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Abstract

Whole-genome sequencing (WGS) is finding important applications in the surveillance of antimicrobial resistance (AMR), providing the most granular data and broadening the scope of niches and locations that can be surveilled. A common but often overlooked application of WGS is to replace or augment reference laboratory services for AMR surveillance. WGS has supplanted traditional strain subtyping in many comprehensive reference laboratories and is now the gold standard for rapidly ruling isolates into or out of suspected outbreak clusters. These and other properties give WGS the potential to serve in AMR reference functioning where a reference laboratory did not hitherto exist. In this perspective, we describe how we have employed a WGS approach, and an academic–public health system collaboration, to provide AMR reference laboratory services in Nigeria, as a model for leapfrogging to national AMR surveillance.

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2022-08-18
2024-05-05
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References

  1. WHO National antimicrobial resistance surveillance systems and participation in the Global Antimicrobial Resistance Surveillance System (GLASS): a guide to planning, implementation, and monitoring and evaluation World Health Organization; 2016b
    [Google Scholar]
  2. WHO Global action plan on antimicrobial resistance. Resolution WHA68.7; 2015 World Health Organization; 2016a
    [Google Scholar]
  3. NCDC: Nigeria Centre for Disease Control, Federal Ministry of Health, Federal Ministry of Agriculture & Federal Ministry of Environment National Action Plan for Antimicrobial Resistance (2017-2022) Abuja, Nigeria: Nigeria Centre for Disease Control (NCDC); 2017a
    [Google Scholar]
  4. Tacconelli E, Sifakis F, Harbarth S, Schrijver R, van Mourik M et al. Surveillance for control of antimicrobial resistance. Lancet Infect Dis 2018b; 18:e99–e106 [View Article]
    [Google Scholar]
  5. Argimón S, Masim MAL, Gayeta JM, Lagrada ML, Macaranas PKV et al. Integrating whole-genome sequencing within the national antimicrobial resistance surveillance program in the Philippines. Nat Commun 2020; 11:2719 [View Article] [PubMed]
    [Google Scholar]
  6. Abubakar I, Dalglish SL, Angell B, Sanuade O, Abimbola S et al. The Lancet Nigeria Commission: investing in health and the future of the nation. Lancet 2022; 399:1155–1200 [View Article]
    [Google Scholar]
  7. Fleming KA, Horton S, Wilson ML, Atun R, DeStigter K et al. The Lancet Commission on diagnostics: transforming access to diagnostics. Lancet 2021; 398:1997–2050 [View Article] [PubMed]
    [Google Scholar]
  8. Okeke IN. Divining without Seeds: The Case for Strengthening Laboratory Medicine in Africa Ithaca: ILR/ Cornell University Press; 2011 [View Article]
    [Google Scholar]
  9. Ombelet S, Ronat J-B, Walsh T, Yansouni CP, Cox J et al. Clinical bacteriology in low-resource settings: today’s solutions. Lancet Infect Dis 2018; 18:e248–e258 [View Article] [PubMed]
    [Google Scholar]
  10. Maxmen A. Nigeria’s disease detective. Nature 2019; 566:310–313 [View Article]
    [Google Scholar]
  11. Ibrahim RA, Teshal AM, Dinku SF, Abera NA, Negeri AA et al. Antimicrobial resistance surveillance in Ethiopia: implementation experiences and lessons learned. Afr J Lab Med 2018; 7:770 [View Article] [PubMed]
    [Google Scholar]
  12. Nabadda S, Kakooza F, Kiggundu R, Walwema R, Bazira J et al. Implementation of the World Health Organization global antimicrobial resistance surveillance system in Uganda, 2015-2020: mixed-methods study using national surveillance data. JMIR Public Health Surveill 2021; 7:e29954 [View Article] [PubMed]
    [Google Scholar]
  13. WHO GLASS guidance for national reference laboratories 2020b
    [Google Scholar]
  14. Tacconelli E, Carrara E, Savoldi A, Harbarth S, Mendelson M et al. Discovery, research, and development of new antibiotics: the WHO priority list of antibiotic-resistant bacteria and tuberculosis. Lancet Infect Dis 2018a; 18:318–327 [View Article] [PubMed]
    [Google Scholar]
  15. Kinh NV, Wertheim HFL, Thwaites GE, Khue LN, Thai CH et al. Developing an antimicrobial resistance reference laboratory and surveillance programme in Vietnam. Lancet Glob Health 2017; 5:e1186–e1187 [View Article] [PubMed]
    [Google Scholar]
  16. NCDC: Nigeria Centre for Disease Control, Federal Ministry of Health, Federal Ministry of Agriculture & Federal Ministry of Environment Antimicrobial use and resistance in Nigeria: situation analysis and recommendations Abuja, Nigeria: Nigeria Centre for Disease Control (NCDC); 2017b
    [Google Scholar]
  17. Dacombe R, Bates I, Gopul B, Sarkinfada F, Owusu-Ofori A. Overview of the antimicrobial resistance surveillance systems for Ghana, Malawi, Nepal and Nigeria The Fleming Fund; 2016
    [Google Scholar]
  18. Aanensen DM, Carlos CC, Donado-Godoy P, Okeke IN, Ravikumar KL et al. Implementing whole-genome sequencing for ongoing surveillance of antimicrobial resistance: exemplifying insights into Klebsiella pneumoniae. Clin Infect Dis 2021; 73:S255–S257 [View Article] [PubMed]
    [Google Scholar]
  19. Afolayan AO, Bernal JF, Gayeta JM, Masim ML, Shamanna V et al. Overcoming data bottlenecks in genomic pathogen surveillance. Clin Infect Dis 2021a; 73:S267–S274 [View Article] [PubMed]
    [Google Scholar]
  20. Harste HJ, Kiff G, Okeke IN, Adebiyi AO, Ravikumar KL et al. Good financial grant practice: a tool for developing and demonstrating institutional financial and grant management capacity in global health. Clin Infect Dis 2021; 73:S275–S282 [View Article] [PubMed]
    [Google Scholar]
  21. Kekre M, Arevalo SA, Valencia MF, Lagrada ML, Macaranas PKV et al. Integrating scalable genome sequencing into microbiology laboratories for routine antimicrobial resistance surveillance. Clin Infect Dis 2021; 73:S258–S266 [View Article] [PubMed]
    [Google Scholar]
  22. Chinen I, Campos J, Dorji T, Pérez Gutiérrez E. PulseNet Latin America and the Caribbean Network: present and future. Foodborne Pathog Dis 2019; 16:489–497 [View Article] [PubMed]
    [Google Scholar]
  23. Smith AM. Review of molecular subtyping methodologies used to investigate outbreaks due to multidrug-resistant enteric bacterial pathogens in sub-Saharan Africa. Afr J Lab Med 2019; 8:760 [View Article] [PubMed]
    [Google Scholar]
  24. Opintan JA, Newman MJ, Arhin RE, Donkor ES, Gyansa-Lutterodt M et al. Laboratory-based nationwide surveillance of antimicrobial resistance in Ghana. Infect Drug Resist 2015; 8:379–389 [View Article] [PubMed]
    [Google Scholar]
  25. Nkrumah K. The Academy Of Sciences Dinner, After Dinner Speech in Selected Speeches: Kwame Nkrumah. In Obeng S. eds Fourth Anniversary of the Academy of Sciences Ghana: Afram Publishers (Ghana) Ltd; 1963 pp 161–167
    [Google Scholar]
  26. Parkhill J, Dougan G, James KD, Thomson NR, Pickard D et al. Complete genome sequence of a multiple drug resistant Salmonella enterica serovar Typhi CT18. Nature 2001; 413:848–852 [View Article] [PubMed]
    [Google Scholar]
  27. White DG, Acar J, Anthony F, Franklin A, Gupta R et al. Antimicrobial resistance: standardisation and harmonisation of laboratory methodologies for the detection and quantification of antimicrobial resistance. Rev Sci Tech 2001; 20:849–858 [View Article] [PubMed]
    [Google Scholar]
  28. Harris SR, Cartwright EJP, Török ME, Holden MTG, Brown NM et al. Whole-genome sequencing for analysis of an outbreak of meticillin-resistant Staphylococcus aureus: a descriptive study. Lancet Infect Dis 2013; 13:130–136 [View Article] [PubMed]
    [Google Scholar]
  29. Reuter S, Ellington MJ, Cartwright EJP, Köser CU, Török ME et al. Rapid bacterial whole-genome sequencing to enhance diagnostic and public health microbiology. JAMA Intern Med 2013; 173:1397–1404 [View Article] [PubMed]
    [Google Scholar]
  30. Okeke IN, Feasey N, Parkhill J, Turner P, Limmathurotsakul D et al. Leapfrogging laboratories: the promise and pitfalls of high-tech solutions for antimicrobial resistance surveillance in low-income settings. BMJ Glob Health 2020; 5:e003622 [View Article] [PubMed]
    [Google Scholar]
  31. Grant K, Jenkins C, Arnold C, Green J, Zambon M. Implementing Pathogen Genomics: A case study Public Health England; 2018 p 32
    [Google Scholar]
  32. Kapatai G, Sheppard CL, Al-Shahib A, Litt DJ, Underwood AP et al. Whole genome sequencing of Streptococcus pneumoniae: development, evaluation and verification of targets for serogroup and serotype prediction using an automated pipeline. PeerJ 2016; 4:e2477 [View Article] [PubMed]
    [Google Scholar]
  33. Ndlangisa KM, du Plessis M, Lo S, de Gouveia L, Chaguza C et al. A Streptococcus pneumoniae lineage usually associated with pneumococcal conjugate vaccine (PCV) serotypes is the most common cause of serotype 35B invasive disease in South Africa, following routine use of PCV. Microb Genom 2022; 8: [View Article] [PubMed]
    [Google Scholar]
  34. Nouws S, Bogaerts B, Verhaegen B, Denayer S, Crombé F et al. The benefits of whole genome sequencing for foodborne outbreak investigation from the perspective of a National Reference Laboratory in a smaller country. Foods 2020; 9:1030 [View Article] [PubMed]
    [Google Scholar]
  35. WHO GLASS whole-genome sequencing for surveillance of antimicrobial resistance 2020a
    [Google Scholar]
  36. Afolayan AO, Oaikhena AO, Aboderin AO, Olabisi OF, Amupitan AA et al. Clones and clusters of antimicrobial-resistant Klebsiella from Southwestern Nigeria. Clin Infect Dis 2021b; 73:S308–S315 [View Article] [PubMed]
    [Google Scholar]
  37. Stachel A, Pinto G, Stelling J, Fulmer Y, Shopsin B et al. Implementation and evaluation of an automated surveillance system to detect hospital outbreak. Am J Infect Control 2017; 45:1372–1377 [View Article] [PubMed]
    [Google Scholar]
  38. Odih EE, Irek EO, Obadare TO, Oaikhena AO, Afolayan AO et al. Rectal colonization and nosocomial transmission of carbapenem-resistant Acinetobacter baumannii in an intensive care unit, Southwest Nigeria. Front Med (Lausanne) 2022; 9:846051 [View Article] [PubMed]
    [Google Scholar]
  39. NCDC: Nigeria Centre for Disease Control, Federal Ministry of Health The Nigerian manual of infection prevention and control Abuja, Nigeria: NCDC; 2021 p 284
    [Google Scholar]
  40. Zocher U, Dan-Nwafor C, Yahya D, Ita OI, Kloth S et al. Participatory approach to quality development in infection prevention and control (IPC) in Nigerian health facilities. Infect Prev Pract 2019; 1:100012 [View Article] [PubMed]
    [Google Scholar]
  41. Ekeng E, Tchatchouang S, Akenji B, Issaka BB, Akintayo I et al. Regional sequencing collaboration reveals persistence of the T12 Vibrio cholerae O1 lineage in West Africa. Elife 2021; 10:e65159 [View Article] [PubMed]
    [Google Scholar]
  42. Kwambana-Adams BA, Amaza RC, Okoi C, Rabiu M, Worwui A et al. Meningococcus serogroup C clonal complex ST-10217 outbreak in Zamfara State, Northern Nigeria. Sci Rep 2018; 8:14194 [View Article] [PubMed]
    [Google Scholar]
  43. International Typhoid C, Wong VK, Holt KE, Okoro C, Baker S et al. Molecular surveillance identifies multiple transmissions of typhoid in West Africa. PLoS Negl Trop Dis 2016; 10:e0004781 [View Article] [PubMed]
    [Google Scholar]
  44. Park SE, Pham DT, Boinett C, Wong VK, Pak GD et al. The phylogeography and incidence of multi-drug resistant typhoid fever in sub-Saharan Africa. Nat Commun 2018; 9:5094 [View Article] [PubMed]
    [Google Scholar]
  45. Ikhimiukor OO, Oaikhena AO, Afolayan AO, Fadeyi A, Kehinde A et al. n.d Genomic characterization of invasive typhoidal and non-typhoidal Salmonella in southwestern Nigeria. PLoS Negl Trop Dis [View Article]
    [Google Scholar]
  46. Choi M, Hegerle N, Nkeze J, Sen S, Jamindar S et al. The diversity of Lipopolysaccharide (O) and Capsular Polysaccharide (K) antigens of invasive Klebsiella pneumoniae in a multi-country collection. Front Microbiol 2020; 11:1249 [View Article] [PubMed]
    [Google Scholar]
  47. Adetifa IMO, Antonio M, Okoromah CAN, Ebruke C, Inem V et al. Pre-vaccination nasopharyngeal pneumococcal carriage in a Nigerian population: epidemiology and population biology. PLoS One 2012; 7:e30548 [View Article] [PubMed]
    [Google Scholar]
  48. Abrudan M, Matimba A, Nikolic D, Hughes D, Argimón S et al. Train-the-trainer as an effective approach to building global networks of experts in genomic surveillance of antimicrobial resistance (AMR). Clin Infect Dis 2021; 73:S283–S289 [View Article]
    [Google Scholar]
  49. Okeke IN. Dreams and dream spaces of West African molecular microbiology. Africa 2020; 90:167–187 [View Article]
    [Google Scholar]
  50. O’Brien TF, Stelling JM. WHONET: an information system for monitoring antimicrobial resistance. Emerg Infect Dis 1995; 1:66 [View Article] [PubMed]
    [Google Scholar]
  51. O’Brien TF, Clark A, Peters R, Stelling J. Why surveillance of antimicrobial resistance needs to be automated and comprehensive. J Glob Antimicrob Resist 2019; 17:8–15 [View Article] [PubMed]
    [Google Scholar]
  52. Turner P, Rupali P, Opintan JA, Jaoko W, Feasey NA et al. Laboratory informatics capacity for effective antimicrobial resistance surveillance in resource-limited settings. Lancet Infect Dis 2021; 21:e170–e174 [View Article] [PubMed]
    [Google Scholar]
  53. Feagins AR, Vuong J, Fernandez K, Njanpop-Lafourcade BM, Mwenda JM et al. The strengthening of laboratory systems in the meningitis belt to improve meningitis surveillance, 2008-2018: a partners’ perspective. J Infect Dis 2019; 220:S175–S181 [View Article] [PubMed]
    [Google Scholar]
  54. Gandra S, Alvarez-Uria G, Turner P, Joshi J, Limmathurotsakul D et al. Antimicrobial resistance surveillance in low- and middle-income countries: progress and challenges in eight South Asian and Southeast Asian countries. Clin Microbiol Rev 2020; 33:e00048–00019 [View Article] [PubMed]
    [Google Scholar]
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