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    Distribution of Neisseria meningitidis isolates from blood and cerebrospinal fluid, by year, Bangladesh.

  • 1

    World Health Organization, 2000. Meningococcal Disease. WHO Report on Global Surveillance of Epidemic Prone Infectious Disease. Geneva: World Health Organization. WHO/CDS/ CSR/ISR/2000.1.

  • 2

    World Health Organization, 1999. Laboratory Methods for the Diagnosis of Meningitis Caused by Neisseria meningitidis, Streptococcus pneumoniae and Hemophilus influenzae. Geneva: World Health Organization, WHO/CDC/CSR/EDC/99.7.

  • 3

    Youssef FG, El-Sakka H, Azab A, Eloun S, Chapman GD, Ismail T, Mansour H, Hallaj Z, Mahoney F, 2004. Etiology, antimicrobial susceptibility profiles, and mortality associated with bacterial meningitis among children in Egypt. Ann Epidemiol 14 :44–48.

    • Search Google Scholar
    • Export Citation
  • 4

    Razafindralambo M, Ravelomanana N, Randriamiharisoa FA, Migliani R, Clouzeau J, Raobijaona H, Rasamoelisoa J, Pfister P, 2004. Haemophilus influenzae, the second cause of bacterial meningitis in children in Madagascar. Bull Soc Pathol Exot 97 :100–103.

    • Search Google Scholar
    • Export Citation
  • 5

    Al-Mazrou YY, Al-Jeffri MH, Al-Haggar SH, Musa EK, Mohamed OM, Abdalla MN, 2004. Haemophilus type B meningitis in Saudi children under 5 years old. J Trop Pediatr 50 :131–136.

    • Search Google Scholar
    • Export Citation
  • 6

    Dominguez A, Cardenosa N, Panella H, Orcau A, Companys M, Alseda M, Oviedo M, Carmona G, Minguell S, Salleras L, 2004. Working Group on the Study of Meningococcal Disease in Catalonia, 1990–1997. The case fatality rate of meningococcal disease in Catalonia, 1990–1997. Scand J Infect Dis 36 :274–279.

    • Search Google Scholar
    • Export Citation
  • 7

    Cochi SL, Markowitz L, Joshi DD, Owens RC, Stenhouse DH, Regmi DN, Shresta RP, Lacharya I, Mandhar M, Gurubacharya VL, Owens D, Reingold A, 1987. Control of epidemic group A meningococcal meningitis in Nepal. Int J Epidemiol 16 :91–97.

    • Search Google Scholar
    • Export Citation
  • 8

    Rosenstein NE, Perkins BA, Stephens DS, Lefkowitz L, Cartter ML, Danila R, Cieslak P, Shutt KA, Popovic T, Schuchat A, Harrison LH, Reingold AL, 1999. The changing epidemiology of meningococcal disease in the United States, 1992–1996. J Infect Dis 180 :1894–1901.

    • Search Google Scholar
    • Export Citation
  • 9

    Mastrantonio P, Stefanelli P, Fazio C, Sofia T, Neri A, La RG, Marianelli C, Muscillo M, Caporali MG, Salmaso S, 2003. Serotype distribution, antibiotic susceptibility, and genetic relatedness of Neisseria meningitidis strains recently isolated in Italy. Clin Infect Dis 36 :422–428.

    • Search Google Scholar
    • Export Citation
  • 10

    Yazdankhah SP, Kriz P, Tzanakaki G, Kremastinou J, Kalmusova J, Musilek M, Alvestad T, Jolley KA, Wilson DJ, McCarthy ND, Caugant DA, Maiden MC, 2004. Distribution of serogroups and genotypes among disease-associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J Clin Microbiol 42 :5146–5153.

    • Search Google Scholar
    • Export Citation
  • 11

    Pusponegoro HD, Oswari H, Astrawinata D, Fridawati V, 1998. Epidemiologic study of bacterial meningitis in Jakarta and Tangerang: preliminary report. Pediatr Infect Dis J 17 :S176–S178.

    • Search Google Scholar
    • Export Citation
  • 12

    Choo KE, Ariffin WA, Ahmad T, Lim WL, Gururaj AK, 1990. Pyogenic meningitis in hospitalized children in Kelantan, Malaysia. Ann Trop Paediatr 10 :89–98.

    • Search Google Scholar
    • Export Citation
  • 13

    Manchanda V, Gupta S, Bhalla P, 2006. Meningococcal disease: history, epidemiology, pathogenesis, clinical manifestations, diagnosis, antimicrobial susceptibility and prevention. Indian J Med Microbiol 24 :7–19.

    • Search Google Scholar
    • Export Citation
  • 14

    Singhal S, Purnapatre KP, Kalia V, Dube S, Nair D, Deb M, Aggarwal P, Gupta S, Upadhyay DJ, Rattan A, Raj VS, 2007. Ciprofloxacin resistant Neisseria meningitidis, Delhi, India. Emerg Infect Dis 13 :1614–1616.

    • Search Google Scholar
    • Export Citation
  • 15

    Usman J, Butt T, Jamal S, 2007. Waterhouse-Friderichsen syndrome due to a meningococcal strain unusual in Pakistan. Pak J Pathol 18 :71–72.

    • Search Google Scholar
    • Export Citation
  • 16

    Clinical and Laboratory Standard Institute (CLSI), 2005. Performance Standards for Antimicrobial Susceptibility Testing. Fifteenth Informational Supplement M100-S15; 25 (1). Wayne, PA: CLSI.

  • 17

    Lingappa JR, Al-Rabeah MA, Hajjeh R, Mustafa T, Fatani A, Al-BassamT, Badukhan A, Turkistani AH, Makki S,Al-Hamdan N, Al-Jeffri M, Mazrou YA, Perkins BA, Popovic T, Mayer LW, Rosenstein NE, 2003. Serogroup W-135 meningococcal disease during the Hajj, 2000. Emerg Infect Dis 9 :665–671.

    • Search Google Scholar
    • Export Citation
  • 18

    Aguilera JF, Perrocheau A, Meffre C, Hahne S, 2002. W135 Working Group. Outbreak of serogroup W135 meningococcal disease after the Hajj pilgrimage, Europe, 2000. Emerg Infect Dis 8 :761–767.

    • Search Google Scholar
    • Export Citation
  • 19

    Lindsay AP, Hope V, Marshall RJ, Salinger J, 2002. Meningococcal disease and meteorological conditions in Auckland, New Zealand. Aust N Z Public Health 26 :212–218.

    • Search Google Scholar
    • Export Citation
  • 20

    Jensen ES, Lundbye-Christensen S, Pedersen L, Sorensen HT, Schonheyder HC, 2003. Seasonal variation in meningococcal disease in Denmark: relation to age and meningococcal phenotype. Scand J Infect Dis 35 :226–229.

    • Search Google Scholar
    • Export Citation
  • 21

    Brooks WA, Hossain A, Goswami D, Sharmeen AT, Nahar K, Alam K, Ahmed N, Naheed A, Nair GB, Luby S, Breiman RF, 2005. Bacteremic typhoid fever in children in an urban slum, Bangladesh. Emerg Infect Dis 11 :326–329.

    • Search Google Scholar
    • Export Citation
  • 22

    Botha P, 1988. Penicillin-resistant Neisseria meningitidis in Southern Africa. Lancet ii :54.

  • 23

    Fontanals D, Pineda V, Pons I, Rojo JC, 1989. Penicillin-resistant beta-lactamase producing Neisseria meningitidis in Spain. Eur J Clin Microbiol Infect Dis 8 :90–91.

    • Search Google Scholar
    • Export Citation
  • 24

    Florez C, Garcia-Lopez JL, Martin-Mazuelos E, 1997. Susceptibilities of 55 strains of Neisseria meningitidis isolated in Spain in 1993 and 1994. Chemotherapy 43 :168–170.

    • Search Google Scholar
    • Export Citation
  • 25

    Canica M, Dias R, Nunes B, Carbalho L, Ferreira E, 2004. Meningococcal study group. Invasive culture-confirmed Neisseria meningitidis in Portugal: evaluation of serogroups in relation to different variables and antimicrobial susceptibility (2000–2001). J Med Microbiol 53 :921–925.

    • Search Google Scholar
    • Export Citation

 

 

 

 

Increasing Isolations of Neisseria meningitides Serogroup A from Blood and Cerebrospinal Fluid in Dhaka, Bangladesh, 1999–2006

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  • 1 International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh; Centers for Disease Control and Prevention, Kisumu, Kenya

During 1999–2006, 156 isolates of Neisseria meningitidis grew from culture of blood or cerebrospinal fluid at International Centre for Diarrhoeal Disease Research, Bangladesh, in Dhaka, Bangladesh. Serogroup A was the most prevalent strain (97.7%); the rest were serogroup B (2.3%). Most cases of invasive meningococcal disease (88.5%) were identified in 2002–2004 and most (87.5%) occurred in children, teenagers, and young adults, which reflected a community-wide increase in meningococcal disease incidence during this period, which was not recognized previously. All isolates were susceptible to penicillin, ampicillin, chloramphenicol, ciprofloxacin, and ceftriaxone. Cotrimoxazole resistance steadily increased from 50% to 100% during 2002–2006. Resistance to azithromycin emerged in 2002 (5%), increased to 31% in 2004, but isolates in 2005–2006 were susceptible. Information from broader hospital settings and population-based data would precisely assess trends and impact to define strategies for optimal prevention and empiric therapy.

Bacterial meningitis is a significant cause of death and disability worldwide.1 Of one million estimated annual cases of bacterial meningitis globally, 200,000 die.2 Depending upon age group and etiologic agent, 11–39% of cases result in death.35 A substantial proportion of survivors (12–15%) develop neurologic sequelae, including deafness and mental retardation.2

Infections with Neisseria meningitides, especially meningitis and meningococcemia, are a global concern. 1,68 Neisseria meningitidis is a genetically highly diverse species and only a limited number of serogroups are responsible for most meningococcal disease. Twelve serogroups (A, B, C, H, I, K, L, W135, X,Y, Z, and 29E), on the basis of capsular polysaccharides, are currently recognized.2 Serogroups A, B, C, W135, and Y are the most common causes of meningitis; serogroups A, B, and C account for more than 90% of meningococcal disease. 2,9,10 Serogroup A is the major cause of meningitis outbreaks or epidemics, especially in the African meningitis belt and in Asia. 1,2 Except for Mongolia and China, data on epidemic meningococcal disease and the serogroup pattern of its causative agent from south Asia are limited. 7,1113 Occasional outbreaks caused by serogroup A have been reported from India, Pakistan, and Nepal, 7,14,15 and no data are available from Bangladesh. During review of data on blood isolates, additional N. meningitidis isolates were observed in recent years. We examined data and isolates from blood and cerebrospinal fluid (CSF) to define trends for N. meningitidis isolation, the prevalent serogroups, and antimicrobial drug susceptibility.

Blood and CSF culture results available at the Clinical Microbiology Laboratory of the International Centre for Diarrheal Disease Research, Bangladesh (ICDDR,B) were analyzed from January 1999 through December 2006. The laboratory receives specimens from patients of ICDDR,B Dhaka hospital (who come from a wide geographic area) and those referred to our laboratory from patients admitted to public or private hospitals and clinics in Dhaka, which constitutes approximately 50% of the samples. Thus, it is impossible to estimate a catchment population for this study (which would be needed for incidence rate calculations). Submission of a single set of specimens of blood and/or CSF is the usual practice; multiple sampling from the same patient is rare. There were no changes in methods for isolation of bacteria from blood or CSF during the study period.

A case of suspected meningitis was defined as when dual specimens from blood and CSF from a patient were submitted, and a case of invasive meningococcal disease was defined as a patient from whom N. meningitidis was isolated from blood and/or CSF (isolation either from blood or CSF of a patient was counted as one isolate). Isolation rate was calculated by dividing the number of isolates per year by the number of patients with blood and/or CSF cultures processed per year. Demographic characteristics of patients were obtained from the laboratory record books. This retrospective data analysis was done as pilot activity, which could be useful for future research protocols, and did not require an institutional review board approval.

Isolates of N. meningitidis from blood and CSF were characterized by Gram stain and oxidase and carbohydrate use pattern (positive for glucose and maltose and negative for sucrose and lactose).2 All isolates of N. meningitidis were preserved in chocolate agar slants at −86°C and retrieved for serogrouping. Serogrouping was done by slide agglutination using antibody-coated latex particles polyvalent antisera available commercially (bioMérieux, Marcy l’Etoile, France). Simultaneously, 20 randomly selected isolates were serogrouped at the Centers for Disease Control and Prevention (Atlanta, GA) and identified as serogroup A (Popovic T, unpublished data). These 20 strains were also blindly serogrouped at this laboratory to validate the methods; all strains were correctly identified as serogroup A.

Drug susceptibility for penicillin (10 μg), ampicillin (10 μg), chloramphenicol (30 μg), cotrimoxazole (25 μg), ciprofloxacin (5 μg), ceftriaxone (30 μg), and azithromycin (15 μg) was performed by disk diffusion using Mueller-Hinton agar with 5% heated sheep blood following recommendations of the Clinical and Laboratory Standard Institute (CLSI). 16 Isolates resistant to cotrimoxazole and azithromycin were assessed for minimum inhibitory concentration (MIC) by the E-Test method (AB BIODISK, Solna, Sweden). For cotrimoxazole MIC values, CLSI interpretive breakpoint concentrations for Streptococcus pneumoniae (American Type Culture Collection no. 49619) were applied (susceptible at ≤ 0.5/9.5 μg/mL). For azithromycin, an MIC testing value ≥ 2 μg/mL was considered resistant. 16 For the paired strains from 20 patients who had N. meningitidis isolated from blood and CSF, the serogroup and antimicrobial drug resistance pattern were identical. Thus, we included information from only one isolate for each patient when presenting data on aggregate serogroup and antimicrobial drug resistance.

A total of 53,139 blood and 3,319 CSF specimens were obtained. We focused on the 3,072 dual specimens (i.e., CSF and blood from same patients), of which pathogens were isolated from 628 (20.4%), including N. meningitidis (n = 156, 24.8%), Haemophilus influenzae (n = 31, 4.9%), and S. pneumoniae (n = 71, 11.3%). The remaining blood isolates were S. enterica serovar Typhi (n = 188, 29.9%) and other isolates (n = 182, 29%) included Escherichia coli, Staphylococcus aureus, S. pyogenes, Klebsiella spp., and Pseudomonas spp. Neisseria meningitidis was detected only by latex agglutination in nine specimens, four from CSF and five from blood. These results were not included in this analysis, which focuses on culture-positive specimens.

Of the 156 N. meningitidis isolates, 89 (57%) were from blood and 67 (43%) from CSF, including those from 20 patients who had N. meningitidis isolated from blood and CSF (Figure 1). Most cases of invasive meningococcal disease (88.5%) were identified during 2002–2004 from a higher number of specimens processed during those years. The rate (proportion) of isolation from blood cultures during 2002–2004 increased nearly 5-fold when compared with 2001 and > 15-fold when compared with 1999 and 2000. The rate of isolation from CSF increased > 5-fold in 2002 through 2004 when compared with 2001 and > 6-fold when compared with 1999 and 2000. The highest number of cases occurred in 2004. It was noteworthy that there were no changes in the isolation rates for S. pneumoniae and S. enterica serovar Typhi during the study period. However, the isolation rate of N. meningitidis from blood and CSF decreased in 2005 and 2006.

Serogrouping was done on isolates from 132 patients (4 isolates from 1999 and 2000 were not serogrouped); 129 isolates (97.7%) were serogroup A and 3 (2.3%) were serogroup B. Meningococcal disease had no distinct seasonality. However, during 2002–2004, 41 isolates (42%) were obtained during the cool and dry months of January through March. Most (60.2%) patients were > 15 years of age; 29.4% were 6–14 years of age and 10.3% were less than five years of age (Table 1). All but 13 patients were less than 40 years of age. For the 123 patients for whom sex information was available, 87 (70.7%) were males.

All meningococcal isolates (156) were susceptible to penicillin, ampicillin, chloramphenicol, ceftriaxone, and ciprofloxacin. Azithromycin resistance appeared during 2002–2004 (none was resistant in 1999–2001), 5% resistance was found in 2002, 27% in 2003, and 31% in 2004, but all isolates in 2005–2006 were susceptible. Isolates resistant to azithromycin showed high MIC values (ranging from ≥ 4 to 256 μg/mL; 25% of the isolates had MICs ≥ 256 μg/mL). Resistance to cotrimoxazole increased from 50% in 2000 to 80% in 2001, 89% in 2002, and 100% since 2003. All strains resistant to cotrimoxazole had MICs ≥ 4–76 μg/mL.

Epidemic meningococcal disease caused by N. meningitidis has had a devastating effect in sub-Saharan Africa.1 Although there is no known “similar meningococcal belt” in Asia, outbreaks associated with overcrowded settings, refugee camps, and gatherings such as the Hajj represent immense public health challenges because infected people can become ill after returning home, resulting in spread of illness through respiratory secretions and outbreaks to people in a large number of countries. 17,18 In China and in the African meningitis belt, serogroup A remains the major cause of meningococcal-associated death.2 Recent Hajj-associated epidemics have involved N. meningitidis serogroup W-135 and serogroup A. 17,18 This study documented a disproproportionate number of meningococcal disease cases (nearly all serogroup A) in Bangladesh during 2002–2004 when compared with earlier or later years. We were not able to obtain information on genotype, which might have been useful in comparing strains from Bangladesh with those of other countries in the region and in the African meningitis belt.

The increased isolation rate of N. meningitidis may have reflected a community-wide change in meningococcal disease incidence. The increase in isolation rate and presumably the disease incidence was likely caused by outbreaks. Although we did not document marked seasonality, there was a slightly increased rate of isolation during the cool dry season (January through March) and some decrease during monsoon season (July through September), which is consistent with patterns noted in Nepal in 1983–1984,7 in Delhi in 2006, 12,13 and in other countries. 19,20 In the absence of changes in methods during the study period, the increased isolation in 2002–2004 likely reflected a valid increase in meningococcal meningitis disease, not merely increased isolation caused by greater specimen flow in the laboratory or enhanced capacity to isolate the bacteria.

The increased number of isolates in specimens from patients at ICDDR,B Hospital, as well as from other public private facilities, is consistent with the notion that there may have been community outbreaks ongoing during that period. Because no national surveillance data on meningitis exist in Bangladesh, we cannot be certain that our observations represent national trends. Surveillance is needed in a number of hospital settings in Bangladesh to better characterize disease patterns. Data from this study do not provide population denominators with which incidence rates can be calculated.

Of substantial interest, outside the scope of this report, is the high number of cases of bacteremic typhoid fever in patients suspected to have meningitis. Salmonella Typhi appears to be a major cause of bacteremia in an urban slum area of Dhaka, 20 and may represent an important vaccine-preventable disease.

Monitoring of antimicrobial drug resistance patterns is important to guide empiric therapy and reduce morbidity and mortality where case-based antimicrobial drug susceptibility testing is limited. Although reported elsewhere, 21 we did not find meningococcal isolates resistant to penicillin and chloramphenicol. In contrast to reports from Delhi in 2005 and 2006, 13 we did not find resistance to ciprofloxacin or ceftriaxone. Cephalosporin-resistant strains of serogroup B and C meningococci caused by β-lactamase have also been reported. 22,23 Our study suggests that cotrimoxazole is not useful for therapy in Bangladesh, as reported elsewhere. 24,25 Emergence of azithromycin resistance among the isolates in 2002–2004 was alarming, but the isolates in 2005–2006 were susceptible. The shift was likely caused by cycling in and out of various strains of N. meningitidis within communities in Bangladesh. Active surveillance for meningococcal disease would be helpful to define high-risk populations and impact of disease, which could suggest strategies for focused targeted prevention and control measures such as vaccine use in Bangladesh.

Table 1

Age and sex distribution of patients infected with Neisseria meningitidis from blood and cerebrospinal fluid, Bangladesh, 1999–2006

Table 1
Figure 1.
Figure 1.

Distribution of Neisseria meningitidis isolates from blood and cerebrospinal fluid, by year, Bangladesh.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 4; 10.4269/ajtmh.2009.80.615

*

Address correspondence to M. Anowar Hossain, Clinical Laboratory Services, Laboratory Sciences Division, International Centre for Diarrhoeal Disease Research, Bangladesh, 68 Shahid Tajuddin Ahmed Sarani, Mohakhali, Dhaka 1212, Bangladesh. E-mail: anowar@icddrb.org

Authors’ addresses: M. Anowar Hossain, Dilruba Ahmed, Tahmeed Ahmed, and Nazrul Islam, International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh. Robert F. Breiman, Centers for Disease Control and Prevention, Kisumu, Kenya.

Acknowledgments: We thank all donors for support and commitment to the Centre’s research efforts. We also thank Dr. Tanja Popovic (Centers for Disease Control and Prevention, Atlanta, GA) for confirmation of serogrouping of 20 strains within her laboratory, and Shahriar Bin Elahi (Clinical Laboratory Services) for compilation of laboratory data.

Financial support: This study was supported by the ICDDR, B and its donors, who provide unrestricted support to the centre for its operations and research. Current donors providing unrestricted support include the Australian International Development Agency, the Canadian International Development Agency, the Department for International Development, United Kingdom, the Government of Bangladesh, the Government of Japan, the Government of Sri Lanka, the Government of the Netherlands, the Swedish International Development Cooperative Agency, and the Swiss Development Cooperation.

REFERENCES

  • 1

    World Health Organization, 2000. Meningococcal Disease. WHO Report on Global Surveillance of Epidemic Prone Infectious Disease. Geneva: World Health Organization. WHO/CDS/ CSR/ISR/2000.1.

  • 2

    World Health Organization, 1999. Laboratory Methods for the Diagnosis of Meningitis Caused by Neisseria meningitidis, Streptococcus pneumoniae and Hemophilus influenzae. Geneva: World Health Organization, WHO/CDC/CSR/EDC/99.7.

  • 3

    Youssef FG, El-Sakka H, Azab A, Eloun S, Chapman GD, Ismail T, Mansour H, Hallaj Z, Mahoney F, 2004. Etiology, antimicrobial susceptibility profiles, and mortality associated with bacterial meningitis among children in Egypt. Ann Epidemiol 14 :44–48.

    • Search Google Scholar
    • Export Citation
  • 4

    Razafindralambo M, Ravelomanana N, Randriamiharisoa FA, Migliani R, Clouzeau J, Raobijaona H, Rasamoelisoa J, Pfister P, 2004. Haemophilus influenzae, the second cause of bacterial meningitis in children in Madagascar. Bull Soc Pathol Exot 97 :100–103.

    • Search Google Scholar
    • Export Citation
  • 5

    Al-Mazrou YY, Al-Jeffri MH, Al-Haggar SH, Musa EK, Mohamed OM, Abdalla MN, 2004. Haemophilus type B meningitis in Saudi children under 5 years old. J Trop Pediatr 50 :131–136.

    • Search Google Scholar
    • Export Citation
  • 6

    Dominguez A, Cardenosa N, Panella H, Orcau A, Companys M, Alseda M, Oviedo M, Carmona G, Minguell S, Salleras L, 2004. Working Group on the Study of Meningococcal Disease in Catalonia, 1990–1997. The case fatality rate of meningococcal disease in Catalonia, 1990–1997. Scand J Infect Dis 36 :274–279.

    • Search Google Scholar
    • Export Citation
  • 7

    Cochi SL, Markowitz L, Joshi DD, Owens RC, Stenhouse DH, Regmi DN, Shresta RP, Lacharya I, Mandhar M, Gurubacharya VL, Owens D, Reingold A, 1987. Control of epidemic group A meningococcal meningitis in Nepal. Int J Epidemiol 16 :91–97.

    • Search Google Scholar
    • Export Citation
  • 8

    Rosenstein NE, Perkins BA, Stephens DS, Lefkowitz L, Cartter ML, Danila R, Cieslak P, Shutt KA, Popovic T, Schuchat A, Harrison LH, Reingold AL, 1999. The changing epidemiology of meningococcal disease in the United States, 1992–1996. J Infect Dis 180 :1894–1901.

    • Search Google Scholar
    • Export Citation
  • 9

    Mastrantonio P, Stefanelli P, Fazio C, Sofia T, Neri A, La RG, Marianelli C, Muscillo M, Caporali MG, Salmaso S, 2003. Serotype distribution, antibiotic susceptibility, and genetic relatedness of Neisseria meningitidis strains recently isolated in Italy. Clin Infect Dis 36 :422–428.

    • Search Google Scholar
    • Export Citation
  • 10

    Yazdankhah SP, Kriz P, Tzanakaki G, Kremastinou J, Kalmusova J, Musilek M, Alvestad T, Jolley KA, Wilson DJ, McCarthy ND, Caugant DA, Maiden MC, 2004. Distribution of serogroups and genotypes among disease-associated and carried isolates of Neisseria meningitidis from the Czech Republic, Greece, and Norway. J Clin Microbiol 42 :5146–5153.

    • Search Google Scholar
    • Export Citation
  • 11

    Pusponegoro HD, Oswari H, Astrawinata D, Fridawati V, 1998. Epidemiologic study of bacterial meningitis in Jakarta and Tangerang: preliminary report. Pediatr Infect Dis J 17 :S176–S178.

    • Search Google Scholar
    • Export Citation
  • 12

    Choo KE, Ariffin WA, Ahmad T, Lim WL, Gururaj AK, 1990. Pyogenic meningitis in hospitalized children in Kelantan, Malaysia. Ann Trop Paediatr 10 :89–98.

    • Search Google Scholar
    • Export Citation
  • 13

    Manchanda V, Gupta S, Bhalla P, 2006. Meningococcal disease: history, epidemiology, pathogenesis, clinical manifestations, diagnosis, antimicrobial susceptibility and prevention. Indian J Med Microbiol 24 :7–19.

    • Search Google Scholar
    • Export Citation
  • 14

    Singhal S, Purnapatre KP, Kalia V, Dube S, Nair D, Deb M, Aggarwal P, Gupta S, Upadhyay DJ, Rattan A, Raj VS, 2007. Ciprofloxacin resistant Neisseria meningitidis, Delhi, India. Emerg Infect Dis 13 :1614–1616.

    • Search Google Scholar
    • Export Citation
  • 15

    Usman J, Butt T, Jamal S, 2007. Waterhouse-Friderichsen syndrome due to a meningococcal strain unusual in Pakistan. Pak J Pathol 18 :71–72.

    • Search Google Scholar
    • Export Citation
  • 16

    Clinical and Laboratory Standard Institute (CLSI), 2005. Performance Standards for Antimicrobial Susceptibility Testing. Fifteenth Informational Supplement M100-S15; 25 (1). Wayne, PA: CLSI.

  • 17

    Lingappa JR, Al-Rabeah MA, Hajjeh R, Mustafa T, Fatani A, Al-BassamT, Badukhan A, Turkistani AH, Makki S,Al-Hamdan N, Al-Jeffri M, Mazrou YA, Perkins BA, Popovic T, Mayer LW, Rosenstein NE, 2003. Serogroup W-135 meningococcal disease during the Hajj, 2000. Emerg Infect Dis 9 :665–671.

    • Search Google Scholar
    • Export Citation
  • 18

    Aguilera JF, Perrocheau A, Meffre C, Hahne S, 2002. W135 Working Group. Outbreak of serogroup W135 meningococcal disease after the Hajj pilgrimage, Europe, 2000. Emerg Infect Dis 8 :761–767.

    • Search Google Scholar
    • Export Citation
  • 19

    Lindsay AP, Hope V, Marshall RJ, Salinger J, 2002. Meningococcal disease and meteorological conditions in Auckland, New Zealand. Aust N Z Public Health 26 :212–218.

    • Search Google Scholar
    • Export Citation
  • 20

    Jensen ES, Lundbye-Christensen S, Pedersen L, Sorensen HT, Schonheyder HC, 2003. Seasonal variation in meningococcal disease in Denmark: relation to age and meningococcal phenotype. Scand J Infect Dis 35 :226–229.

    • Search Google Scholar
    • Export Citation
  • 21

    Brooks WA, Hossain A, Goswami D, Sharmeen AT, Nahar K, Alam K, Ahmed N, Naheed A, Nair GB, Luby S, Breiman RF, 2005. Bacteremic typhoid fever in children in an urban slum, Bangladesh. Emerg Infect Dis 11 :326–329.

    • Search Google Scholar
    • Export Citation
  • 22

    Botha P, 1988. Penicillin-resistant Neisseria meningitidis in Southern Africa. Lancet ii :54.

  • 23

    Fontanals D, Pineda V, Pons I, Rojo JC, 1989. Penicillin-resistant beta-lactamase producing Neisseria meningitidis in Spain. Eur J Clin Microbiol Infect Dis 8 :90–91.

    • Search Google Scholar
    • Export Citation
  • 24

    Florez C, Garcia-Lopez JL, Martin-Mazuelos E, 1997. Susceptibilities of 55 strains of Neisseria meningitidis isolated in Spain in 1993 and 1994. Chemotherapy 43 :168–170.

    • Search Google Scholar
    • Export Citation
  • 25

    Canica M, Dias R, Nunes B, Carbalho L, Ferreira E, 2004. Meningococcal study group. Invasive culture-confirmed Neisseria meningitidis in Portugal: evaluation of serogroups in relation to different variables and antimicrobial susceptibility (2000–2001). J Med Microbiol 53 :921–925.

    • Search Google Scholar
    • Export Citation
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