Abstract
We report for the first time in Portugal a serotype c Haemophilus influenzae isolated from an adult, with HIV-1 infection. Whole-genome sequencing characterized the isolate as clonal complex ST-7, albeit with a novel MLST (ST2754) due to a unique atpG profile. Integration of this genome with other available H. influenzae serotype c genomes from PubMLST revealed its overall genetic distinctiveness, with the closest related isolate being identified in France in 2020. This surveillance study, involving collaboration among hospitals and reference laboratory, successfully contributed to the identification and characterization of this rare serotype.
Data availability
Reads sequencing data were deposited in the European Nucleotide Archive (Accession #ERR11588142), and genome assembly was deposited in the PubMLST website (Id #25086).
Code availability
Not applicable.
References
Agrawal A, Murphy TF (2011) Haemophilus influenzae infections in the H. influenzae type b conjugate vaccine era. J Clin Microbiol 49(11):3728–3732. https://doi.org/10.1128/JCM.05476-11
Garmendia J, Martí-Lliteras P, Moleres J, Puig C, Bengoechea JÁ (2012) Genotypic and phenotypic diversity of the noncapsulated Haemophilus influenzae: adaptation and pathogenesis in the human airways. Int Microbiol 15(4):159–172. https://doi.org/10.2436/20.1501.01.169
Butler DF, Myers AL (2018) Changing epidemiology of Haemophilus influenzae in children. Infect Dis Clin North Am 32(1):119–128. https://doi.org/10.1016/j.idc.2017.10.005
Pittman M (1931) Variation and type specificity in the bacterial species Haemophilus influenzae. J Exp Med 53(4):471–492. https://doi.org/10.1084/jem.53.4.471
Kroll JS, Zamze S, Loynds B, Moxon ER (1989) Common organization of chromosomal loci for production of different capsular polysaccharides in Haemophilus influenzae. J Bacteriol 171(6):3343–3347. https://doi.org/10.1128/jb.171.6.3343-3347.1989
Bijlmer HA (1991) World-wide epidemiology of Haemophilus influenzae meningitis; industrialized versus non-industrialized countries. Vaccine 9(Suppl):S5-9. https://doi.org/10.1016/0264-410x(91)90172-3.
Peltola H (2000) Worldwide Haemophilus influenzae type b disease at the beginning of the 21st century: global analysis of the disease burden 25 years after the use of the polysaccharide vaccine and a decade after the advent of conjugates. Clin Microbiol Rev 13(2):302–317. https://doi.org/10.1128/CMR.13.2.302
Ladhani SN, Collins S, Vickers A, Litt DJ, Crawford C, Ramsay ME, Slack MP (2012) Invasive Haemophilus influenzae serotype e and f disease, England and Wales. Emerg Infect Dis 18(5):725–732. https://doi.org/10.3201/eid1805.111738
Ulanova M, Tsang RSW (2014) Haemophilus influenzae serotype a as a cause of serious invasive infections. Lancet Infect Dis 14(1):70–82. https://doi.org/10.1016/S1473-3099(13)70170-1
Giufrè M, De Chiara M, Censini S, Guidotti S, Torricelli G, De Angelis G, Cardines R, Pizza M, Muzzi A, Cerquetti M, Soriani M (2015) Whole-genome sequences of nonencapsulated Haemophilus influenzae strains isolated in Italy. Genome Announc 3(2):e00110-e115. https://doi.org/10.1128/genomeA.00110-15
Suga S, Ishiwada N, Sasaki Y, Akeda H, Nishi J, Okada K, Fujieda M, Oda M, Asada K, Nakano T, Saitoh A, Hosoya M, Togashi T, Matsuoka M, Kimura K, Shibayama K (2018) A nationwide population-based surveillance of invasive Haemophilus influenzae diseases in children after the introduction of the Haemophilus influenzae type b vaccine in Japan. Vaccine 36(38):5678–5684. https://doi.org/10.1016/j.vaccine.2018.08.029
Bajanca P, Caniça M, Multicenter Study Group (2004) Emergence of nonencapsulated and encapsulated non-b-type invasive Haemophilus influenzae isolates in Portugal (1989–2001). J Clin Microbiol 42(2):807–810. https://doi.org/10.1128/JCM.42.2.807-810.2004
Bajanca-Lavado MP, Simões AS, Betencourt CR, Sá-Leão R, Portuguese group for study of Haemophilusinfluenzae invasive infection (2014) characteristics of Haemophilus influenzae invasive isolates from Portugal following routine childhood vaccination against H. influenzae serotype b (2002–2010). Eur J Clin Microbiol Infect Dis 33(4):603–610. https://doi.org/10.1007/s10096-013-1994-6
Calado R, Betencourt C, Gonçalves H, Cristino N, Calhau P, Lavado PB (2011) Complicated meningitis caused by a rare serotype of Haemophilus influenzae in Portugal. Diagn Microbiol Infect Dis 69(1):111–113. https://doi.org/10.1016/j.diagmicrobio.2010.08.029
Heliodoro CIM, Bettencourt CR, Bajanca-Lavado MP, Portuguese group for the study of Haemophilusinfluenzae invasive infection (2020) molecular epidemiology of invasive Haemophilus influenzae disease in Portugal: an update of the post-vaccine period, 2011–2018. Eur J Clin Microbiol Infect Dis 39(8):1471–1480. https://doi.org/10.1007/s10096-020-03865-0
Jolley KA, Bray JE, Maiden MCJ (2018) Open-access bacterial population genomics: BIGSdb software, the PubMLST.org website and their applications. Wellcome Open Res 3:124. https://doi.org/10.12688/wellcomeopenres.14826.1
European Committee on Antimicrobial Susceptibility Testing (2023) breakpoint tables for interpretation of MICs and zone diameters. Version 13.0, 2023. https://www.eucast.org/fileadmin/src/media/PDFs/EUCAST_files/Breakpoint_tables/v_13.0_Breakpoint_Tables.pdf. Accessed 4 February 2023.
Falla TJ, Crook DW, Brophy LN, Maskell D, Kroll JS, Moxon ER (1994) PCR for capsular typing of Haemophilus influenzae. J Clin Microbiol 32(10):2382–2386. https://doi.org/10.1128/jcm.32.10.2382-2386.1994
Llarena A-K, Ribeiro-Gonçalves BF, Nuno Silva D, Halkilahti J, Machado MP, Da Silva MS, Jaakkonen A, Isidro J, Hämäläinen C, Joenperä J, Borges V, Viera L, Gomes JP, Correia C, Lunden J, Laukkanen-Ninios R, Fredriksson-Ahomaa M, Bikandi J, San Millan R, Martinez-Ballesteros I, Laorden L, Mäesaar M, Grantina-Ievina L, Hilbert F, Garaizar J, Oleastro M, Nevas M, Salmenlinna S, Hakkinen M, Carriço JA, Rossi M (2018) INNUENDO: a cross-sectoral platform for the integration of genomics in the surveillance of food-borne pathogens. EFSA supporting publication 2018:15(11):EN-1498. 142 pp. https://doi.org/10.2903/sp.efsa.2018.EN-1498
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30(15):2114–2120. https://doi.org/10.1093/bioinformatics/btu170
Bankevich A, Nurk S, Antipov D, Gurevich AA, Dvorkin M, Kulikov AS, Lesin VM, Nikolenko SI, Pham S, Prjibelski AD, Pyshkin AV, Sirotkin AV, Vyahhi N, Tesler G, Alekseyev MA, Pevzner PA (2012) SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J Comput Biol 19(5):455–477. https://doi.org/10.1089/cmb.2012.0021
Walker BJ, Abeel T, Shea T, Priest M, Abouelliel A, Sakthikumar S, Cuomo CA, Zeng Q, Wortman J, Young SK, Earl AM (2014) Pilon: an integrated tool for comprehensive microbial variant detection and genome assembly improvement. PLoS One 9(11):e112963. https://doi.org/10.1371/journal.pone.0112963
Pinto M, González-Díaz A, Machado MP, Duarte S, Vieira L, Carriço JA, Marti S, Bajanca-Lavado MP, Gomes JP (2019) Insights into the population structure and pan-genome of Haemophilus influenzae. Infect Genet Evol 67:126–135. https://doi.org/10.1016/j.meegid.2018.10.025
Treangen TJ, Ondov BD, Koren S, Phillippy AM (2014) The harvest suite for rapid core-genome alignment and visualization of thousands of intraspecific microbial genomes. Genome Biol 15(11):524. https://doi.org/10.1186/s13059-014-0524-x
Bortolaia V, Kaas RS, Ruppe E, Roberts MC, Schwarz S, Cattoir V, Philippon A, Allesoe RL, Rebelo AR, Florensa AF, Fagelhauer L, Chakraborty T, Neumann B, Werner G, Bender JK, Stingl K, Nguyen M, Coppens J, Xavier BB, Malhotra-Kumar S, Westh H, Pinholt M, Anjum MF, Duggett NA, Kempf I, Nykäsenoja S, Olkkola S, Wieczorek K, Amaro A, Clemente L, Mossong J, Losch S, Ragimbeau C, Lund O, Aarestrup FM (2020) ResFinder 4.0 for predictions of phenotypes from genotypes. J Antimicrob Chemother 75(12):3491–3500. https://doi.org/10.1093/jac/dkaa345
Potts CC, Topaz N, Rodriguez-Rivera LD, Hu F, Chang HY, Whaley MJ, Schmink S, Retchless AC, Chen A, Ramos E, Doho GH, Wang X (2019) Genomic characterization of Haemophilus influenzae: a focus on the capsule locus. BMC Genomics 20(1):733. https://doi.org/10.1186/s12864-019-6145-8
Price EP, Sarovich DS, Nosworthy E, Beissbarth J, Marsh RL, Pickering J, Kirkham LA, Keil AD, Chang AB, Smith-Vaughan HC (2015) Haemophilus influenzae: using comparative genomics to accurately identify a highly recombinogenic human pathogen. BMC Genomics 16(1):641. https://doi.org/10.1186/s12864-015-1857-x
Slotved HC, Johannesen TB, Stegger M, Dalby T, Fuursted K (2023) National Danish surveillance of invasive clinical Haemophilus influenzae isolates and their resistance profile. Front Microbiol 14:1307261. https://doi.org/10.3389/fmicb.2023.1307261
Funding
The authors declare that no funds, grants, or other support were received during the preparation of this manuscript. This work was fully supported by Instituto Nacional de Saúde Doutor Ricardo Jorge, Lisboa, Portugal.
Author information
Authors and Affiliations
Contributions
Maria Paula Bajanca-Lavado coordinated the study. The first draft of the manuscript was written by Maria Paula Bajanca-Lavado and Miguel Pinto. Maria Paula Bajanca-Lavado, Miguel Pinto, Maria Dinah Carvalho, Gonçalo Jantarada Domingos, and José Melo-Cristino commented on previous versions of the manuscript. Maria Paula Bajanca-Lavado and Maria Dinah Carvalho performed laboratory work. Miguel Pinto performed bioinformatics data analysis. Gonçalo Jantarada Domingos attended the patient and wrote clinical history. Maria Paula Bajanca-Lavado, Miguel Pinto, Maria Dinah Carvalho, Gonçalo Jantarada Domingos, and José Melo-Cristino read and approved the final version of the manuscript.
Corresponding author
Ethics declarations
Ethics approval
Not applicable. Despite being a clinical case, there is no information that identifies the patient, as all data are completely anonymized at the originating hospital. The aim of the paper is to characterize the isolate and only a brief summary of the clinical history is provided.
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Competing interests
The authors declare no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Maria Paula Bajanca-Lavado and Miguel Pinto contributed equally to this article and shared the first authorship.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Bajanca-Lavado, M.P., Pinto, M., Carvalho, M.D. et al. Rare serotype c Haemophilus influenzae invasive isolate: characterization of the first case in Portugal. Eur J Clin Microbiol Infect Dis 43, 791–795 (2024). https://doi.org/10.1007/s10096-024-04774-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10096-024-04774-2