Nasopharyngeal colonisation dynamics of bacterial pathogens in patients with fever in rural Burkina Faso: an observational study

BMC Infectious Diseases - Tập 22 - Trang 1-10 - 2022
Liesbeth Martens1,2,3, Bérenger Kaboré3,4,5, Annelies Post3,4, Christa E. van der Gaast-de Jongh1,3, Jeroen D. Langereis1,3, Halidou Tinto5, Jan Jacobs6,7, André J. van der Ven3,4, Quirijn de Mast3,4, Marien I. de Jonge1,3
1Department of Laboratory Medicine, Laboratory of Medical Immunology, Radboud University Medical Center, Nijmegen, The Netherlands
2Department of Medical Microbiology, Radboud University Medical Center, Nijmegen, The Netherlands
3Radboudumc Center for Infectious Diseases, Radboud university medical center, Nijmegen, the Netherlands
4Department of Internal Medicine, Radboud University Medical Center, Nijmegen, The Netherlands
5Institut de Recherche en Sciences de la Santé/Clinical Research Unit of Nanoro, Nanoro, Burkina Faso
6Department of Clinical Sciences, Institute of Tropical Medicine, Antwerp, Belgium
7Department of Microbiology, Immunology and Transplantation, KU Leuven, Leuven, Belgium

Tóm tắt

Nasopharyngeal colonisation with clinically relevant bacterial pathogens is a risk factor for severe infections, such as pneumonia and bacteraemia. In this study, we investigated the determinants of nasopharyngeal carriage in febrile patients in rural Burkina Faso. From March 2016 to June 2017, we recruited 924 paediatric and adult patients presenting with fever, hypothermia or suspicion of severe infection to the Centre Medical avec Antenne Chirurgicale Saint Camille de Nanoro, Burkina Faso. We recorded a broad range of clinical data, collected nasopharyngeal swabs and tested them for the presence of Streptococcus pneumoniae, Haemophilus influenzae, Moraxella catarrhalis, Staphylococcus aureus and Klebsiella pneumoniae by quantitative polymerase chain reaction. Using logistic regression, we investigated the determinants of carriage and aimed to find correlations with clinical outcome. Nasopharyngeal colonisation with S. pneumoniae, H. influenzae and M. catarrhalis was highly prevalent and strongly dependent on age and season. Females were less likely to be colonised with S. pneumoniae (OR 0.71, p = 0.022, 95% CI 0.53–0.95) and M. catarrhalis (OR 0.73, p = 0.044, 95% CI 0.54–0.99) than males. Colonisation rates were highest in the age groups < 1 year and 1–2 years of age and declined with increasing age. Colonisation also declined towards the end of the rainy season and rose again during the beginning of the dry season. K. pneumoniae prevalence was low and not significantly correlated with age or season. For S. pneumoniae and H. influenzae, we found a positive association between nasopharyngeal carriage and clinical pneumonia [OR 1.75, p = 0.008, 95% CI 1.16–2.63 (S. pneumoniae) and OR 1.90, p = 0.004, 95% CI 1.23–2.92 (H. influenzae)]. S. aureus carriage was correlated with mortality (OR 4.01, p < 0.001, 95% CI 2.06–7.83), independent of bacteraemia caused by this bacterium. Age, sex and season are important determinants of nasopharyngeal colonisation with S. pneumoniae, H. influenzae and M. catarrhalis in patients with fever in Burkina Faso. S. pneumoniae and H. influenzae carriage is associated with clinical pneumonia and S. aureus carriage is associated with mortality in patients with fever. These findings may help to understand the dynamics of colonisation and the associated transmission of these pathogens. Furthermore, understanding the determinants of nasopharyngeal colonisation and the association with disease could potentially improve the diagnosis of febrile patients.

Tài liệu tham khảo

Weiser JN, Ferreira DM, Paton JC. Streptococcus pneumoniae: transmission, colonization and invasion. Nat Rev Microbiol. 2018;16(6):355–67. https://doi.org/10.1038/s41579-018-0001-8. Agrawal A, Murphy TF. Haemophilus influenzae infections in the H. influenzae type b conjugate vaccine era. J Clin Microbiol. 2011;49(11):3728–32. https://doi.org/10.1128/JCM.05476-11. Goldstein EJC, Murphy TF, Parameswaran GI. Moraxella catarrhalis, a human respiratory tract pathogen. Clin Infect Dis. 2009;49(1):124–31. https://doi.org/10.1086/599375. Sakr A, Brégeon F, Mège JL, Rolain JM, Blin O. Staphylococcus aureus nasal colonization: an update on mechanisms, epidemiology, risk factors, and subsequent infections. Front Microbiol. 2018;9:2419. https://doi.org/10.3389/fmicb.2018.02419. Martin RM, Bachman MA. Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Front Cell Infect Microbiol. 2018;8:4. https://doi.org/10.3389/fcimb.2018.00004. Aston SJ. Pneumonia in the developing world: characteristic features and approach to management. Respirology. 2017;22(7):1276–87. https://doi.org/10.1111/resp.13112. Iroezindu MO, Chima EI, Isiguzo GC, Mbata GC, Onyedum CC, Onyedibe KI, Okoli LE. Sputum bacteriology and antibiotic sensitivity patterns of community-acquired pneumonia in hospitalized adult patients in Nigeria: a 5-year multicentre retrospective study. Scand J Infect Dis. 2014;46(12):875–87. https://doi.org/10.3109/00365548.2014.954263. Adegbola RA, DeAntonio R, Hill PC, Roca A, Usuf E, Hoet B, Greenwood BM. 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. https://doi.org/10.1371/journal.pone.0103293. Bojang A, Jafali J, Egere UE, Hill PC, Antonio M, Jeffries D, Greenwood BM, Roca A. Seasonality of pneumococcal nasopharyngeal carriage in rural Gambia determined within the context of a cluster randomized pneumococcal vaccine trial. PLoS ONE. 2015;10(7): e0129649. https://doi.org/10.1371/journal.pone.0129649. Bottomley C, Bojang A, Smith PG, Darboe O, Antonio M, Foster-Nyarko E, Kampmann B, Greenwood B, D’Alessandro U, Roca A. The impact of childhood vaccines on bacterial carriage in the nasopharynx: a longitudinal study. Emerg Themes Epidemiol. 2015;12(1):1. https://doi.org/10.1186/s12982-014-0022-3. Kaboré L, Adebanjo T, Njanpop-Lafourcade BM, Ouangraoua S, Tarbangdo FT, Meda B, Velusamy S, Bicaba B, Aké F, McGee L, Yaro S, Betsem E, Gervaix A, Gessner BD, Whitney CG, Moïsi JC, Van Beneden CA. Pneumococcal carriage in Burkina Faso after 13-valent pneumococcal conjugate vaccine introduction: results from 2 cross-sectional population-based surveys. J Infect Dis. 2021;224(Supplement_3):S258–66. https://doi.org/10.1093/infdis/jiab037. Wolf B, Gama A, Rey L, Fonseca W, Roord J, Fleer A, Verhoef J. Striking differences in the nasopharyngeal flora of healthy Angolan, Brazilian and Dutch children less than 5 years old. Ann Trop Paediatr. 1999;19(3):287–92. Eibach D, Nagel M, Hogan B, Azuure C, Krumkamp R, Dekker D, Gajdiss M, Brunke M, Sarpong N, Owusu-Dabo E, May J. Nasal carriage of Staphylococcus aureus among children in the Ashanti Region of Ghana. PLoS ONE. 2017;12(1): e0170320. https://doi.org/10.1371/journal.pone.0170320. Adetifa IMO, Adamu AL, Karani A, Waithaka M, Odeyemi KA, Okoromah CAN, Bello MM, Abubakar IS, Inem V, Scott JAG. Nasopharyngeal pneumococcal carriage in Nigeria: a two-site, population-based survey. Sci Rep. 2018;8(1):3509. https://doi.org/10.1038/s41598-018-21837-5. Baggett HC, Watson NL, Deloria Knoll M, Brooks WA, Feikin DR, Hammitt LL, Howie SRC, Kotloff KL, Levine OS, Madhi SA, Murdoch DR, Scott JAG, Thea DM, Antonio M, Awori JO, Baillie VL, DeLuca AN, Driscoll AJ, Duncan J, Ebruke BE, Goswami D, Higdon MM, Karron RA, Moore DP, Morpeth SC, Mulindwa JM, Park DE, Paveenkittiporn W, Piralam B, Prosperi C, Sow SO, Tapia MD, Zaman K, Zeger SL, O'Brien KL, PERCH Study Group. Density of upper respiratory colonization with Streptococcus pneumoniae and its role in the diagnosis of pneumococcal pneumonia among children aged < 5 years in the PERCH study. Clin Infect Dis. 2017;64(suppl_3):S317–27. https://doi.org/10.1093/cid/cix100. Dano ID, Ousmane S, Moumouni K, Lagare A, Issa I, Testa J. Risk factors associated with Streptococcus pneumonia carriage in children under five years old with acute respiratory infection in Niger. Pan Afr Med J. 2019;33:239. https://doi.org/10.11604/pamj.2019.33.239.15945. Egyir B, Guardabassi L, Esson J, Nielsen SS, Newman MJ, Addo KK, Larsen AR. Insights into nasal carriage of Staphylococcus aureus in an urban and a rural community in Ghana. PLoS ONE. 2014;9(4): e96119. https://doi.org/10.1371/journal.pone.0096119. Foster-Nyarko E, Kwambana B, Aderonke O, Ceesay F, Jarju S, Bojang A, McLellan J, Jafali J, Kampmann B, Ota MO, Adetifa I, Antonio M. Associations between nasopharyngeal carriage of Group B Streptococcus and other respiratory pathogens during early infancy. BMC Microbiol. 2016;16:97. https://doi.org/10.1186/s12866-016-0714-7. Odutola A, Antonio M, Owolabi O, Bojang A, Foster-Nyarko E, Donkor S, Adetifa I, Taylor S, Bottomley C, Greenwood B, Ota M. Comparison of the prevalence of common bacterial pathogens in the oropharynx and nasopharynx of Gambian infants. PLoS ONE. 2013;8(9): e75558. https://doi.org/10.1371/journal.pone.0075558. Park DE, Baggett HC, Howie SRC, Shi Q, Watson NL, Brooks WA, Deloria Knoll M, Hammitt LL, Kotloff KL, Levine OS, Madhi SA, Murdoch DR, O'Brien KL, Scott JAG, Thea DM, Ahmed D, Antonio M, Baillie VL, DeLuca AN, Driscoll AJ, Fu W, Gitahi CW, Olutunde E, Higdon MM, Hossain L, Karron RA, Maiga AA, Maloney SA, Moore DP, Morpeth SC, Mwaba J, Mwenechanya M, Prosperi C, Sylla M, Thamthitiwat S, Zeger SL, Feikin DR, PERCH Study Group. Colonization density of the upper respiratory tract as a predictor of pneumonia-Haemophilus influenzae, Moraxella catarrhalis, Staphylococcus aureus, and Pneumocystis jirovecii. Clin Infect Dis. 2017;64(suppl_3):S328–36. https://doi.org/10.1093/cid/cix104. Post A, Kaboré B, Reuling IJ, Bognini J, van der Heijden W, Diallo S, Lompo P, Kam B, Herssens N, Lanke K, Bousema T, Sauerwein RW, Tinto H, Jacobs J, de Mast Q, van der Ven AJ. The XN-30 hematology analyzer for rapid sensitive detection of malaria: a diagnostic accuracy study. BMC Med. 2019;17(1):103. https://doi.org/10.1186/s12916-019-1334-5. Post A, Kaboré B, Bognini J, Diallo S, Lompo P, Kam B, Herssens N, van Opzeeland F, van der Gaast-de Jongh CE, Langereis JD, de Jonge MI, Rahamat-Langendoen J, Bousema T, Wertheim H, Sauerwein RW, Tinto H, Jacobs J, de Mast Q, van der Ven AJ. Infection Manager System (IMS) as a new hemocytometry-based bacteremia detection tool: a diagnostic accuracy study in a malaria-endemic area of Burkina Faso. PLoS Negl Trop Dis. 2021;15(3): e0009187. https://doi.org/10.1371/journal.pntd.0009187. Kaboré B, Post A, Lompo P, Bognini JD, Diallo S, Kam BTD, Rahamat-Langendoen J, Wertheim HFL, van Opzeeland F, Langereis JD, de Jonge MI, Tinto H, Jacobs J, van der Ven AJ, de Mast Q. Aetiology of acute febrile illness in children in a high malaria transmission area in West Africa. Clin Microbiol Infect. 2021;27(4):590–6. https://doi.org/10.1016/j.cmi.2020.05.029.f. Derra K, Rouamba E, Kazienga A, Ouedraogo S, Tahita MC, Sorgho H, Valea I, Tinto H. Profile: Nanoro health and demographic surveillance system. Int J Epidemiol. 2012;41(5):1293–301. https://doi.org/10.1093/ije/dys159. District sanitaire de Nanoro. Plan d’action de l’année 2019 du district Sanitaire de Nanoro; 2019. Revised WHO classification and treatment of childhood pneumonia at health facilities. Geneva: World Health Organization; 2014. http://apps.who.int/iris/bitstream/handle/10665/137319/9789241507813_eng.pdf. Ngocho JS, Minja L, van der Gaast-de Jongh CE, Rahamat-Langendoen JC, Langereis JD, Mmbaga BT, de Jonge MI. Viral-bacterial (co-)occurrence in the upper airways and the risk of childhood pneumonia in resource-limited settings. J Infect. 2020. https://doi.org/10.1016/j.jinf.2020.06.013. Ter Horst R, Jaeger M, Smeekens SP, Oosting M, Swertz MA, Li Y, Kumar V, Diavatopoulos DA, Jansen AFM, Lemmers H, Toenhake-Dijkstra H, van Herwaarden AE, Janssen M, van der Molen RG, Joosten I, Sweep FCGJ, Smit JW, Netea-Maier RT, Koenders MMJF, Xavier RJ, van der Meer JWM, Dinarello CA, Pavelka N, Wijmenga C, Notebaart RA, Joosten LAB, Netea MG. Host and environmental factors influencing individual human cytokine responses. Cell. 2016;167(4):1111-1124.e13. https://doi.org/10.1016/j.cell.2016.10.018. Mueller JE, Yaro S, Ouédraogo MS, Levina N, Njanpop-Lafourcade BM, Tall H, Idohou RS, Sanou O, Kroman SS, Drabo A, Nacro B, Millogo A, van der Linden M, Gessner BD. Pneumococci in the African meningitis belt: meningitis incidence and carriage prevalence in children and adults. PLoS ONE. 2012;7(12): e52464. https://doi.org/10.1371/journal.pone.0052464. Kwambana BA, Barer MR, Bottomley C, Adegbola RA, Antonio M. Early acquisition and high nasopharyngeal co-colonisation by Streptococcus pneumoniae and three respiratory pathogens amongst Gambian new-borns and infants. BMC Infect Dis. 2011;11:175. https://doi.org/10.1186/1471-2334-11-175. Tenenbaum T, Franz A, Neuhausen N, Willems R, Brade J, Schweitzer-Krantz S, Adams O, Schroten H, Henrich B. Clinical characteristics of children with lower respiratory tract infections are dependent on the carriage of specific pathogens in the nasopharynx. Eur J Clin Microbiol Infect Dis. 2012;31(11):3173–82. https://doi.org/10.1007/s10096-012-1682-y.