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Lower respiratory tract infections among children attending a tertiary hospital in Benin City, Nigeria.

INTRODUCTION

Respiratory diseases are major causes of mortality and morbidity worldwide (1). Respiratory tract infections (RTIs) are perhaps the most frequently reported of all human infection (2). RTIs are one of the major public health problem affecting both children and adult, and is more serious when located in the lower respiratory tract (3). RTIs are the main cause of children's morbidity and mortality in the developing and the developed countries (4). Acute respiratory infections (ARI), particularly lower RTIs, are the leading cause of death among children under 5years of age and are estimated to be responsible for between 1.9-2.2 million deaths globally with 42% of the ARI-associated deaths occurring in Africa (5). In non-affluent communities, LRTI in children is a major cause of pediatric morbidity and mortality (6).

In the United Kingdom (UK), the estimated incidence of LRTI is 30 per 1000 children per year. UK data for children seen at hospital with pneumonia (using clinical findings and chest X-ray) 2001-2002 found overall incidence rates of 14.4 per 10, 000 in children aged 0-16years per annum and 33.8 for those aged [less than or equal to] 5years (7). In Nigeria, 1.3 episodes of pneumonia per child per year have been reported (8). Age, gender, season, indoor air quality and crowding affect the prevalence of LRTI (4,9,10). Other risk factors include malnutrition, exposure to environmental pollutants such as smoke from domestic cooking with firewood, poor parental income and education, and man-made or natural disasters with consequent living in squatter/refugee conditions (11).

Children with LRTIs may present life-threatening complications such as massive parapneumonic or pleural effusion, sepsis empyema, pericarditis with cardiac tamponade and venous thromboembolism (3). These complications and death from LRTIs can be prevented by early diagnosis and treatment with appropriate antimicrobial agents. However, the etiology and symptomatology of respiratory disease vary with age, gender, season, type of population at risk and other factors (2).

A variety of micro-organisms can cause LRTIs in children, including bacteria, viruses, parasites and fungi (3). However, the World Heath Organization (WHO) reports bacterial infections as the leading cause of LRTIs, especially as a cause of severe illness, among children in developing countries (12). Therapy for bacterial LRTIs is often empirical with the initial choice of antibiotics often based on the knowledge of local epidemiology, the most likely microbial agent and their antibiotic susceptibility pattern (13). Bacterial agents of LRTIs and their susceptibility profiles vary from area to area and with time (14,15). This coupled with reports of increasing resistance of etiological agents of respiratory infections necessitates periodic review for optimal treatment of LRTIs in children. Against these backgrounds, this study aimed to determine the bacterial prevalence of LRTIs among children attending a tertiary hospital in Benin City, Nigeria. Susceptibility profiles of bacterial isolates were also determined.

MATERIALS AND METHODS

Study population

A total of 176 children consisting of 76 in-patients and 100 outpatients with ages ranging from one day to 18years were recruited for this study. All out-patients were attending the chest clinic while the in-patients were on admission, both in the University of Benin Teaching Hospital, a tertiary hospital with referral status. All patients had symptoms of LRTIs. Informed consent was obtained from parents/guardians of the children before specimen collection. The Ethical Committee of the University of Benin Teaching Hospital approved this study.

Collection and processing of specimen

Early morning sputum specimens were collected from each subject while lung aspirates were collected from infants and neonates. Specimens were collected into a wide-mouthed sterile container and transported to the laboratory. Films were made from the sputum specimens and stained by Gram's method. The presence of numerous pus cells confirmed true sputum and only such specimens were cultured.

Each specimen was inoculated on chocolate, blood and MacConkey agar plates. All plates were incubated aerobically at 37[degrees]C for 24 to 48 h except the chocolate agar plates that were incubated in a candle jar. Emergent bacterial colonies were identified using standard techniques (16). All yeast colonies were identified with CHROMagar[TM] candida (Paris, France) as previously described (17). Susceptibility test for bacterial isolates was performed using the British Society for Antimicrobial Chemotherapy (BSAC) method (18).

Statistical analysis

The data obtained were analyzed using Chi square ([chi square]) test and odd ratio analysis using the statistical software INSTAT[R] (GraphPad Software Inc., La Jolla, CA, USA).

RESULTS

A total of 82 (46.6%) out of 176 children with signs and symptoms of LRTIs were culture-positive. Children's gender did not significantly (p = 0.824) affect the prevalence of culture-positive LRTIs, nor did mixed infections (p = 0.107). The prevalence dropped to 32.1% in the age group 7-9 years and thereafter began to rise. The prevalence of culture-positive LRTI was significantly affected by age (p = 0.04) with the age group [less than or equal to] 1-3 years having the highest prevalence of 70%. Children who were in-patients had significantly higher prevalence of LRTIs compared with their out-patient counterparts (p = 0.0055). Similarly, in-patient children had a significantly 1 to 72-fold risk of having mixed infection than out -patient children (p = 0.0435) (Table 1).

A total of 89 microbial isolates were recovered with more from males (54) than females (35). Generally and among males, Klebsiella pneumoniae was the most prevalent isolate followed by Staphylococcus aureus. S. aureus was the most prevalent bacterial pathogen in females followed by Klebsiella pneumoniae and Haemophilus influenza, both with a prevalence of 25.7% each (Table 2).

The susceptibility profiles of bacterial isolates from in-patient and out-patient children are shown in Tables 4 and 5 respectively. Generally, the susceptibility profiles ranged from poor to high depending on the isolates and the antibacterial agent. In both in- and out-patients, ofloxacin was the most active antibacterial agent.

DISCUSSION

Pneumonia--a type of LRTI, is the leading cause of death among children worldwide (11). The prevalence, etiology and antibiotic susceptibility pattern of LRTIs vary with location and time (14, 15), necessitating periodic review for optimal management of children with LRTIs. Against this background, this study was conducted.

An overall prevalence of 46.6% of bacterial LRTI was observed in this study. This is higher than 27%, 24.2% and 18.9% previously reported (10,13,15). The reported prevalence observed in this study is comparable to 47.2% reported by Egbagbe and Mordi (19), but lower than 59.4% reported by Ozyilmaz et al. (14) and 58.4% by Ramana et al. (20). It has been reported that the prevalence of diarrhea varies with geographic locations, region within the same country and even over time in the same location and population (21). In relation to location Ozyilmaz et al. study was conducted in Turkey (14) and Ramana et al. study was conducted in India (20), as against our study in Nigeria. In relation to region within the same country, the study by Okesola and Ige was in Ibadan (13) while the study by Akingbade et al. was in Abeokuta (10), both in South West Nigeria. Our study was in Benin City in South-South Nigeria. In relation to the same location, the studies by Egbagbe and Mordi (19) and Egbe et al. (15) were carried out in the same institution as our current study. It is pertinent to note that these studies cover all age groups in contrast to our study that focused on children.

The prevalence of LRTIs was higher in males (47.7%) than in females (44.8%) which is in agreement with previous studies (10,15,22). The higher prevalence in males has been attributed to decreased local immunity in the respiratory tract due to smoking, use of tobacco and alcohol consumption amongst other factors (23). This reason may only suffice for children between 14 to 18 years. However, this is an unlikely reason as children [less than or equal to] 1 to 3 years old had a significantly higher prevalence than other age groups in this study (p = 0.04). However, LRTIs have been reported as the leading cause of death among children under 5years (5). This may explain our finding in relation to age.

Children who were in-patients had a significantly higher prevalence of LRTI than their out-patient counter-part (p = 0.0055). In-patient children may be in the intensive care unit and be immuno-compromised, have other immunosuppressive conditions such as cancer, or have debilitating conditions that may increase their susceptibility to LRTIs (3). Indeed, diarrhea has been reported as a risk factor for acute LRTIs in young children below 3 years in low income settings (24). These conditions may have been present in our in-patient subjects and may explain the findings of our study.

A total of seven out of the 176 specimens (4.0%) yielded mixed microbial growth. The finding of mixed infections have previously been reported (2,3). Gender did not significantly affect the prevalence of mixed LRTI (p = 0.107). Mixed LRTI was significantly associated with in-patients (OR = 8.49; 95% CI = 0.999-72.09, p = 0.044). It is important to note that 94 (53.4%) of the specimens yielded no growth. These may have contained viruses or other microorganisms that could not be detected by the techniques employed in our study.

Generally, K. pneumoniae was the most predominant microbial isolate in our study. This agrees with findings from other locations in Nigeria (10,13,15,19). However, studies from other parts of the world report different organisms as the predominant isolate causing LRTI. For example, Brad et al. in Timisoara, Romania, reported Pseudomonas aeruginosa as the most prevalent bacteria causing LRTI (3). In relation to gender, K. pneumoniae was most prevalent in males while S. aureus predominated in females in our study, while K. pneumoniae was the most prevalent isolate recovered from both in- and out-patients. Acinetobacter species were recovered only from in-patients. This agrees with reports that Acinetobacter species are associated with hospital-acquired LRTIs (25,26). Other isolates have been reported as causes of LRTIs (13,15).

It is expected that nosocomial isolates would be more antimicrobially resistant than community isolates. This was true only for K. pneumoniae isolates. Other bacterial isolates show different patterns depending on the isolate and antibacterial agent. It has been reported that the highest volumes of antibiotic being prescribed and consumed are in ambulatory care (27). Prescription of antibiotics without laboratory guidance, as well as over the counter sales of antibiotics without prescription, are rife in Nigeria and both practices have been implicated as possible reasons for increased antimicrobial resistance observed across the country (28,29). This may explain why some bacterial isolates from out-patients were more resistant to some antibacterial agents than their counterparts from in-patients. Although ofloxacin was the most active antibacterial agent against all bacterial isolates from inpatients and out-patients, it is contraindicated in children.

In conclusion, an overall prevalence of 46.6% of culture-positive LRTIs was observed among children, with in-patients a having higher risk of the infection. K. pneumoniae was the most prevalent organism causing LRTIs. Prudent use of antibacterial agents is advocated.

REFERENCES

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(8.) Fagbule D, Parakoyi DB, Spiegel R. Acute respiratory infections in Nigerian children: prospective cohort study of incidence and case management. J Trop Pediatr 1994; 40: 279-284.

(9.) Kovesi T, Gilbert NL, Stocco C, Fugler D, Dales RE, Guay M, et al. Indoor air quality and the risk of lower respiratory tract infections in young Canadian Inuit children CMAJ 2007; 177: 155-160.

(10.) Akingbade OA, Ogiogwa JI, Okerentugba PO, Innocent-Adiele HC, Onoh CC, Nwanze JC. et al. Prevalence and antibiotic susceptibility pattern of bacterial agents involved in lower respiratory tract infections in Abeokuta, Ogun State, Nigeria. Rep Opinion 2012; 4: 25-30.

(11.) Johnson WBR, Abdulkarim AA. Childhood pneumonia in developing countries Afr J Resp Med 2013; 8: 4-9.

(12.) World Health Organization (WHO). Management of the young child with acute lower respiratory tract infection. WHO Programme for the Control of Acute Respiratory Infections. WHO, Geneva. 1990.

(13.) Okesola AO, Ige OM. Trends in bacterial pathogens of lower respiratory tract infections. Indian J Chest Dis Allied Sci 2008; 50: 269-272.

(14.) Ozyilmaz E, Akan OA, Gulhan M, Ahmed K, Nagatake T. Major bacteria of community-acquired respiratory tract infections in Turkey. Jpn J Infect Dis 2005; 58: 50-52.

(15.) Egbe CA, Ndiokwere C, Omoregie R. Microbiology of lower respiratory tract infections in Benin City, Nigeria. Malays J Med Sci 2011; 18: 27-31.

(16.) Barrow GI, Feltham RKA. Cowan and Steel's Manual for the Identification Medical Bacteria. 3rd Edn. Cambridge (UK). Cambridge University Press Cambridge. 2003.

(17.) Paritpokee S, Hall G, Procop G. Rapid identification of yeast isolates using BD BBLTM CHROMagar Candida. Paper presented at the 105th General Meeting of the American Society for Microbiology. 2005; 1-2.

(18.) Andrew JM. BSAC standardized disc susceptibility testing method (version 8). J Antimicrob Chemother 2009; 64: 454-489.

(19.) Egbagbe EE, Mordi RM. Aetiology of lower respiratory tract infection in Benin City, Nigeria. J Med Biomed Res 2006; 5: 22-27.

(20.) Ramana KV, Kalaskar A, Rao M, Rao SD. Aetiology and antimicrobial susceptibility patterns of lower respiratory tract infections (LTRI's) in a rural tertiary care teaching hospital at Karimnagar, South India. Am J Infect Dis Microbiol 2013; 1: 101-105.

(21.) Petri WA Jr, Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL. Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 2008; 118: 1277-1290.

(22.) Taura DW, Hassan A, Yayo AM, Takalmawa H. Bacterial isolates of the respiratory tract infection and their current sensitivity pattern among patients attending Aminu Kano Teaching Hospital, Kano, Nigeria. Int Res J Microbiol 2013; 4: 226-231.

(23.) Gauchan P, Lekhak B, Sherchand JB. The prevalence of lower respiratory tract infection in adults visiting Tribhuvan University Teaching Hospital. J Institute Med 2006; 28: 10-14.

(24.) Walker CL, Perin J, Katz J, Tielsch JM, Black RE. Diarrhea as a risk factor for acute lower respiratory tract infections among young children in low income settings. J Glob Health 2013; 3: 010402.

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AUTHOR INFORMATION

Philomena I Ogbogu, MPhil MSc AMLSCN, Principal Medical Laboratory Scientist [1]

Rosemary E. Omijie MSc FMLSCN, Assistant Chief Medical Laboratory Scientist [1]

Michael I Ogbogu, MBBS, Chief Medical Officer [2]

[1] Department of Medical Microbiology, University of Benin Teaching Hospital, Benin City, Nigeria

[2] Department of Health Services, University of Benin, Benin City, Nigeria

Corresponding author: Philomena Ogbogu.

Email: philogbogu@vahoo.com

Philomena I Ogbogu [1], Rosemary E Omijie [1] and Michael I Ogbogu [2]

[1] University of Benin Teaching Hospital and [2] University of Benin, Benin City, Nigeria
Table 1. Prevalence of lower respiratory tract infection
in relation to gender, age and source of patients

Characteristic    No. tested   No. infected    OR
                                   (%)

Gender

Male                 109        52 (47.7)     1.13
Female                67        30 (44.8)

Mixed infection

Male                 109          2(1.8)      0.23
Female                67          5(7.5)

Age (days)

< 1-3                 10         7 (70.0)
4-6                   25        16 (64.0)
7-9                   28         9 (32.1)
10-12                 45        15 (33.3)
13-15                 31        15 (48.4)
16-18                 37        20 (54.0)

Patients

In-patient            76        45 (59.2)     2.47
Out-patient          100        37 (37.0)

Mixed infection

In-patient            76          6(7.9)      8.49
Out-patient          100         1 (1.0)

Characteristic      95% CI        p

Gender

Male               0.61-2.07    0.824
Female

Mixed infection

Male              0.044-1.23    0.107
Female

Age (days)

< 1-3                           0.040
4-6
7-9
10-12
13-15
16-18

Patients

In-patient         1.34-4.56    0.0055
Out-patient

Mixed infection

In-patient        0.999-72.09   0.0435
Out-patient

OR = odd ratio; CI = Confidence interval

Table 2. Distribution of microbial isolates in relation to
gender

Organism                          Gender              Total

                           Male (%)    Female (%)

Klebsiella pneumoniae      24 (44.4)    9 (25.7)    33 (37.1)
Proteus vulgaris            1 (1.9)     0 (0.0)      1 (1.1)
Proteus mirabilis           1 (1.9)     0 (0.0)      1 (1.1)
Providencia spp             0 (0.0)     1 (2.9)      1 (1.1)
Acinetobacter spp           2 (3.7)     0 (0.0)      2 (2.3)
Alcaligenes spp             5 (9.3)     0 (0.0)      5 (5.6)
Haemophilus influenzae     6 (11.1)     9 (25.7)    15 (16.9)
Pseudomonas aeruginosa      2 (3.7)     0 (0.0)      2 (2.3)
Staphylococcus aureus      9 (16.7)    11 (31.4)    20 (22.5)
Streptococcus pneumoniae    2 (3.7)     0 (0.0)      2 (2.3)
Candida albicans            2 (3.7)     5 (14.3)     7 (7.9)
Total                      54 (60.7)   35 (39.3)    89 (100.0)

Table 3. Distribution of microbial isolates among
in- and out-patients.

Organism                   In-patient   Out-patient      Total
                              (%)           (%)           (%)

Klebsiella pneumoniae      17 (33.3)     16 (42.1)     33 (37.1)
Proteus vulgaris            1 (2.0)       0 (0.0)       1 (1.1)
Proteus mirabilis           1 (2.0)       0 (0.0)       1 (1.1)
Providencia spp             1 (2.0)       0 (0.0)       1 (1.1)
Acinetobacter spp           2 (3.9)       0 (0.0)       2 (2.3)
Alcaligenes spp             2 (3.9)       3 (7.9)       5 (5.6)
Haemophilus influenzae      6 (11.8)      9 (23.7)     15 (16.9)
Pseudomonas aeruginosa      2 (3.9)       0 (0.0)       2 (2.3)
Staphylococcus aureus      12 (23.5)      8 (21.1)     20 (22.5)
Streptococcus pneumoniae    2 (3.9)       0 (0.0)       2 (2.3)
Candida albicans            5 (9.8)       2 (5.3)       7 (7.9)
Total                      51 (57.3)     38 (42.7)     89 (100.0)

AUG = Amoxicillin-clavulanate; CAZ = ceftazidime; CRO = Ceftriaxone;
CXM = Cefuroxime; OB = Cloxacilli; CN = Gentamicin; E = Erythromycin;
OFX = Ofloxacin; ND = Not done; NA = Not applicable.

Table 4. Susceptibility profiles of isolates recovered
from in-patients.

Organism                         Antibacterial agents ([micro]g/disc)

                                 AUG 30[micro]g   CAZ 30 [micro]g

Klebsiella pneumonia (n=17)        2 (11.8%)         1 (5.9%)
Proteus vulgaris (n=1)                 0                 0
Proteus mirabilis (n=1)                0             1 (100%)
Providencia spp. (n=1)                 0             1 (100%)
Acinetobacter spp. (n=2)               NA               NA
Alcaligenes spp. (n=2)                 0                 0
Haemophilus influenza (n=6)        3 (50.0%)         1 (16.7%)
Pseudomonas aeruginosa (n=2)           NA                0
Staphylococcus aureus (n=12)       4 (33.3%)            NA
Streptococcus pneumonia (n=2)      1 (50.0%)         1 (50.0%)

Organism                         Antibacterial agents ([micro]g/disc)

                                 CRO 30 [micro]g   CXM 30 [micro]g

Klebsiella pneumonia (n=17)         5 (29.4%)         1 (5.9%)
Proteus vulgaris (n=1)              1 (100%)              0
Proteus mirabilis (n=1)                 0             1 (100%)
Providencia spp. (n=1)                  0             1 (100%)
Acinetobacter spp. (n=2)               NA                NA
Alcaligenes spp. (n=2)                  0             1 (50.0%)
Haemophilus influenza (n=6)         4 (66.7%)         1 (16.7%)
Pseudomonas aeruginosa (n=2)            0                NA
Staphylococcus aureus (n=12)           NA                NA
Streptococcus pneumonia (n=2)       1 (50.0%)         1 (50.0%)

Organism                         Antibacterial agents ([micro]g/disc)

                                 OB 5 [micro]g   CN 10 [micro]g

Klebsiella pneumonia (n=17)           ND           3 (17.7%)
Proteus vulgaris (n=1)                ND            1 (100%)
Proteus mirabilis (n=1)               ND            1 (100%)
Providencia spp. (n=1)                ND            1 (100%)
Acinetobacter spp. (n=2)              ND            2 (100%)
Alcaligenes spp. (n=2)                ND            2 (100%)
Haemophilus influenza (n=6)           ND               NA
Pseudomonas aeruginosa (n=2)          ND               0
Staphylococcus aureus (n=12)          ND           7 (58.3%)
Streptococcus pneumonia (n=2)         ND           1 (50.0%)

Organism                         Antibacterial agents ([micro]g/disc)

                                 E 5 [micro]g   OFX 5 [micro]g

Klebsiella pneumonia (n=17)           ND          10 (58.8%)
Proteus vulgaris (n=1)                ND           1 (100%)
Proteus mirabilis (n=1)               ND           1 (100%)
Providencia spp. (n=1)                ND           1 (100%)
Acinetobacter spp. (n=2)              ND           2 (100%)
Alcaligenes spp. (n=2)                ND           2 (100%)
Haemophilus influenza (n=6)           ND          5 (83.3%)
Pseudomonas aeruginosa (n=2)          ND           2 (100%)
Staphylococcus aureus (n=12)      3 (25.00)       9 (95.0%)
Streptococcus pneumonia (n=2)     1 (50.0%)        2 (10%)

Table 5. Susceptibility profiles of isolates recovered from
out-patients.

Organism                  Antibacterial agents ([micro]g/disc)

                            AUG           CAZ           CRO
                        30 [micro]g   30 [micro]g   30 [micro]g

Klebsiella pneumonia     3 (18.8%)     7 (43.8%)    11 (68.8%)
(n=16)

Acinetobacter spp.          NA            NA            NA
(n=3)

Haemophilus influenza    3 (33.3%)     3 (33.3%)     7 (77.8%)
(n=9)

Staphylococcus aureus    6 (75.0%)        NA            NA
(n=8)

Organism                  Antibacterial agents ([micro]g/disc)

                            CXM           OB           CN
                        30 [micro]g   5 [micro]g   10 [micro]g

Klebsiella pneumonia     5 (31.3%)        ND       12 (75.0%)
(n=16)

Acinetobacter spp.          NA            ND        2 (66.7%)
(n=3)

Haemophilus influenza    4 (44.4%)        ND           NA
(n=9)

Staphylococcus aureus       NA            0         4 (50.0%)
(n=8)

Organism                  Antibacterial agents
                             ([micro]g/disc)

                            E           OFX
                        5 [micro]g   5 [micro]g

Klebsiella pneumonia        ND       13 (81.3%)
(n=16)

Acinetobacter spp.          ND        3 (100%)
(n=3)

Haemophilus influenza       ND       5 (55.6%)
(n=9)

Staphylococcus aureus   4 (50.0%)    5 (62.5%)
(n=8)

AUG = Amoxicillin-clavulanate; CAZ = ceftazidime;
CRO = Ceftriaxone; CXM = Cefuroxime; OB = Cloxacillin;
CN = Gentamicin; E = Erythromycin; OFX = Ofloxacin;
ND = Not done; NA = Not applicable.
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Title Annotation:ORIGINAL ARTICLE
Author:Ogbogu, Philomena I.; Omijie, Rosemary E.; Ogbogu, Michael I.
Publication:New Zealand Journal of Medical Laboratory Science
Article Type:Report
Date:Aug 1, 2015
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