The Open Microbiology Journal




ISSN: 1874-2858 ― Volume 14, 2020
RESEARCH ARTICLE

Nasopharyngeal Carriage of Streptococcus pneumoniae and Associated Factors among Children in Southwest Ethiopia



Dejene Derseh Abateneh1, 2, *, Abera Kumalo Shano2, 3, Teshale Worku Dedo2
1 Kotebe Metropolitan University, Menelik II College of Medicine and Health Sciences, Addis Ababa, Ethiopia
2 Department of Medical Laboratory Sciences, College of Health Sciences, Mizan-Tepi University, Mizan Teferi, Ethiopia
3 Department of Medical Laboratory Sciences, College of Medicine and Health Sciences, Wolaita Sodo University, Sodo, Ethiopia

Abstract

Background:

In Ethiopia, Streptococcus pneumoniae is the predominant causative agent of pneumonia. About, 95% of bacterial pneumonia cases in under five years of children are caused by pneumococci.

Objective:

To assess the nasopharyngeal carriage of Streptococcus pneumoniae, its antibiotic susceptibility pattern, and associated factors among children in Southwest Ethiopia.

Methods:

A cross-sectional study was conducted from October 01, 2018, to December 30, 2018. A total of 293 children aged ≤15 years were included in the study using a systematic random sampling technique. A nasopharyngeal swab was collected using a sterile cotton swab and cultured on blood agar supplemented with 5μg/ml gentamicin. The antimicrobial susceptibility testing was performed using the Kirby-Bauer disc diffusion technique.

Results:

The ages of participants ranged from 5 months to 14 years. The carriage rate of Streptococcus pneumoniae was 74/293 (25.3%). Being within the age group <3 years, the habit of sleeping with parent(s)/guardians and numbers of rooms per household were significantly associated with pneumococcal carriage. Streptococcus pneumoniae showed the highest resistance to Tetracycline, 36 (48.65%), and Trimethoprim/sulfamethoxazole, 29 (39.2%), and was found to be susceptible to Chloramphenicol, 54 (77%), and Erythromycin, 38 (51.4%).

Conclusion:

The nasopharyngeal carriage rate of Streptococcus pneumoniae is considerably high. High antimicrobial resistance of Streptococcus pneumoniae against Tetracycline and Trimethoprim/sulfamethoxazole was observed. Living in a house with a single room, children’s habit of sleeping with parents/guardians and age are associated factors of high pneumococcal carriage. Strategies need to be designed to address the modifiable associated factors and the bacterium antibiotic resistance pattern should be monitored regularly.

Keywords: Streptococcus pneumoniae, Nasopharyngeal carriage, Antibiotics susceptibility, Children, Ethiopia, Trimethoprim/sulfamethoxazole.


Article Information


Identifiers and Pagination:

Year: 2020
Volume: 14
First Page: 171
Last Page: 178
Publisher Id: TOMICROJ-14-171
DOI: 10.2174/1874285802014010171

Article History:

Received Date: 10/4/2020
Revision Received Date: 15/6/2020
Acceptance Date: 18/6/2020
Electronic publication date: 30/07/2020
Collection year: 2020

© 2020 Abateneh et al.

open-access license: This is an open access article distributed under the terms of the Creative Commons Attribution 4.0 International Public License (CC-BY 4.0), a copy of which is available at: (https://creativecommons.org/licenses/by/4.0/legalcode). This license permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.


* Address correspondence to this author at the Kotebe Metropolitan University, Menelik II College of Medicine and Health Sciences, Department of Medical Laboratory Sciences, Addis Ababa, Ethiopia; P.O. Box: 3268. Ethiopia; Tel: +251920514158; E- mail: dejenieh@gmail.com





1. INTRODUCTION

Streptococcus pneumoniae or pneumococci is the etiology of bacterial pneumonia, bacteremia, meningitis, otitis media, and sinusitis mainly in children, the elderly, and immune-compromised patients [1Pneumococcal vaccines WHO position paper - 2012 - recommendations. Vaccine 2012; 30(32): 4717-8.
[http://dx.doi.org/10.1016/j.vaccine.2012.04.093] [PMID: 22621828]
]. The human nasopharynx is the primary reservoir of Streptococcus pneumoniae [2Henriques-Normark B, Tuomanen EI. The pneumococcus: epidemiology, microbiology, and pathogenesis. Cold Spring Harb Perspect Med 2013; 3(7)a010215
[http://dx.doi.org/10.1101/cshperspect.a010215] [PMID: 23818515]
, 3Schrag SJ, Beall B, Dowell S, Organization WH. Resistant pneumococcal infections: the burden of disease and challenges in monitoring and controlling antimicrobial resistance 2001.]. Asymptomatic carriage is a precondition for pneumococcal diseases and serves as the main source of person-to-person transmission [4Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 2004; 4(3): 144-54.
[http://dx.doi.org/10.1016/S1473-3099(04)00938-7] [PMID: 14998500]
, 5Bogaert D, van Belkum A, Sluijter M, et al. Colonisation by Streptococcus pneumoniae and Staphylococcus aureus in healthy children. Lancet 2004; 363(9424): 1871-2.
[http://dx.doi.org/10.1016/S0140-6736(04)16357-5] [PMID: 15183627]
]. Nasopharyngeal isolates reflect the epidemiological aspects of diseases caused by Streptococcus pneumoniae in the community [6Adegbola RA, DeAntonio R, Hill PC, et al. Carriage of Streptococcus pneumoniae and other respiratory bacterial pathogens in low and lower-middle income countries: a systematic review and meta-analysis. PLoS One 2014; 9(8)e103293
[http://dx.doi.org/10.1371/journal.pone.0103293] [PMID: 25084351]
, 7Brueggemann AB, Griffiths DT, Meats E, Peto T, Crook DW, Spratt BG. Clonal relationships between invasive and carriage Streptococcus pneumoniae and serotype- and clone-specific differences in invasive disease potential. J Infect Dis 2003; 187(9): 1424-32.
[http://dx.doi.org/10.1086/374624] [PMID: 12717624]
], and which indicates the infection-causing strains currently circulating within the community [8Faden H, Duffy L, Wasielewski R, Wolf J, Krystofik D, Tung Y. Relationship between nasopharyngeal colonization and the development of otitis media in children. Tonawanda/Williamsville Pediatrics. J Infect Dis 1997; 175(6): 1440-5.
[http://dx.doi.org/10.1086/516477] [PMID: 9180184]
]. The isolates can be used as an estimate of the incidence of resistance in systemic isolates [9Musher DM. Infections caused by Streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin Infect Dis 1992; 14(4): 801-7.
[http://dx.doi.org/10.1093/clinids/14.4.801] [PMID: 1576274]
].

The global distribution of children dying from pneumonia is uneven, in which the majority of the cases occur in developing countries. The bacterium is grouped as microorganism of serious public health threat [101CDC. Antibiotic resistance threats in the United States 2013.]. Antibiotic-resistant pneumococci is an increasing global concern and it is the principal cause of treatment failures for acute respiratory illness (ARI) and meningitis in developing countries since ARI is often treated empirically with antibiotics [4Bogaert D, De Groot R, Hermans PW. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect Dis 2004; 4(3): 144-54.
[http://dx.doi.org/10.1016/S1473-3099(04)00938-7] [PMID: 14998500]
]. Streptococcus pneumoniae has developed resistance to drugs in the penicillin and erythromycin groups. In recent years, the spread of Streptococcus pneumoniae strains that are resistant to more than one antibiotic has increased in many countries. The rapid emergence of resistance to multiple antimicrobial agents has further complicated the problem of the disease. The rapid increase in resistance to penicillin and other antimicrobial agents worldwide has made the choice of antimicrobial drugs for pneumococci infections more difficult [11Quintero B, Araque M. [Serotype profile and antibiotyping of Streptococcus pneumoniae strains isolated from nasal carriage in pediatric patients]. Invest Clin 2006; 47(1): 17-26.
[PMID: 16562641]
, 12Schultsz C, Vien M, Campbell JI, et al. Changes in the nasal carriage of drug-resistant Streptococcus pneumoniae in urban and rural Vietnamese schoolchildren. Trans R Soc Trop Med Hyg 2007; 101(5): 484-92.
[http://dx.doi.org/10.1016/j.trstmh.2006.08.010] [PMID: 17113613]
].

In sub-Saharan Africa, Streptococcus pneumoniae accounts for about 25% to 30% of meningitis cases and 30% to 50% pneumonia cases in children under 5 years [13Black RE, Cousens S, Johnson HL, et al. Global, regional, and national causes of child mortality in 2008: a systematic analysis. Lancet 2010; 375(9730): 1969-87.
[http://dx.doi.org/10.1016/S0140-6736(10)60549-1] [PMID: 20466419]
-15Lob-Levyt J. Contribution of the GAVI Alliance to improving health and reducing poverty. Philosophical Transactions of the Royal Society B. Biol Sci 2011; 366(1579): 2743-7.
[http://dx.doi.org/10.1098/rstb.2011.0040]
]. Diseases caused by pneumococci are the leading causes of childhood mortality in low and middle-income countries [16Zar HJ, Madhi SA, Aston SJ, Gordon SB. Pneumonia in low and middle income countries: progress and challenges. Thorax 2013; 68(11): 1052-6.
[http://dx.doi.org/10.1136/thoraxjnl-2013-204247] [PMID: 23956020]
].

Ethiopia is grouped in the top 10 countries in which two-third of deaths are reported due to pneumonia [17Lema K, Murugan R, Tachbele E. Prevalence and associated factors of pneumonia among under-five children at public hospitals in Jimma zone, South West of Ethiopia. J Pulmonol Clin Res 2018; 2(1): 25-31.-19Ethiopia UNICEF. In Ethiopia, pneumonia is a leading single disease killing under-five children 2014.https://unicefethiopia.org/2014/11/13], which means that one in every four deaths among children under five years of age is caused by pneumonia. The mortality rate under five years of children due to Streptococcus pneumoniae is high although Pneumococcal Conjugate Vaccine 10 (PCV-10) was introduced in 2011 [20Torres-Rueda S, Kitaw Y, Molla M, Mounier-Jack S. Introduction of PCV-10 in Ethiopia: Effects on the health system. Ethiop J Health Dev 2015; 29(1) [EJHD]., 21Negera A, Abelti G, Bogale T, Gebreselassie T, Pearson R. An analysis of the trends, differentials and key proximate determinants of infant and under-five mortality in Ethiopia 2013.]. Streptococcus pneumoniae is identified in most cases of pneumonia, which accounts for 95% of bacterial pneumonia cases, and it is therefore considered the biggest infectious killer of children aged below 5 years [14Rodríguez L, Cervantes E, Ortiz R. Malnutrition and gastrointestinal and respiratory infections in children: a public health problem. Int J Environ Res Public Health 2011; 8(4): 1174-205.
[http://dx.doi.org/10.3390/ijerph8041174] [PMID: 21695035]
, 15Lob-Levyt J. Contribution of the GAVI Alliance to improving health and reducing poverty. Philosophical Transactions of the Royal Society B. Biol Sci 2011; 366(1579): 2743-7.
[http://dx.doi.org/10.1098/rstb.2011.0040]
].

Data on pneumococci is limited in the country studied and antimicrobial resistance pattern of Streptococcus pneumoniae is not regularly monitored. Therefore, this study aimed to assess the nasopharyngeal carriage, antibiotic susceptibility pattern, and associated factors of Streptococcus pneumoniae among children in Southwest Ethiopia.

2. MATERIALS AND METHODS

2.1. Study Site, Design, and Participants

A cross-sectional study was conducted in Mizan Tepi University teaching hospital, Mizan Teferi, Southwest Ethiopia. It is a public hospital located in the Bench Maji zone, Southwest region of Ethiopia, 561 km far from the capital city, Addis Ababa. The area has a latitude and longitude of 7°0’N 35°35’E/7.000°N35.583°E with an elevation of 1451 meters above sea level. The hospital provides medical services for people in Southwest Ethiopia and its surroundings. The study site is in a district where pastoral, semi-pastoral, and agrarian communities reside.

The study was conducted from October 01, 2018, to December 30, 2018. All children aged ≤ 15 years and visiting the pediatric outpatient department (OPD) of a hospital for seeking care were included as the study population. The study participants were selected systematically at regular intervals from their sequence of visits using a systematic random sampling technique. An average 15 pediatric visits occurred in the hospital every day based on the previous records of the pediatrics OPD. Considering the daily flow of pediatric visits along with the study period, sampling interval (k) three was calculated and used. The first participant to be included in the study was selected by the lottery method from the order of the first three. Thereafter, at every third interval, participants were included in the study until the total sample size was achieved.

The minimum sample size (n) was determined using single population proportion sample size formula [n = (Z α/2)2 P (1-P) /d2], where Zα/2 = the value under the standard normal table at the 95% level of confidence which was 1.96, d= precision which was set at 5%, P= the prevalence of nasopharyngeal carriage rate of Streptococcus pneumoniae, i.e. 41.03% taken from a previous study conducted in Gondar University Hospital, Ethiopia [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.]. Considering sample size correction and a 10% nonresponse rate, the final minimum sample size included 293 children.

2.2. Data Collection and Laboratory Methods

2.2.1. Socio-demographic and Clinical Characteristics

A semi-structured questionnaire adapted from peer-reviewed literature [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.-24Ndosa A, Kidenya BR, Mushi MF, Mirambo MM, Hokororo A, Mshana SE. Factors associated with colonization of Streptococcus pneumoniae among under-fives attending clinic in Mwanza City, Tanzania. Tanzan J Health Res 2015; 17(1)] was used to collect socio-demographic and other clinical characteristics by trained data collectors. Socio-demographic factors included age of the child, sex of the child, parents’ or guardians’ educational status, religion, occupation, socioeconomic living conditions such as family size, presence of <5 years siblings, presence of siblings ≥5 years, number of rooms in a house, the habit of sleeping with parents/guardians, previous antibiotic use, previous hospitalization, and respiratory tract infections.

2.2.2. Specimen Collection and Processing

After written informed consent was obtained from each participant’s parent(s) or guardian, a single nasopharyngeal swab was collected from each participant using a sterile cotton swab inserted through the nostrils into the posterior according to the recommendation of Centers for Diseases Control and Prevention guidelines. The swab was rotated at 180°, withdrawn and inserted in Amies transport medium (Oxoid, Basingstoke, Hampshire, England). The nasopharyngeal swab with Amies transport medium was transported to the Mizan Tepi University biomedical laboratory within 4hrs at room temperature and vortexed for approximately 10-20 seconds for culture.

The nasopharyngeal swab was cultured on sheep blood agar supplemented with 5μg/ml gentamicin which was used as a selective medium to culture pneumococci, and incubated overnight at 37°C in a 5-10% CO2 enriched atmosphere by using a candle jar; then finally, the identification of Streptococcus pneumoniae was done based on colony morphology, hemolysis pattern, sensitivity to optochin, and bile solubility test [25Perilla MJ. Manual for the laboratory identification and antimicrobial susceptibility testing of bacterial pathogens of public health importance in the developing world; Haemophilus influenzae, Neisseria meningitidis, Streptococcus pneumoniae, Neisseria gonorrhoeae, Salmonella serotype Typhi, Shigella, and Vibrio cholerae 2003.]. A typical colony of Streptococcus pneumoniae was small, grayish, moist and watery surrounded by a greenish zone of alpha hemolysis of the medium around the colony. As a confirmatory test of Streptococcus pneumoniae, the alpha-hemolytic colony was sub-cultured on blood agar with 5 μg optochin disc and was read after overnight incubation in a candle jar at 37°C. Isolates with a zone of inhibition > 14 mm diameter were considered susceptible to optochin and identified as Streptococcus pneumoniae. Isolates with zones of inhibition ranging from 9 mm to 13 mm diameter were tested for bile solubility for confirmation of Streptococcus pneumoniae using 2% Sodium deoxycholate (bile salt) (Oxoid, Basingstoke, Hampshire, England) (Supplementary file S1).

2.2.3. Antimicrobial Susceptibility Testing

The antimicrobial susceptibility test was done using the Kirby-Bauer disc diffusion technique on Mueller–Hinton agar (MHA) (Oxoid, Basingstoke, Hampshire, England) supplemented with 5% sheep blood [26Wayne P. Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: Twenty-fourth informational supplement, M100-S24. Clin Lab Standards Institute (CLSI) 2014; 34(1)]. Direct colony suspension, equivalent to a 0.5 McFarland standard, was prepared using colonies from an overnight incubated (18 to 20 hours) sheep blood agar plate. A sterile cotton swab was dipped into the standardized solution and used for evenly inoculating Mueller–Hinton plates. The plates were then allowed to dry. Antibiotic disks with the following concentrations were placed on the plates: Oxacillin (1μg), Erythromycin (15μg), Chloramphenicol (30μg), Tetracycline (30μg) and Trimethoprim/Sulfamethoxazole (TMP/SMX) (1.25/ 23.75μg).

The antimicrobial susceptibility patterns of Streptococcus pneumoniae isolates were classified as susceptible, intermediately resistant, or resistant to the selected antibiotics based on Clinical Laboratory Standard Institute guidelines (CLSI) 2014 recommendation [26Wayne P. Clinical and Laboratory Standards Institute: Performance standards for antimicrobial susceptibility testing: Twenty-fourth informational supplement, M100-S24. Clin Lab Standards Institute (CLSI) 2014; 34(1)]. As per the CLSI guidelines, for nonmeningitic isolates of Streptococcus pneumoniae, interpretation of penicillin susceptibility testing was performed using Oxacillin (1μg) disks (Supplementary file S2). Isolates of pneumococci with Oxacillin zone sizes of ≥20 mm were susceptible to Penicillin. However, penicillin’s minimum inhibitory concentration should be determined for those isolates with Oxacillin inhibition zones ≤19mm to report penicillin resistance. The antimicrobial agents were selected based on the prescription practices in hospitals and the Ethiopian standard treatment guideline for the treatment of Streptococcus pneumoniae infection as well as the susceptibility test type affordability. The antibiotics were well spaced in order to prevent the overlapping of inhibition zones. The plates were incubated at 37°C for 24 hours. Quality control for susceptibility testing was performed daily using S. pneumoniae ATCC49619 control strain.

2.3. Statistical Analysis

Data were entered by using Epi info version 7.0 and transferred onto SPSS version 16 for cleaning, categorization, and analysis. Frequencies and proportions were calculated as univariate analysis to describe the study population in relation to relevant variables. Bivariate analysis was conducted to identify the association between each independent variable with the outcome variable. Multivariate analysis was employed to identify independent predictors associated with the outcome variable. In the multinomial model, the adjusted odds ratio (AOR) and corresponding 95% confidence interval (CI) were retrieved. Those variables with a p-value of less than 0.05 were considered as statistically significant.

2.4. Data Quality Control

The data collectors were trained, and supervision was made during data collection. All necessary materials were prepared and inspected before sample collection. A control organism was used for each test or a new set of testing conditions to guarantee the accuracy of the susceptibility test result. Standard strain, Streptococcus pneumoniae ATCC 49619 control strain, was used. Zone diameters obtained for the control strain were compared with CLSI 2014 guideline. The optochin disk was tested with positive and negative controls. As a positive control, Streptococcus pneumoniae ATCC 49619 was used, and Streptococcus mitis strain ATCC 49456 as a negative control. Then the results of the laboratory tests were recorded in a well-prepared format carefully and finally were attached to the questionnaire.

3. RESULTS

3.1. Socio-demographic Characteristics of the Participants

A total of 293 participants were enrolled in the study. Most of the participants were males, 170 (58%). Only 6.1% of participants had a history of hospitalization. Most of the study participants, (78.2%) were living in a family size of > 5 members per household. The ages of participants ranged from 5 months to 14 years with mean age, 5±3.8 years and most of the study participants were within the age group < 3 years, 123 (42%) (Table 1).

Table 1
Sociodemographic characteristics and distribution of nasopharyngeal carriage rate of Streptococcus pneumoniae among children (N=293).


Table 2
Bivariate and multivariate logistic regression analysis of nasopharyngeal carriage rate of Streptococcus pneumoniae with independent variables (N=293).


3.2. The Nasopharyngeal Carriage Rate of Streptococcus pneumoniae

From a total of 293 nasopharyngeal swab specimens, Streptococcus pneumoniae was isolated from 74 of them yielding a carriage rate of 25.3%. The carriage rate was high in the age group <3 years, 37/74 (50%) and males, 46/74 (62.2%) (Table 1).

3.3. Factors Associated with Nasopharyngeal Carriage Rate of Streptococcus pneumoniae

Bivariate logistic regression analysis of socio-demographic variables demonstrated that only age group <3 years, (COR 3.298, 95% CI ([1.296-8.393]), p= 0.012) and age group 3-9 years, (COR 2.732, 95% CI ([1.062-7.024Ndosa A, Kidenya BR, Mushi MF, Mirambo MM, Hokororo A, Mshana SE. Factors associated with colonization of Streptococcus pneumoniae among under-fives attending clinic in Mwanza City, Tanzania. Tanzan J Health Res 2015; 17(1)]), p=0.037), were significantly associated with carriage rate of Streptococcus pneumoniae. In addition, bivariate logistic regression analysis of related factors with carriage rate showed number of rooms per household (COR 2.438, 95% CI ([1.764-2.762]), p=0.020) and habit of sleeping with parents/guardians (COR 2.056, 95% CI ([1.243-17.367]), p=0.048) to be significantly associated with nasopharyngeal carriage rate of Streptococcus pneumoniae. The other sociodemographic characteristics such as sex, religion, educational status of parents/guardians, marital status of parents, and parents/guardian’s occupation were not significantly associated with pneumococcal carriage (Table 2).

Variables with a p-value of ≤0.25 in the bivariate analysis were candidate variables for multivariate analysis. After adjusting the possible confounders, age group < 3 years, the habit of sleeping with parent(s)/guardians, and the number of rooms per household were independent predictors of carriage rate.

Children of younger age group <3 years were three times more likely to carry Streptococcus pneumoniae in their nasopharynx compared to the age group 9-15 years (AOR 2.9, 95% CI ([1.042-8.27Ueno M, Ishii Y, Tateda K, et al. Prevalence and risk factors of nasopharyngeal carriage of Streptococcus pneumoniae in healthy children in Japan. Jpn J Infect Dis 2013; 66(1): 22-5.
[http://dx.doi.org/10.7883/yoken.66.22] [PMID: 23429080]
]), p=0.042). Those who had a habit of sleeping with parent(s)/guardians were two times more likely to carry Streptococcus pneumoniae in their nasopharynx compared to those who did not (AOR 2.26, 95% CI ([1.25-20.24Ndosa A, Kidenya BR, Mushi MF, Mirambo MM, Hokororo A, Mshana SE. Factors associated with colonization of Streptococcus pneumoniae among under-fives attending clinic in Mwanza City, Tanzania. Tanzan J Health Res 2015; 17(1)]) and those who lived in a house with a single room were two times more likely to carry Streptococcus pneumoniae in their nasopharynx compared to those living in a house with more than two rooms (AOR 2.36, 95% CI ([1.68-2.717Lema K, Murugan R, Tachbele E. Prevalence and associated factors of pneumonia among under-five children at public hospitals in Jimma zone, South West of Ethiopia. J Pulmonol Clin Res 2018; 2(1): 25-31.]), p=0.038) (Table 2).

3.4. Antimicrobial Susceptibility Pattern of Streptococcus pneumoniae

Susceptibility test for applied antibiotics was done on MHA with a 5% sheep blood supplement following CLSI recommendation. Only 10 isolates showed susceptibility to all applied antibiotics. Twenty-one isolates (28.4%) were resistant to two antimicrobial agents and 14 (18.9%) isolates were resistant to three or more antibiotics. The isolates were susceptible to Erythromycin, 38 (51.4%), and Chloramphenicol, 57 (77%). Forty-nine (66.2%) isolates of pneumococci showed Oxacillin zone size > 20mm which were susceptible to penicillin. Whereas, 36 (48.65%) and 29 (39.2%) of Streptococcus pneumoniae isolates were resistant to Tetracycline and Trimethoprim/sulfamethoxazole, respectively. About 25 (33.8%) isolates of pneumococci showed Oxacillin zone of inhibition <19mm diameter, in which the minimum inhibitory concertation (MIC) of penicillin needs to be determined in order to report the penicillin resistance and intermediate resistance. However, the MIC of penicillin was not determined due to the scarcity of resources in the current study (Table 3).

4. DISCUSSION

This study provides insights into the nasopharyngeal carriage rate of Streptococcus pneumoniae and its antimicrobial susceptibility pattern among children. The nasopharyngeal carriage rate of 25.3% in the current study is higher than a study conducted in Japan, 22% [27Ueno M, Ishii Y, Tateda K, et al. Prevalence and risk factors of nasopharyngeal carriage of Streptococcus pneumoniae in healthy children in Japan. Jpn J Infect Dis 2013; 66(1): 22-5.
[http://dx.doi.org/10.7883/yoken.66.22] [PMID: 23429080]
]. Whereas, the result is in harmony with a study carried out in India, 27.9% [28Kumar KL, Ashok V, Ganaie F, Ramesh AC. Nasopharyngeal carriage, antibiogram & serotype distribution of Streptococcus pneumoniae among healthy under five children. Indian J Med Res 2014; 140(2): 216-20.
[PMID: 25297353]
] and far lower than studies done in Brazil, 55% [29Menezes AP, Azevedo J, Leite MC, et al. Nasopharyngeal carriage of Streptococcus pneumoniae among children in an urban setting in Brazil prior to PCV10 introduction. Vaccine 2016; 34(6): 791-7.
[http://dx.doi.org/10.1016/j.vaccine.2015.12.042] [PMID: 26742946]
], Gambia, 58.6% [30Darboe MK, Fulford AJ, Secka O, Prentice AM. The dynamics of nasopharyngeal streptococcus pneumoniae carriage among rural Gambian mother-infant pairs. BMC Infect Dis 2010; 10(1): 195.
[http://dx.doi.org/10.1186/1471-2334-10-195] [PMID: 20602782]
], Uganda, 33% [31Rutebemberwa E, Mpeka B, Pariyo G, et al. High prevalence of antibiotic resistance in nasopharyngeal bacterial isolates from healthy children in rural Uganda: A cross-sectional study. Ups J Med Sci 2015; 120(4): 249-56.
[http://dx.doi.org/10.3109/03009734.2015.1072606] [PMID: 26305429]
], Ghana, 48.9% [32Mills RO, Twum-Danso K, Owusu-Agyei S, Donkor ES. Epidemiology of pneumococcal carriage in children under five years of age in Accra, Ghana. Infect Dis (Lond) 2015; 47(5): 326-31.
[http://dx.doi.org/10.3109/00365548.2014.994185] [PMID: 25761718]
], Nigeria, 52.5% [33Adetifa IM, Antonio M, Okoromah CA, et al. Pre-vaccination nasopharyngeal pneumococcal carriage in a Nigerian population: epidemiology and population biology. PLoS One 2012; 7(1)e30548
[http://dx.doi.org/10.1371/journal.pone.0030548] [PMID: 22291984]
], and Kenya, 51% [34Abdullahi O, Karani A, Tigoi CC, et al. The prevalence and risk factors for pneumococcal colonization of the nasopharynx among children in Kilifi District, Kenya. PLoS One 2012; 7(2)e30787
[http://dx.doi.org/10.1371/journal.pone.0030787] [PMID: 22363489]
]. Compared to previous studies in Ethiopia, the result is lower as compared to studies conducted in Gondar, 41.03% [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.], and Jimma, 43.8% [23Gebre T, Tadesse M, Aragaw D, et al. Nasopharyngeal carriage and antimicrobial susceptibility patterns of Streptococcus pneumoniae among children under five in Southwest Ethiopia. Children (Basel) 2017; 4(4): 27.
[http://dx.doi.org/10.3390/children4040027] [PMID: 28422083]
]. The difference might be because most of the above studies were conducted among children under 5 years old. Streptococcus pneumoniae carriage rate has a downward proportion with age and the prevalence of colonization is higher in young children and reaches a peak at two and three years old. Whereas, the current study included children aged < 15 years. Therefore, an age difference of the target population might contribute to the difference. The difference might be also due to differences in the study settings, in which some of the above studies were carried out in daycare centers of preschool-age children only. Daycare centers such as kindergartens have been identified as risk factors for the nasopharyngeal colonization of pneumococci. In addition, the difference might be due to socioeconomic differences in the study population.

Age was found as a significantly associated factor for the nasopharyngeal carriage rate of Streptococcus pneumoniae. A similar study from Brazil documented children under 2 years of age group to be associated with pneumococcal colonization [29Menezes AP, Azevedo J, Leite MC, et al. Nasopharyngeal carriage of Streptococcus pneumoniae among children in an urban setting in Brazil prior to PCV10 introduction. Vaccine 2016; 34(6): 791-7.
[http://dx.doi.org/10.1016/j.vaccine.2015.12.042] [PMID: 26742946]
]. In addition, a study from India indicated the progressive decrease in the carriage rate with the increasing age of the children [28Kumar KL, Ashok V, Ganaie F, Ramesh AC. Nasopharyngeal carriage, antibiogram & serotype distribution of Streptococcus pneumoniae among healthy under five children. Indian J Med Res 2014; 140(2): 216-20.
[PMID: 25297353]
]. Being within the young age group and living with younger children were identified as risk factors of pneumococcal carriage in a study conducted at Gondar University Hospital, Ethiopia [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.]. Carriage of Streptococcus pneumoniae was significantly higher in children living with siblings < 5 years old. The previous study conducted in Ethiopia also indicated that age (being 5 and 6 years) was significantly associated with S. pneumoniae carriage rate [23Gebre T, Tadesse M, Aragaw D, et al. Nasopharyngeal carriage and antimicrobial susceptibility patterns of Streptococcus pneumoniae among children under five in Southwest Ethiopia. Children (Basel) 2017; 4(4): 27.
[http://dx.doi.org/10.3390/children4040027] [PMID: 28422083]
]. The decline in the Streptococcus pneumoniae carriage rate with increasing age may reflect the gradual acquisition of mucosal immunity and reduction of exposure.

In the current study, the habit of sleeping with parents (AOR 2.258, 95% C.I (1.252-20.239), p=0.031), and the number of rooms per household (AOR 2.359, 95% C.I (1.680-2.717), p=0.038) were significantly associated with carriage rate of Streptococcus pneumoniae. Those children who live in a house with a single room and those who have the habit of sleeping with parent(s)/guardians are two times more likely to carry Streptococcus pneumoniae. A similar finding was reported from the previous study in Northwest Ethiopia [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.] and Southwest Ethiopia [23Gebre T, Tadesse M, Aragaw D, et al. Nasopharyngeal carriage and antimicrobial susceptibility patterns of Streptococcus pneumoniae among children under five in Southwest Ethiopia. Children (Basel) 2017; 4(4): 27.
[http://dx.doi.org/10.3390/children4040027] [PMID: 28422083]
] in which the carriage rate of Streptococcus pneumoniae was significantly associated with the number of rooms per household. These factors are related to overcrowded conditions that favor the high transmission and acquisition of Streptococcus pneumoniae.

In the current study, only 10 (13.5%) Streptococcus pneumoniae isolates were susceptible to all applied antibiotics. About a quarter (28.4%) of isolates were resistant to two antimicrobial agents and 14 (18.9%) isolates were resistant to three or more antibiotics. Similar findings were reported from studies in India, Gambia and Gondar, Ethiopia in which 19% [28Kumar KL, Ashok V, Ganaie F, Ramesh AC. Nasopharyngeal carriage, antibiogram & serotype distribution of Streptococcus pneumoniae among healthy under five children. Indian J Med Res 2014; 140(2): 216-20.
[PMID: 25297353]
], 26.3% [30Darboe MK, Fulford AJ, Secka O, Prentice AM. The dynamics of nasopharyngeal streptococcus pneumoniae carriage among rural Gambian mother-infant pairs. BMC Infect Dis 2010; 10(1): 195.
[http://dx.doi.org/10.1186/1471-2334-10-195] [PMID: 20602782]
], and 19.8% [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.] of isolates, respectively, were resistant to three or more antimicrobials.

The high number of Streptococcus pneumoniae isolates showed resistance against Tetracycline, 36 (48.65%), and TMP/SMX, 29 (39.2%). A similar finding was observed in a study from India, in which 36% of isolates were resistant to Tetracycline [28Kumar KL, Ashok V, Ganaie F, Ramesh AC. Nasopharyngeal carriage, antibiogram & serotype distribution of Streptococcus pneumoniae among healthy under five children. Indian J Med Res 2014; 140(2): 216-20.
[PMID: 25297353]
]. In addition, 73.8% and 82.6% of resistance to TMP/SMX were reported from studies conducted in Brazil [29Menezes AP, Azevedo J, Leite MC, et al. Nasopharyngeal carriage of Streptococcus pneumoniae among children in an urban setting in Brazil prior to PCV10 introduction. Vaccine 2016; 34(6): 791-7.
[http://dx.doi.org/10.1016/j.vaccine.2015.12.042] [PMID: 26742946]
] and Tanzania [35Moyo SJ, Steinbakk M, Aboud S, et al. Penicillin resistance and serotype distribution of Streptococcus pneumoniae in nasopharyngeal carrier children under 5 years of age in Dar es Salaam, Tanzania. J Med Microbiol 2012; 61(Pt 7): 952-9.
[http://dx.doi.org/10.1099/jmm.0.042598-0] [PMID: 22442292]
], respectively. Related findings were reported from studies in other African countries, Uganda, 97% resistance to TMP/SMX [31Rutebemberwa E, Mpeka B, Pariyo G, et al. High prevalence of antibiotic resistance in nasopharyngeal bacterial isolates from healthy children in rural Uganda: A cross-sectional study. Ups J Med Sci 2015; 120(4): 249-56.
[http://dx.doi.org/10.3109/03009734.2015.1072606] [PMID: 26305429]
], Gambia, 39% resistance to

Table 3
Antimicrobial susceptibility pattern of Streptococcus pneumoniae isolates (n =74).


TMP/SMX, and 32.3% resistance to Tetracycline [30Darboe MK, Fulford AJ, Secka O, Prentice AM. The dynamics of nasopharyngeal streptococcus pneumoniae carriage among rural Gambian mother-infant pairs. BMC Infect Dis 2010; 10(1): 195.
[http://dx.doi.org/10.1186/1471-2334-10-195] [PMID: 20602782]
], Ethiopia, 43.9% resistance to TMP/SMX [23Gebre T, Tadesse M, Aragaw D, et al. Nasopharyngeal carriage and antimicrobial susceptibility patterns of Streptococcus pneumoniae among children under five in Southwest Ethiopia. Children (Basel) 2017; 4(4): 27.
[http://dx.doi.org/10.3390/children4040027] [PMID: 28422083]
]. Resistance to Tetracycline in the current study was higher compared to a previous study done in Gondar, Ethiopia, i.e. 22.9% [22Assefa A, Gelaw B, Shiferaw Y, Tigabu Z. Nasopharyngeal Carriage Rate and Antimicrobial Susceptibility Pattern of Potential Pathogenic Bacteria among Paediatrics Outpatients at Gondar University Teaching Hospital, Ethiopia. J Infect Dis Ther 2013; 1: 2.].

In the current study, a relatively low number of isolates showed resistance to Chloramphenicol, 17 (23%), and Erythromycin, 20 (27%). A similar result was reported from a study in Tanzania with 3.5% resistance to Chloramphenicol, and 6% resistance to Erythromycin [24Ndosa A, Kidenya BR, Mushi MF, Mirambo MM, Hokororo A, Mshana SE. Factors associated with colonization of Streptococcus pneumoniae among under-fives attending clinic in Mwanza City, Tanzania. Tanzan J Health Res 2015; 17(1)]. In addition, a study from Gambia reported that 6.3% isolates were resistant to Chloramphenicol [30Darboe MK, Fulford AJ, Secka O, Prentice AM. The dynamics of nasopharyngeal streptococcus pneumoniae carriage among rural Gambian mother-infant pairs. BMC Infect Dis 2010; 10(1): 195.
[http://dx.doi.org/10.1186/1471-2334-10-195] [PMID: 20602782]
]. A previous study in Ethiopia reported 8.4% isolates to be resistant to Chloramphenicol and 15.9% to Erythromycin [23Gebre T, Tadesse M, Aragaw D, et al. Nasopharyngeal carriage and antimicrobial susceptibility patterns of Streptococcus pneumoniae among children under five in Southwest Ethiopia. Children (Basel) 2017; 4(4): 27.
[http://dx.doi.org/10.3390/children4040027] [PMID: 28422083]
]. This difference could be attributed to the difference in bacterial serotype distribution, the difference in the general consumption of antimicrobial agents, and socioeconomic difference. Indiscriminate use of antibiotics and managing bacterial infections without having determined local antimicrobial sensitivity result contribute to the emergence of antimicrobial-resistant strains.

As a limitation of the current study, serotyping of the pneumococci was not performed which could have been significant to assess the vaccine and nonvaccine serotype distribution of pneumococci. In addition, the minimum inhibitory concentration of penicillin was not performed, and as a result, we could not able to report penicillin-resistant isolates of pneumococci.

CONCLUSION

The nasopharyngeal carriage of Streptococcus pneumoniae among children was considerably high. High antimicrobial resistance against Tetracycline and susceptibility to Chloramphenicol were observed. The findings indicated children’s habit of sleeping with parent(s)/guardians, being within a young age group, and living in a house with a single room as associated with the high rate of Streptococcus pneumoniae carriage. Strategies should be designed to prevent pneumococcal nasopharyngeal carriage with a focus on modifiable associated factors and the bacterium antibiotic resistance pattern should be monitored regularly. Further researches on the distribution of pneumococci serotypes and drivers for antibiotic resistance are recommended.

LIST OF ABBREVIATIONS

ARI  = Acute respiratory illness
CLSI  = Clinical Laboratory Standard Institute
MHA  = Mueller Hinton agar
OPD  = Outpatient’s department
PCV-10  = Pneumococcal Conjugate Vaccine 10
TMP/SMX  = Trimethoprim/sulfamethoxazole

AUTHORS' CONTRIBUTIONS

DDA was involved in proposal writing and design, data collection, analysis, interpretation, drafting of the manuscript, supervised data collection and analysis, TWD was involved in the study design, reviewing of the proposal and manuscript, supervised data collection. AKS was involved in the study design, reviewing of the proposal and manuscript, supervised data collection. All authors read and approved the final manuscript.

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

Ethical clearance was obtained from the Institute of research and community service of Mizan Tepi University (Ref No: MTU/14/13/3/44/09) and official permission was obtained from the hospital.

HUMAN AND ANIMAL RIGHTS

Not applicable.

CONSENT FOR PUBLICATION

After explaining the objectives of the study, written consent was obtained from each study participant’s parent(s)/legal guardian(s). For the participant’s parent(s)/legal guardian(s) who were not able to read and write, a fingerprint was used as a signature.

AVAILABILITY OF DATA AND MATERIALS

All relevant data are within the paper, but any additional data required by the journal can be available anytime from the primary author.

FUNDING

Funding for this study was made possible through grants offered by Mizan Tepi University, Ethiopia (Ref No: MTU/14/13/3/44/09).

CONFLICTS OF INTEREST

The author declares no conflict of interest, financial or otherwise.

ACKNOWLEDGEMENTS

Our earnest gratitude goes to the staff of Mizan Tepi University teaching hospital for their technical assistance and kind cooperation during specimen collection. Special thanks also to all the study participants for their cooperation during data and sample collection. We are grateful for Dr. Cipriano Nead Tucky Jr. for his revision, grammar edition, and valuable suggestions during the manuscript preparation.

SUPPLEMENTARY MATERIAL

Supplementary material is available on the publisher’s web site along with the published article.


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