Date Published: January 20, 2017
Publisher: Public Library of Science
Author(s): Daniel Eibach, Michael Nagel, Benedikt Hogan, Clinton Azuure, Ralf Krumkamp, Denise Dekker, Mike Gajdiss, Melanie Brunke, Nimako Sarpong, Ellis Owusu-Dabo, Jürgen May, Herminia de Lencastre.
Nasal carriage with Staphylococcus aureus is a common risk factor for invasive infections, indicating the necessity to monitor prevalent strains, particularly in the vulnerable paediatric population. This surveillance study aims to identify carriage rates, subtypes, antimicrobial susceptibilities and virulence markers of nasal S. aureus isolates collected from children living in the Ashanti region of Ghana.
Nasal swabs were obtained from children < 15 years of age on admission to the Agogo Presbyterian Hospital between April 2014 and January 2015. S. aureus isolates were characterized by their antimicrobial susceptibility, the presence of genes encoding for Panton-Valentine leukocidin (PVL) and toxic shock syndrome toxin-1 (TSST-1) and further differentiated by spa-typing and multi-locus-sequence-typing. Out of 544 children 120 (22.1%) were colonized with S. aureus, with highest carriage rates during the rainy seasons (27.2%; p = 0.007), in females aged 6–8 years (43.7%) and males aged 8–10 years (35.2%). The 123 isolates belonged to 35 different spa-types and 19 sequence types (ST) with the three most prevalent spa-types being t355 (n = 25), t84 (n = 18), t939 (n = 13), corresponding to ST152, ST15 and ST45. Two (2%) isolates were methicillin-resistant S. aureus (MRSA), classified as t1096 (ST152) and t4454 (ST45), and 16 (13%) were resistant to three or more different antimicrobial classes. PVL and TSST-1 were detected in 71 (58%) and 17 (14%) isolates respectively. S. aureus carriage among Ghanaian children seems to depend on age, sex and seasonality. While MRSA rates are low, the high prevalence of PVL is of serious concern as these strains might serve not only as a source for severe invasive infections but may also transfer genes, leading to highly virulent MRSA clones.
Staphylococcus aureus contributes significantly to morbidity and mortality worldwide, causing a broad spectrum of diseases [1,2]. S. aureus nasal colonization has been identified as the most important risk factor for subsequent invasive infections . An estimated 30% of humans are nasal carriers of S. aureus , however carriage rates vary with geographic location, seasonality, age and sex . Studies among Dutch children revealed a decreasing carriage rate during the first year of life, remaining stable at 20–30% until it increases again to 40–50% between the age of 6 to 12 years [5,6]. In West Africa those rates might be considerably different due to co-colonization with other pathogens or particular living conditions, such as large family sizes and lower sanitary standards, which are all associated with S. aureus nasal carriage [7,8]. Studies from West and Central Africa show carriage rates ranging from 21% in Ghana  to 29% in Gabon  and 36% in Senegal , but none of these studies focus on children.
Nasal swabs from 544 children were collected during the study period. The most common causes for admission were malaria (57.7%), lower respiratory tract infections (31.1%), urinary tract infections (16.7%) and gastrointestinal infections (13.6%). The median age of patients was 2 (IQR: 1–5) years and 255 (46.9%) study children were female. In total 120 (22.1%) swabs were positive for S. aureus of which 3 revealed two different S. aureus isolates, resulting in a total of 123 S. aureus isolates. S. aureus carriage was similarly distributed (p = 0.33) among girls (n = 61/255; 23.9%) and boys (n = 59/289; 20.4%) (Table 1).
The present study identifies an age- (p = 0.004) and season-dependent (p = 0.007) nasal S. aureus colonisation and genotype pattern among children living in rural Ghana. Similar age-dependent parabolic carriage rates have been described in the Netherlands, however peak incidences occurred at a slightly older age (10 years) . Earlier colonisation after the first year of life might be caused by different exposures in rural Ghana compared to industrialized countries. For instance large family sizes and lower socio-economic development have been associated with S. aureus carriage [7,25]. However, the total rate of S. aureus carriers in the present study (22.1%) tends to be lower than in industrialized countries, such as the United States (36.9%; age-group 1–19 years) and the Netherlands (36,0%; age-group 1–19 years) [5,26]. Children aged 2–15 years from The Gambia revealed a carriage rate of 27.3% . Other carriage studies from West Africa do not allow a comparison, as either children were not included or rates were not stratified by age-groups [9,11,28].
The results of the present study suggest that nasal S. aureus carriage among children in Ghana is dependent on age and seasonality, with children above one year being colonized at a younger age compared to previous studies from industrialized countries. To what extent socioeconomic conditions, climatic factors or co-colonization with other pathogens play a role for nasal S. aureus carriage in this geographic region needs to be investigated in further studies. High PVL rates can be considered a serious threat for the development of virulent MRSA in the future. Already today, physicians must be aware of increasing antibiotic resistance among paediatric S. aureus isolates when comparing to previous Ghanaian studies.