Presence and Abundance of Malaria Vector Species in Miami-Dade County, Florida

doi:10.21203/rs.3.rs-3345274/v1

Download PDF

Research Article

Presence and Abundance of Malaria Vector Species in Miami-Dade County, Florida

https://doi.org/10.21203/rs.3.rs-3345274/v1

This work is licensed under a CC BY 4.0 License

Version 1

posted

You are reading this latest preprint version

Malaria outbreaks have sporadically occurred in the United States, with Anopheles quadrimaculatus serving as the primary vector in the eastern region. Anopheles crucians, while considered a competent vector, have not been directly implicated in human transmission. Considering the locally acquired Plasmodium vivax cases in Sarasota County, Florida (7 confirmed cases) and Cameron County, Texas (one confirmed case) in the summer of 2023, we hypothesized that other major urban areas in the United States harbor conducive conditions for local malaria transmission. Thus, our objective is to profile the most abundant Anopheles vector species in Miami-Dade, Florida – An. crucians and An. quadrimaculatus. We analyzed high-resolution mosquito surveillance data from 2020 to 2022 in Miami-Dade County, Florida. A total of 36,589 An. crucians and 9,943 An. quadrimaculatus were collected during this study by the surveillance system (which comprises 322 CO₂-based traps). Our findings reveal a highly heterogeneous distribution of An. crucians and An. quadrimaculatus in Miami-Dade County, highlighting the presence of highly conducive environments in transition zones between natural/rural and urban areas. Anopheles quadrimaculatus, and to a lesser extent An. crucians, pose a considerable risk of malaria transmission during an outbreak, given their high abundance and close proximity to humans. Understanding the factors driving Anopheles vector species' proliferation, population dynamics, and spatial distribution is vital for implementing effective mosquito control and reducing the risk of malaria outbreaks in the United States.

Anopheles

Anopheles crucians

Anopheles quadrimaculatus

Epidemiology

Plasmodium

Malaria is an infectious disease caused by Plasmodium parasites. There are five known species of Plasmodium that cause malaria in humans, P. falciparum, P. vivax, P. ovale, P. malariae, and P. knowlesi [1]. Plasmodium parasites are primarily transmitted to humans through the bites of infected female Anopheles mosquitoes (Diptera: Culicidae). Malaria continues to pose a significant public health challenge, particularly in tropical and subtropical regions of Africa, Asia, and South America [2–6]. Africa is the most affected region concentrating most cases and deaths [7]. Although effective drugs are available [8, 9], the gold standard for preventing malaria transmission remains the control of Anopheles mosquitoes [10, 11].

Sporadic malaria outbreaks have been reported in the United States [12–15]. Anopheles quadrimaculatus Say and Anopheles freeborni Aitken are the primary vectors of malaria in the region [13, 16]. Anopheles crucians Wiedemann is considered a competent vector but has not been directly implicated in malaria transmission to humans [17]. Anopheles freeborni is commonly found in the western part of the United States, while An. quadrimaculatus and An. crucians are more prevalent in the eastern regions [18–21]. The anthropophilic behavior of An. quadrimaculatus and, to a lesser extent, An. crucians make these species significant threats for malaria transmission [22, 23].

Anopheles quadrimaculatus and An. crucians were abundant in Palm Beach County, Florida, and implicated as probable vectors during the 2003 malaria outbreak. All seven cases of malaria identified during the outbreak in Florida were attributed to P. vivax. Construction workers and unsheltered homeless individuals were the most affected, underscoring the role of disparities in the risk of mosquito-borne disease transmission [14]. After 20 years without reported locally acquired malaria infections in the continental US [24], in the summer of 2023, the Centers for Disease Control and Prevention (CDC) responded to locally acquired P. vivax malaria cases. A total of 8 cases have been reported, seven in Sarasota County, Florida, and one Cameron County, Texas [15]. Three of the seven cases in Sarasota County occurred in people experiencing homelessness [25].

Miami-Dade County, Florida is one of the most important gateways into the United States. Miami-Dade County is not only one of the most important touristic destinations, receiving an average of over 120 million visitors every year, but it is also a pivotal operational hub for the cruise ship industry, serving as the main port for cruise ships supplying the Caribbean and Gulf of Mexico [26]. Miami-Dade is also a hub for freight cargo ships that routinely transport goods from Miami-Dade to Caribbean countries and vice versa, including Haiti, Dominican Republic, and Cuba, increasing the risk of pathogen importation into the United States [27]. The most recent malaria outbreak in Sarasota County (approximately 300 km from Miami-Dade County) highlights the need to improve surveillance and outbreak preparedness and response to respond to this increasing threat in Miami-Dade, Florida, and the United States.

Given the recent history of malaria outbreaks in the United States, we hypothesize that other major urban areas harbor conducive conditions for local transmission of malaria. Therefore, our objective is to create a profile of the most abundant Anopheles vector species in Miami-Dade, Florida, An. crucians and An. quadrimaculatus to guide mosquito control strategies and enhance preparedness and response measures for potential malaria outbreaks.

The Miami-Dade County Mosquito Control surveillance grid consists of 322 traps, including 283 BG-Sentinel traps (Biogents AG, Regensburg, Germany) and 39 CDC traps (Fig. 1). In 2020, 68 BG-Sentinel traps were incorporated into the surveillance system, and an additional 72 traps were added in 2021. Furthermore, 3 CDC traps were introduced in 2020. Each trap was deployed weekly for 24 hours from January 2020 to December 2022. All traps were baited with CO₂ using a container filled with 1 Kg of dry ice pellets [28]. All collected mosquitoes were transported to the Miami-Dade County Mosquito Control Laboratory and morphologically identified using taxonomic keys [29].

Here we focus solely on female mosquito specimens because both BG-Sentinel and CDC traps are designed to attract predominantly females seeking blood feeding. Consequently, any male mosquitoes collected were regarded as accidental catches and were not considered relevant for the analyses. To assess variations in the relative abundance of An. crucians and An. quadrimaculatus, we calculated the ratio by dividing the total number of mosquitoes collected by each individual trap in 2022 by the number of mosquitoes collected by the same trap in 2020. Traps that were not part of the surveillance system in 2020 were excluded from this analysis.

To identify conducive areas for the proliferation of mosquitoes and identify sentinel traps for the early detection of mosquito abundance increases, we followed the same approach used in Wilke et al. [30]. Briefly, we calculated the distance between all traps in the surveillance system (linear distance in meters) and created a 4 km buffer radius around each trap in the surveillance system. We established buffer sizes with an optimum number of traps in each buffer (mean: >15 traps) to enable a robust statistical analysis and still maintain sufficient spatial resolution for informing local control operations. Traps with no data were removed from the analysis. To calculate the mean buffer values, we excluded outliers within each buffer by eliminating observations lying outside the expected range of mean variability according to the standard definition (\(median\pm 1.58\times \frac{IQR}{\sqrt{n}}\), where IQR is interquartile range and n is the number of observations in the buffer. This analysis was conducted in R (version 4.2.2).

In 2020, a total of 10,638 An. crucians specimens were collected, 20,844 in 2021, and 5,107 in 2022, summing up to 36,589 specimens collected over the three years of this study. Meanwhile, for An. quadrimaculatus, 2,189 specimens were collected in 2020, 4,151 in 2021, and 3,603 in 2022, resulting in a total of 9,943 specimens collected during the study period.

Both An. crucians and An. quadrimaculatus were abundant in transition zones between natural and urban areas and reached high abundances in specific locations (10% of the traps collected the highest number of mosquitoes, with individual traps collecting up to 14,713 An. crucians and 2,336 An. quadrimaculatus over the 3-year period) in the northwestern and western parts of the county. An. quadrimaculatus was also abundant in the southern part of Miami-Dade County, with several traps collecting a high number of specimens in recently urbanized areas. Both species were also abundant in Oleta Park in the northeast region of the county. Anopheles crucians and An. quadrimaculatus were not collected in significant numbers within urban areas (Fig. 2).

The ratio analysis revealed substantial fluctuations in the abundance of An. crucians and An. quadrimaculatus in specific areas of Miami-Dade County. Anopheles crucians increased in abundance in selected traps in the southern part of the county; however, the majority of the traps showed a decrease in the number of collected specimens. Conversely, An. quadrimaculatus increased in abundance in several traps located in the southern part of the county (i.e., Homestead) that has recently undergone intense urbanization [31]. On the other hand, the number of An. quadrimaculatus collected in the western part of the county decreased over time.

The identification of areas conducive to mosquito proliferation and influential traps (defined as traps yielding an average number of mosquitoes at the 97.5th percentile of the cluster) to serve as sentinels in early warning systems are vital in detecting increases in mosquito vector species abundance. Recognizing hotspot areas and influential traps enables strategic mosquito control operations, focusing efforts on locations favorable for mosquito proliferation and identifying local-level drivers supporting their population growth. Of the 322 traps in the surveillance system, 176 collected An. crucians. From those, 85 collected An. crucians above their buffer average and 36 traps were considered influential traps. Similarly, of the 322 traps in the surveillance system, 194 traps collected An. quadrimaculatus. From those, 86 collected An. quadrimaculatus above their buffer average and 32 traps were considered influential traps (Fig. 4).

The population dynamics of An. crucians and An. quadrimaculatus exhibited high heterogeneity, showing no distinct seasonal trend. Among An. crucians, the highest average number of specimens per trap was observed in March 2020, with an average of 4.88 mosquitoes collected per trap per month, followed by 3.44 in June 2020, and 2.86 in December 2021. Conversely, the lowest averages were recorded in July 2021, with an average number of 0.002 An. crucians collected per trap. For An. quadrimaculatus, the highest average number of specimens per month occurred in December 2020, with an average of 0.6 mosquitoes collected per month, followed by 0.51 in October 2020, and 0.48 in September 2021. The lowest averages were observed in July 2022, with an average number of 0.02 An. quadrimaculatus collected per trap.

The risk of malaria transmission in the United States depends on imported human cases and the presence of mosquito vector species. The United States reports approximately 2,000 imported cases of malaria every year [24], and many regions have established mosquito vector populations able to transmit Plasmodium parasites, leading to sporadic local malaria transmission [12, 14, 15, 32, 33]. Our results show that malaria vectors An. crucians and An. quadrimaculatus in Miami-Dade County, Florida, are abundant and their spatial distribution highly heterogeneous. Both species were highly abundant in transition zones between natural/rural and urban areas but were not found in great numbers in more urbanized areas within the county. This spatial pattern likely results from these mosquitoes' inherent biological and physiological requirements, which are not adequately met in urban environments.

Anopheles crucians and An. quadrimaculatus have a high tolerance to brackish water and other environmental conditions that are otherwise detrimental to other mosquito species [34, 35]. Our spatial analysis reveals the existence of highly conducive environments, characterized by an overabundance of resources supporting the proliferation of An. crucians and An. quadrimaculatus in well-defined areas. Notably, 10% of the traps collected the highest number of mosquitoes, with individual traps collecting up to 14,713 An. crucians and 2,336 An. quadrimaculatus throughout the study period. In contrast, 90% of the traps collected significantly fewer mosquitoes, with counts ranging below 18 An. crucians and 29 An. quadrimaculatus.

The comparison between the number of mosquitoes collected by specific traps showed that the majority of traps had a decreasing trend in mosquito counts over time. However, a subset of traps displayed a substantial increase. For An. crucians, the number of collected mosquitoes decreased in most traps but exhibited an increase in specific traps situated in transition zones between natural/rural and urban regions. Conversely, An. quadrimaculatus exhibited an increase in abundance in several traps located in the southern part of the county, which recently underwent intense urbanization processes. For example, the population of Homestead, Florida increased from 60,512 in 2010 to 80,734 in 2022 (~ 33% increase) [36]. The increased mosquito abundance is likely attributed to the availability of resources in both natural and rural areas, conducive to the proliferation of An. quadrimaculatus, as well as the additional resources available in the recently urbanized areas, including human hosts for blood feeding. These findings indicate a heightened level of human exposure to Anopheles vectors in specific regions of Miami-Dade County, with a notable increase in exposure specifically to An. quadrimaculatus in the southern part of the county.

The increasing threat of insecticide resistance requires the development and implementation of targeted tailor-made mosquito control strategies [37]. The analysis aimed to identify sentinel traps that collected a significantly higher number of either An. crucians or An. quadrimaculatus compared to other traps in their buffer suggest that the availability of resources at the local scale played a key role in their proliferation. To effectively control mosquito populations and mitigate the risk of disease transmission, the strategic use of sentinel traps plays a vital role. Sentinel traps could serve as early warning systems, helping to identify areas with higher mosquito abundance and providing valuable data for informed decision-making. This targeted approach would allow for the efficient allocation of resources, focusing on locations where mosquito populations pose the most significant threat to public health.

Effective mosquito control strategies are crucial to enhance preparedness and response for dealing with malaria outbreaks in the United States. The high abundance of An. quadrimaculatus, and to a lesser extent An. crucians, in close proximity to humans, pose an elevated risk of malaria transmission. Gaining a better understanding of the drivers enabling the proliferation of Anopheles vector species, along with their population dynamics and spatial distribution, is essential to implement effective mosquito control to mitigate the risk posed by the influx of travelers carrying malaria into the United States.

Ethical Approval

Not applicable

Competing interests

M.A. has received research funding from Seqirus unrelated to this manuscript. The other authors declare no competing interests.

Authors' contributions

Conceptualization: A.B.B.W. and M.A.

Data curation: C.V., J.M, and I.U.

Formal analysis: A.B.B.W., C.V.

Investigation: A.B.B.W.

Supervision: C.V, J.B, M.A.

Writing – original draft: A.B.B.W.

Writing – review & editing: C.V., J.M., I.U., J.C., M.A.

Funding

This research was supported by the Miami-Dade Mosquito Control Division and by the CDC (https:// www. cdc. gov/) grant U01CK000662: Southeastern Regional Center of Excellence in Vector-Borne Diseases: The Gateway Program. CDC had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript.

Availability of data and materials

The data supporting the findings of this study will be made available upon request.

Sato S. Plasmodium-a brief introduction to the parasites causing human malaria and their basic biology. J Physiol Anthropol. 2021;40:1.
Multini LC, Marrelli MT, Beier JC, Wilke ABB. Increasing complexity threatens the elimination of Extra-Amazonian Malaria in Brazil. Trends Parasitol. 2019;35:383-387.
Nkumama IN, O'Meara WP, Osier FHA. changes in malaria epidemiology in Africa and new challenges for elimination. Trends Parasitol. 2017;33:128-140.
Saavedra MP, Conn JE, Alava F, Carrasco-Escobar G, Prussing C, Bickersmith SA, et al. Higher risk of malaria transmission outdoors than indoors by Nyssorhynchus darlingi in riverine communities in the Peruvian Amazon. Parasit Vectors. 2019;12:1–15.
Chu VM, Sallum MAM, Moore TE, Lainhart W, Schlichting CD, Conn JE. Regional variation in life history traits and plastic responses to temperature of the major malaria vector Nyssorhynchus darlingi in Brazil. Sci Rep. 9;9:5356.
von Seidlein L, Peto TJ, Tripura R, Pell C, Yeung S, Kindermans JM, et al. Novel approaches to control malaria in forested areas of Southeast Asia. Trends Parasitol. 2019;35:388–98.
World Health Organization. World malaria report 2022. Available at: https://www.who.int/teams/global-malaria-programme
White NJ. The treatment of malaria. New England Journal of Medicine. 1996;335:800–6.
Tschan S, Kremsner PG, Mordmüller B. Emerging drugs for malaria. Expert Opin Emerg Drugs. 2012;17:319–33.
Hemingway J, Shretta R, Wells TNC, Bell D, Djimdé AA, Achee N, et al. Tools and strategies for malaria control and elimination: What do we need to achieve a grand convergence in malaria? PLoS Biol. 2016;14:e1002380
Chanda E, Ameneshewa B, Bagayoko M, Govere JM, Macdonald MB. Harnessing Integrated Vector Management for enhanced disease prevention. Trends Parasitol. 2017;33:30–41.
Robert LL, Santos-Ciminera PD, Andre RG, Schultz GW, Phillip G. Plasmodium-infected Anopheles mosquitoes collected in Virginia and Maryland following local transmission of Plasmodium vivax malaria in Loudoun county, Virginia. J Am Mosq Control Assoc. 2005;21:187-93.
Dye-Braumuller KC, Kanyangarara M. Malaria in the USA: How vulnerable are we to future outbreaks? Curr Trop Med Rep. 2021;8:43-51.
Centers for Disease Control and Prevention. Local transmission of Plasmodium vivax malaria-Palm Beach County, Florida, 2003. MMWR Morb Mortal Wkly Rep. 2003;52:908–11.
Centers for Disease Control and Prevention. Locally Acquired Cases of Malaria in Florida and Texas. Available at: https://www.cdc.gov/malaria/new_info/2023/malaria_florida.html.
Sinka ME, Bangs MJ, Manguin S, Rubio-Palis Y, Chareonviriyaphap T, Coetzee M, et al. A global map of dominant malaria vectors. Parasit Vectors. 2012;5:69.
Wilkerson RC, Reinert JF, Li AC. Ribosomal DNA ITS2 sequences differentiate six species in the Anopheles crucians complex (Diptera: Culicidae). J. Med. Entomol. 2004;41:392-401.
Levine RS, Townsend Peterson A, Benedict MQ. Distribution of members of Anopheles quadrimaculatus Say s.l. (Diptera: Culicidae) and Implications for their roles in malaria transmission in the United States. J. Med. Entomol. 2004;41:607-13
Global Biodiversity Information Facility. Anopheles crucians Wiedemann, 1828. Available at: https://www.gbif.org/species/1650546.
Global Biodiversity Information Facility. Anopheles freeborni Aitken, 1939. Available at: https://www.gbif.org/species/1650116.
Global Biodiversity Information Facility. Anopheles quadrimaculatus Say, 1824. Available at: https://www.gbif.org/species/1650395.
Gingrich JB, Williams, Gregory M. Host-feeding patterns of suspected West Nile virus mosquito vectors in Delaware, 2001-2002. J Am Mosq Control Assoc. 2005;21:194-200.
Sinka ME, Rubio-Palis Y, Manguin S, Patil AP, Temperley WH, Gething PW, et al. The dominant Anopheles vectors of human malaria in the Americas: Occurrence data, distribution maps and bionomic précis. Parasit Vectors. 2011;4:210.
Mace KE, Lucchi NW, Tan KR. Malaria surveillance — United States, 2018. MMWR Surveillance Summaries. 2022;71:1–35.
Young C. CDC and Sarasota County officials address malaria outbreak. 2023. Available at: https://www.wmnf.org/cdc-and-sarasota-county-officials-address-malaria-outbreak/.
United States Bureau of Transportation Statistics. 2016 Annual and December U.S. Airline Traffic Data. Available at: https://www.bts.gov/newsroom/2016-annual-and-december-us-airline-traffic-data
Wilke ABB, Vasquez C, Carvajal A, Moreno M, Petrie WD, Beier JC. Mosquito surveillance in maritime entry ports in Miami-Dade County, Florida to increase preparedness and allow the early detection of invasive mosquito species. PLoS One. 2022;17:e0267224.
Wilke ABB, Vasquez C, Medina J, Carvajal A, Petrie W, Beier JC. Community composition and year-round abundance of vector species of mosquitoes make Miami-Dade County, Florida a receptive gateway for arbovirus entry to the United States. Sci Rep. 2019;9:8732.
Darsie, Jr. RF, Morris CD. Keys to the Adult Females and Fourth Instar Larvae of the Mosquitoes of Florida (Diptera, Culicidae). 1st ed. Technical Bulletin of the Florida Mosquito Control Association. Bulletin of the Florida mosquito control association; 2000.
Wilke ABB, Damian D, Litvinova M, Byrne T, Zardini A, Poletti P, et al. Spatiotemporal distribution of vector mosquito species and areas at risk for arbovirus transmission in Maricopa County, Arizona. Acta Trop. 2023;240:1–9.
Miami-Dade County. Miami-Dade County building permits. Available at: http://www.miamidade.gov/permits/
MacArthur JR, Holtz TH, Jenkins J, Newell JP, Koehler JE, Parise ME, et al. Probable locally acquired mosquito-transmitted malaria in Georgia, 1999. Clin Infect Dis. 2001;32:E124-8.
Mace KE, Lucchi NW, Tan KR. Malaria Surveillance — United States, 2018. MMWR Surveill Summ 2022;71:1–29.
Yee DA, Dean C, Webb C, Henke JA, Perezchica-Harvey G, White GS, et al. No evidence that salt water ingestion kills adult mosquitoes (Diptera: Culicidae). J Med Entomol. 2021;58:767–72
Hu GY, Lounibos LP, Escher RL. Seasonal abundance, age composition, and body size of salt-marsh Anopheles (Diptera: Culicidae) in south Florida. J Med Entomol. 1993;30:883-7.
United States Census Bureau. QuickFacts Homestead City, Florida. Available at: https://www.census.gov/quickfacts/fact/table/homesteadcityflorida/POP060210
Pridgeon JW, Pereira RM, Becnel JJ, Allan SA, Clark GG, Linthicum KJ. Susceptibility of Aedes aegypti, Culex quinquefasciatus Say, and Anopheles quadrimaculatus Say to 19 pesticides with different modes of action. J. Med. Entomol. 2008;45:82-7

Download PDF

Version 1

posted

You are reading this latest preprint version

Presence and Abundance of Malaria Vector Species in Miami-Dade County, Florida

Status:

Version 1

Abstract

Figures

Introduction

Methods

Results

Discussion

Declarations

References

Status:

Version 1