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 Table of Contents  
ORIGINAL ARTICLE
Year : 2015  |  Volume : 2  |  Issue : 2  |  Page : 79-84

Epidemiology and Clinical Outcomes of Community Acquired Pneumococcal Infection in North-West Nigeria


1 Department of Medicine, Faculty of Clinical Science, College of Health Sciences, Bayero University Kano, Kano, Nigeria
2 Department of Microbiology, Aminu Kano Teaching Hospital, Kano, Nigeria

Date of Submission23-Dec-2014
Date of Acceptance12-Mar-2015
Date of Web Publication20-May-2015

Correspondence Address:
Dr. Garba Iliyasu
Department of Medicine, College of Health Sciences, Bayero University Kano, Kano
Nigeria
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DOI: 10.4103/2384-5147.157429

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  Abstract 

Introduction: Pneumococcal infection is a leading cause of morbidity and mortality worldwide. There is a paucity of data on pneumococcal infection in Nigeria. We aimed to determine the epidemiology and clinical outcome of pneumococcal infection in a Tertiary Referral Center in Northwestern Nigeria. Materials and Methods: We conducted a prospective, hospital-based study on patients with community acquired pneumococcal infections. All studied subjects had clinical evaluation and relevant laboratory investigations. The outcome was defined as mortality. Analysis was carried out using descriptive statistics with differences and relationships determined using Student's t-test, Chi-squared and Fisher's exact tests as appropriate, with P < 0.05 regarded as significant. Result: Three hundred and two cases of bacteriologically proven community acquired pneumonia (241/302), bacteremia (38/302) and meningitis (23/302) were screened, out of which 125/241 (51.7%), 7/23 (30.4%) and 8/38 (21.1%) were pneumococcal pneumonia, pneumococcal meningitis and pneumococcal bacteremia, respectively. Most of the patients, 87/140 (69.3%) had comorbidity conditions. The overall mortality rate was 12.9%. Chronic heart disease (odds ratio [OR] = 1.143; 95% confidence interval [CI] = 0.032-0.638), human immunodeficiency virus infection (OR = 2.309; 95% CI = 1.258-4.241), age ≥65 years (OR = 6.397; 95% CI = 2.181-18.746), and infection with multi-drug resistant Pneumococcus (OR = 4.089; 95% CI = 1.274-13.125) were identified as independent risk factors for mortality. Conclusion: The Pneumococcus is a common cause of community acquired infections among adults in northwestern Nigeria, with associated high mortality.

Keywords: Community acquired, infection, Nigeria, pneumococcal


How to cite this article:
Iliyasu G, Habib AG, Mohammed AB, Borodo MM. Epidemiology and Clinical Outcomes of Community Acquired Pneumococcal Infection in North-West Nigeria. Sub-Saharan Afr J Med 2015;2:79-84

How to cite this URL:
Iliyasu G, Habib AG, Mohammed AB, Borodo MM. Epidemiology and Clinical Outcomes of Community Acquired Pneumococcal Infection in North-West Nigeria. Sub-Saharan Afr J Med [serial online] 2015 [cited 2019 Sep 21];2:79-84. Available from: http://www.ssajm.org/text.asp?2015/2/2/79/157429


  Introduction Top


Streptococcus pneumoniae, otherwise call the Pneumococcus has remained an extremely important human bacterial pathogen since its initial recognition in the late 1800 s. Worldwide, it remains the most common cause of community-acquired pneumonia (CAP), sporadic bacterial meningitis and bacteremia. [1],[2] It is an important public health concern throughout the world and as a leading cause of lower respiratory tract infection, its global burden in causing disease and deaths is comparable to that of the human immunodeficiency virus (HIV), malaria and tuberculosis. [3] Africa and Asia account for the greatest proportion of pneumococcal infection worldwide, and together they account for 66% of cases worldwide. [4] Nigeria accounts for 5% of the total burden at the third place after India and China. [3] Since no population-based data on pneumococcal infection in most developing countries are available, the estimates of disease burden are based on small clinical studies, vaccine trials, extrapolation from data in developed countries, and studies of persons at high risk for disease. Incidence rate of 416 and 388/100,000 were reported among children <5 and 3 years in Mozambique and Gambia, respectively. [5],[6] While in Europe and the United States, the annual incidence of invasive pneumococcal infections (IPI) ranges from 10 to 100/100,000 with a mortality rate of 10-50%; the highest values were seen in elderly subjects aged 65 years or more. [7] In a prospective study of adults with bacteremic pneumococcal pneumonia in Canada, an overall incidence of 9.7 cases/100,000 population was found. [8] The World Health Organization estimated that 1.6 million people die from pneumococcal disease every year, [9] with developing countries bearing the greatest burden. [10]

Risk factors for IPI include; extremes of age, certain racial and ethnic groups, and underlying medical conditions such as diabetes mellitus, chronic heart disease (CHD), chronic pulmonary disease, chronic renal failure, alcohol abuse, functional (such as sickle cell anemia) or anatomic asplenia etc. [11],[12],[13],[14],[15] HIV infection can also substantially increase the risk of pneumococcal infection. [16],[17] Among adults aged 18-55 years with HIV infection, Breiman et al., [18] found that African Americans, current smokers, and persons who had close contact with children were at increased risk.

Knowledge on pneumococcal infection among the adult population in Nigeria is lacking. The main objective of this study was to describe the epidemiology and outcome of community-acquired pneumococcal infections among adults, as seen in a Tertiary Referral Hospital in North-western Nigeria.


  Materials and Methods Top


We conducted a prospective study among patients attending Aminu Kano Teaching Hospital (AKTH) between June 2009 and January 2011. All adult 18 years and above with a diagnosis of either CAP, meningitis or bacteremia were included. The hospital provides tertiary care and serves as a major referral center for other states in North-western Nigeria and neighboring Niger republic. It has 550 beds and offers specialist inpatient and outpatient care, across various specialties.

Participants

All adult patients who were admitted over the study period with features compatible with CAP, meningitis and bacteremia were screened for inclusion. Patients <18 years and those who did not consent were excluded from the study. A sputum specimen was collected in a clean, sterile container from patients with the clinical diagnosis of pneumonia. Blood samples were collected from all the patients and inoculated directly into each of brain-heart infusion and thioglycolate culture medium, with the use of standard aseptic procedures for aerobic and anaerobic cultures, respectively. All those who presented with clinical features of compatible with meningitis had a lumbar puncture provided no contraindications exist. The cerebrospinal fluid (CSF) samples were collected in a clean, sterile container and were sent to the laboratories for microbiological analysis, cell count and for glucose and protein measurement. A blood sample was drawn for random plasma glucose measurement just before the lumbar puncture was performed, for comparison with the CSF glucose level. All Samples were taken before administering antibiotic whenever feasible and transported to the laboratory immediately. All patients who consented were screened for HIV infection using two consecutive rapid tests (determine and unigold). Posttest counseling was done for those who tested positive and enrolled in to HIV care program, those that tested negative were enlightened on how to remain negative.

Laboratory Analysis

The laboratory operates 24 h/day and is able to process CSF specimen within 30 min of receipt. All samples of sputum and CSF were inoculated onto 5% sheep blood agar and incubated at 37°C. Inoculated plates were incubated in a candle jar so as to create a reduced oxygen tension (5-10% additional CO 2 tension). Inoculated blood culture bottles were incubated in the laboratory at 37°C and observed for bacterial growth within 24-72 h and then until day 7 if there was no bacterial growth earlier. Inoculated media were sub-cultured onto blood agar plates and incubated as per CSF and sputum twice, on days 2 and 3 after incubation. Plates were examined for growth, by the use of standard procedures. Samples of all typical pneumococcal colonies obtained were subjected to further identification methods (presence of α-haemolysis, colony morphology and ethylhydrocupreine hydrochloride (optochin) sensitivity. Only samples with microbiologically proven isolates were finally selected for the study.

Microbial susceptibility tests were carried out on all confirmed pneumococcal isolates to penicillin G, cefotaxime, ceftriaxone, tetracycline, trimethoprim/sulfamethoxazole, erythromycin, ofloxacin and chloramphenicol using E-test strips (AB BIODISK, Sweden). Minimum inhibitory concentration was measured and strains were divided into resistant, intermediate or sensitive according to the Clinical and Laboratory Standard Institute guidelines. [19] Multi-drug resistant (MDR) Pneumococcus was defined as resistance to at least ≥3 classes of antibiotics. [20]

Definitions

pneumococcal pneumonia was defined based on clinical plus chest radiographic findings consistent with pneumonia, in addition to a positive culture of S. pneumonia from an ideal sputum specimen defined as the presence of more than 25 white cells and <10 squamous epithelial cells per low power field. Pneumococcal meningitis was defined as isolation of S. pneumoniae from a CSF sample in a patient with clinical evidence of meningitis. Pneumococcal bacteremia was defined as isolation of S. pneumonia from the blood sample collected aseptically.

The following clinical data of all patients with bacteriologically proven IPI were collected and analyzed: Demographic data, clinical features, co-morbidities, HIV serostatus, antibiotic susceptibility result and outcome (mortality) at 1-month after discharge. All patients were managed according to the hospital's standard protocol for IPI, and none of the patients received steroids.

Data Analysis

Analysis was carried out using descriptive statistics with differences and relationships determined using Student's t-test, Chi-square and Fisher's exact tests as appropriate, with P ≤ 0.05 regarded as significant. Determinants and predictors were explored using univariate and multivariable analysis with unadjusted (crude) odds ratio (OR) and logistic regression adjusted, respectively. Statistical Package for Social Sciences version 16.0 was used (SPSS, Illinois Chicago, USA).

Ethics Approval

Ethical clearance was obtained from the ethics committee of AKTH. Informed consent was obtained from the patients or their legal representatives.


  Results Top


The ages of the patients ranged from 18 to 82 years, with a mean age of 42.7 years (±18.74). The peak age groups were 55-64 years and ≥65 years [Figure 1]. There were 73/140 (52.1%) males and 67/140 (47.9%) females with a male-to-female ratio of 1.09. Out of the 140 patients, 98 (74.2%) consented for HIV screening and 19 (19.4%) were positive.
Figure 1: Age and sex distribution of patients

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During the study period, 302 cases of bacteriologically proven community-acquired infections (241 pneumonia, 38 bacteremia, 23 meningitis) were screened, out of which 125/241 (51.7%), 7/23 (30.4%) and 8/38 (21.1%) were pneumococcal pneumonia, pneumococcal meningitis and pneumococcal bacteremia syndromes, respectively [Table 1]. This translates to 140/302 (46.4%) of the total community acquired infections seen during the study period. Of the 125 patients with pneumococcal pneumonia, there were 6 (4.8%) cases of bacteremic pneumonia. Pneumococcal vaccination was not documented in any of the patients.
Table 1: Demographic and clinical characteristics of the patients

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Significant number of the patients, 67/140 (47.9%) had at least one comorbidity while 20 had at least two comorbid conditions. The most common being chronic pulmonary disease 23/67 (34.3%), HIV 19/67 (28.4%), sickle cell anemia 15/67 (22.4%), CHD 10/67 (14.9%). While 20/140 (14.3%) of the patients were smokers [Table 1].

Eight patients were lost to follow-up; all among those with pneumonia and 17 died; giving an overall mortality of 17/132 (12.9%), at 1-month. [Table 2] shows the outcomes for each pneumococcal syndrome; with the highest mortality seen in those with meningitis. Out of the 17 patients who died, 10/17 (58.8%) were aged 65 years or older while the remaining 7/17 (41.2%) were in the 15-64 year age brackets (P = 0.001), there was a slight peak at the 35-44 year age group with 3/17 (17.6%) deaths while no death was recorded in the 25-34 year age group. There was significantly higher mortality among those who were HIV positive compared to HIV negative patients (6/19 [31.6%] vs. 8/79 [10.1%], P = 0.016).
Table 2: Outcome of the patients, according to clinical syndrome

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One hundred and thirty two pneumococcal isolates were tested against panels of commonly used antibiotics; 19/132 (14.4%) were resistant to at least one class of antibiotic, 42/132 (31.8%) were resistant to two classes of antibiotics while 71/132 (53.8%) were resistant to three or more classes of antibiotics (MDR). None of the isolates was susceptible to all the antibiotics tested. Most of the isolates were sensitive to ceftriaxone (96.2%), chloramphenicol (80.3%) and amoxicillin (78.8%), while most were resistant to trimethoprim/sulfamethoxazole (96.2%). Mortality was higher among those infected with MDR Pneumococcus2 = 9.315, P = 0.003) [Table 3].
Table 3: Outcomes, according to number of class of antibiotic resistance

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On multiple logistic regression analysis the only factors predictive of mortality were CHD (OR = 1.143; 95% CI = 0.032-0.638), HIV (OR = 2.309; 95% CI = 1.258-4.241), age ≥65 years (OR = 6.397; 95% CI = 2.181-18.746), and infection with MDR Pneumococcus (OR = 4.089; 95% CI = 1.274-13.125).


  Discussion Top


There is a paucity of data on pneumococcal infection in Nigeria, even though there is a large body of information on the same subject from the western literature. This is primarily a clinical study on pneumococcal infection which addresses the epidemiology, pattern of presentation and clinical outcomes of the major pneumococcal syndromes, as observed in a Tertiary Teaching Hospital in North-western Nigeria.

The Pneumococcus is the commonest cause of CAP, meningitis and bacteremia worldwide. [1],[2] In this study, it represented 46.4% of CAP, community acquired meningitis and community acquired bacteremia, with pneumonia being the commonest syndrome 125/140 (89.3%). This is similar to a report by Rueda et al., where they found a rate of 85%, 5.1% and 3.7% for pneumonia, bacteremia and meningitis, respectively. [21] A higher rate of bacteraemia and meningitis in children compared to adults has been previously reported. [22] In the past three decades, studies of the etiology of CAP in Nigeria reported Pneumococcus as the most common cause. [23],[24],[25],[26] It was also shown to be the most prevalent isolate among patients with community acquired sporadic meningitis in northeastern Nigeria. [27] Data on the prevalence of community acquired pneumococcal bacteremia in Nigeria is scanty, however this study highlighted the significance of Pneumococcus as an important cause of community acquired bacteremia in northwestern Nigeria, which is in keeping with reports from other parts of the world. [2] Pneumococcal infection is believed to have been under-reported in Nigeria because of the fastidious nature of the organism and the use of human blood for preparation of blood agar. We used sheep blood in this study. Our case definition for pneumococcal pneumonia was limited to clinical findings, chest X-ray features and isolation of S. pneumonia from sputum specimen, because of the restriction in our ethical approval. This was a major limitation as our data might not have described true invasive pneumococcal pneumonia.

Invasive pneumococcal infection is known to be a disease of the very young and the elderly. [5] We noted a significant number of patients within the 55-64 year age group and 65 years and above. The lower number among those aged ≥65 years may be explained by the low life expectancy in Nigeria with fewer people above 65 years of age, while the small peak at 35-45 year age group may have been as a result of the high HIV (identified as one of the major risk factors in this study) prevalence within this age group, this pattern was also observed by Kyaw et al. in Australia. [28] There was also a notable higher incidence among males compared to females, with a relative increase in number of females over males between 18 and 44 years (female reproductive age group). Female gender has been previously shown to be a risk factor for pneumococcal infections, because of close proximity to children. [18],[29],[30]

Although it was a hospital based study, high rate of HIV infection (19.4%) was observed among the patients studied when compared with Nigerian prevalence of 5%. [31] HIV infection has been associated with increased risk of IPI in several studies. [16],[32],[33],[34]

The overall mortality rate of 12.6% was lower than the mortality rate of 39% reported in the 1980 s in Zaria, Nigeria, [29] this might be as a result of the differences in the study population and probable change in the serotype and virulence of the pneumococcal strain involved. Mortality rate of 12% and 16% were reported by Klemets et al. [35] and Rueda et al.[36] Mortality in IPI varies according to the syndrome, with meningitis having the most fatal outcome followed by bacteremic pneumonia. We found statistically significant higher mortality among patients with meningitis and less among those with nonbacteremic pneumonia. Poor outcome in pneumococcal meningitis has been linked to the persistence of bacteria and their products in the CSF following effective antibiotic treatment in contrast to rapid clearance in meningococcal meningitis. [37] Even though the number of patients with bacteremic pneumococcal pneumonia in our study was small, the mortality among this group was relatively high, which is similar to what has been reported elsewhere. [38],[39],[40] In addition to being at higher absolute risk for disease, older adults are also at much higher risk of death following IPI. [41],[42] This is reflected in our study where the mortality in those aged ≥65 years was significantly higher compared to those <65 years.

There is documented evidence that pneumococcal infections outside the central nervous system, caused by pneumococci with reduced susceptibility to penicillin respond well to penicillin given in appropriate doses. [43] Majority of the patients in this study had pneumonia, this could have explained the lack of independent association between penicillin resistance and mortality, however there was a statistically significant increase in mortality among those infected with MDR Pneumococcus (P < 0.003).

Human immunodeficiency virus-infected patients in Africa are vulnerable to severe recurrent infection with Pneumococcus; they also have higher mortality. [44] In our analysis, mortality was significantly higher among those who were HIV positive, compared to HIV negative patients, this has been shown in other studies. [34],[45] Degree of immunosuppression has been shown to be the most relevant factor associated with mortality; [45] this a major limitation in our finding.

Using logistic regression, age ≥65 years, CHD, HIV, and infection with MDR pneumococci were identified as predictors of mortality, which is in agreement with most studies. [34],[40],[41],[46],[47],[48],[49]


  Conclusion Top


Streptococcus pneumonia is a common cause of community-acquired infection among adult in North-western Nigeria, and mortality rate is high. Resistance to commonly used antibiotics is common which also impacts on the outcome. The findings of this study underscore the need for pneumococcal vaccination among at-risk individuals and provide important baseline data on antimicrobial resistance for continuous surveillance in this region. There is also a need for a community based pneumococcal disease surveillance including pneumococcal serotypes for effective vaccine introduction in Nigeria.

 
  References Top

1.
Marston BJ, Plouffe JF, File TM Jr, Hackman BA, Salstrom SJ, Lipman HB, et al. Incidence of community-acquired pneumonia requiring hospitalization. Results of a population-based active surveillance Study in Ohio. The Community-Based Pneumonia Incidence Study Group. Arch Intern Med 1997;157:1709-18.  Back to cited text no. 1
    
2.
Schuchat A, Robinson K, Wenger JD, Harrison LH, Farley M, Reingold AL, et al. Bacterial meningitis in the United States in 1995. Active Surveillance Team. N Engl J Med 1997;337:970-6.  Back to cited text no. 2
    
3.
World Health Organisation. The Global Burden of Disease: 2014 Update. Geneva, Switzerland. Available from: http://www.who.int/healthinfo/global burden disease/GBD report 2014 update. [Last accessed on 2015 Jan 26].  Back to cited text no. 3
    
4.
O′Brien KL, Wolfson LJ, Watt JP, Henkle E, Deloria-Knoll M, McCall N, et al. Burden of disease caused by Streptococcus pneumoniae in children younger than 5 years: Global estimates. Lancet 2009;374:893-902.  Back to cited text no. 4
    
5.
Roca A, Sigaúque B, Quintó L, Mandomando I, Vallè]s X, Espasa M, et al. Invasive pneumococcal disease in children<5 years of age in rural Mozambique. Trop Med Int Health 2006;11:1422-31.  Back to cited text no. 5
    
6.
Cutts FT, Zaman SM, Enwere G, Jaffar S, Levine OS, Okoko JB, et al. Efficacy of nine-valent pneumococcal conjugate vaccine against pneumonia and invasive pneumococcal disease in the Gambia: Randomised, double-blind, placebo-controlled trial. Lancet 2005;365:1139-46.  Back to cited text no. 6
    
7.
Cartwright K. Pneumococcal disease in Western Europe: Burden of disease, antibiotic resistance and management. Eur J Pediatr 2002;161:188-95.  Back to cited text no. 7
    
8.
Shariatzadeh MR, Huang JQ, Tyrrell GJ, Johnson MM, Marrie TJ. Bacteremic pneumococcal pneumonia: A prospective study in Edmonton and neighboring municipalities. Medicine (Baltimore) 2005;84:147-61.  Back to cited text no. 8
    
9.
Pneumococcal conjugate vaccine for childhood immunization - WHO position paper. Wkly Epidemiol Rec 2007;82:93-104.  Back to cited text no. 9
    
10.
Scott JA. The preventable burden of pneumococcal disease in the developing world. Vaccine 2007;25:2398-405.  Back to cited text no. 10
    
11.
Gentile JH, Sparo MD, Mercapide ME, Luna CM. Adult bacteremic pneumococcal pneumonia acquired in the community. A prospective study on 101 patients. Medicina (B Aires) 2003;63:9-14.  Back to cited text no. 11
    
12.
Laupland KB, Gregson DB, Zygun DA, Doig CJ, Mortis G, Church DL. Severe bloodstream infections: A population-based assessment. Crit Care Med 2004;32:992-7.  Back to cited text no. 12
    
13.
Talbot TR, Hartert TV, Mitchel E, Halasa NB, Arbogast PG, Poehling KA, et al. Asthma as a risk factor for invasive pneumococcal disease. N Engl J Med 2005;352:2082-90.  Back to cited text no. 13
    
14.
Romney MG, Hull MW, Gustafson R, Sandhu J, Champagne S, Wong T, et al. Large community outbreak of Streptococcus pneumoniae serotype 5 invasive infection in an impoverished, urban population. Clin Infect Dis 2008;47:768-74.  Back to cited text no. 14
    
15.
Chi RC, Jackson LA, Neuzil KM. Characteristics and outcomes of older adults with community-acquired pneumococcal bacteremia. J Am Geriatr Soc 2006;54:115-20.  Back to cited text no. 15
    
16.
Nuorti JP, Butler JC, Gelling L, Kool JL, Reingold AL, Vugia DJ. Epidemiologic relation between HIV and invasive pneumococcal disease in San Francisco County, California. Ann Intern Med 2000;132:182-90.  Back to cited text no. 16
    
17.
Turett GS, Blum S, Telzak EE. Recurrent pneumococcal bacteremia: Risk factors and outcomes. Arch Intern Med 2001;161:2141-4.  Back to cited text no. 17
    
18.
Breiman RF, Keller DW, Phelan MA, Sniadack DH, Stephens DS, Rimland D, et al. Evaluation of effectiveness of the 23-valent pneumococcal capsular polysaccharide vaccine for HIV-infected patients. Arch Intern Med 2000;160:2633-8.  Back to cited text no. 18
    
19.
Clinical and Laboratory Standard Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing; Sixteenth Informational Supplement. (2007) CLSI document M100-S16. (ISBN 1-56238-588-7) Wayne, PA: CLSI; 2006.  Back to cited text no. 19
    
20.
Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect 2012;18:268-81.  Back to cited text no. 20
    
21.
Rueda AM, Serpa JA, Matloobi M, Mushtaq M, Musher DM. The spectrum of invasive pneumococcal disease at an adult tertiary care hospital in the early 21 st century. Medicine (Baltimore) 2010;89:331-6.  Back to cited text no. 21
    
22.
Albrich WC, Baughman W, Schmotzer B, Farley MM. Changing characteristics of invasive pneumococcal disease in Metropolitan Atlanta, Georgia, after introduction of a 7-valent pneumococcal conjugate vaccine. Clin Infect Dis 2007;44:1569-76.  Back to cited text no. 22
    
23.
Nwosu CM, Anisiuba BC. A hospital study of adult community acquired pneumonia: Clinical and microbiological characteristics and response to penicillin. Orient J Med 1991;3:138-41.  Back to cited text no. 23
    
24.
Macfarlane JT, Adegboye DS, Warrell MJ. Mycoplasma pneumoniae and the aetiology of lobar pneumonia in northern Nigeria. Thorax 1979;34:713-9.  Back to cited text no. 24
    
25.
Osoagbaka OU, Njoku-Obi AN. Bacterial aetiology of lower respiratory tract infections in eastern Nigeria. Niger J Microbiol 1982;2:131-40.  Back to cited text no. 25
    
26.
Iliyasu G, Habib AG, Borodo MM, Babashani M, Ahmed M. Pneumococcal infection in Nigeria: Preparing for the vaccine. Sub Saharan Afr J Med 2014;1:15-9.  Back to cited text no. 26
    
27.
Ozumba UC. Changing pattern of acute bacterial meningitis in Enugu, Nigeria. East Afr Med J 1994;71:300-3.  Back to cited text no. 27
    
28.
Kyaw MH, Lynfield R, Schaffner W, Craig AS, Hadler J, Reingold A, et al. Effect of introduction of the pneumococcal conjugate vaccine on drug-resistant Streptococcus pneumoniae. N Engl J Med 2006;354:1455-63.  Back to cited text no. 28
    
29.
Onyemelukwe GC, Greenwood BM. Pneumococcal serotypes, epidemiological factors and vaccine strategy in Nigerian patients. J Infect 1982;5:157-63.  Back to cited text no. 29
    
30.
Buie KA, Klugman KP, von Gottberg A, Perovic O, Karstaedt A, Crewe-Brown HH, et al. Gender as a risk factor for both antibiotic resistance and infection with pediatric serogroups/serotypes, in HIV-infected and -uninfected adults with pneumococcal bacteremia. J Infect Dis 2004;189:1996-2000.  Back to cited text no. 30
    
31.
WHO/UNAIDS. Global facts and Figures; 2009.  Back to cited text no. 31
    
32.
Jordano Q, Falcó V, Almirante B, Planes AM, del Valle O, Ribera E, et al. Invasive pneumococcal disease in patients infected with HIV: Still a threat in the era of highly active antiretroviral therapy. Clin Infect Dis 2004;38:1623-8.  Back to cited text no. 32
    
33.
Gilks CF, Ojoo SA, Ojoo JC, Brindle RJ, Paul J, Batchelor BI, et al. Invasive pneumococcal disease in a cohort of predominantly HIV-1 infected female sex-workers in Nairobi, Kenya. Lancet 1996;347:718-23.  Back to cited text no. 33
    
34.
Redd SC, Rutherford GW 3 rd , Sande MA, Lifson AR, Hadley WK, Facklam RR, et al. The role of human immunodeficiency virus infection in pneumococcal bacteremia in San Francisco residents. J Infect Dis 1990;162:1012-7.  Back to cited text no. 34
    
35.
Klemets P, Lyytikäinen O, Ruutu P, Ollgren J, Nourti JP. Invasive pneumococcal infections among persons with and without underlying medical condition: Implication for prevention strategies. BMC Infect Dis 2008;8:96.  Back to cited text no. 35
    
36.
Rueda AM, Serpa JA, Matloobi M, Mushtaq M, Musher DM. The spectrum of invasive pneumococcal disease at an adult tertiary care hospital in the early 21 st century. Medicine (Baltimore) 2010;89:331-6.  Back to cited text no. 36
    
37.
Greenwood BM, Hassan-King M, Cleland PG, Macfarlane JT, Yahaya HN. Sequential bacteriological findings in the cerebrospinal fluid of Nigerian patients with pneumococcal meningitis. J Infect 1986;12:49-56.  Back to cited text no. 37
    
38.
Musher DM, Alexandraki I, Graviss EA, Yanbeiy N, Eid A, Inderias LA, et al. Bacteremic and nonbacteremic pneumococcal pneumonia. A prospective study. Medicine (Baltimore) 2000;79:210-21.  Back to cited text no. 38
    
39.
Yu VL, Chiou CC, Feldman C, Ortqvist A, Rello J, Morris AJ, et al. An international prospective study of pneumococcal bacteremia: Correlation with in vitro resistance, antibiotics administered, and clinical outcome. Clin Infect Dis 2003;37:230-7.  Back to cited text no. 39
    
40.
Kalin M, Ortqvist A, Almela M, Aufwerber E, Dwyer R, Henriques B, et al. Prospective study of prognostic factors in community-acquired bacteremic pneumococcal disease in 5 countries. J Infect Dis 2000;182:840-7.  Back to cited text no. 40
    
41.
Robinson KA, Baughman W, Rothrock G, Barrett NL, Pass M, Lexau C, et al. Epidemiology of invasive Streptococcus pneumoniae infections in the United States, 1995-1998: Opportunities for prevention in the conjugate vaccine era. JAMA 2001;285:1729-35.  Back to cited text no. 41
    
42.
Centers for Disease Control and Prevention. ABCs Report: Streptococcus pneumonia; 2010. Available from: http://www.cdc.gov/abcs/index.htm. [Last accessed on March 2014].  Back to cited text no. 42
    
43.
Heffelfinger JD, Dowell SF, Jorgensen JH, Klugman KP, Mabry LR, Musher DM, et al. Management of community-acquired pneumonia in the era of pneumococcal resistance: A report from the Drug-Resistant Streptococcus pneumoniae Therapeutic Working Group. Arch Intern Med 2000;160:1399-408.  Back to cited text no. 43
    
44.
Gordon SB, Chaponda M, Walsh AL, Whitty CJ, Gordon MA, Machili CE, et al. Pneumococcal disease in HIV-infected Malawian adults: Acute mortality and long-term survival. AIDS 2002;16:1409-17.  Back to cited text no. 44
    
45.
Feldman C, Klugman KP, Yu VL, Ortqvist A, Choiu CC, Chedid MB, et al. Bacteraemic pneumococcal pneumonia: Impact of HIV on clinical presentation and outcome. J Infect 2007;55:125-35.  Back to cited text no. 45
    
46.
Alanee SR, McGee L, Jackson D, Chiou CC, Feldman C, Morris AJ, et al. Association of serotypes of Streptococcus pneumoniae with disease severity and outcome in adults: An international study. Clin Infect Dis 2007;45:46-51.  Back to cited text no. 46
    
47.
Fariñas-Alvarez C, Fariñas MC, García-Palomo JD, González-Ruiz M, Fernández-Mazarrasa C, Parra JA, et al. Prognostic factors for pneumococcal bacteremia in a university hospital. Eur J Clin Microbiol Infect Dis 2000;19:733-41.  Back to cited text no. 47
    
48.
Mufson MA, Stanek RJ. Bacteremic pneumococcal pneumonia in one American City: A 20-year longitudinal study, 1978-1997. Am J Med 1999;107:34-43.  Back to cited text no. 48
    
49.
Bliss SJ, O′Brien KL, Janoff EN, Cotton MF, Musoke P, Coovadia H, et al. The evidence for using conjugate vaccines to protect HIV-infected children against pneumococcal disease. Lancet Infect Dis 2008;8:67-80.  Back to cited text no. 49
    


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