Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study

Ella M. Meumann; Kristy Horan; Anna P. Ralph; Belinda Farmer; Maria Globan; Elizabeth Stephenson; Tracy Popple; Rowena Boyd; Mirjam Kaestli; Torsten Seemann; Koen Vandelannoote; Christopher Lowbridge; Robert W. Baird; Timothy P. Stinear; Deborah A. Williamson; Bart J. Currie; Vicki L. Krause

doi:10.1016/j.lanwpc.2021.100229

Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study

Ella M. Meumann, Kristy Horan, Anna P. Ralph, Belinda Farmer, Maria Globan, Elizabeth Stephenson, Tracy Popple, Rowena Boyd, Mirjam Kaestli, Torsten Seemann, Koen Vandelannoote, Christopher Lowbridge, Robert W. Baird, Timothy P. Stinear, Deborah A. Williamson, Bart J. Currie, Vicki L. Krause

Global and Tropical Health

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Abstract

Background: The Northern Territory (NT) has the highest tuberculosis (TB) rate of all Australian jurisdictions. We combined TB public health surveillance data with genomic sequencing of Mycobacterium tuberculosis isolates in the tropical ‘Top End’ of the NT to investigate trends in TB incidence and transmission.

Methods: This retrospective observational study included all 741 culture-confirmed cases of TB in the Top End over three decades from 1989–2020. All 497 available M. tuberculosis isolates were sequenced. We used contact tracing data to define a threshold pairwise SNP distance for hierarchical single linkage clustering, and examined putative transmission clusters in the context of epidemiologic information.

Findings: There were 359 (48%) cases born overseas, 329 (44%) cases among Australian First Nations peoples, and 52 (7%) cases were Australian-born and non-Indigenous. The annual incidence in First Nations peoples from 1989-2019 fell from average 50.4 to 11.0 per 100,000 (P<0·001). First Nations cases were more likely to die from TB (41/329, 12·5%) than overseas-born cases (11/359, 3·1%; P<0·001). Using a threshold of ≤12 SNPs, 28 clusters of between 2–64 individuals were identified, totalling 250 cases; 214 (86%) were First Nations cases and 189 (76%) were from a remote region. The time between cases and past epidemiologically- and genomically-linked contacts ranged from 4·5 months to 24 years.

Interpretation: Our findings support prioritisation of timely case detection, contact tracing augmented by genomic sequencing, and latent TB treatment to break transmission chains in Top End remote hotspot regions.

Original language	English
Article number	100229
Pages (from-to)	1-11
Number of pages	11
Journal	The Lancet Regional Health - Western Pacific
Volume	15
Early online date	Jul 2021
DOIs	https://doi.org/10.1016/j.lanwpc.2021.100229
Publication status	Published - Oct 2021

Bibliographical note

Funding Information:
This research was funded under the Australian National Health and Medical Research Council (NHMRC) grant number 1131932 (The HOT NORTH initiative), a NHMRC postgraduate scholarship to Ella Meumann (1114696), NHMRC investigator grants to Deborah Williamson (GNT1174555) and Timothy Stinear (GNT1194325), and a NHMRC fellowship to Anna Ralph (1142011). The funding source had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the paper for publication

Publisher Copyright:
© 2021 The Authors

Copyright:
Copyright 2021 Elsevier B.V., All rights reserved.

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10.1016/j.lanwpc.2021.100229

44858048-oaFinal published version, 1.89 MBLicence: CC BY-NC-ND
PIIS2666606521001383 (1)E-pub ahead of print, 1.88 MBLicence: CC BY-NC-ND

Cite this

Meumann, E. M., Horan, K., Ralph, A. P., Farmer, B., Globan, M., Stephenson, E., Popple, T., Boyd, R., Kaestli, M., Seemann, T., Vandelannoote, K., Lowbridge, C., Baird, R. W., Stinear, T. P., Williamson, D. A., Currie, B. J., & Krause, V. L. (2021). Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study. The Lancet Regional Health - Western Pacific, 15, 1-11. Article 100229. https://doi.org/10.1016/j.lanwpc.2021.100229

@article{adbbe9d67a8347ac8ee215a9b088eba7,

title = "Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study",

abstract = "Background: The Northern Territory (NT) has the highest tuberculosis (TB) rate of all Australian jurisdictions. We combined TB public health surveillance data with genomic sequencing of Mycobacterium tuberculosis isolates in the tropical {\textquoteleft}Top End{\textquoteright} of the NT to investigate trends in TB incidence and transmission. Methods: This retrospective observational study included all 741 culture-confirmed cases of TB in the Top End over three decades from 1989–2020. All 497 available M. tuberculosis isolates were sequenced. We used contact tracing data to define a threshold pairwise SNP distance for hierarchical single linkage clustering, and examined putative transmission clusters in the context of epidemiologic information. Findings: There were 359 (48%) cases born overseas, 329 (44%) cases among Australian First Nations peoples, and 52 (7%) cases were Australian-born and non-Indigenous. The annual incidence in First Nations peoples from 1989-2019 fell from average 50.4 to 11.0 per 100,000 (P<0·001). First Nations cases were more likely to die from TB (41/329, 12·5%) than overseas-born cases (11/359, 3·1%; P<0·001). Using a threshold of ≤12 SNPs, 28 clusters of between 2–64 individuals were identified, totalling 250 cases; 214 (86%) were First Nations cases and 189 (76%) were from a remote region. The time between cases and past epidemiologically- and genomically-linked contacts ranged from 4·5 months to 24 years. Interpretation: Our findings support prioritisation of timely case detection, contact tracing augmented by genomic sequencing, and latent TB treatment to break transmission chains in Top End remote hotspot regions.",

author = "Meumann, {Ella M.} and Kristy Horan and Ralph, {Anna P.} and Belinda Farmer and Maria Globan and Elizabeth Stephenson and Tracy Popple and Rowena Boyd and Mirjam Kaestli and Torsten Seemann and Koen Vandelannoote and Christopher Lowbridge and Baird, {Robert W.} and Stinear, {Timothy P.} and Williamson, {Deborah A.} and Currie, {Bart J.} and Krause, {Vicki L.}",

note = "Funding Information: This research was funded under the Australian National Health and Medical Research Council (NHMRC) grant number 1131932 (The HOT NORTH initiative), a NHMRC postgraduate scholarship to Ella Meumann (1114696), NHMRC investigator grants to Deborah Williamson (GNT1174555) and Timothy Stinear (GNT1194325), and a NHMRC fellowship to Anna Ralph (1142011). The funding source had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the paper for publication Publisher Copyright: {\textcopyright} 2021 The Authors Copyright: Copyright 2021 Elsevier B.V., All rights reserved.",

year = "2021",

month = oct,

doi = "10.1016/j.lanwpc.2021.100229",

language = "English",

volume = "15",

pages = "1--11",

journal = "The Lancet Regional Health - Western Pacific",

issn = "2666-6065",

publisher = "Elsevier",

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Meumann, EM, Horan, K, Ralph, AP, Farmer, B, Globan, M, Stephenson, E, Popple, T, Boyd, R, Kaestli, M, Seemann, T, Vandelannoote, K, Lowbridge, C, Baird, RW, Stinear, TP, Williamson, DA, Currie, BJ & Krause, VL 2021, 'Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study', The Lancet Regional Health - Western Pacific, vol. 15, 100229, pp. 1-11. https://doi.org/10.1016/j.lanwpc.2021.100229

TY - JOUR

T1 - Tuberculosis in Australia's tropical north

T2 - A population-based genomic epidemiological study

AU - Meumann, Ella M.

AU - Horan, Kristy

AU - Ralph, Anna P.

AU - Farmer, Belinda

AU - Globan, Maria

AU - Stephenson, Elizabeth

AU - Popple, Tracy

AU - Boyd, Rowena

AU - Kaestli, Mirjam

AU - Seemann, Torsten

AU - Vandelannoote, Koen

AU - Lowbridge, Christopher

AU - Baird, Robert W.

AU - Stinear, Timothy P.

AU - Williamson, Deborah A.

AU - Currie, Bart J.

AU - Krause, Vicki L.

N1 - Funding Information: This research was funded under the Australian National Health and Medical Research Council (NHMRC) grant number 1131932 (The HOT NORTH initiative), a NHMRC postgraduate scholarship to Ella Meumann (1114696), NHMRC investigator grants to Deborah Williamson (GNT1174555) and Timothy Stinear (GNT1194325), and a NHMRC fellowship to Anna Ralph (1142011). The funding source had no role in study design; in the collection, analysis, and interpretation of data; in the writing of the report; or in the decision to submit the paper for publication Publisher Copyright: © 2021 The Authors Copyright: Copyright 2021 Elsevier B.V., All rights reserved.

PY - 2021/10

Y1 - 2021/10

N2 - Background: The Northern Territory (NT) has the highest tuberculosis (TB) rate of all Australian jurisdictions. We combined TB public health surveillance data with genomic sequencing of Mycobacterium tuberculosis isolates in the tropical ‘Top End’ of the NT to investigate trends in TB incidence and transmission. Methods: This retrospective observational study included all 741 culture-confirmed cases of TB in the Top End over three decades from 1989–2020. All 497 available M. tuberculosis isolates were sequenced. We used contact tracing data to define a threshold pairwise SNP distance for hierarchical single linkage clustering, and examined putative transmission clusters in the context of epidemiologic information. Findings: There were 359 (48%) cases born overseas, 329 (44%) cases among Australian First Nations peoples, and 52 (7%) cases were Australian-born and non-Indigenous. The annual incidence in First Nations peoples from 1989-2019 fell from average 50.4 to 11.0 per 100,000 (P<0·001). First Nations cases were more likely to die from TB (41/329, 12·5%) than overseas-born cases (11/359, 3·1%; P<0·001). Using a threshold of ≤12 SNPs, 28 clusters of between 2–64 individuals were identified, totalling 250 cases; 214 (86%) were First Nations cases and 189 (76%) were from a remote region. The time between cases and past epidemiologically- and genomically-linked contacts ranged from 4·5 months to 24 years. Interpretation: Our findings support prioritisation of timely case detection, contact tracing augmented by genomic sequencing, and latent TB treatment to break transmission chains in Top End remote hotspot regions.

AB - Background: The Northern Territory (NT) has the highest tuberculosis (TB) rate of all Australian jurisdictions. We combined TB public health surveillance data with genomic sequencing of Mycobacterium tuberculosis isolates in the tropical ‘Top End’ of the NT to investigate trends in TB incidence and transmission. Methods: This retrospective observational study included all 741 culture-confirmed cases of TB in the Top End over three decades from 1989–2020. All 497 available M. tuberculosis isolates were sequenced. We used contact tracing data to define a threshold pairwise SNP distance for hierarchical single linkage clustering, and examined putative transmission clusters in the context of epidemiologic information. Findings: There were 359 (48%) cases born overseas, 329 (44%) cases among Australian First Nations peoples, and 52 (7%) cases were Australian-born and non-Indigenous. The annual incidence in First Nations peoples from 1989-2019 fell from average 50.4 to 11.0 per 100,000 (P<0·001). First Nations cases were more likely to die from TB (41/329, 12·5%) than overseas-born cases (11/359, 3·1%; P<0·001). Using a threshold of ≤12 SNPs, 28 clusters of between 2–64 individuals were identified, totalling 250 cases; 214 (86%) were First Nations cases and 189 (76%) were from a remote region. The time between cases and past epidemiologically- and genomically-linked contacts ranged from 4·5 months to 24 years. Interpretation: Our findings support prioritisation of timely case detection, contact tracing augmented by genomic sequencing, and latent TB treatment to break transmission chains in Top End remote hotspot regions.

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U2 - 10.1016/j.lanwpc.2021.100229

DO - 10.1016/j.lanwpc.2021.100229

M3 - Article

C2 - 34528010

AN - SCOPUS:85111484024

SN - 2666-6065

VL - 15

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JO - The Lancet Regional Health - Western Pacific

JF - The Lancet Regional Health - Western Pacific

M1 - 100229

ER -

Tuberculosis in Australia's tropical north: A population-based genomic epidemiological study

Abstract

Bibliographical note

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