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Journal of Neurological Sciences [Turkish] 31:(1)# 39; 175-187, 2014 http://www.jns.dergisi.org/text.php3?id=758

Research Article

Brain Abcesses: Clinical Analysis of Twenty-five Cases

Tevfik YILMAZ1, Aylin GÜL2, Yahya TURAN1, Pınar AYDIN1, Cüneyt GÖÇMEZ1, Kağan KAMAŞAK1, Salih HATTAPOĞLU3, Adnan CEVİZ1

1Dicle University, Neurosurgery, Diyarbakır, Türkiye 2Dicle Üniversity, Otorhinolaryngology, Diyarbakır, Türkiye 3Dicle Üniversity, Radiology, Diyarbakır, Türkiye

Summary

Objective: The aim of this study is to determine the clinical, radiological, and surgical characteristics of brain abscesses and to share our experience in their management. Method: Medical records of 25 patients with brain abscess were retrospectively reviewed. The clinical picture, radiological examinations, treatment methods, and patient outcomes were analysed. Results: Of 25 patients included in our study, 16 (64%) were male and 9 (36%) were female. The age range was 2 months to 60 years, with a mean age of 12 years. Fifteen patients had a predisposing condition. The main source of the abscess was extension of an ear or nose infection to brain (n=9; 36%). In 10 (40%) patients the source could not be shown. Eighteen (72%) patients had a solitary abscess while 7 (28%) had multiple abscesses. No proliferation was observed in bacteriological cultures in 13 (52%) patients. No recurrences were seen in patients undergoing abscess excision with craniotomy. Conclusion: A brain abscess is a surgical emergency. Abcess excision with cranitomy is an effective treatment method in brain abcess cases. The most important sources of brain abcess were neigboring ear and nose infections. Diagnosis and treatment of these infections can prevent formation of brain abcess.Early diagnosis and treatment of cases with brain abscess can save patients from life-threatening complications of this disease. Key words: Brain abcesses, treatment, surgery, CT scan, MR imaging

Beyin Apseleri: Yirmibeş Olgunun Klinik Analizi Özet

Amaç: Bu çalışmanın amacı beyin apselerinin klinik, radyolojik ve cerrahi özelliklerini belirlemek ve yönetiminde tecrübemizi paylaşmaktır. Yöntem: Beyin apsesi olan 25 hastanın tıbbi kayıtları retrospektif olarak gözden geçirilmiştir. Hastaların klinik tabloları, radyolojik incelemeleri, tedavi yöntemleri ve sonuçları analiz edildi. Bulgular: Çalışmamıza dahil edilen 25 hastanın 16 (% 64) ‘sı erkek, 9 (% 36)' u kadın idi. Yaş aralığı 2 ay – 60 yaş arasında değişmekte olup ortalama yaş 30 olarak değerlendirildi. 15 hastada predispozan faktör mevcuttu. Apsenin en önemli kaynağını 9 hastada (% 36) kulak ve burun enfeksiyonlarını takiben komşuluk yoluyla yayılma oluşturdu. 10 olguda (%40) kaynak belirlenemedi. Hastaların 18(%72)inde apse tek yerleşimli iken 7(%28)sinde ise multiple yerleşimliydi. 13 olguda bakteriyolojik incelemede üreme olmadı. Kranitomi ile apse eksizyonu yapılan hastalarda nüks görülmedi. Sonuç: Beyin apsesi acil olarak tedavi edilmesi gereken bir durumdur. Kranitomi ile apse eksizyonu beyin abselerinde etkili bir tedavi yöntemidir. Absenin en önemli kaynağını oluşturan kulak ve burun enfeksiyonlarının zamanında tanı ve tedavisi beyin abselerinin

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gelişmesini önleyebilir.Beyin apseli hastaların erken teşhisi ve yönetimi bu hastalığın hayatı tehdit eden ciddi komplikasyonlarından koruyabilir. Anahtar Kelimeler: Beyin apseleri, tedavi, cerrahi, CT tarama, MR görüntüleme

INTRODUCTION

Brain abscess (BA) is a neursurgical emergency and is usually fatal if left untreated. It is more common between 20-40 years of age in adults and 4-7 years of age in children(2,7,13,19,26). The incidence increases in those with immune deficiency(14). BA often develops by direct extension of neighboring infections including chronic otitis media, mastoiditis, or dental caries; hematological seeding of microorganisms in patients with infective endocarditis, pulmonary infection, or cyanotic congenital heart disease; or penetrating head trauma or neurosurgical procedures(2,9).

Although the most common signs and symptoms of the brain abscesses are fever, headache, and neurological deficit, it often has a more insidious clinical picture(37). Thanks to advances in imaging technology, antimicrobial agents, and surgical techniques, the mortality of brain abscess has dropped to around 10% from about 30-60%(2,21,23,36,39). Still, with a mortality rate of 17-32%, it continues to be a major health problem in many countries(13,19). Misdiagnosed and falsely treated patients have a particularly increased mortality and morbidity(5). A brain abscess that grows in size, becomes more edematous, and opens into the ventricle is associated with increased rates of mortality and morbidity(38). A high level of suspicion as well as early diagnosis and treatment are of utmost importance in management of brain abscesses.

In this study we discussed the clinical, radiological, and surgical characteristics of 25 patients with brain abscess and reviewed the relevant literature.

MATERIAL AND METHODS

We retrospectively reviewed medical records of 25 cases diagnosed with cerebral or cerebellar abscess and operated at Dicle University Faculty of Medicine, Department of Neurosurgery between February 2009 and September 2013. The source of abscess, predisposing conditions, clinical and imaging findings, complications, and treatment outcomes were evaluated. The preoperative diagnostic protocol included standard neurological examination, systemic examination, routine laboratory tests. In addition, sedimentation rate, C-reactive protein (CRP) level, computerized tomography (CT) (Figure 1) with and without contrast agent, and magnetic resonance imaging (MRI) (Figure 2) were performed. Abscess material was sent for culture analysis. The antibiotics against abscess were decided under the guidance of an infectious diseases specialist and by predicting the possible culprit microorganism according to the source of the microorganism and the localization of the abscess. The treatment protocol was revised under the guidance of the infectious diseases specialist according to culture antibiogram results. Parenteral antibiotics were continued for at least 4-6 weeks. Since improvement on CT images may be delayed when compared to clinical improvement, the treatment protocol was guided by peripheral leucocytosis, erythrocyte sedimentation rate, and CRP levels. Steroids were used in patients with edema induced by significant mass. Antiepileptics were administered in every patient to prevent epileptic attacks as per study protocol. The surgical technique consisted of aspiration through a Burr-hole, abscess drainage with craniotomy,

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and capsule excision. CT (Figure 3) and MRI (Figure 4,5) were obtained from each patient at the early postoperative period. A mean of 11 (4–18) months of follow-up

was completed in all patients with the exception of three patients who died at postoperative period.

Figure 1: A hypodense abscess of approximately 5x4 cm with peripheral contrast uptake located in cerebellum is shown on preoperative axial CT

Figure 2: A right cerebellar lesion consistent with an abscess measuring 50X40 cm with peripheral contrast uptake, which appeared hypointense on T1A sequence is shown on coronal MRI.

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Figure 3: The image of the left temporal located abscess on postoperative axial CT

Figure 4: The image of the excised left temporal located abscess is shown on T1A coronal and axial MRI with contrast

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RESULTS

Clinical Findings

Of 25 patients included in our study, 16 (64%) were male and 9 (36%) were female. The age range was 2 months to 60 years, with a mean age of 12 years. Fever, a sign of a general infection, was present in 10 (40%) patients. The mean time for symptom onset was 13 days before the patients applied to the hospital. The most common clinical signs were focal neurological deficits (hemiparesia, ataxia, visual disturbance, drop foot), signs associated with increased intracranial pressure (headache, nausea, vomiting), and changes in mental status. Focal neurological deficit was observed in 7 patients, of whom 4 had hemiparesia, 1 had ataxia, 1 had visual disturbance, and 1 had drop foot. Changes associated with inreased intracranial pressure were the most common abnormalities. Twenty-one patients had headache and 15 patients had nausea and vomiting. Five patients had seizure attacks (Table 1).

Neurological status of each patient was assessed by the Glascow coma scale. Two patients had 10, 3 had 12, 3 had 13, 6 had 14, and 11 had 15 points.

The patients were evaluated using cranial CT with and without contrast and MRI.

Etiology And The Predisposing Factors

Fifteen patients had a predisposing condition. Six had chronic otitis media (COM), 3 had a complication of sinusitis, 2 had tetralogy of fallot, 1 had a history of operation for intracranial mass, 1 had a fruncle in the frontal region, 1 had a history of fall from a height, and 1 had a history of gunshot wound. Six (24%) patients had a history of meningitis following COM. The otorhinolaryngology department operated these patients with radical mastoidectomy for COM, and the rest of the therapy was completed by our department. One patient had chronic frontal sinusitis, 2 had a complication of ethmoidal sinusitis (orbital cellulitis and periorbital abscess). The source of infection could not be determined in 10 (40%) patients (Table 1).

Figure 5: The image of the excised left temporal located abscess is shown on T1A coronal and axial MRI with contrast

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Characteristics of Abscess

Eighteen patients had a solitary abscess (Figure 6) while 7 (28%) had multiple abscesses (Figure 7). The localizations of abscesses were as follows: 5 temporal, 4 cerebellum, 5 frontal, 6 parietal, and 5 frontoparietooccipital. Mean abscess

diameter was 33.5 (10-60) mm. While the abscesses following sinusitis were at multiple locations, abscesses following chronic otitis media were located at the temporal lobe and cerebellum (Table 2).

Table 1. The distribution of patients according to clinical findings. 

  Number of patients (%) 

Signs and Symptoms    Hemiparesis  4(%16)  Ataxia  1(%4)  Defect of vision  1(%4)  Foot drop   1(%4)  Headache  21(%84)  Nausea-vomiting   15(%60)  Seizures   5(%20)  Fever  10(%40)    Predisposing Factors     Fallot Tetralogy   2(%8)  Postoperative  1(%4)  Chronic otitis media  6(%24)  Paranasal sinus infection   3(%12)  Frontal furuncles   1(%4)  Falling down   1(%4)  Gunshot injury   1(%4)  Idiopathic   10(%40) 

Microbiological Evaluation

Thirteen (52%) abscess materials did not show any culture proliferation. Among the aerobic microorganisms, streptococci and staphylococci proliferated the most; bacteriodes fragilis was the most common proliferated microorganism among the anaerobes.

Laboratory Results

The laboratory examinations included peripheral white blood cell count (WBC),

erythrocyte sedimentation rate (ESR), and C-reactive protein (CRP). Although these parameters were not disease-specific, they were monitored at follow-up. WBC count was elevated (˃12.000/mm3) in 21 patients and 4 patients had WBC counts above 20.000/mm3. The erythrocyte sedimentation rate was elevated in all patients. CRP level (normal 0-3 mg/L) was normal in 5 patients and elevated in 20 patients (Table 2).

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Table 2. According to the analysis of clinical characteristics of patients

       Number of patients  25     The mean age and distribution        The mean age  12      0-14 age  18(%72)      15-40 age  4(%16)      41-60 age  3(%12)     Characteristics of abscesses  One   18(%72)      Multiple   7(%28)      Average diameter  32.5 mm      Frontal   5(%20)      Parietal   6(%24)      Cerebellum  4(%16)      Temporal   5(%20)      Frontoparietooksipital 5(%20) Duration of symptoms(day) 13 The presence of predisposing factors  present  15(%60)      none  10(%40)     Fever (≥38.5)   present  10(%40)      none  15(%60)     WBC (˃12.000/mm3) 25(%100) Erythrocyte sedimentation rate 25(%100) C reaktif protein değeri (0-3 mg/L) Normal   5(%20)     İncreased   20(%80)     Glasgow coma scale   15  11(%44)      13-14  9(%36)      9-12  5(%20)     Surgical technique   Burr hole aspiration         1   11(%44)      2   1(%4)      3   2(%8)      Craniotomy and excision   14(%56)     

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Figure 6: An abscess with peripheral contrast uptake located in right temporal region is shown on T1A axial MRI

Figure 7: Multiple abscesses with peripheral contrast uptake in right temporal region are shown on axial CT

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Treatment

All patients underwent both medical and surgical therapy. A combination of a third generation cephalosporin such as ceftriaxone, metronidazole, and vancomycin were used for medical therapy until culture antibiogram results were available. The treatment was refined by an infectious diseases specialist according to results of the culture antibiogram. The parenteral antibiotherapy was continued for at least 4-6 weeks.

Surgical techniques included burr-hole aspiration in 11 (44%) patients and abscess drainage and capsule excision with craniotomy in 14 (56%). Of patients who underwent burr-hole aspiration, 3 had recurrences requiring repeat aspiration. Two patients underwent aspiration procedure twice and 1 patient underwent 1 additional aspiration procedure.

Outcomes

Three (12%) patients died after the operation. One of them had multiple abscesses and tetralogy of fallot while the others had cerebellar abscesses. Focal infections were the most common cause of brain abscesses in 0-14 and 15-40 years age groups, while the source of the abscesses remained undetermined in the majority of patients in the 41-60 years age group. Eight percent of the patients had tetralogy of fallot. Ten (40%) patients had an abscess of undetermined origin. The most common sources of the abscesses were ear infections (n=6; 24%) and nose infections (n=3; 12%). No recurrences were observed in patients undergoing abscess excision with craniotomy.

DISCUSSION

Brain abscesses continue to have high rates mortality and fatal central nervous system infection despite advanced surgical methods, effective antimicrobial treatment, and modern imaging techniques(13,21-

23,29,33,36). Therefore, early diagnosis and

therapy is of utmost importance in management of brain abscesses. The etiology of brain abscesses shows variations by geographical location and patients' socio-economic level, although the incidence of autogenous abscesses has recently decreased whereas it tends to increase in immune suppressed patients(10,23). In developed countries, however, the incidence of brain abscesses has increased because of the increased number of organ transplantations, immunosuppression treatment, patients on antineoplastic drugs, and cases diagnosed with HIV(15).

Forty to sixty percent of brain abscesses spread through direct extension of the neighboring infections such as paranasal sinusitis, meningitis, otitis media, mastoiditis, and dental infections(11,24,28,39). The most common source of the abscess is the direct extension of the ear and nose infections, as was the case in 9 (36%) of our patients(1). Brain abscesses occuring as a result of hematogenous spread are more common in patients with a right-to-left shunt or congenital heart disease(12). Abscess formation after open head trauma or neurosurgical procedures is less common(15). It has been reported that the source of the abscess remains undetermined in 15-48% of cases(15,37,38). In our series, 10 (40%) patients had an undetermined source.

The most common signs and symptoms with brain abscesses are signs of increased intracranial pressure (headache, nausea, vomiting) although fever, focal neurological deficits, general signs of infection, and mental status changes may also be observed(5,8,11,13,21-23,29,33,36,39). Fever is a common sign; however, its absence should not be used as an exclusion criterion(4). The initial signs are usually related to size and location of an abscess, and extension of the abscess depends on both the virulence of the pathogens and health status of the host(23). A recently

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developed meningeal irritation and worsening headache should make the clinician consider the possibility of abscess rupture into the ventricle that is highly fatal(2,14,16,33,35,37,38). Brain abscesses may precipitate epileptic activity. Likewise, 5 (20%) patients in our study presented with seizure attack.

Routine laboratory tests are not helpful in the diagnostic process(22,23,29). Lumbar puncture (LP) has been considered hazardous due to the risk of herniation in patients with brain abscess(4,5,22,24,32,33,39). LP should not be performed unless a cranial imaging is done. In patients undergoing LP, CSF findings are generally

nonspecific and cultures are only rarely positive(5,23). We also did not perform LP owing to herniation risk.

CT and MRI provide important information for diagnosis of brain abscesses. A mature pyogenic brain abscess appears hypointense on T1 images and hyperintense on T2 images of MRI. A peripheral contrast uptake is observed(20). Many studies have shown that MRI is more sensitive for imaging cerebral edema and early-phase cerebritis(23,29). Furthermore, MRI is more sensitive for diagnosis of abscesses located at the brain stem and posterior fossa(23,29) (Figure 8,9).

Figure 8: A hardly visible hypodense lesion located in the left cerebellar hemisphere?

Figure 9: An abscess located in the left cerebellar hemisphere is clearly shown on T2A axial MRI

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Various series have reported a rate of 1-50% for multiple abscesses; especially a high rate as 61% has been reported in infants(21,23). In this study 80% of multiple abscesses were in the pediatric age group. The reason of higher mortality rate in multiple abscesses is the delay in diagnosis and treatment of these lesions(21,23). In our study 1 of 3 patients who died had multiple abscesses.

Some studies in the literature have reported a higher isolation rate of aerobic microorganisms(13,19,36) while some others have reported a higher rate of anaerobic(3,17) microorganisms. In this study the most commonly isolated aerobic microorganisms were Staphylococcus and Streptococcus species(10,22,24,30,39). The most common anaerobes were Bacteroides and anaerobic streptococci. We usually observed mixed proliferation(33). Despite a careful microbiological examination, culture studies of the abscess materials are often sterile because such patients often receive antibiotics(6,12,22,24,35). Literature data suggest a 24-63% culture negativity rate(6,26,27,32). In our study, no microorganisms could be isolated in 13 (52%) patients since majority of them received antibiotics for at least 5 days before the culture study.

Every patient diagnosed with brain abscess was empirically given a third generation cephalosporin with CNS penetration. Metronidazole was added in abscesses developing after otitis, sinusitis, and dental infections, and vancomycin after neurosurgical interventions and trauma. Metronidazole or vancomycin was added to third generation cephalosporin when the infection source was unclear(31). The duration of antimicrobial therapy for brain abscesses remains debated(5,21). Many studies have suggested a treatment duration of 3-6 weeks(2,5,25). In our study the treatment duration was 4-6 weeks for parenteral therapy and 2-6 weeks for oral therapy. Literature reports recommend

steroids for treatment of diffuse cerebral edema that is a common cause of death(21,23,33). We used steroids for cerebral edema in 5 patients.

The primary treatment for brain abscesses consists of a combination of surgical therapy and antimicrobial therapy(18). Surgical therapy consists of aspiration of abscess content or abscess excision. There has been much debate surrounding the optimal procedure. We often used excision (n=14; 56%) and aspiration through a single burrhole (n=11; 44%). The advantages of aspiration are its ease and reduced surgical trauma and morbidity. The advantages of excision are lower rate of recurrence and shorter duration of hospital stay(31,34,39). T. Hakan et al. reported that they performed more than one procedure in 19% patients treated by aspiration method(10). We applied burrhole aspiration more than once in 3 (12%) patients.

Neurological status at the time of admission is the most important determinant of prognosis and mortality. More favorable outcomes have been achieved with higher GCS. However, no evidence has yet been reported to suggest that GCS is one of the primary factors determining the prognosis(16,26,37,38). Higher mortality rates have been reported in patients with a shorter symptom duration, severe mental changes, and a more rapid neurological deterioration(22,23,33). Mortality rates as high as 80-100% have been reported in comatose patients or in patients with abscess rupture into ventricle. Ventricular rupture has been reported more commonly in cases with congenital heart disease(23,29). Older series have reported mortality rates as high as 40% for brain abscesses(5,12,30,39). However, subsequent studies using CT, MRI, and novel antibiotics have reported mortality rates of 4-25%(2,5,9,10,21,22,27,38). We found a mortality rate of 12%.

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CONCLUSION

In conclusion, brain abscesses are medical emergencies. A surgical approach should always be considered to relieve mass effect, determine the pathology, and make the microbiological diagnosis. Abcess drainage and capsule excision with cranitomy is an effective treatment method in brain abcess cases. The most important sources of brain abcess were neigboring ear and nose infections. Diagnosis and treatment of these infections can prevent formation of brain abcess. A successful management of a brain abscess requires suspicion of the infection, detection of subtle clinical alterations, timely diagnosis with imaging methods, and appropriate surgical and antimicrobial treatment.

Correspondence to: Tevfik Yılmaz E-mail: kartaltevfik@hotmail.com Received by: 14 January 2014 Revised by: 04 March 2014 Accepted: 07 March 2014 The Online Journal of Neurological Sciences (Turkish) 1984-2014 This e-journal is run by Ege University Faculty of Medicine, Dept. of Neurological Surgery, Bornova, Izmir-35100TR as part of the Ege Neurological Surgery World Wide Web service. Comments and feedback: E-mail: editor@jns.dergisi.org URL: http://www.jns.dergisi.org Journal of Neurological Sciences (Turkish) Abbr: J. Neurol. Sci.[Turk] ISSNe 1302-1664

REFERENCES

1. Beller AJ, Sahar A, Praiss I. Brain abscess. Review of 89 cases over a period of 30 years. J Neurol Neurosurg Psychiatry 1973;36:757-68.

2. Carpenter J, Stapleton S, Holliman R. Retrospective analysis of 49 cases of brain abscess and review of the literature. Eur J Clin Microbiol Infect Dis 2007;26:1-11.

3. Chaudhry R, Dhawan B, Laxmi BV, et al. The microbial spectrum of brain abscess with special reference to anaerobic bacteria. Br J Neurosurg 1998;12:127-30.

4. Chun CH, Johnson JD, Hofstetter M, et al. Brain abscess. A study of 45 consecutive cases. Medicine (Baltimore) 1986;65:415-31.

5. Cochrane DD. Consultation with the specialist. Brain abscess. Pediatr Rev 1999;20:209-15.

6. de Louvois J. Bacteriological examination of pus from abscesses of the central nervous system. J Clin Pathol 1980;33:66-71.

7. Fellows GA, Kalsi PS, Martin AJ. Nocardia farcinica brain abscess in a patient without immunocompromise. Br J Neurosurg 2007;21:301-3.

8. Friedlander RM, Gonzalez RG, Afridi NA, et al. Case records of the Massachusetts General Hospital. Weekly clinicopathological exercises. Case 16-2003. A 58-year-old woman with left-sided weakness and a right frontal brain mass. N Engl J Med 2003;348:2125-32.

9. Goodkin HP, Harper MB, Pomeroy SL. Intracerebral abscess in children: historical trends at Children's Hospital Boston. Pediatrics 2004;113:1765-70.

10. Hakan T, Ceran N, Erdem I, et al. Bacterial brain abscesses: an evaluation of 96 cases. J Infect 2006;52:359-66.

11. Jennett B, Bond M. Assessment of outcome after severe brain damage. Lancet 1975;1:480-4.

12. Kagawa M, Takeshita M, Yato S, et al. Brain abscess in congenital cyanotic heart disease. J Neurosurg 1983;58:913-7.

13. Kao PT, Tseng HK, Liu CP, et al. Brain abscess: clinical analysis of 53 cases. J Microbiol Immunol Infect 2003;36:129-36.

14. Kapsalaki EZ, Gotsis ED, Fountas KN. The role of proton magnetic resonance spectroscopy in the diagnosis and categorization of cerebral abscesses. Neurosurg Focus 2008;24:E7.

15. Kothari M, Goel A. Brain abscess: a cogent clarifier of the confused concept of immunity. Neurosurg Focus 2008;24:E16.

16. Landriel F, Ajler P, Hem S, et al. Supratentorial and infratentorial brain abscesses: surgical treatment, complications and outcomes--a 10-year single-center study. Acta Neurochir (Wien) 2012;154:903-11.

17. Le Moal G, Landron C, Grollier G, et al. Characteristics of brain abscess with isolation of anaerobic bacteria. Scand J Infect Dis 2003;35:318-21.

18. Lee TH, Chang WN, Su TM, et al. Clinical features and predictive factors of

J.Neurol.Sci.[Turk]

187

intraventricular rupture in patients who have bacterial brain abscesses. J Neurol Neurosurg Psychiatry 2007;78:303-9.

19. Lu CH, Chang WN, Lin YC, et al. Bacterial brain abscess: microbiological features, epidemiological trends and therapeutic outcomes. Qjm 2002;95:501-9.

20. Luthra G, Parihar A, Nath K, et al. Comparative evaluation of fungal, tubercular, and pyogenic brain abscesses with conventional and diffusion MR imaging and proton MR spectroscopy. AJNR Am J Neuroradiol 2007;28:1332-8.

21. Mamelak AN, Mampalam TJ, Obana WG, et al. Improved management of multiple brain abscesses: a combined surgical and medical approach. Neurosurgery 1995;36:76-85; discussion -6.

22. Mampalam TJ, Rosenblum ML. Trends in the management of bacterial brain abscesses: a review of 102 cases over 17 years. Neurosurgery 1988;23:451-8.

23. Mathisen GE, Johnson JP. Brain abscess. Clin Infect Dis 1997;25:763-79; quiz 80-1.

24. Morgan H, Wood MW, Murphey F. Experience with 88 consecutive cases of brain abscess. J Neurosurg 1973;38:698-704.

25. Muzumdar D, Jhawar S, Goel A. Brain abscess: an overview. Int J Surg 2011;9:136-44.

26. Nathoo N, Nadvi SS, Narotam PK, et al. Brain abscess: management and outcome analysis of a computed tomography era experience with 973 patients. World Neurosurg 2011;75:716-26; discussion 612-7.

27. Prasad KN, Mishra AM, Gupta D, et al. Analysis of microbial etiology and mortality in patients with brain abscess. J Infect 2006;53:221-7.

28. Rosenfeld EA, Rowley AH. Infectious intracranial complications of sinusitis, other than meningitis, in children: 12-year review. Clin Infect Dis 1994;18:750-4.

29. Saez-Llorens X. Brain abscess in children. Semin Pediatr Infect Dis 2003;14:108-14.

30. Samson DS, Clark K. A current review of brain abscess. Am J Med 1973;54:201-10.

31. Sarmast AH, Showkat HI, Bhat AR, et al. Analysis and management of brain abscess; a ten year hospital based study. Turk Neurosurg 2012;22:682-9.

32. Schliamser SE, Backman K, Norrby SR. Intracranial abscesses in adults: an analysis of 54 consecutive cases. Scand J Infect Dis 1988;20:1-9.

33. Seydoux C, Francioli P. Bacterial brain abscesses: factors influencing mortality and sequelae. Clin Infect Dis 1992;15:394-401.

34. Stephanov S. Surgical treatment of brain abscess. Neurosurgery 1988;22:724-30.

35. Takeshita M, Kagawa M, Yato S, et al. Current treatment of brain abscess in patients with congenital cyanotic heart disease. Neurosurgery 1997;41:1270-8; discussion 8-9.

36. Tattevin P, Bruneel F, Clair B, et al. Bacterial brain abscesses: a retrospective study of 94

patients admitted to an intensive care unit (1980 to 1999). Am J Med 2003;115:143-6.

37. Tseng JH, Tseng MY. Brain abscess in 142 patients: factors influencing outcome and mortality. Surg Neurol 2006;65:557-62; discussion 62.

38. Xiao F, Tseng MY, Teng LJ, et al. Brain abscess: clinical experience and analysis of prognostic factors. Surg Neurol 2005;63:442-9; discussion 9-50.

39. Yang SY. Brain abscess: a review of 400 cases. J Neurosurg 1981;55:794-9.