International Journal of Pediatric Otorhinolaryngology 77 (2013) 817–820
Contents lists available at SciVerse ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Microbiology and antimicrobial treatment of pediatric cervical lymphadenitis requiring surgical intervention Laura Neff a, Jason G. Newland b,d,**, Kevin J. Sykes a, Rangaraj Selvarangan c,d, Julie L. Wei a,e,* a
Department of Otolaryngology-Head and Neck Surgery, University of Kansas Medical Center, Kansas City, KS, United States Section of Infectious Diseases, Children’s Mercy Hospitals and Clinics, Kansas City, MO, United States c Department of Pathology and Laboratory Medicine, Children’s Mercy Hospitals and Clinics, Kansas City, MO, United States d University of Missouri-Kansas City School of Medicine, Kansas City, MO, United States e Section of Otolaryngology-Head and Neck Surgery, Children’s Mercy Hospitals and Clinics, Kansas City, MO, United States b
A R T I C L E I N F O
A B S T R A C T
Article history: Received 8 January 2013 Received in revised form 9 February 2013 Accepted 12 February 2013 Available online 24 March 2013
Background: Acute cervical lymphadenitis is a common condition often times requiring antibiotic therapy and possible surgical drainage. The objective of this study was to describe the clinical characteristics, diagnostic and therapeutic management of children requiring surgical drainage for acute cervical lymphadenitis. Methods: A retrospective, descriptive study was performed at a Midwestern US tertiary-care children’s hospital on all immunocompetent children who underwent an incision and drainage procedure of cervical lymphadenitis from January 1999 to July 2009. Results: A total of 277 patients were identified. Males represented 51% and the median age was 28 months (IQR: 13–59). Lymphadenitis was unilateral in 243 (87.7%) cases and bilateral in 19 (6.9%). Median length of hospital stay was 4 days (IQR: 3–5). Aerobic, anaerobic, acid fast bacillus (AFB), and fungal cultures were obtained intraoperatively in 99%, 98%, 82%, and 78% of cases, respectively. However no fungal cultures were positive and only 1% of anaerobic and 2% of AFB cultures were positive. The most common bacterial etiology was Staphylococcus aureus (35.7%) and Streptococcus pyogenes (18.8%). Of all cultures, 32% were negative. Overall, 22% were positive for methicillin susceptible S. aureus (MSSA) and 13.7% for methicillin resistant S. aureus (MRSA), with 96% MSSA and 100% MRSA susceptible to clindamycin. Median duration of discharge antibiotics prescribed was 10 days (IQR: 7–11). Only 12 (4.5%) patients required a repeat incision and drainage within 3 months. Conclusions: A single antibiotic that treats S. pyogenes and S. aureus should be the empiric antibiotic for cervical lymphadenitis requiring incision and drain. We recommend sending only aerobic cultures intraoperatively as a routine practice as other pathogens are rare. ß 2013 Elsevier Ireland Ltd. All rights reserved.
Keywords: Neck abscess Cervical lymphadenitis Incision and drainage MRSA
1. Introduction Cervical lymphadenitis is a common pediatric infection that often requires both medical and surgical management. Studies have found that the most common bacterial causes include Staphylococcus aureus and Streptococcus pyogenes, representing 40– 80% of cases [1–4]. Additionally, methicillin resistant S. aureus
* Corresponding author at: Department of Otolaryngology-Head and Neck Surgery, University of Kansas Medical Center, 3901 Rainbow Boulevard, Mail Stop 3010, Kansas City, KS 66160, United States. Tel.: +1 913 588 6754; fax: +1 913 588 6708. ** Co-corresponding author at: Section of Infectious Diseases, Children’s Mercy Hospital and Clinics, 2401 Gillham Road, Kansas City, MO 64108, United States. Tel.: +1 816 234 3061; fax: +1 816 346 1328. E-mail addresses:
[email protected] (J.G. Newland),
[email protected] (J.L. Wei). 0165-5876/$ – see front matter ß 2013 Elsevier Ireland Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijporl.2013.02.018
(MRSA) has been found to comprise almost 30% of all S. aureus isolated in pediatric neck infections [5,6]. Other bacterial causes include nontuberculous mycobacteria, Streptococcus agalactiae, Mycobacterium tuberculosis, Bartonella henselae and Francisella tularensis. Anaerobic bacteria are rare and are associated with dental caries and periodontal disease [7,8]. Due to this broad differential of pathogens, many surgeons request aerobic, anaerobic, fungal and acid fast bacillus cultures to be performed. No study has evaluated the epidemiology of cervical lymphadenitis and its impact on microbiological culture data. The emergence of MRSA in children over the past decade has led to significant changes in the use of antibiotics. Herigon et al. observed a 42% increase in clindamycin use from 1999 to 2009 [9]. In our own institution, clindamycin resistant S. aureus has increased from approximately 12% to almost 20% among all isolates. Recent guidelines on the treatment of MRSA published by the Infectious Diseases Society of America (IDSA) recommends that
818
L. Neff et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 817–820
clindamycin no longer be used as empiric therapy when the overall clindamycin resistant rate is greater than 10% [10]. Alternatives to this agent, vancomycin and linezolid, are also not ideal due to their broad-spectrum coverage, potential for adverse reactions, difficulties in administration, and cost. However, it is unclear whether or not the use of clindamycin might still be effective as empiric therapy for children with suppurative cervical lymphadenitis. The objectives of this study were to: (1) describe the diagnostic and treatment strategies of culture confirmed suppurative cervical lymphadenitis in children and (2) evaluate the identification and susceptibility profile of the causative bacteria to help determine the most appropriate empiric therapy for these patients. 2. Methods 2.1. Study design We performed a retrospective review of patients 18 years or younger with the diagnosis of cervical lymphadenitis seen by pediatric otolaryngology from January 1999 to July 2009. Children included in the study had to have all of the following: (1) underwent surgical incision and drainage; (2) had intraoperative cultures performed; and (3) were admitted to the regional tertiary children’s hospital, Children’s Mercy Hospitals and Clinics. We excluded patients with cystic fibrosis, were immunocompromised by medication or underlying condition, and those who underwent excisional biopsy for lymphadenopathy that were not acute cervical lymphadenitis. The study was approved by both the University of Kansas Medical Center Institutional Review Board and the Children’s Mercy Hospital and Clinics Institutional Review Board. Data was abstracted from the medical record utilizing a standardized data collection form. Data elements obtained included patient demographics, presenting history and physical exam, antibiotic use prior to admission, time to surgical intervention, microbiology and susceptibility results from all cultures, inpatient antibiotics used and discharge antibiotics. All data was entered into a password-protected Microsoft Access database. 2.2. Data analysis Data were collected in a Microsoft Access database. Statistical analysis was performed with SPSS, version 17.0 (SPSS Inc., Chicago, IL, USA). Demographics and other categorical variables are summarized by frequencies and percents. Quantitative variables are summarized by medians and distribution statistics. 3. Results A total of 277 patients were included in this study. Gender distribution was nearly equal with 51% males. Patient characteristics are presented in Table 1. Most common presenting symptoms included neck mass (86%), pain (86%), and fever (61%). Approximately 67% of patients had already been prescribed and taking an oral systemic antibiotic prior to admission, with over 50% of the antibiotics prescribed being amoxicillin or amoxicillin/ clavunate. The median age at time of incision and drainage (I&D) was 28 months (IQR: 13–59). Approximately half of the patients received surgical intervention within 24 h of admission while the other half underwent I&D more than 24 h after admission. Computed tomography (CT) of the neck with contrast was ordered by our Emergency Department or upon admission in 76% (n = 209) of cases, and mean abscess size on CT scan was 26.6 mm (SD = 11.9). Ring enhancement was reported in 59.8% (n = 125) of cases. Intraoperatively, frank purulence was identified in 85% (n = of
Table 1 Patient characteristics.
Gender Female Male Racea Asian/Pacific Islander Black Other White Imaging CT scan performed Ring enhancement Time to surgeryb <12 h 12–24 h >24 h
Age at surgical intervention (months) CT abscess size (mm) a b
n
%
137 140
49 51
7 56 36 174
3 21 13 64
209 125
76 60
54 67 123
22.1 27.5 50.4
Mean
Std. dev.
Median
43.6 26
43.8 12.3
28 24
Data was missing in 4 patients. Unable to reliably determine time to surgery in 33 patients.
cases). An additional 14% of cases did not have purulence, but had either necrotic debris or phlegmon at the time of surgical intervention. Median length of hospital stay was 4 days (IQR: 3– 5). Only 12 of 265 (4.5%) patients required a repeat I&D within three months. A summary of microbiology and susceptibility of all identifiable bacteria is presented in Table 2. Culture data was not available in 2 patients. Aerobic, anaerobic, fungal, and AFB cultures were ordered and sent intra-operatively in 100%, 98%, 79%, and 82% of cases respectively. The most common bacteria isolated from intraoperative cultures were S. aureus (99/275) and S. pyogenes (52/ 275). There were 61 (22%) cases of methicillin susceptible S. aureus (MSSA) and 38 (14%) cases of methicillin resistant S. aureus (MRSA). Among the surgical cultures that were positive for MRSA or MSSA, 100% and 96% were susceptible to clindamycin, respectively (Table 2). Both MSSA and MRSA were 100% susceptible to trimethoprim/sulfamethoxazole. Other bacterial pathogens isolated on culture included atypical mycobacteria (n = 7), anaerobic (n = 4), Gram negative bacillus (n = 4) and Francisella tularensis (n = 1). No fungal cultures were positive in this study. Of the 75 patients in whom there was documentation of testing for S. pyogenes upon admission, 30 were positive (24 by rapid antigen test, 6 by positive cultures). Admission antibiotics were identified in 203 patients. Of those, 121 (60%) patients were started on intravenous clindamycin, while 44 (22%) were started on both intravenous clindamycin and
Table 2 Microbiology and susceptibility (N = 183). Organisms
n (%)
Staphylococcus aureus Methicillin Sensitive (MSSA) Clindamycin sensitive Trimethoprim/Sulfamethoxasole Methicillin Resistant (MRSA) Clindamycin sensitive Trimethoprim/Sulfamethoxasole
99 (36) 61 (22) 53/55 (96) 55/55 (100) 38 (14) 38/38 (100) 36/38 (95)
Streptococcus pyogenes Nontuberculous mycobacteria Gram negative bacillus Anaerobes Francisella tularensis Other
52 (19) 7 (3) 4 (2) 4 (2) 1 (0.4) 16 (6)
L. Neff et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 817–820
ceftriaxone. Other antibiotics used in the treatment of these children included oxacillin, rifampin, ampicillin, vancomycin, or ticarcillin/clavulanic acid. Upon discharge, 185 (67%) children were identified to be receiving oral systemic therapy. Clindamycin alone was the most commonly prescribed (113.61%), followed by amoxicillin/clavulanate (36, 20%), cephalosporins or macrolide (28.15%), and 7 were prescribed oral clindamycin plus another antibiotic of a different class. Median duration of discharge antibiotics was 10 days (IQR: 7–11).
819
Table 3 Cost per culture in US dollars. Culture type
Cost per culture
Estimated costs for entire group
Aerobic Anaerobic Acid fast bacillus Fungal
$98.00 $108.00 $100.00 $96.00
$14,798.00 $29,700.00a $27,300.00a $25,920.00a
Total
$402.00 (per patient)
$109,870.00
a
Potentially avoidable costs for the study group if cultures were not obtained.
4. Discussion In this study we summarize the microbiology, susceptibility, and antibiotic prescribing patterns in immunocompetent children diagnosed with suppurative cervical lymphadenitis requiring surgical intervention. We observed a large proportion of children receiving CT scans. Additionally, a significant amount of variability in admission and discharge antibiotic use was identified. Furthermore many unnecessary microbiological cultures are obtained in these children. This data demonstrates a need to develop guidelines for the diagnostic workup and treatment of children with suppurative cervical lymphadenitis. Presentation of neck infection was unilateral in the majority of cases (87.7%) and rarely bilateral (6.9%). We did not record the exact location of the infection, which may be of interest if the focus was on lymphadenitis due to atypical mycobacterial infections. CT scans were performed in the majority (76%) of the children in this study. Ring enhancement was noted in 60% of CT scans while frank purulence was reported in over 85% of cases, demonstrating that ring enhancement is not a sensitive predictor of presence of purulence and should not influence the decision for surgical intervention. Since the completion of this study we have collaborated with our Emergency Department colleagues to minimize the use of CT scans for cases of uncomplicated suppurative lymphadenitis in compliance with the Image Gently Campaign and the American College of Radiology Appropriateness Criteria Recommendation guidelines [11,12]. We support the use of ultrasound as the diagnostic test of choice in the evaluation of children who have a single neck mass and are febrile, suggestive of acute suppurative cervical lymphadenitis when determining candidacy for surgical intervention. Several studies have demonstrated the efficacy of ultrasound in the management of cervical lymphadenitis in children in regards to examining the involvement, size, characteristics, and location of the lymph node without the radiation exposure associated with a CT scan [13,14]. Most surgeons sent all four types of cultures at the time of surgical incision and drainage; aerobic, anaerobic, fungal, and acid fast bacilli (AFB). However, almost all of the positive cultures were from aerobic cultures and only 2% of the anaerobic cultures were positive. While 80% of cases had fungal cultures ordered, no positive fungal cultures were identified. Finally, only 7 cases of AFB were isolated among the 80% that had an AFB culture performed. The costs of cultures at Children’s Mercy for aerobic, anaerobic, fungal, and AFB cultures are 98.00, 108.00, 102.00, and 96.00, in US dollars respectively (Table 3). Eliminating anaerobic and fungal cultures would have produced a savings of $47,422.00 in US dollars for the patients in this study alone. There are little negative cost implications of missing a positive anaerobic culture since in this series, anaerobic cultures were positive in only 4 cases (1.4%), as was Gram negative (4 cases, 1.4%). In our experience, clindamycin is generally the antibiotic of choice upon discharge from the hospital which provides anaerobic coverage. In this series, missing a positive anaerobic culture would have little cost implication since there were only 4 cases of anaerobic culture positive infections (1.4%). We found only 4 cases (1.4%) of Gram negative suppurative lymphadenitis in this series. Finally, we found no
complications from refractory infections requiring further surgical and medical intervention. Nontuberculous mycobacteria are another etiology in children with cervical adenitis. Acid fast bacillus cultures were sent in 82% of the cases and only 7 were positive. AFB testing costs approximately $100 per patient for culture ($42.00) and stain ($58.00) and resulted in patient charges of $22,714.00. Atypical mycobacterial infections generally have a subacute presentation and history, and violaceous skin appearance with predilection for submandibular or preauricular location [15]. Most cases may be suspected prior to surgical intervention. Furthermore, intraoperatively there is usually distinction in the affected node compared to typical purulence encountered in an abscess. We believe a more cost-effective approach would be to obtain AFB cultures only when there is high index of suspicions and not on every routine surgical intervention for neck abscess. The common bacterial causes of suppurative lymphadenopathy in this study were: MSSA (22%), S. pyogenes (19%), and MRSA (14%). These findings are consistent with the previous studies, which quote 40–80% of acute bacterial lymphadenitis to be caused by S. aureus and S. pyogenes [1,5,6]. Recent studies in head and neck infections have noted that MRSA has emerged as an important bacterial pathogen in these infections [5,6]. No growth was noted on 32% of the aerobic cultures, which may be attributed to 68% of patients having been on systemic antibiotics prior to admission. We found that at the time of admission for uncomplicated cervical lymphadenitis, many patients were started on two intravenous antibiotics, clindamycin plus ceftriaxone. Based on this study’s findings a single antimicrobial agent that treats S. aureus and S. pyogenes should be sufficient for treating suppurative lymphadenitis in immunocompetent patients. In our institution with an MRSA rate among all S. aureus isolates being over 50%, clindamycin has become the empiric antibiotic used in these children. However, recent local data has demonstrated a clindamycin resistance rates to all S. aureus approaching 20% (Newland et al., 2012, unpublished data). The MRSA guidelines from IDSA suggest that when the clindamycin resistance rate is greater than 10%, this antibiotic should not be used empirically [10]. When examining the clindamycin resistance rates of our isolates none of the MRSAs isolated were resistant and only 2 (4%) of the MSSAs were resistant. This is in contrast to our recently published study in post-tympanostomy tube otorrhea in which 67% of MRSA identified were clindamycin resistant [16]. The treatment length on discharge was on average 11 days. It remains unclear what the correct length of therapy should be for these children. Experts have called for more studies evaluating lengths of therapy to be conducted to help limit the rate of increasing antibiotic resistance [17]. In the era of emerging antimicrobial resistance, common infections such as cervical adenitis should be studied to help identify the optimal duration of therapy that leads to the best outcomes with minimal impact on bacterial resistance.
820
L. Neff et al. / International Journal of Pediatric Otorhinolaryngology 77 (2013) 817–820
This study has limitations. This is a retrospective review and therefore, we were unable to obtain important clinical and antibiotic use data in all patients. However, we believe that the variability in the antibiotic prescribing observed in the patients identified would likely not have impacted our findings significantly. Additionally, this study was performed at a single center and therefore may not be generalizable. Importantly, studies have shown that variability in susceptibilities among S. aureus can vary by geographic region [18]. As all the patients reviewed in this study were cervical lymphadenitis which required surgical intervention, we acknowledge the potential bias in selecting a group of children in whom systemic antibiotics alone was not sufficient in treating the infection. It is not possible to speculate whether these patients had infections of a greater severity or from more strains of organisms resistant to routine antimicrobial treatments. 5. Conclusion A single, empiric antibiotic with activity against S. aureus and S. pyogenes should be administered for immunocompetent children with suppurative cervical lymphadenitis. Furthermore, based on our microbiology findings, we recommend sending only aerobic cultures intraoperatively, with AFB cultures ordered based on high clinical suspicion. Implementing these changes will result in cost saving for the facility and the patients, as well as, avoid overutilization of resources for unnecessary antibiotics and microbiology cultures. Funding None of the authors have financial disclosures. Conflicts of interest None of the authors have conflicts of interests in regards to this work.
References [1] L.L. Barton, R.D. Feigin, Childhood cervical lymphadenitis: a reappraisal, J. Pediatr. 84 (1974) 846–852. [2] A.S. Dajani, R.E. Garcia, E. Wolinsky, Etiology of cervical lymphadenitis in children, N. Engl. J. Med. 268 (1963) 1329–1333. [3] W.G. Scobie, Acute suppurative adenitis in children: a review of 964 cases, Scott. Med. J. 14 (1969) 352–354. [4] T. Yamauchi, P. Ferrieri, B.F. Anthony, The aetiology of acute cervical adenitis in children: serological and bacteriological studies, J. Med. Microbiol. 13 (1980) 37–43. [5] J.C. Inman, M. Rowe, M. Ghostine, T. Fleck, Pediatric neck abscesses: changing organisms and empiric therapies, Laryngoscope 118 (2008) 2111–2114. [6] J. Guss, K. Kazahaya, Antibiotic-resistant Staphylococcus aureus in community-acquired pediatric neck abscesses, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 943–948. [7] J.R. Gosche, L. Vick, Acute, subacute, and chronic cervical lymphadenitis in children, Semin. Pediatr. Surg. 15 (2006) 99–106. [8] A.K. Leung, W.L. Robson, Childhood cervical lymphadenopathy, J. Pediatr. Health Care 18 (2004) 3–7. [9] J.C. Herigon, A.L. Hersh, J.S. Gerber, T.E. Zaoutis, J.G. Newland, Antibiotic management of Staphylococcus aureus infections in US children’s hospitals, 1999–2008, Pediatrics 125 (2010) e1294–e1300. [10] C. Liu, The bundled approach to MRSA surgical site infection prevention: is the whole greater than the sum of its parts? Comment on ‘‘Sustained reduction in methicillin-resistant Staphylococcus aureus wound infections after cardiothoracic surgery’’, Arch. Intern. Med. 171 (2011) 73–74. [11] M. Sidhu, M.J. Goske, B. Connolly, J. Racadio, T.T. Yoshizumi, K.J. Strauss, et al., Image gently, step lightly: promoting radiation safety in pediatric interventional radiology, Am. J. Roentgenol. 195 (2010) W299–W301. [12] K.J. Strauss, M.J. Goske, S.C. Kaste, D. Bulas, D.P. Frush, P. Butler, et al., Image gently: ten steps you can take to optimize image quality and lower CT dose for pediatric patients, Am. J. Roentgenol. 194 (2010) 868–873. [13] M.F. Dulin, T.P. Kennard, L. Leach, R. Williams, Management of cervical lymphadenitis in children, Am. Fam. Physician 78 (2008) 1097–1098. [14] G. Niedzielska, M. Kotowski, A. Niedzielski, E. Dybiec, P. Wieczorek, Cervical lymphadenopathy in children – incidence and diagnostic management, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 51–56. [15] R. Penn, M.K. Steehler, A. Sokohl, E.H. Harley, Nontuberculous mycobacterial cervicofacial lymphadenitis – a review and proposed classification system, Int. J. Pediatr. Otorhinolaryngol. 75 (2011) 1599–1603. [16] I. Fishman, K.J. Sykes, R. Horvat, R. Selvarangan, J. Newland, J.L. Wei, Demographics and microbiology of otorrhea through patent tubes failing ototopical and/or oral antibiotic therapy, Otolaryngol. Head Neck Surg. 145 (2011) 1025–1029. [17] L.B. Rice, The Maxwell Finland Lecture: for the duration-rational antibiotic administration in an era of antimicrobial resistance and Clostridium difficile, Clin. Infect. Dis. 46 (2008) 491–496. [18] P.C. Schreckenberger, E. Ilendo, K.L. Ristow, Incidence of constitutive and inducible clindamycin resistance in Staphylococcus aureus and coagulase-negative staphylococci in a community and a tertiary care hospital, J. Clin. Microbiol. 42 (2004) 2777–2779.