Epidemiologic and environmental characterization of the Re-emergence of St. Louis Encephalitis Virus in California, 2015-2020.

St. Louis encephalitis virus (SLEV) is an endemic flavivirus in the western and southeastern United States, including California. From 1938 to 2003, the virus was detected annually in California, but after West Nile virus (WNV) arrived in 2003, SLEV was not detected again until it re-emerged in Riverside County in 2015. The re-emerging virus in California and other areas of the western US is SLEV genotype III, which previously had been detected only in Argentina, suggesting a South American origin. This study describes SLEV activity in California since its re-emergence in 2015 and compares it to WNV activity during the same period. From 2015 to 2020, SLEV was detected in 1,650 mosquito pools and 26 sentinel chickens, whereas WNV was detected concurrently in 18,108 mosquito pools and 1,542 sentinel chickens from the same samples. There were 24 reported human infections of SLEV in 10 California counties, including two fatalities (case fatality rate: 8%), compared to 2,469 reported human infections of WNV from 43 California counties, with 143 fatalities (case fatality rate: 6%). From 2015 through 2020, SLEV was detected in 17 (29%) of California's 58 counties, while WNV was detected in 54 (93%). Although mosquitoes and sentinel chickens have been tested routinely for arboviruses in California for over fifty years, surveillance has not been uniform throughout the state. Of note, since 2005 there has been a steady decline in the use of sentinel chickens among vector control agencies, potentially contributing to gaps in SLEV surveillance. The incidence of SLEV disease in California may have been underestimated because human surveillance for SLEV relied on an environmental detection to trigger SLEV patient screening and mosquito surveillance effort is spatially variable. In addition, human diagnostic testing usually relies on changes in host antibodies and SLEV infection can be indistinguishable from infection with other flaviviruses such as WNV, which is more prevalent.

Evaluation of the effectiveness of the California mosquito-borne virus surveillance & response plan, 2009-2018.

Local vector control and public health agencies in California use the California Mosquito-Borne Virus Surveillance and Response Plan to monitor and evaluate West Nile virus (WNV) activity and guide responses to reduce the burden of WNV disease. All available data from environmental surveillance, such as the abundance and WNV infection rates in Culex tarsalis and the Culex pipiens complex mosquitoes, the numbers of dead birds, seroconversions in sentinel chickens, and ambient air temperatures, are fed into a formula to estimate the risk level and associated risk of human infections. In many other areas of the US, the vector index, based only on vector mosquito abundance and infection rates, is used by vector control programs to estimate the risk of human WNV transmission. We built models to determine the association between risk level and the number of reported symptomatic human disease cases with onset in the following three weeks to identify the essential components of the risk level and to compare California's risk estimates to vector index. Risk level calculations based on Cx. tarsalis and Cx. pipiens complex levels were significantly associated with increased human risk, particularly when accounting for vector control area and population, and were better predictors than using vector index. Including all potential environmental components created an effective tool to estimate the risk of WNV transmission to humans in California.

Characterizing Areas with Increased Burden of West Nile Virus Disease in California, 2009-2018.

West Nile virus (WNV) is a mosquito-borne flavivirus that can cause severe neurological disease in humans, for which there is no treatment or vaccine. From 2009 to 2018, California has reported more human disease cases than any other state in the United States. We sought to identify smaller geographic areas within the 10 California counties with the highest number of WNV cases that accounted for disproportionately large numbers of human cases from 2009 to 2018. Eleven areas, consisting of groups of high-burden ZIP codes, were identified in nine counties within southern California and California's Central Valley. Despite containing only 2% of California's area and 17% of the state's population, these high-burden ZIP codes accounted for 44% of WNV cases reported and had a mean annual incidence that was 2.4 times the annual state incidence. Focusing mosquito control and public education efforts in these areas would lower WNV disease burden.

A Comparison of Questing Substrates and Environmental Factors That Influence Nymphal Ixodes pacificus (Acari: Ixodidae) Abundance and Seasonality in the Sierra Nevada Foothills of California.

In California, the western blacklegged tick, Ixodes pacificus Cooley and Kohls, is the principal vector of the Borrelia burgdorferi sensu lato (sl) complex (Spirochaetales: Spirochaetaceae, Johnson et al.), which includes the causative agent of Lyme disease (B. burgdorferi sensu stricto). Ixodes pacificus nymphs were sampled from 2015 to 2017 at one Sierra Nevada foothill site to evaluate our efficiency in collecting this life stage, characterize nymphal seasonality, and identify environmental factors affecting their abundance and infection with B. burgdorferi sl. To assess sampling success, we compared the density and prevalence of I. pacificus nymphs flagged from four questing substrates (logs, rocks, tree trunks, leaf litter). Habitat characteristics (e.g., canopy cover, tree species) were recorded for each sample, and temperature and relative humidity were measured hourly at one location. Generalized linear mixed models were used to assess environmental factors associated with I. pacificus abundance and B. burgdorferi sl infection. In total, 2,033 substrates were sampled, resulting in the collection of 742 I. pacificus nymphs. Seasonal abundance of nymphs was bimodal with peak activity occurring from late March through April and a secondary peak in June. Substrate type, collection year, month, and canopy cover were all significant predictors of nymphal density and prevalence. Logs, rocks, and tree trunks had significantly greater nymphal densities and prevalences than leaf litter. Cumulative annual vapor pressure deficit was the only significant climatic predictor of overall nymphal I. pacificus density and prevalence. No associations were observed between the presence of B. burgdorferi sl in nymphs and environmental variables.

Identification and Monitoring of International Travelers During the Initial Phase of an Outbreak of COVID-19 - California, February 3-March 17, 2020.

The threat of introduction of coronavirus disease 2019 (COVID-19) into the United States with the potential for community transmission prompted U.S. federal officials in February 2020 to screen travelers from China, and later Iran, and collect and transmit their demographic and contact information to states for follow-up. During February 5-March 17, 2020, the California Department of Public Health (CDPH) received and transmitted contact information for 11,574 international travelers to 51 of 61 local health jurisdictions at a cost of 1,694 hours of CDPH personnel time. If resources permitted, local health jurisdictions contacted travelers, interviewed them, and oversaw 14 days of quarantine, self-monitoring, or both, based on CDC risk assessment criteria for COVID-19. Challenges encountered during follow-up included errors in the recording of contact information and variation in the availability of resources in local health jurisdictions to address the substantial workload. Among COVID-19 patients reported to CDPH, three matched persons previously reported as travelers to CDPH. Despite intensive effort, the traveler screening system did not effectively prevent introduction of COVID-19 into California. Effectiveness of COVID-19 screening and monitoring in travelers to California was limited by incomplete traveler information received by federal officials and transmitted to states, the number of travelers needing follow-up, and the potential for presymptomatic and asymptomatic transmission. More efficient methods of collecting and transmitting passenger data, including electronic provision of flight manifests by airlines to federal officials and flexible text-messaging tools, would help local health jurisdictions reach out to all at-risk travelers quickly, thereby facilitating timely testing, case identification, and contact investigations. State and local health departments should weigh the resources needed to implement incoming traveler monitoring against community mitigation activities, understanding that the priorities of each might shift during the COVID-19 pandemic.

Long-Term Rodent Surveillance after Outbreak of Hantavirus Infection, Yosemite National Park, California, USA, 2012.

In 2012, a total of 9 cases of hantavirus infection occurred in overnight visitors to Yosemite Valley, Yosemite National Park, California, USA. In the 6 years after the initial outbreak investigation, the California Department of Public Health conducted 11 rodent trapping events in developed areas of Yosemite Valley and 6 in Tuolumne Meadows to monitor the relative abundance of deer mice (Peromyscus maniculatus) and seroprevalence of Sin Nombre orthohantavirus, the causative agent of hantavirus pulmonary syndrome. Deer mouse trap success in Yosemite Valley remained lower than that observed during the 2012 outbreak investigation. Seroprevalence of Sin Nombre orthohantavirus in deer mice during 2013-2018 was also lower than during the outbreak, but the difference was not statistically significant (p = 0.02). The decreased relative abundance of Peromyscus spp. mice in developed areas of Yosemite Valley after the outbreak is probably associated with increased rodent exclusion efforts and decreased peridomestic habitat.

Detection of Arbovirus Transmission via Sugar Feeding in a Laboratory Setting.

Most species of mosquitoes consume sugar to survive and during sugar feeding can expectorate virus. Scientists have used this behavior to develop novel methods of mosquito control and arbovirus surveillance. In this study, we use sugar feeding and corresponding viral expectoration to develop an affordable method of monitoring individual mosquitoes for longitudinal data collection. Female Culex tarsalis Coquillett (Diptera: Culicidae) that consumed an infectious bloodmeal of West Nile virus were placed into separate containers and offered a sucrose-soaked cotton wick. Wicks were then collected daily and tested for virus with similar results to those from standard capillary tube method. This yielded a direct longitudinal estimate of the extrinsic incubation period, while using fewer mosquitoes. This approach could be used to further characterize variation in the amount and diversity of expectorated virus over the life span of individual mosquitoes.

The Impact of Cycling Temperature on the Transmission of West Nile Virus.

West Nile virus (WNV) is an important cause of disease in humans and animals. Risk of WNV infection varies seasonally, with the greatest risk during the warmest parts of the year due in part to the accelerated extrinsic incubation rate of the virus in mosquitoes. Rates of extrinsic incubation have been shown in constant-temperature studies to increase as an approximately linear function of temperature, but for other vector-borne pathogens, such as malaria or dengue virus, nonlinear relationships have been demonstrated under cycling temperatures near the thermal limits of pathogen replication. Using typical daily air temperature profiles from three key periods of WNV amplification in a hyperendemic area of WNV activity in California's Central Valley, as well as a fourth temperature profile based on exposures that would result from daily mosquito host-seeking and resting behavior, we explored the impacts of cycling temperatures on WNV transmission by Culex tarsalis Coquillett, one of the principal vectors in the western United States. The daily cycling temperature ranges studied were representative of those that occur across much of California, but they did not significantly alter the extrinsic incubation period of WNV compared with estimates from mean temperatures alone. This suggests that within the relatively broad range we studied, WNV incubation rates are a simple function of mean temperature. Realistic daily temperature patterns that reflected mosquitoes' avoidance of daytime high temperatures during summer reduced transmission over time compared with air temperatures, indicating that adjustment for mosquito exposure temperatures would be prudent for calculating risk.

Extrinsic Incubation Rate is Not Accelerated in Recent California Strains of West Nile Virus in Culex tarsalis (Diptera: Culicidae).

The efficiency of West Nile virus (WNV) transmission by competent mosquito vectors is driven by temperature and defined, in part, by the extrinsic incubation period, which is the time from a mosquito's consumption of an infected bloodmeal until it becomes capable of transmitting the virus to the next vertebrate host. The extrinsic incubation period can be altered by a variety of factors involved in vector-pathogen interactions, and in North America, the WN02 strain of WNV emerged and displaced the founding NY99 strain reportedly because the duration of the extrinsic incubation period in Culex mosquitoes was shortened by a single positively selected mutation. However, recent work has suggested that this change is not universal and may depend on vector species or strain. In the current study, we estimated the extrinsic incubation periods at 22 and 30°C in Culex tarsalis Coquillett. We found that the time to transmission of the original North American WNV strain, NY99, was not different from two more recent California isolates of the WN02 genotype: one of the earliest California isolates from the southeastern deserts, and a more recent 2011 isolate from a hyperendemic region in the Central Valley. We conclude with a model-based assessment of the epidemiological effects of temperature on the duration of mosquitoes' infectious life, which estimated that most mosquitoes have an infectious life of only a few days, but its duration expands markedly at warmer temperatures.