Indian J Pediatr DOI 10.1007/s12098-015-1771-x
CLINICAL BRIEF
Is Sinusitis Innocent?– Unilateral Subdural Empyema in an Immunocompetent Child Sevim Şahin 1 & Uğur Yazar 2 & Ali Cansu 1 & Sibel Kul 3 & Selçuk Kaya 4 & Elif Bahat Özdoğan 5
Received: 8 December 2014 / Accepted: 9 April 2015 # Dr. K C Chaudhuri Foundation 2015
Abstract Subdural empyema related to Streptococcus constellatus is extremely rare in an immunocompetent child, and also there is no reported case along with Staphylococcus lugdunensis infection. Although Streptococcus constellatus has been determined as a co-pathogen with anerobic bacteria in many infections, it has not been reported in combination with Staphylococcus lugdunensis. The authors describe a case of previously healthy 16-y-old child with unilateral subdural empyema due to these bacteria. Sinusitis was the only predisposing factor in the index case. The authors propose that some cases of culture-negative intracranial infections may be due to these infectious agents. Therefore, these agents should be considered as causes of intracranial infection in persistent complaints such as fever and headache after sinusitis in children. It is important to treat them with effective antibiotics and early surgical intervention for favorable outcome, because fatal cases were reported due to Streptococcus constellatus infections.
* Sevim Şahin [email protected] 1
Department of Pediatric Neurology, School of Medicine, Karadeniz Technical University, 61000 Trabzon, Turkey
2
Department of Neurosurgery, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
3
Department of Radiology, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
4
Department of Infectious Diseases and Clinical Microbiology, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
5
Department of Pediatrics, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
Keywords Streptococcus constellatus . Staphylococcus lugdunensis . Subdural empyema . Child
Introduction Intracranial empyema, though rare in children is an emergency due to life-threatening complications [1]. Herein, the authors describe a previously healthy child with unilateral subdural empyema (SDE) related to Streptococcus constellatus and Staphylococcus lugdunensis. SDE associated with Streptococcus constellatus has been described in only one case [2] in the English literature, and there is no case associated with Staphylococcus lugdunensis, to the authors’ knowledge. Also, the presence of co-pathogens such as Streptococcus constellatus and its combination with Staphylococcus lugdunensis has not been previously reported. This case is presented to ensure consideration of these rare microorganisms as causes of SDE even in immunocompetent children.
Case Report A 16-y-old boy was referred to the Emergency department with complaints of projectile vomiting and lethargy for one day, headache for 3d, and fever for 2d. The headache was especially on the right side, and fever was up to 39 °C. He had been started oral antibiotic treatment 2d ago for sinusitis. His past medical and family history were unremarkable. The physical examination revealed somnolence and anisocoria. He had eye opening and localized motor response to pain, but no verbal response. Also, generalized tonic-clonic seizure were observed. In laboratory examination, his leukocyte count (12,100/mm3) and C-
Indian J Pediatr
reactive protein (20.62mg/dl) were increased. Brain magnetic resonance imaging (MRI) revealed SDE surrounding the right cerebral hemisphere (Fig. 1). There was compression of the ventricles, anterior displacement of the brain stem and subfalcine herniation on the left. Inflammatory changes were present in the maxillary sinus and ethmoid cells. Right frontoparietal craniotomy was performed, and subdural empyema was drained at the Neurosurgery department. Treatment with vancomycin (60mg/kg/d), ceftriaxone (100mg/kg/d) and metronidazole (30mg/kg/d) was initiated. Acyclovir treatment (30mg/kg/d) was added for probable herpes simplex virus (HSV) infection, and continued with positive results of HSV type 1 and type 2 immunoglobulin M (IgM) in the serum. Studies of the lymphocyte subgroups and immunoglobulins were normal. Streptococcus constellatus was isolated in the abscess material; it was sensitive to ceftriaxone. Postoperatively, Babinski’s sign and decrease in score of motor strength (3/5) on the left side were present. On day 5, although the patient remained stable clinically, subdural empyema enlarged in the interhemispheric fissure (Fig. 1). On day 17, brain MRI showed enlargement of SDE in the posterior interhemispheric fissure (Fig. 1).
Fig. 1 Axial images on brain MRI study of the case. T2 (1, 3) and T1-weighted (2, 4) images on admission (A), on the 5th day after surgical drainage (B), on day 17 prior to second surgical drainage (C) and 2 mo after the second surgery (D). (A) Subdural empyema surrounding the right cerebral hemisphere (arrow). Signal hypointensity on T1-weighted images (A2, A4) and signal hyperintensity on T2-weighted images (A1, A3) may be seen. There is light shift of midline structures to the left. (B) Subdural empyema in the interhemispheric fissure with signal hyperintensity on T2-weighted images (B1, B3) and signal hypointensity on T1weighted images (B2, B4). (C) Increase in the size of the empyema is more pronounced in the posterior of interhemispheric fissure. (D) Disappearance of subdural empyema
Subfalcine herniation of midline structures to the left and compression of the third and lateral ventricles were present. Therefore, surgical drainage was performed again, and considering penicillin sensitivity tests, antibiotic treatment was switched to high-dose ampicillin treatment (8g/d ampicillin-sulbactam in addition to ampicillin of 4g/d). Staphylococcus lugdunensis was isolated from the latter abscess material. In follow-up, hemiparesis of the patient improved gradually and SDE regressed completely (Fig. 1). Ampicillin treatment was completed in 2mo.
Discussion The only case of SDE associated with Streptococcus constellatus in the English literature is of a 7-y-old girl [2]. Unilateral SDE in that case showed fatal outcome [2]. Streptococcus constellatus is a commensal of oropharyngeal flora [3]. Infections with empyema related to Streptococcus constellatus are mostly present in the thoracal region. It causes purulent infections of pleuro-pulmonary, intra-abdominal, genitourinary, soft tissue and rarely central nervous system (CNS) [2, 3]. Streptococcus constellatus has been rarely
Number of patients with SDE
4
31
33
70 extraaxial (epidural and SDE)
23
Bair-Merritt et al., 2005 [7]
Wu et al., 2008 [8]
Legrand et al., 2009 [1]
Gupta et al., 2011 [9]
Cole et al., 2012 [10]
None
27 (38.6)
7 (21.2)
None
1 (25)
S. milleri group infections n (%) Streptococcus salivarius, Group A streptococcus, Group D streptococcus, Peptostreptococcus, Prevotella, Clostridium spp., nontypable Haemophilus influenzae, Alfa-hemolytic streptococcus, Beta-hemolytic streptococcus Streptococcus pneumoniae, Group B streptococcus, Methicillin-sensitive Staphylococcus aureus, Haemophilus influenzae type b, Salmonella spp., Escherichia coli, Pseudomonas aeruginosa, Haemophilus parainfluenzae, Enterobacter cloacae Anaerobes, Group B streptococcus, Streptococcus pneumoniae, Enterobacteriaceae, Staphylococcus aureus, P. aeruginosa, Haemophilus S. aureus, Streptococcus pneumoniae, other β-hemolytic streptococci spp, Haemophilus influenzae, other α-hemolytic streptococci spp, Escherichia coli, coagulase-negative Staphylococci spp, cryptogenic gram-negative bacilli spp. Pneumococcus, H. influenzae type B, Coagulase negative Staphylococcus, Lactobacillus, Abiotrophia adiacens, Enterobacter cloacae, Meningococcus, S. aureus
Other microorganisms
Comparison of various studies in pediatric patients with subdural empyema (SDE)
Author
Table 1
1 child died. Permanent neurological deficits in 3 children
• Bacterial meningitis in 10 infants • Sinusitis in 18 cases • Otitis in one case • Tonsillitis in one case • Sinusitis • Otitis • Meningitis • Previous neurosurgery • Spinal infections • Miscellaneous • Sinusitis in 12 cases • Meningitis in 6 cases • Neurosurgery in 2 cases
1 child with ventriculoperitoneal shunt died. 20% with neurological sequelae.
84.3% without neurological sequelae. Developmental delay, residual focal neurological deficit.
3 children died. 38.7% without neurological sequelae. 51.6% neurological deficit.
Seizures in the case of S. milleri group. Seizures, dysarthria expressive aphasia, hemiplegia.
Neurological outcome
Otorhinolaryngeal infections, head trauma or surgery.
Sinusitis
Identified etiology
Indian J Pediatr
Indian J Pediatr
reported with brain abscess [4], spinal epidural abscess [5] and meningitis [6] in adult patients. Sinusitis might have been the predisposing factor in the index case. No other predisposing factors, such as dental or oropharyngeal intervention, trauma, any surgical operation or immunodeficiency were detected. Sinusal infections have been reported as major predisposing factors for intracranial infections in immunocompetent children [7]. Streptococcus milleri group including Streptococcus constellatus has been reported as a cause of SDE. Its frequency varies in different studies (Table 1). Streptococcus intermedius in Streptococcus milleri group is the main microorganism that cause CNS infections, and a small proportion is caused by Streptococcus anginosus. Streptococcus constellatus is very rare in CNS infections [11]. Although there is no marked difference between the dates of the studies compared in Table 1, wide range of the rates of Streptococcus milleri group infections between 0 and 38.6% is remarkable. The most important reason for that is probably some studies focused on complications after sinusitis or may had difficulty in identifying these agents. Streptococcus milleri group and anerobic bacteria are the most common pathogens in suppurative intracranial complications after sinusitis in previously healthy children [7]. Probably all the infections of Streptococcus milleri group cannot be detected. In a study, Streptococcus milleri group was detected in three cases with culture-negative brain abscess by 16S rRNA gene amplification and sequencing methods [12]. Staphylococcus lugdunensis, another agent in the index case, is a coagulase negative staphylococcus and causes skin and soft tissue infections. Severe infections such as endocarditis, septic shock, peritonitis, osteomyelitis, spondylodiscitis, septic arthritis, epidural abscess, brain abscess and infection of prosthetic devices have also been reported [13]. The present case indicates that Streptococcus constellatus and Staphylococcus lugdunensis may cause SDE even in immunocompetent children. CNS infections should be considered in cases of increasing symptoms after sinusitis. High dose antibiotic treatment is necessary to provide penetration into the abscess [2]. These infections, although probability of fatal outcome, can be treated with early surgical intervention, close neuroimaging and effective antibiotic treatment as in the index case. Brain MRI should be considered for
initial diagnosis and at follow-up in these patients to prevent further complications. Conflict of Interest None. Source of Funding None.
References 1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
Legrand M, Roujeau T, Meyer P, Carli P, Orliaguet G, Blanot S. Paediatric intracranial empyema: differences according to age. Eur J Pediatr. 2009;168:1235–41. Bouziri A, Khaldi A, Smaoui H, Menif K, Jaballah BN. Fatal subdural empyema caused by Streptococcus constellatus and Actinomyces viscosus in a child–case report. J Microbiol Immunol Infect. 2011;44:394–6. Junckerstorff RK, Robinson JO, Murray RJ. Invasive Streptococcus anginosus group infection-does the species predict the outcome? Int J Infect Dis. 2014;18:38–40. Göbels K, Teichmann D, Grobusch MP, Halle E, Suttorp N. A case of multiple brain abscesses due to Streptococcus constellatus. Eur J Clin Microbiol Infect Dis. 2002;21:156–7. Dhariwal DK, Patton DW, Gregory MC. Epidural spinal abscess following dental extraction – a rare and potentially fatal complication. Br J Oral Maxillofac Surg. 2003;41:56–8. Chang WN, Wu JJ, Huang CR, Tsai YC, Chien CC, Lu CH. Identification of viridans streptococcal species causing bacterial meningitis in adults in Taiwan. Eur J Clin Microbiol Infect Dis. 2002;21:393–6. Bair-Merritt MH, Shah SS, Zaoutis TE, Bell LM, Feudtner C. Suppurative intracranial complications of sinusitis in previously healthy children. Pediatr Infect Dis J. 2005;24:384–6. Wu TJ, Chiu NC, Huang FY. Subdural empyema in children—20-y experience in a medical center. J Microbiol Immunol Infect. 2008;41:62–7. Gupta S, Vachhrajani S, Kulkarni AV, et al. Neurosurgical management of extraaxial central nervous system infections in children. J Neurosurg Pediatr. 2011;7:441–51. Cole TS, Clark ME, Jenkins AJ, Clark JE. Pediatric focal intracranial suppuration: a UK single-center experience. Childs Nerv Syst. 2012;28:2109–14. Whiley RA, Beighton D, Winstanley TG, Fraser HY, Hardie JM. Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol. 1992;30:243–4. Petti CA, Simmon KE, Bender J, et al. Culture-negative intracerebral abscesses in children and adolescents from Streptococcus anginosus group infection: a case series. Clin Infect Dis. 2008;46: 1578–80. Ebright JR, Penugonda N, Brown W. Clinical experience with Staphylococcus lugdunensis bacteremia: a retrospective analysis. Diagn Microbiol Infect Dis. 2004;48:17–21.
CLINICAL BRIEF
Is Sinusitis Innocent?– Unilateral Subdural Empyema in an Immunocompetent Child Sevim Şahin 1 & Uğur Yazar 2 & Ali Cansu 1 & Sibel Kul 3 & Selçuk Kaya 4 & Elif Bahat Özdoğan 5
Received: 8 December 2014 / Accepted: 9 April 2015 # Dr. K C Chaudhuri Foundation 2015
Abstract Subdural empyema related to Streptococcus constellatus is extremely rare in an immunocompetent child, and also there is no reported case along with Staphylococcus lugdunensis infection. Although Streptococcus constellatus has been determined as a co-pathogen with anerobic bacteria in many infections, it has not been reported in combination with Staphylococcus lugdunensis. The authors describe a case of previously healthy 16-y-old child with unilateral subdural empyema due to these bacteria. Sinusitis was the only predisposing factor in the index case. The authors propose that some cases of culture-negative intracranial infections may be due to these infectious agents. Therefore, these agents should be considered as causes of intracranial infection in persistent complaints such as fever and headache after sinusitis in children. It is important to treat them with effective antibiotics and early surgical intervention for favorable outcome, because fatal cases were reported due to Streptococcus constellatus infections.
* Sevim Şahin [email protected] 1
Department of Pediatric Neurology, School of Medicine, Karadeniz Technical University, 61000 Trabzon, Turkey
2
Department of Neurosurgery, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
3
Department of Radiology, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
4
Department of Infectious Diseases and Clinical Microbiology, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
5
Department of Pediatrics, School of Medicine, Karadeniz Technical University, Trabzon, Turkey
Keywords Streptococcus constellatus . Staphylococcus lugdunensis . Subdural empyema . Child
Introduction Intracranial empyema, though rare in children is an emergency due to life-threatening complications [1]. Herein, the authors describe a previously healthy child with unilateral subdural empyema (SDE) related to Streptococcus constellatus and Staphylococcus lugdunensis. SDE associated with Streptococcus constellatus has been described in only one case [2] in the English literature, and there is no case associated with Staphylococcus lugdunensis, to the authors’ knowledge. Also, the presence of co-pathogens such as Streptococcus constellatus and its combination with Staphylococcus lugdunensis has not been previously reported. This case is presented to ensure consideration of these rare microorganisms as causes of SDE even in immunocompetent children.
Case Report A 16-y-old boy was referred to the Emergency department with complaints of projectile vomiting and lethargy for one day, headache for 3d, and fever for 2d. The headache was especially on the right side, and fever was up to 39 °C. He had been started oral antibiotic treatment 2d ago for sinusitis. His past medical and family history were unremarkable. The physical examination revealed somnolence and anisocoria. He had eye opening and localized motor response to pain, but no verbal response. Also, generalized tonic-clonic seizure were observed. In laboratory examination, his leukocyte count (12,100/mm3) and C-
Indian J Pediatr
reactive protein (20.62mg/dl) were increased. Brain magnetic resonance imaging (MRI) revealed SDE surrounding the right cerebral hemisphere (Fig. 1). There was compression of the ventricles, anterior displacement of the brain stem and subfalcine herniation on the left. Inflammatory changes were present in the maxillary sinus and ethmoid cells. Right frontoparietal craniotomy was performed, and subdural empyema was drained at the Neurosurgery department. Treatment with vancomycin (60mg/kg/d), ceftriaxone (100mg/kg/d) and metronidazole (30mg/kg/d) was initiated. Acyclovir treatment (30mg/kg/d) was added for probable herpes simplex virus (HSV) infection, and continued with positive results of HSV type 1 and type 2 immunoglobulin M (IgM) in the serum. Studies of the lymphocyte subgroups and immunoglobulins were normal. Streptococcus constellatus was isolated in the abscess material; it was sensitive to ceftriaxone. Postoperatively, Babinski’s sign and decrease in score of motor strength (3/5) on the left side were present. On day 5, although the patient remained stable clinically, subdural empyema enlarged in the interhemispheric fissure (Fig. 1). On day 17, brain MRI showed enlargement of SDE in the posterior interhemispheric fissure (Fig. 1).
Fig. 1 Axial images on brain MRI study of the case. T2 (1, 3) and T1-weighted (2, 4) images on admission (A), on the 5th day after surgical drainage (B), on day 17 prior to second surgical drainage (C) and 2 mo after the second surgery (D). (A) Subdural empyema surrounding the right cerebral hemisphere (arrow). Signal hypointensity on T1-weighted images (A2, A4) and signal hyperintensity on T2-weighted images (A1, A3) may be seen. There is light shift of midline structures to the left. (B) Subdural empyema in the interhemispheric fissure with signal hyperintensity on T2-weighted images (B1, B3) and signal hypointensity on T1weighted images (B2, B4). (C) Increase in the size of the empyema is more pronounced in the posterior of interhemispheric fissure. (D) Disappearance of subdural empyema
Subfalcine herniation of midline structures to the left and compression of the third and lateral ventricles were present. Therefore, surgical drainage was performed again, and considering penicillin sensitivity tests, antibiotic treatment was switched to high-dose ampicillin treatment (8g/d ampicillin-sulbactam in addition to ampicillin of 4g/d). Staphylococcus lugdunensis was isolated from the latter abscess material. In follow-up, hemiparesis of the patient improved gradually and SDE regressed completely (Fig. 1). Ampicillin treatment was completed in 2mo.
Discussion The only case of SDE associated with Streptococcus constellatus in the English literature is of a 7-y-old girl [2]. Unilateral SDE in that case showed fatal outcome [2]. Streptococcus constellatus is a commensal of oropharyngeal flora [3]. Infections with empyema related to Streptococcus constellatus are mostly present in the thoracal region. It causes purulent infections of pleuro-pulmonary, intra-abdominal, genitourinary, soft tissue and rarely central nervous system (CNS) [2, 3]. Streptococcus constellatus has been rarely
Number of patients with SDE
4
31
33
70 extraaxial (epidural and SDE)
23
Bair-Merritt et al., 2005 [7]
Wu et al., 2008 [8]
Legrand et al., 2009 [1]
Gupta et al., 2011 [9]
Cole et al., 2012 [10]
None
27 (38.6)
7 (21.2)
None
1 (25)
S. milleri group infections n (%) Streptococcus salivarius, Group A streptococcus, Group D streptococcus, Peptostreptococcus, Prevotella, Clostridium spp., nontypable Haemophilus influenzae, Alfa-hemolytic streptococcus, Beta-hemolytic streptococcus Streptococcus pneumoniae, Group B streptococcus, Methicillin-sensitive Staphylococcus aureus, Haemophilus influenzae type b, Salmonella spp., Escherichia coli, Pseudomonas aeruginosa, Haemophilus parainfluenzae, Enterobacter cloacae Anaerobes, Group B streptococcus, Streptococcus pneumoniae, Enterobacteriaceae, Staphylococcus aureus, P. aeruginosa, Haemophilus S. aureus, Streptococcus pneumoniae, other β-hemolytic streptococci spp, Haemophilus influenzae, other α-hemolytic streptococci spp, Escherichia coli, coagulase-negative Staphylococci spp, cryptogenic gram-negative bacilli spp. Pneumococcus, H. influenzae type B, Coagulase negative Staphylococcus, Lactobacillus, Abiotrophia adiacens, Enterobacter cloacae, Meningococcus, S. aureus
Other microorganisms
Comparison of various studies in pediatric patients with subdural empyema (SDE)
Author
Table 1
1 child died. Permanent neurological deficits in 3 children
• Bacterial meningitis in 10 infants • Sinusitis in 18 cases • Otitis in one case • Tonsillitis in one case • Sinusitis • Otitis • Meningitis • Previous neurosurgery • Spinal infections • Miscellaneous • Sinusitis in 12 cases • Meningitis in 6 cases • Neurosurgery in 2 cases
1 child with ventriculoperitoneal shunt died. 20% with neurological sequelae.
84.3% without neurological sequelae. Developmental delay, residual focal neurological deficit.
3 children died. 38.7% without neurological sequelae. 51.6% neurological deficit.
Seizures in the case of S. milleri group. Seizures, dysarthria expressive aphasia, hemiplegia.
Neurological outcome
Otorhinolaryngeal infections, head trauma or surgery.
Sinusitis
Identified etiology
Indian J Pediatr
Indian J Pediatr
reported with brain abscess [4], spinal epidural abscess [5] and meningitis [6] in adult patients. Sinusitis might have been the predisposing factor in the index case. No other predisposing factors, such as dental or oropharyngeal intervention, trauma, any surgical operation or immunodeficiency were detected. Sinusal infections have been reported as major predisposing factors for intracranial infections in immunocompetent children [7]. Streptococcus milleri group including Streptococcus constellatus has been reported as a cause of SDE. Its frequency varies in different studies (Table 1). Streptococcus intermedius in Streptococcus milleri group is the main microorganism that cause CNS infections, and a small proportion is caused by Streptococcus anginosus. Streptococcus constellatus is very rare in CNS infections [11]. Although there is no marked difference between the dates of the studies compared in Table 1, wide range of the rates of Streptococcus milleri group infections between 0 and 38.6% is remarkable. The most important reason for that is probably some studies focused on complications after sinusitis or may had difficulty in identifying these agents. Streptococcus milleri group and anerobic bacteria are the most common pathogens in suppurative intracranial complications after sinusitis in previously healthy children [7]. Probably all the infections of Streptococcus milleri group cannot be detected. In a study, Streptococcus milleri group was detected in three cases with culture-negative brain abscess by 16S rRNA gene amplification and sequencing methods [12]. Staphylococcus lugdunensis, another agent in the index case, is a coagulase negative staphylococcus and causes skin and soft tissue infections. Severe infections such as endocarditis, septic shock, peritonitis, osteomyelitis, spondylodiscitis, septic arthritis, epidural abscess, brain abscess and infection of prosthetic devices have also been reported [13]. The present case indicates that Streptococcus constellatus and Staphylococcus lugdunensis may cause SDE even in immunocompetent children. CNS infections should be considered in cases of increasing symptoms after sinusitis. High dose antibiotic treatment is necessary to provide penetration into the abscess [2]. These infections, although probability of fatal outcome, can be treated with early surgical intervention, close neuroimaging and effective antibiotic treatment as in the index case. Brain MRI should be considered for
initial diagnosis and at follow-up in these patients to prevent further complications. Conflict of Interest None. Source of Funding None.
References 1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
Legrand M, Roujeau T, Meyer P, Carli P, Orliaguet G, Blanot S. Paediatric intracranial empyema: differences according to age. Eur J Pediatr. 2009;168:1235–41. Bouziri A, Khaldi A, Smaoui H, Menif K, Jaballah BN. Fatal subdural empyema caused by Streptococcus constellatus and Actinomyces viscosus in a child–case report. J Microbiol Immunol Infect. 2011;44:394–6. Junckerstorff RK, Robinson JO, Murray RJ. Invasive Streptococcus anginosus group infection-does the species predict the outcome? Int J Infect Dis. 2014;18:38–40. Göbels K, Teichmann D, Grobusch MP, Halle E, Suttorp N. A case of multiple brain abscesses due to Streptococcus constellatus. Eur J Clin Microbiol Infect Dis. 2002;21:156–7. Dhariwal DK, Patton DW, Gregory MC. Epidural spinal abscess following dental extraction – a rare and potentially fatal complication. Br J Oral Maxillofac Surg. 2003;41:56–8. Chang WN, Wu JJ, Huang CR, Tsai YC, Chien CC, Lu CH. Identification of viridans streptococcal species causing bacterial meningitis in adults in Taiwan. Eur J Clin Microbiol Infect Dis. 2002;21:393–6. Bair-Merritt MH, Shah SS, Zaoutis TE, Bell LM, Feudtner C. Suppurative intracranial complications of sinusitis in previously healthy children. Pediatr Infect Dis J. 2005;24:384–6. Wu TJ, Chiu NC, Huang FY. Subdural empyema in children—20-y experience in a medical center. J Microbiol Immunol Infect. 2008;41:62–7. Gupta S, Vachhrajani S, Kulkarni AV, et al. Neurosurgical management of extraaxial central nervous system infections in children. J Neurosurg Pediatr. 2011;7:441–51. Cole TS, Clark ME, Jenkins AJ, Clark JE. Pediatric focal intracranial suppuration: a UK single-center experience. Childs Nerv Syst. 2012;28:2109–14. Whiley RA, Beighton D, Winstanley TG, Fraser HY, Hardie JM. Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus (the Streptococcus milleri group): association with different body sites and clinical infections. J Clin Microbiol. 1992;30:243–4. Petti CA, Simmon KE, Bender J, et al. Culture-negative intracerebral abscesses in children and adolescents from Streptococcus anginosus group infection: a case series. Clin Infect Dis. 2008;46: 1578–80. Ebright JR, Penugonda N, Brown W. Clinical experience with Staphylococcus lugdunensis bacteremia: a retrospective analysis. Diagn Microbiol Infect Dis. 2004;48:17–21.
