Abstract

Targeted vector control strategies aiming to prevent mosquito borne disease are severely limited by the logistical burden of vector surveillance, the monitoring of an area to understand mosquito species composition, abundance and spatial distribution. We describe development of an imaging system within a mosquito trap to remotely identify caught mosquitoes, including selection of the image resolution requirement, a design to meet that specification, and evaluation of the system. The necessary trap image resolution was determined to be 16 lp/mm, or 31.25um. An optics system meeting these specifications was implemented in a BG-GAT mosquito trap. Its ability to provide images suitable for accurate specimen identification was evaluated by providing entomologists with images of individual specimens, taken either with a microscope or within the trap and asking them to provide a species identification, then comparing these results. No difference in identification accuracy between the microscope and the trap images was found; however, due to limitations of human species classification from a single image, the system is only able to provide accurate genus-level mosquito classification. Further integration of this system with machine learning computer vision algorithms has the potential to provide near-real time mosquito surveillance data at the species level.

© 2020 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref]

2019 (3)

A. B. B. Wilke, A. Carvajal, J. Medina, M. Anderson, V. J. Nieves, M. Ramirez, C. Vasquez, W. Petrie, G. Cardenas, and J. C. Beier, “Assessment of the effectiveness of BG-Sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in Miami-Dade County, Florida,” PLoS One 14(2), e0212688 (2019).
[Crossref]

K. Okayasu, K. Yoshida, M. Fuchida, and A. Nakamura, “Vision-Based Classification of Mosquito Species: Comparison of Conventional and Deep Learning Methods,” Appl. Sci. 9(18), 3935 (2019).
[Crossref]

D. Motta, AÁB Santos, I. Winkler, B. A. S. Machado, D. A. D. I. Pereira, A. M. Cavalcanti, E. O. L. Fonseca, F. Kirchner, and R. Badaró, “Application of convolutional neural networks for classification of adult mosquitoes in the field,” PLoS One 14(1), e0210829 (2019).
[Crossref]

2017 (1)

J. E. Cilek, J. R. Weston, and A. G. Richardson, “Comparison of Adult Mosquito Abundance From Biogents-2 Sentinel and Biogents Gravid Aedes Traps In Northeastern Florida,” J. Am. Mosq. Control Assoc. 33(4), 358–360 (2017).
[Crossref]

2016 (3)

K. L. Ebi and J. Nealon, “Dengue in a changing climate,” Environ. Res. 151, 115–123 (2016).
[Crossref]

Y. Shi, X. Liu, S. Y. Kok, J. Rajarethinam, S. Liang, G. Yap, C. S. Chong, K. S. Lee, S. S. Y. Tan, C. K. Y. Chin, A. Lo, W. Kong, L. C. Ng, and A. R. Cook, “Three-month real-time dengue forecast models: An early warning system for outbreak alerts and policy decision support in Singapore,” Environ. Health Perspect. 124(9), 1369–1375 (2016).
[Crossref]

E. Tambo, J. H. Chen, X. N. Zhou, and E. I. M. Khater, “Outwitting dengue threat and epidemics resurgence in Asia-Pacific countries: Strengthening integrated dengue surveillance, monitoring and response systems,” Infect. Dis. Poverty 5(1), 56 (2016).
[Crossref]

2015 (1)

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

2014 (1)

Á. E. Eiras, T. S. Buhagiar, and S. A. Ritchie, “Development of the Gravid Aedes Trap for the Capture of Adult Female Container-Exploiting Mosquitoes (Diptera: Culicidae),” J. Med. Entomol. 51(1), 200–209 (2014).
[Crossref]

2013 (1)

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

2011 (1)

M. S. Chang, E. M. Christophel, D. Gopinath, and R. M. Abdur, “Challenges and future perspective for dengue vector control in the Western Pacific Region,” West. Pac. Surveill. Response 2(2), e1 (2011).
[Crossref]

2010 (1)

L. Lambrechts, T. W. Scott, and D. J. Gubler, “Consequences of the expanding global distribution of aedes albopictus for dengue virus transmission,” PLoS Neglected Trop. Dis. 4(5), e646 (2010).
[Crossref]

2008 (2)

W. H. Meeraus, J. S. Armistead, and J. R. Arias, “Field Comparison of Novel and Gold Standard Traps for Collecting Aedes albopictus in Northern Virginia,” J. Am. Mosq. Control Assoc. 24(2), 244–248 (2008).
[Crossref]

L. C. Harrington and R. L. Poulson, “Considerations for Accurate Identification of Adult Culex Restuans (Diptera: Culicidae) in Field Studies,” J. Med. Entomol. 45(1), 1–8 (2008).
[Crossref]

2004 (1)

M. A. H. Braks, N. A. HonóRio, H. HonóRio, L. P. Lounibos, R. LourençO-De-Oliveira, and S. A. Juliano, “Interspecific Competition Between Two Invasive Species Of Container Mosquitoes, Aedes Aegypti And Aedes Albopictus (Diptera: Culicidae), In Brazil,” Ann. Entomol. Soc. Am. 97(1), 1–5 (2004).
[Crossref]

Abdur, R. M.

M. S. Chang, E. M. Christophel, D. Gopinath, and R. M. Abdur, “Challenges and future perspective for dengue vector control in the Western Pacific Region,” West. Pac. Surveill. Response 2(2), e1 (2011).
[Crossref]

Anderson, M.

A. B. B. Wilke, A. Carvajal, J. Medina, M. Anderson, V. J. Nieves, M. Ramirez, C. Vasquez, W. Petrie, G. Cardenas, and J. C. Beier, “Assessment of the effectiveness of BG-Sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in Miami-Dade County, Florida,” PLoS One 14(2), e0212688 (2019).
[Crossref]

Arias, J. R.

W. H. Meeraus, J. S. Armistead, and J. R. Arias, “Field Comparison of Novel and Gold Standard Traps for Collecting Aedes albopictus in Northern Virginia,” J. Am. Mosq. Control Assoc. 24(2), 244–248 (2008).
[Crossref]

Armistead, J. S.

W. H. Meeraus, J. S. Armistead, and J. R. Arias, “Field Comparison of Novel and Gold Standard Traps for Collecting Aedes albopictus in Northern Virginia,” J. Am. Mosq. Control Assoc. 24(2), 244–248 (2008).
[Crossref]

Badaró, R.

D. Motta, AÁB Santos, I. Winkler, B. A. S. Machado, D. A. D. I. Pereira, A. M. Cavalcanti, E. O. L. Fonseca, F. Kirchner, and R. Badaró, “Application of convolutional neural networks for classification of adult mosquitoes in the field,” PLoS One 14(1), e0210829 (2019).
[Crossref]

Barker, C. M.

C. M. Barker, J. M. Conlon, C. R. Connelly, M. Debboun, E. Dormuth, K. K. Fujioka, G. V. Mosquito, K. Smith, and G. B. White, Best Practices For Mosquito Control 2017: A Focused Update (American Mosquito Control Association, 2017).

Beier, J. C.

A. B. B. Wilke, A. Carvajal, J. Medina, M. Anderson, V. J. Nieves, M. Ramirez, C. Vasquez, W. Petrie, G. Cardenas, and J. C. Beier, “Assessment of the effectiveness of BG-Sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in Miami-Dade County, Florida,” PLoS One 14(2), e0212688 (2019).
[Crossref]

Bhatt, S.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Boldt, H. L.

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

Brady, O. J.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Braks, M. A. H.

M. A. H. Braks, N. A. HonóRio, H. HonóRio, L. P. Lounibos, R. LourençO-De-Oliveira, and S. A. Juliano, “Interspecific Competition Between Two Invasive Species Of Container Mosquitoes, Aedes Aegypti And Aedes Albopictus (Diptera: Culicidae), In Brazil,” Ann. Entomol. Soc. Am. 97(1), 1–5 (2004).
[Crossref]

Brownstein, J. S.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Buhagiar, T. S.

Á. E. Eiras, T. S. Buhagiar, and S. A. Ritchie, “Development of the Gravid Aedes Trap for the Capture of Adult Female Container-Exploiting Mosquitoes (Diptera: Culicidae),” J. Med. Entomol. 51(1), 200–209 (2014).
[Crossref]

Cardenas, G.

A. B. B. Wilke, A. Carvajal, J. Medina, M. Anderson, V. J. Nieves, M. Ramirez, C. Vasquez, W. Petrie, G. Cardenas, and J. C. Beier, “Assessment of the effectiveness of BG-Sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in Miami-Dade County, Florida,” PLoS One 14(2), e0212688 (2019).
[Crossref]

Carvajal, A.

A. B. B. Wilke, A. Carvajal, J. Medina, M. Anderson, V. J. Nieves, M. Ramirez, C. Vasquez, W. Petrie, G. Cardenas, and J. C. Beier, “Assessment of the effectiveness of BG-Sentinel traps baited with CO2 and BG-Lure for the surveillance of vector mosquitoes in Miami-Dade County, Florida,” PLoS One 14(2), e0212688 (2019).
[Crossref]

Cavalcanti, A. M.

D. Motta, AÁB Santos, I. Winkler, B. A. S. Machado, D. A. D. I. Pereira, A. M. Cavalcanti, E. O. L. Fonseca, F. Kirchner, and R. Badaró, “Application of convolutional neural networks for classification of adult mosquitoes in the field,” PLoS One 14(1), e0210829 (2019).
[Crossref]

Chanda, J.

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

Chang, M. S.

M. S. Chang, E. M. Christophel, D. Gopinath, and R. M. Abdur, “Challenges and future perspective for dengue vector control in the Western Pacific Region,” West. Pac. Surveill. Response 2(2), e1 (2011).
[Crossref]

Chen, J. H.

E. Tambo, J. H. Chen, X. N. Zhou, and E. I. M. Khater, “Outwitting dengue threat and epidemics resurgence in Asia-Pacific countries: Strengthening integrated dengue surveillance, monitoring and response systems,” Infect. Dis. Poverty 5(1), 56 (2016).
[Crossref]

Chin, C. K. Y.

Y. Shi, X. Liu, S. Y. Kok, J. Rajarethinam, S. Liang, G. Yap, C. S. Chong, K. S. Lee, S. S. Y. Tan, C. K. Y. Chin, A. Lo, W. Kong, L. C. Ng, and A. R. Cook, “Three-month real-time dengue forecast models: An early warning system for outbreak alerts and policy decision support in Singapore,” Environ. Health Perspect. 124(9), 1369–1375 (2016).
[Crossref]

Chinula, D.

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

Chong, C. S.

Y. Shi, X. Liu, S. Y. Kok, J. Rajarethinam, S. Liang, G. Yap, C. S. Chong, K. S. Lee, S. S. Y. Tan, C. K. Y. Chin, A. Lo, W. Kong, L. C. Ng, and A. R. Cook, “Three-month real-time dengue forecast models: An early warning system for outbreak alerts and policy decision support in Singapore,” Environ. Health Perspect. 124(9), 1369–1375 (2016).
[Crossref]

Christophel, E. M.

M. S. Chang, E. M. Christophel, D. Gopinath, and R. M. Abdur, “Challenges and future perspective for dengue vector control in the Western Pacific Region,” West. Pac. Surveill. Response 2(2), e1 (2011).
[Crossref]

Cilek, J. E.

J. E. Cilek, J. R. Weston, and A. G. Richardson, “Comparison of Adult Mosquito Abundance From Biogents-2 Sentinel and Biogents Gravid Aedes Traps In Northeastern Florida,” J. Am. Mosq. Control Assoc. 33(4), 358–360 (2017).
[Crossref]

Clark-Carter, D.

D. Clark-Carter, “z Scores,” in Wiley StatsRef: Statistics Reference Online (John Wiley & Sons, Ltd, 2014).

Collins, F. H.

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

Conlon, J. M.

C. M. Barker, J. M. Conlon, C. R. Connelly, M. Debboun, E. Dormuth, K. K. Fujioka, G. V. Mosquito, K. Smith, and G. B. White, Best Practices For Mosquito Control 2017: A Focused Update (American Mosquito Control Association, 2017).

Connelly, C. R.

C. M. Barker, J. M. Conlon, C. R. Connelly, M. Debboun, E. Dormuth, K. K. Fujioka, G. V. Mosquito, K. Smith, and G. B. White, Best Practices For Mosquito Control 2017: A Focused Update (American Mosquito Control Association, 2017).

Cook, A. R.

Y. Shi, X. Liu, S. Y. Kok, J. Rajarethinam, S. Liang, G. Yap, C. S. Chong, K. S. Lee, S. S. Y. Tan, C. K. Y. Chin, A. Lo, W. Kong, L. C. Ng, and A. R. Cook, “Three-month real-time dengue forecast models: An early warning system for outbreak alerts and policy decision support in Singapore,” Environ. Health Perspect. 124(9), 1369–1375 (2016).
[Crossref]

Deason, N. A.

N. F. Lobo, B. St. Laurent, C. H. Sikaala, B. Hamainza, J. Chanda, D. Chinula, S. M. Krishnankutty, J. D. Mueller, N. A. Deason, Q. T. Hoang, H. L. Boldt, J. Thumloup, J. Stevenson, A. Seyoum, and F. H. Collins, “Unexpected diversity of Anopheles species in Eastern Zambia: Implications for evaluating vector behavior and interventions using molecular tools,” Sci. Rep. 5(1), 17952 (2015).
[Crossref]

Debboun, M.

C. M. Barker, J. M. Conlon, C. R. Connelly, M. Debboun, E. Dormuth, K. K. Fujioka, G. V. Mosquito, K. Smith, and G. B. White, Best Practices For Mosquito Control 2017: A Focused Update (American Mosquito Control Association, 2017).

Dormuth, E.

C. M. Barker, J. M. Conlon, C. R. Connelly, M. Debboun, E. Dormuth, K. K. Fujioka, G. V. Mosquito, K. Smith, and G. B. White, Best Practices For Mosquito Control 2017: A Focused Update (American Mosquito Control Association, 2017).

Drake, J. M.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Ebi, K. L.

K. L. Ebi and J. Nealon, “Dengue in a changing climate,” Environ. Res. 151, 115–123 (2016).
[Crossref]

Eiras, Á. E.

Á. E. Eiras, T. S. Buhagiar, and S. A. Ritchie, “Development of the Gravid Aedes Trap for the Capture of Adult Female Container-Exploiting Mosquitoes (Diptera: Culicidae),” J. Med. Entomol. 51(1), 200–209 (2014).
[Crossref]

Farlow, A. W.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Farrar, J. J.

S. Bhatt, P. W. Gething, O. J. Brady, J. P. Messina, A. W. Farlow, C. L. Moyes, J. M. Drake, J. S. Brownstein, A. G. Hoen, O. Sankoh, M. F. Myers, D. B. George, T. Jaenisch, G. R. William Wint, C. P. Simmons, T. W. Scott, J. J. Farrar, and S. I. Hay, “The global distribution and burden of dengue,” Nature 496(7446), 504–507 (2013).
[Crossref]

Fonseca, E. O. L.

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Figures (7)

Fig. 1.
Fig. 1. The current workflow of vector surveillance involves (a) Mosquito specimens are caught using a variety of methods; (b) Entomologists morphologically identify mosquito specimens by species; and (c) Hundreds to thousands of mosquitoes are individually sorted under a microscope.
Fig. 2.
Fig. 2. Aedes aegypti and Aedes albopictus can be differentiated by examining the stripes on the dorsal view of the thorax (red arrows), and the spots on the lateral view of the thorax (red circle) [14]. Trained technicians and entomologists examine features like these to determine a mosquito’s species. Determining species informs mosquito control operations. (© 2019 Walter Reed Biosystematics Unit, Smithsonian Institute)
Fig. 3.
Fig. 3. The internal wall of the Gravid Aedes Trap (GAT) is partially cylindrical on the bottom-most part of the inside wall, and majority conical at 5°. A sticky paper is the mosquito capture mechanism for the GAT and is placed on this complex surface. This provides immobilization of mosquito specimens and a surface to image.
Fig. 4.
Fig. 4. The first method of determining the resolution requirement: direct measurement of features of interest on the specimen. The minimum distance between the three spots of primary interest on the Ae. aegypti specimen was determined (a, b, or c, depending on the specimen). The mean and standard deviation of four specimen measurements was used to determine a minimum feature size of 37.8 +- 4.0 µm.
Fig. 5.
Fig. 5. Camera placement given optical constraints. The curved geometry of the wall of the GAT places mosquitoes caught on the sticky paper at different distances from a camera in the trap, requiring the camera to have a large depth of field to include the full sticky paper at a similar resolution. The authors achieved this by placing the camera as far from the sticky paper within the trap as possible, as well as through lens selection. The bottom right image shows the locations within the field of view measured in subsequent testing.
Fig. 6.
Fig. 6. Modulation Transfer Function of the minimum and maximum resolution location of the top and bottom cameras. The minimum resolution in the field of view with a contrast of 10% was 14.73 lp/mm. The average throughout the field of view was 17.36 lp/mm, reaching the resolution requirement determined above in the majority of the field of view.
Fig. 7.
Fig. 7. Examples of paired images shown in the Resolution Verification Survey, where entomologists were shown first an image from our system in the trap and asked to identify the species, and then a microscope image of the same specimen and asked to identify the species.

Tables (3)

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Table 1. Entomologist identification capabilities at depreciating resolutions.

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Table 2. Resolution validation survey results genus and species classification abilities given microscope images and our trap system images. Three entomologists were tested on three species.

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Table 3. Discordance of entomologist mosquito classification abilities between trap images and microscope images.a

Equations (1)

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Contrast = 1 ( 2 × t c /( p 1  -  p 2 ) )

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