• nasopharyngeal colonisation;
  • HIV ;
  • Cambodia;
  • children;
  • bacteria


  1. Top of page
  2. Abstract
  3. References


To determine patterns of nasopharyngeal colonisation in HIV-positive children.


Nasopharyngeal, nasal and ear swabs were prospectively taken from all children living in two paediatric nursing homes for HIV-positive orphans in Cambodia from 2004 to 2011.


A total of 882 swabs were taken, of which 586 tested positive for bacteria. Staphylococcus aureus was the most frequently isolated species (178 isolates; 30.4%) followed by Streptococcus pneumoniae (103 isolates; 17.6%) and Klebsiella pneumoniae (99 isolates; 16.9%). The rate of S. pneumoniae decreased in 2009 when a vaccination programme was introduced.


The respiratory tract of HIV-positive children receiving highly active antiretroviral therapy is commonly colonised by S. aureus and S. pneumoniae, while other species normally found in the respiratory tract, such as Moraxella catarrhalis, are far less frequent.


Déterminer les profils de colonisation du rhinopharynx chez les enfants VIH-positifs.


Des prélèvements par écouvillons du rhinopharynx, du nez et des oreilles ont été prospectivement effectués chez tous les enfants vivant dans deux centres de soins infirmiers pédiatriques pour orphelins VIH-positifs au Cambodge, de 2004 à 2011.


882 prélèvements ont été effectués, dont 586 ont été trouvés positifs pour des bactéries. Staphylococcus aureus était l'espèce la plus fréquemment isolée (178 isolats; 30.4%) suivie de Streptococcus pneumoniae (103 isolats; 17.6%) et Klebsiella pneumoniae (99 isolats; 16.9%). Le taux de S. pneumoniae a diminué en 2009 quand un programme de vaccination a été introduit.


Les voies respiratoires des enfants VIH-positifs recevant un traitement antirétroviral hautement actif est généralement colonisés par S. aureus et S. pneumoniae, tandis que d'autres espèces normalement présentes dans le tractus respiratoire, telle que Moraxella catarrhalis, sont beaucoup moins fréquentes.


Determinar los patrones de la colonización nasofaríngea en niños VIH positivos.


De forma retrospectiva se recogieron frotis nasofaríngeos, nasales y de oído a niños viviendo en dos orfanatos para huérfanos VIH positivos en Cambodia, entre 2004 y 2011.


Se tomaron 882 frotis, de los cuales 586 dieron positivo para bacterias. Staphylococcus aureus era la especie más frecuentemente aislada (178 aislados; 30.4%), seguida por Streptococcus pneumoniae (103 aislados; 17.6%) y Klebsiella pneumoniae (99 aislados; 16.9%). La tasa de S. pneumoniae disminuyó en el 2009 cuando se introdujo el programa de vacunación.


El tracto respiratorio de niños VIH positivos recibiendo terapia antirretroviral de gran actividad normalmente está colonizado por S. aureus y S. pneumoniae, mientras que otras especies normalmente encontradas en el tracto respiratorio, como Moraxella catarrhalis, son mucho menos frecuentes.

Nasopharyngeal colonisation can be significantly changed in HIV-positive children compared with the uninfected population (Kinabo et al. 2013). Due to immune impairments in HIV-positive children and co-trimoxazole prophylaxis, susceptibility to infections may be increased and, also, normal nasopharyngeal colonisation may be influenced (Gill et al. 2008). As we have been running projects for HIV-positive children in Cambodia for 9 years, we wanted to contribute to this field with our observations.

Projects are run in the cities of Phnom Penh and Sihanoukville, where we started to obtain nasopharyngeal swabs in October 2003 from all HIV-positive children (39.4% male; median age 7 years; IQR = 5–9 years). We collected the swabs prospectively every 6 months. By the end of March 2012, we had collected 882 nasal, nasopharyngeal and ear swabs. Of these, 296 (33.6%) tested positive for fungi and 586 (66.4%) for bacteria. They were transported to Slovakia to the Department of Clinical Microbiology, Nitra University Hospital, and to the Slovak Tropical Institute, Bratislava, for identification and susceptibility testing.

Staphylococcus aureus was predominant (178 isolates; 30.4%), followed by Streptococcus pneumoniae (103 isolates; 17.6%) and Klebsiella pneumoniae (99 isolates; 16.9%). Moraxella catarrhalis (35 isolates, 6.0%) and Haemophilus influenzae (20 isolates, 3.4%) were present to a lesser extent (Table 1). Also, one-third of all isolates were identified as fungi, mostly Candida albicans (214 isolates; 72.3%).

Table 1. Spectrum of bacteria isolated from respiratory tract of HIV-positive children from Cambodia
Staphylococcus aureus 17830.4
Streptococcus pneumoniae 10317.6
Klebsiella pneumoniae 9916.9
P. aeruginosa 467.9
Moraxella catarrhalis 356.0
Haemophilus influenzae 203.4
Other species10517.8

Regarding resistance, we found oxacillin resistance (methicillin-resistant S. aureus phenotype – MRSA) to be the most prevalent among S. aureus (112 isolates; 63%), but resistance to other classes of antibiotics was high in this group of pathogens, too (e.g. clindamycin: 59%; erythromycin: 43%). However, susceptibility to vancomycin (100%), linezolid (100%), ciprofloxacin (96%) and co-trimoxazole (95%) was very high. Among S. pneumoniae isolates, penicillin resistance was 35% (36 isolates of 103) and resistance to tetracycline 64%. Of M. catarrhalis isolates, 90% were resistant to penicillin and ampicillin, but sufficiently susceptible to penicillins with penicillinase inhibitors (ampicillin/sulbactam and amoxicillin/clavulanic acid).

Interestingly, Kinabo et al. (2013) in their study among Tanzanian HIV-positive children, reported colonisation with Saureus in 66%, S. pneumoniae in 56%, M. catarrhalis in 50% and H. influenzae in 14% of children at 6 weeks of age, which is in contrast to our findings. There may be a few explanations for these differences.

In Kilimanjaro Hospital, only 8.6% of children were HIV positive and most of the infants were 6 weeks to 6 months old (Kinabo et al. 2013). Many, but not all (60%), received co-trimoxazole prophylaxis, while in our study group, all children were HIV positive and 90% received co-trimoxazole prophylaxis for 26 ± 21 (range 1–85) months. Moreover, many of our patients were repeatedly treated with antibiotics (5–9 treatment courses on average), especially during the first 2 years of highly active antiretroviral therapy (HAART). The majority (88.3%) of our study group received HAART, which can remarkably contribute to regeneration of immune system and therefore indirectly improve the response to respiratory pathogens in a positive way (Shahum et al. 2007).

Importantly, since 2009, all children (older than 2 years) in our project have been vaccinated with 23-valent pneumococcal polysaccharide vaccine, which led to a dramatic decrease in S. pneumoniae infections/colonisation (38.7% in 2007–15.8% in 2009, 4.3% in 2010 and 2.2% in 2011; Table 2) and which confirms the usefulness of the vaccine in preventing pneumococcal diseases in these age groups.

Table 2. Changes in bacterial nasopharyngeal colonisation of HIV-positive children during the 7 years of follow up
  1. Data from 2008 are missing due to personnel dropouts which led to impossibility of taking all swabs.

Overall number of isolates 65%109%65%124%38%94%91%586%
Streptococcus pneumoniae 11.52825.71421.54838.7615.844.322.210317.6
Staphylococcus aureus 1218.52825.71523.14435.52052.61819.14145.117830.4
Moraxella catarrhalis 812.387.357.754.025.333.244.4356.0
Haemophilus influenzae 34.665.5812.310.800.011.111.1203.4

Finally, the age of the children may be an important factor, as the majority of the children in the Tanzanian study were infants younger than 6 months, who probably are still colonised from their mothers.

Apart from these four, there can be many other reasons for such differences. We applaud Kinabo et al. for conducting a 5-year study in difficult resource-limited settings without adequate technical support, and suggest that if their clinical isolates are still viable and available, they test them for antimicrobial susceptibility, especially those isolated from HIV-positive children, to assess the dynamics of resistance changes.


  1. Top of page
  2. Abstract
  3. References
  • Gill CJ, Mwanakasale V, Fox MP et al. (2008) Effect of presumptive co-trimoxazole prophylaxis on pneumococcal colonization rates, seroepidemiology and antibiotic resistance in Zambian infants: a longitudinal cohort study. Bulletin of the World Health Organization 86, 929938.
  • Kinabo GD, van der Ven A, Msuya LJ et al. (2013) Dynamics of nasopharyngeal bacterial colonisation in HIV-exposed young infants in Tanzania. Tropical Medicine & International Health 18, 286295.
  • Shahum A, Benca G, Duong LS et al. (2007) Reversibility of antimicrobial resistance in respiratory isolates in HIV-positive Cambodian children after 36 months of HAART. Journal of Antimicrobial Chemotherapy 60, 194197.