syndrome or immunosuppressive treatments may increase the risk of bacteraemia causing systemic illness. They added that prophylactic antibiotic intake should be restricted to this high risk group of patients However Olina et al (2001) suggested that antibiotic prophylaxis before tonsillectomy is necessary In conclusion, the role of throat swab in management of chronic tosillitis is doubtful. Staph aureus was the commonest isolate from the surface or core of tonsils. The problem of bacterial resistance to commonly used antibiotics is apparent among the study population Post-tonsillectomy bacteraemia occurs in low percent of patients. Further studies are needed to assess the possibility of using fine needle aspiration technique as a diagnostic test in chronic tonsillitis patients, determine the magnitude of antibiotic resistance problem in Egypt and study the role of preoperative antibiotic intake in the incidence and course of post-tonsillectomy bacteraemia

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