Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways
ABSTRACT Tuberculosis (TB) originating from expatriates that hail from high TB-burden countries is hypothesized to play a role in continued TB transmission in Oman. Here, we used whole-genome sequencing (WGS) to assess national TB transmission dynamics. The annual incidence per 100,000 population pe...
| Main Authors: | , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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American Society for Microbiology
2023-10-01
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| Series: | Microbiology Spectrum |
| Subjects: | |
| Online Access: | https://journals.asm.org/doi/10.1128/spectrum.02420-23 |
| _version_ | 1827791982647312384 |
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| author | Hamza A Babiker Amina Al-Jardani Saleh Al-Azri Robert A. Petit Eltaib Saad Sarah Al-Mahrouqi Reham A.H. Mohamed Salama Al-Hamidhi Abdullah A. Balkhair Najma Al Kharusi Laila Al Balushi Samiya Al Zadjali Lucía Pérez-Pardal Albano Beja-Pereira Ahmed Babiker |
| author_facet | Hamza A Babiker Amina Al-Jardani Saleh Al-Azri Robert A. Petit Eltaib Saad Sarah Al-Mahrouqi Reham A.H. Mohamed Salama Al-Hamidhi Abdullah A. Balkhair Najma Al Kharusi Laila Al Balushi Samiya Al Zadjali Lucía Pérez-Pardal Albano Beja-Pereira Ahmed Babiker |
| author_sort | Hamza A Babiker |
| collection | DOAJ |
| description | ABSTRACT Tuberculosis (TB) originating from expatriates that hail from high TB-burden countries is hypothesized to play a role in continued TB transmission in Oman. Here, we used whole-genome sequencing (WGS) to assess national TB transmission dynamics. The annual incidence per 100,000 population per year was calculated for nationals and expatriates. A convenience sample of Mycobacterium tuberculosis (MTB) isolates from 2018 to 2019 was sequenced and analyzed with publicly available TB sequences from Bangladesh, Tanzania, the Philippines, India, and Pakistan. Relatedness was assessed by generating core-genome single nucleotide polymorphism (SNP) distances. The incidence of TB was five cases per 100,000 persons in 2018 and seven cases per 100,000 persons in 2020 (R2 = 0.34, P = 0.60). Incidence among nationals was 3.9 per 100,000 persons in 2018 and 3.5 per 100,000 persons in 2020 (R2 = 0.20, P = 0.70), and incidence among expatriates was 7.2 per 100,000 persons in 2018 and 12.7 per 100,000 persons in 2020 (R2 = 0.74, P = 0.34). Sixty-eight local MTB isolates were sequenced and analyzed with 393 global isolates. Isolates belonged to nine distinct spoligotypes. Two isolates, originating from an expatriate and an Omani national, were grouped into a WGS-based cluster (SNP distance < 12), which was corroborated by an epidemiological investigation. Relatedness of local and global isolates (SNP distance < 100) was also seen. The relatedness between MTB strains in Oman and those in expatriate countries of origin can aid inform TB control policy. Our results provide evidence that WGS can complement epidemiological analysis to achieve the End TB strategy goal in Oman. IMPORTANCE Tuberculosis (TB) incidence in Oman remains above national program control targets. TB transmission originating from expatriates from high TB-burden countries has been hypothesized to play a role. We used whole-genome sequencing (WGS) to assess TB transmission dynamics between expatriates and Omani nationals to inform TB control efforts. Available Mycobacterium tuberculosis isolates from 2018 to 2019 underwent WGS and analysis with publicly available TB sequences from Bangladesh, the Philippines, India, and Pakistan to assess for genetic relatedness. Our analysis revealed evidence of previously unrecognized transmission between an expatriate and an Omani national, which was corroborated by epidemiological investigation. Analysis of local and global isolates revealed evidence of distant relatedness between local and global isolates. Our results provide evidence that WGS can complement classic public health surveillance to inform targeted interventions to achieve the End TB strategy goal in Oman. |
| first_indexed | 2024-03-11T17:55:48Z |
| format | Article |
| id | doaj.art-1f27bac5c4884591850f46f9664053a0 |
| institution | Directory Open Access Journal |
| issn | 2165-0497 |
| language | English |
| last_indexed | 2024-03-11T17:55:48Z |
| publishDate | 2023-10-01 |
| publisher | American Society for Microbiology |
| record_format | Article |
| series | Microbiology Spectrum |
| spelling | doaj.art-1f27bac5c4884591850f46f9664053a02023-10-17T13:04:35ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972023-10-0111510.1128/spectrum.02420-23Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathwaysHamza A Babiker0Amina Al-Jardani1Saleh Al-Azri2Robert A. Petit3Eltaib Saad4Sarah Al-Mahrouqi5Reham A.H. Mohamed6Salama Al-Hamidhi7Abdullah A. Balkhair8Najma Al Kharusi9Laila Al Balushi10Samiya Al Zadjali11Lucía Pérez-Pardal12Albano Beja-Pereira13Ahmed Babiker14Biochemistry Department, College of Medicine and Health Sciences, Sultan Qaboos University , Muscat, OmanCentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanCentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanWyoming Department of Health, Wyoming Public Health Laboratory , Cheyenne, Wyoming, USADepartment of Medicine, Ascension Saint Francis Hospital , Evanston, Illinois, USACentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanBiochemistry Department, College of Medicine and Health Sciences, Sultan Qaboos University , Muscat, OmanBiochemistry Department, College of Medicine and Health Sciences, Sultan Qaboos University , Muscat, OmanDepartment of Medicine, College of Medicine and Health Sciences, Sultan Qaboos University , Muscat, OmanCentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanCentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanCentral Public Health Laboratories, National Tuberculosis Reference Laboratory, Directorate General for Disease Surveillance and Control, Ministry of Health , Muscat, OmanCIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Labora tório Associado, Campus de Vairão, Universidade do Porto, Vairão, Portugal , Vairão, PortugalCIBIO, Centro de Investigação em Biodiversidade e Recursos Genéticos, InBIO Labora tório Associado, Campus de Vairão, Universidade do Porto, Vairão, Portugal , Vairão, PortugalDivision of Infectious Diseases, Department of Medicine, Emory University School of Medicine , Atlanta, Georgia, USAABSTRACT Tuberculosis (TB) originating from expatriates that hail from high TB-burden countries is hypothesized to play a role in continued TB transmission in Oman. Here, we used whole-genome sequencing (WGS) to assess national TB transmission dynamics. The annual incidence per 100,000 population per year was calculated for nationals and expatriates. A convenience sample of Mycobacterium tuberculosis (MTB) isolates from 2018 to 2019 was sequenced and analyzed with publicly available TB sequences from Bangladesh, Tanzania, the Philippines, India, and Pakistan. Relatedness was assessed by generating core-genome single nucleotide polymorphism (SNP) distances. The incidence of TB was five cases per 100,000 persons in 2018 and seven cases per 100,000 persons in 2020 (R2 = 0.34, P = 0.60). Incidence among nationals was 3.9 per 100,000 persons in 2018 and 3.5 per 100,000 persons in 2020 (R2 = 0.20, P = 0.70), and incidence among expatriates was 7.2 per 100,000 persons in 2018 and 12.7 per 100,000 persons in 2020 (R2 = 0.74, P = 0.34). Sixty-eight local MTB isolates were sequenced and analyzed with 393 global isolates. Isolates belonged to nine distinct spoligotypes. Two isolates, originating from an expatriate and an Omani national, were grouped into a WGS-based cluster (SNP distance < 12), which was corroborated by an epidemiological investigation. Relatedness of local and global isolates (SNP distance < 100) was also seen. The relatedness between MTB strains in Oman and those in expatriate countries of origin can aid inform TB control policy. Our results provide evidence that WGS can complement epidemiological analysis to achieve the End TB strategy goal in Oman. IMPORTANCE Tuberculosis (TB) incidence in Oman remains above national program control targets. TB transmission originating from expatriates from high TB-burden countries has been hypothesized to play a role. We used whole-genome sequencing (WGS) to assess TB transmission dynamics between expatriates and Omani nationals to inform TB control efforts. Available Mycobacterium tuberculosis isolates from 2018 to 2019 underwent WGS and analysis with publicly available TB sequences from Bangladesh, the Philippines, India, and Pakistan to assess for genetic relatedness. Our analysis revealed evidence of previously unrecognized transmission between an expatriate and an Omani national, which was corroborated by epidemiological investigation. Analysis of local and global isolates revealed evidence of distant relatedness between local and global isolates. Our results provide evidence that WGS can complement classic public health surveillance to inform targeted interventions to achieve the End TB strategy goal in Oman.https://journals.asm.org/doi/10.1128/spectrum.02420-23Mycobacterium tuberculosismolecular phylogeographyphylogenyOman |
| spellingShingle | Hamza A Babiker Amina Al-Jardani Saleh Al-Azri Robert A. Petit Eltaib Saad Sarah Al-Mahrouqi Reham A.H. Mohamed Salama Al-Hamidhi Abdullah A. Balkhair Najma Al Kharusi Laila Al Balushi Samiya Al Zadjali Lucía Pérez-Pardal Albano Beja-Pereira Ahmed Babiker Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways Microbiology Spectrum Mycobacterium tuberculosis molecular phylogeography phylogeny Oman |
| title | Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways |
| title_full | Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways |
| title_fullStr | Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways |
| title_full_unstemmed | Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways |
| title_short | Mycobacterium tuberculosis epidemiology in Oman: whole-genome sequencing uncovers transmission pathways |
| title_sort | mycobacterium tuberculosis epidemiology in oman whole genome sequencing uncovers transmission pathways |
| topic | Mycobacterium tuberculosis molecular phylogeography phylogeny Oman |
| url | https://journals.asm.org/doi/10.1128/spectrum.02420-23 |
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