doi: 10.12688/gatesopenres.13061.2.
eCollection 2019.
Establishment of w Mel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia
Peter A Ryan
1
, Andrew P Turley
1
, Geoff Wilson
1
, Tim P Hurst
1
2
, Kate Retzki
1
, Jack Brown-Kenyon
1
, Lauren Hodgson
1
, Nichola Kenny
1
, Helen Cook
1
, Brian L Montgomery
1
3
, Christopher J Paton
4
, Scott A Ritchie
1
4
, Ary A Hoffmann
5
, Nicholas P Jewell
6
7
, Stephanie K Tanamas
1
, Katherine L Anders
1
, Cameron P Simmons
1
8
, Scott L O'Neill
1
Affiliations
- PMID: 31667465
- PMCID: PMC6801363
- DOI: 10.12688/gatesopenres.13061.2
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Establishment of w Mel Wolbachia in Aedes aegypti mosquitoes and reduction of local dengue transmission in Cairns and surrounding locations in northern Queensland, Australia
Peter A Ryan et al.
Gates Open Res.
.
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Abstract
Background: The wMel strain of Wolbachia has been successfully introduced into Aedes aegypti mosquitoes and subsequently shown in laboratory studies to reduce transmission of a range of viruses including dengue, Zika, chikungunya, yellow fever, and Mayaro viruses that cause human disease. Here we report the entomological and epidemiological outcomes of staged deployment of Wolbachia across nearly all significant dengue transmission risk areas in Australia. Methods: The wMel strain of Wolbachia was backcrossed into the local Aedes aegypti genotype (Cairns and Townsville backgrounds) and mosquitoes were released in the field by staff or via community assisted methods. Mosquito monitoring was undertaken and mosquitoes were screened for the presence of Wolbachia. Dengue case notifications were used to track dengue incidence in each location before and after releases. Results: Empirical analyses of the Wolbachia mosquito releases, including data on the density, frequency and duration of Wolbachia mosquito releases, indicate that Wolbachia can be readily established in local mosquito populations, using a variety of deployment options and over short release durations (mean release period 11 weeks, range 2-22 weeks). Importantly, Wolbachia frequencies have remained stable in mosquito populations since releases for up to 8 years. Analysis of dengue case notifications data demonstrates near-elimination of local dengue transmission for the past five years in locations where Wolbachia has been established. The regression model estimate of Wolbachia intervention effect from interrupted time series analyses of case notifications data prior to and after releases, indicated a 96% reduction in dengue incidence in Wolbachia treated populations (95% confidence interval: 84 - 99%). Conclusion: Deployment of the wMel strain of Wolbachia into local Ae. aegypti populations across the Australian regional cities of Cairns and most smaller regional communities with a past history of dengue has resulted in the reduction of local dengue transmission across all deployment areas.
Keywords: Aedes aegypti; Dengue; Eliminate Dengue; Wolbachia; World Mosquito Program; community engagement; mosquito release.
Copyright: © 2020 Ryan PA et al.
Conflict of interest statement
No competing interests were disclosed.
Figures
Cooya Beach (CB), Mossman (MO), Mossman Gorge (MG), Mossman North (MN), Port Douglas (PD) (
A) and Cairns (northern) release areas: Clifton Beach (CB), Holloways Beach (HB), Kewarra Beach (KWB), Machans Beach (MB), Palm Cove (PC), Trinity Beach (TRB), Trinity Park (TRP), Smithfield (SMF), Yorkeys Knob (YK) (
B).
Aeroglen (AER), Bayview Heights (BH), Bentley Park (BP), Brinsmead (BRN), Bungalow 1 (BU1), Bungalow 2 (BU2), Bungalow 3 (BU3), Bungalow Ext 1 (BUX1), Bungalow Ext 2 (BUX2), Bungalow Ext 3 (BUX3), Bungalow non-release area (BU NR), Cairns North 1 (CN1), Cairns North Ext (CNX), Earlville (EA), Edge Hill Ext (EHX), Edge Hill/Whitfield (EHW), Edmonton (EDM), Freshwater (FW), Kanimbla (KB), Manoora (MRA), Manoora Ext (MRAX), Manunda (MDA), Manunda non-release area 1 (MDA NR1), Manunda non-release area 2 (MDA NR2), Mooroobool (MOO), Mount Sheridan (MS), Mount Sheridan Ext (MSX), Parramatta Park (PP), Parramatta Park Ext (PPX), Portsmith (POR), Stratford 1 (SF1), Stratford 2 (SF2), Stratford 3 (SF3), Westcourt (WC), Westcourt non-release area (WC NR), Westcourt Ext 1 (WCX1), Westcourt Ext 2 (WCX2), White Rock (WR), White Rock Ext (WRX), Whitfield Ext (WFX), Woree (WO) (
A), Gordonvale (GV) release area and Pyramid Estate non-release area (PE) (
B); Babinda (BA) release area (
C), and Charters Towers (CT) release area (
D).
Belvedere (BEL), Innisfail (INN), Innisfail Estate (IES), Flying Fish Point (FFP), Innisfail East (IAE), Mundoo (MUN), Wagan (WAN), Mourilyan (MOU), South Johnstone (SJO) (
A) and Cassowary Coast – Tully release areas Bingal Bay (BBY), El Arish (ELA), North Mission Beach (NMB), Wongaling Beach (WGB), South Mission Beach (SMB), Tully (TUL) (
B).
Photos illustrating different mosquito release containers used in the deployment. Bucket mosquito release container (MRC) (
A) Single use Mozzie Box MRC (
B) (
O’Neill
et al., 2018).
Line represents median percentage infection rate across 62 individual release areas, box represents interquartile range, Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each area. (
A), Number of release and post-release areas monitored each week (
B).
Collections to week 17 from ovitraps, collections from BG Traps thereafter (
Wolbachia infected adult mosquito releases undertaken weekly for 10 weeks between Jan–Feb 2011, Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each location).
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Edge Hill/Whitfield (EHW), Parramatta Park (PP) and Westcourt (WC) (
A) and Babinda (BA) and Machans Beach (MB) (
B) during release (triangles) and post-release (circles) monitoring periods (
Wolbachia infected adult releases were undertaken weekly for 15–16 weeks between Jan–Apr 2013 in EHW, PP and WC;
Wolbachia infected adult and egg stage releases undertaken weekly for 9–11 weeks between Jul–Sep 2013 in BA and MB, Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each location).
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Stratford 1-3 (SF1-3) (
A) and Bungalow 1-3 (BU1-3) and Cairns North (CN) (
B) and during release (triangles) and post-release (circles) monitoring periods (
Wolbachia infected egg releases were undertaken weekly for 4, 16 and 19 weeks in SF1-3, respectively, from Jun–Nov 2014, and for 12 and 13 weeks in BU1 and BU3, respectively, from Aug–Oct 2014; BU2 had two rounds of egg releases – 8 weekly releases from Aug–Sep 2014, followed by 12 weekly releases from Oct–Dec 2015, Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each location).
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Manunda (MDA), Manoora (MRA), Mooroobool (MOO), Earlville (EA), Woree (WO) and Bungalow Ext 1 (BUX1) (
A), Westcourt Ext 1 (WCX1), Mount Sheridan (MS), White Rock (WR), Bungalow Ext 2 (BUX2) and Westcourt Ext 2 (WCX2) (
B) during release (triangles) and post-release (circles) monitoring periods (
Wolbachia infected egg releases were undertaken every 2 weeks for 9–15 weeks in MDA, MRA, MOO, EA, WO and BUX1 between May–Dec 2015, and for 6–13 weeks in WCX1, MS, WR, BUX2 and WCX2 between Sep–Dec 2015), Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each location).
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Bentley Park (BP), Edmonton (EDM), Bayview Heights (BH), Kanimbla (KB), Mount Sheridan Ext (MSX) and White Rock Ext (WRX) (
A), Brinsmead (BRN), Cairns North Ext (CNX), Edge Hill Ext (EHX), Manoora Ext (MRAX), Parramatta Park Ext (PPX) and Portsmith (POR) (
B), Whitfield Ext (WFX), Bungalow Ext 3 (BUX3), Aeroglen (AER), Holloways Beach (HB), Kewerra Beach (KWB) and Smithfield (SMF) (
C), Trinity Beach (TRB), Clifton Beach (CB), Freshwater (FW), Palm Cove (PC) and Trinity Park (TRP) (
D) during release (triangles) and post-release (circles) monitoring periods (
Wolbachia infected adult releases were undertaken every week for 9–11 weeks in BP, EDM, BH, KB, MSX and WRX between Nov 2016 and May 2017, for 3–9 weeks in BRN, CNX, EHX, MRAX, PPX and POR between Mar–May 2017, for 5–10 weeks in WFX, BUX3, AER, HB, KWB and SMF between Mar–Jul 2017, for 9–10 weeks in TRB, CB, FW, PC and TRP between May–Aug 2017), Week number 1 corresponds to commencement of
Wolbachia mosquito releases in each location).
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Belvedere (BEL), Flying Fish Point (FFP), Innisfail East (IAE), Innisfail Estate (IES), Mundoo (MUN) and Wangan (WAN) (
A) and Innisfail (INN), Mourilyan (MOU) and South Johnstone (SJO) (
B) during release (triangles) and post-release (circles) monitoring periods (
Wolbachia infected adult releases were undertaken in BEL, FFP, IAE, IES, MUN, WAN, INN, MOU and SJO every week for 14–16 weeks between Mar–Jun 2017, Week number 1 corresponds to commencement of
Wolbachia mosquito releases). In INN, MOU and SJO,
wAlbB infected male-only
Ae. aegypti mosquito releases were undertaken between weeks 41–66 in INN and SJO, and between weeks 39–66 in MOU. Shaded horizontal bars correspond to
wAlbB male release period. Estimation of weekly
wMel
Wolbachia mosquito infection rates excluded
wAlbB males from the calculation.
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from Pyramid Estate non-release area (PE NR) (
A), Bungalow non-release area (BUN NR) (
B), Manunda non-release area 1 (MDA NR1) (
C), Manunda non-release area 2 (MDA NR2) (
D) and Westcourt non-release area (WC NR) (
E) non-releases areas. Week number 1 corresponds to commencement of
Wolbachia mosquito monitoring in each non-release area (PE NR week 1 = 21/12/2012, BUN NR week 1 = 11/01/2013, MDA NR1 week 1 = 11/1/2013, MDA NR2 week 1 = 07/06/2013, WC NR week 1 = 11/01/2013). Grey lines show corresponding weekly
Wolbachia infection rates in
Aedes aegypti mosquitoes collected from adjacent release or non-release areas (areas described in
Figure 2 and
Table 1).
Notifications include laboratory-confirmed and probable dengue cases, classified as locally-acquired (
A,
C,
E,
G) or imported (
B,
D,
F,
H) based on a history of overseas travel to a dengue-affected country during the period 3 – 12 days prior to illness onset. Case location was determined from geolocated address information from the Cairns and Townsville public health unit operational databases, where available, otherwise from suburb in the NoCS case record.
The date of case onset is scaled relative to the date that local
Wolbachia releases were completed or, for the five central Cairns non-release areas where
Wolbachia established, the inferred date when local
Wolbachia frequency reached 80%. In the post-intervention period (blue shaded area), imported cases continue to occur (
B) but locally-acquired cases have been effectively eliminated (
A). The post-intervention case surveillance period is variable across the release areas, due to staggered releases from Jan 2011 to May 2017: the median post-intervention observation period is 24 months (IQR 21–41 months, range 17–96 months), as shown in the box plots. The x-axis is left-censored at 15 years pre-release (excludes 8 local cases and 5 imported cases occurring >15 years pre-release).
Notifications of locally-acquired (
A) and imported (
B) dengue cases relative to
Wolbachia deployments, in Cairns, Cassowary Coast, Charters Towers and Douglas local government areas, January 2000 – March 2019. Cases are plotted by date of illness onset, and by grouped intervention area determined from geolocated address, or from suburb where address was unavailable. Intervention areas were grouped by the calendar quarter in which releases were completed or, for the five central Cairns non-release areas where
Wolbachia established, the inferred date when local
Wolbachia frequency reached 80%. Cases located in the four LGAs, but outside of any
Wolbachia established area, are shown in ‘Untreated area’ at the top of each graph. The Y-axis scale is proportionate to the population size of each intervention area (or untreated area). The grouped intervention areas, and the quarter in which they were considered
Wolbachia-treated for epidemiological purposes, were as follows: Group 1: Q1 2011 (GV, YK); Group 2: Q2 2013 (EHW, PP, WC); Group 3: Q3 2013 (BA, MB); Group 4: Q4 2014 (BU1, BU3, CN1, SF1-3); Group 5: Q3 2015 (MDA, MRA, BUN NR, EA); Group 6: Q4 2015 (M BU2, BUX1, BUX2, MDA NR1, MDA NR2, MS, OO, WCX1, WCX2, WO, WR); Group 7: Q1 2016 (WC NR); Group 8: Q4 2016 (CB, CT, MG, MN, MO, PD); Group 9: Q1 2017 (BP, CNX, EDM); Group 10: Q2 2017 (BEL, BH, BRN, BUX3, EHX, FFP, IAE, IES, INN, KB, MOU, MRAX, MSX, MUN, POR, PPX, SJO, WAN, WFX, WRX); Group 11: Q3 2017 (AER, BBY, CB, ELA, HB, FW, KWB, NMB, PC, SMB, SMF, TRB, TRP, TUL, WGB); Group 12: Q4 2017 (PE).
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