https://orcid.org/0000-0001-9390-0937
Figures
Abstract
The impacts of climate change on vector-borne and zoonotic diseases (VBZD) are well founded in some countries but remain poorly understood in Caribbean countries. VBZD impose significant burdens on individuals and healthcare systems, heightening the need for studies and response measures to address epidemics and persistent high prevalence of these diseases in any region. This study analyses the pattern of dengue case distribution in Grenada between 2010–2020 and investigates the relationship between rainfall and cases. The total number of dengue cases in the wet seasons (June to December) and dry seasons (January to May) were 1741 and 458, respectively, indicating higher prevalence of the disease in wet periods. The data also shows that rainfall was not consistently higher during the typical rainy season months. The observed patterns in 2013, 2018 and 2020 show, while these were the driest years, the number of cases were higher than in other years. Two factors may explain high number of cases in the drier years (1) frequent sporadic heavy rainfall and (2) poor water storage practices in dry season. With each 30 mm unit decrease in annual rainfall, the incidence rate ratio of dengue was reduced by a factor of .108 (89.2%). The work of the Vector Control Unit is shown to be effective in managing dengue in Grenada. The study highlights the need for year-round surveillance and interventions to control the mosquito population and dengue transmission.
Citation: Francis K, Edwards O, Telesford L (2023) Climate and dengue transmission in Grenada for the period 2010–2020: Should we be concerned? PLOS Clim 2(6): e0000122. https://doi.org/10.1371/journal.pclm.0000122
Editor: Asif Qureshi, Indian Institute of Technology Hyderabad, INDIA
Received: April 22, 2022; Accepted: April 22, 2023; Published: June 5, 2023
Copyright: © 2023 Francis et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Data is provided in the supporting information file.
Funding: The authors received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
The Caribbean countries are some of the most vulnerable nations affected by climate change [1]. Climate change is indicative of persistent and significant changes in meteorological conditions, primarily temperature and rainfall, observed to affect a large geographical area [2,3]. These changes have direct and indirect impacts on humans mediated through environmental events such as ocean acidification, flooding, heatwaves, droughts and storms [3,4]. Climate change is associated with increasing incidence of both communicable and non-communicable diseases in humans [2]. The effects of changing environments on habitation, reproduction, and other behaviors of animals implicate cross-transmission of pathogens of public health significance [2]. Emerging and endemic VBZD pose serious threats to human health and impose significant burden on healthcare systems in many countries. In the last few decades, the transmission of VBZD to new areas and populations also expanded rapidly [5].
Dengue is transmitted to humans through the bite of an infected Aedes mosquito. An abundance of mosquitoes in an area increases the potential for infections and continuation of the transmission cycle [6]. Climate change is conducive to increasing the spatial and seasonal density of mosquito populations [7]. In tropical and subtropical regions, in particular, there is a high disease burden and, in at least 125 countries, approximately 10,000 deaths annually are relate to dengue [8]. According to the World Health Organization (WHO), an average of less than 1000 global dengue cases were reported annually in the 1950s; however, by 2016, a steady increase up to 3.34 million cases were reported [9]. Half of the world’s population is at risk of dengue with the highest rates of hospitalization and death occurring in children, the most vulnerable group to the disease [10].
Warm conditions encourage mosquito reproduction with reduced time for larvae maturation [11]. Adult female mosquitoes also digest blood more rapidly and feed regularly in warmer conditions, increasing biting rate and the potential for disease transmission [11]. Besides dengue, changes in the patterns of rainfall and temperature have also influenced the transmission of other VBZD, including malaria, chikungunya and zika [12]. Few studies have been conducted in the Caribbean countries to understand the relationships between historical and prevailing weather and VBZD epidemiology. One study conducted in Puerto Rico found a relationship between dengue outbreaks, temperature and precipitation [13]. From 2013 to 2017, the Caribbean region experienced unusual, and in some cases, simultaneous occurrences of dengue, chikungunya, and zika epidemics [14]. Nonetheless, the relationships between VBZD epidemics and the socio-economic and demographic features of the region also remain understudied. Over the past 50 years, in at least 119 countries in which dengue is endemic, there was a 30-fold increase in the reported incidence of disease resulting from factors such as population growth, urbanization, poor sanitation, increased human travel, limited mosquito control measures, and increased reporting capacity [10]. In drought conditions, the common practice of storing water accommodates the breeding of mosquitoes [15]. Tracking the association between dengue cases and weather is also complex [16]. While stagnated water supports mosquito breeding and larva development, excessive rainfall can also remove mosquito breeding sites, causing larva mortality [17]. An estimated US $321.4 million is spent annually in Caribbean countries to treat dengue; excluding the cost of mosquito control measures and other programs targeting the prevention of the disease [14].
In the 1970s, the Caribbean region recorded the first case of dengue in Jamaica and, subsequently, the disease became endemic in several regional countries, including Grenada [18,19]. Grenada is a small tropical island with a population of 112,000 people and is located in the southern part of the Caribbean [20]. To our knowledge, studies were not previously conducted to determine the relationship between rainfall and reported dengue cases on the island. This study includes descriptive and statistical analyses to identify the pattern of dengue cases and investigate the relationship between rainfall and cases from 2010 to 2020.
Materials and methods
Descriptive and statistical analyses were conducted with dengue cases and rainfall data for the period 2010–2020. The weekly rainfall data was measured in millimeters and provided by the Meteorological Office at the Maurice Bishop International Airport in Grenada. The meteorological office also provided average weekly temperature in Celsius measurement. Data on the meteorological variables (rainfall and temperature) were measured on a continuous scale. The Ministry of Health in Grenada provided the data on dengue cases and reported by epidemiological weeks. The dengue cases were recorded as count data.
Negative binomial regression was conducted using IBM SPSS software (v28) to investigate relationships between reported dengue cases and rainfall. Temperature was added as a covariate in the analysis. In Grenada, the dry season spans the period January to May, coinciding with epidemiological weeks 1–22. The wet season spans the period June to December, coinciding with epidemiological weeks 23–53. The weekly meteorological and epidemiological data were also totaled by months and analyzed to generate results to compare outcomes in the dry and wet seasons in Grenada. The statistical analysis did not include years with small total counts (<10) of reported dengue cases. There were seven reported cases in 2015; therefore, that year was not included in the statistical analysis. Data were analyzed at 95% CI with the alpha value at 0.05.
To allow for observations of the effect on the dependent variable (dengue cases) from small unit changes in the independent variable (rainfall and temperature), a narrow range of values were grouped to form categories for each independent variable. The category with the highest values was automatically assigned as the reference and the effects on the dependent variable of all other categories compared to the effect of the reference category. The categories for monthly average temperatures in Celsius measurements were: 26 (C1), 27–28 (C2), 29 (C3 –reference category). The categories for rainfall in mm were: 1–30 (C1), 31–60 (C2), 61–90 (C3), 91–120 (C4), 121–150 (C5), 151–180 (C6), 181–210 (C7), 211–240 (C8), 241–270 (C9), 271–300 (C10-reference category).
Results
Annual distribution of dengue cases
The annual frequency of dengue cases in Grenada from 2010–2020 is shown in Table 1. Over the period, the number of dengue cases totaled 2199. The highest number of cases were reported in 2020 (546) and 2018 (405). Over 200 cases were also reported in 2010 (253) and 2013 (226), and less than 100 cases in 2016 (76) and 2012 (94). Only 7 cases were recorded in 2015.
The data shows fluctuations in the recorded weekly cases across the reporting years. Generally, the highest number of cases were documented between the middle and latter part of each year. In 2020, there was a significant increase in weekly cases, ranging from 30+ to 40+ in the latter part of the year, from weeks 40 to 57, (Fig 1). In 2018, during weeks 24–37, about the middle of the year, there were at least 10 weekly cases recorded, except in weeks 25 and 33 (Fig 2). Fig 3 shows fluctuation in dengue cases in 2013 with the highest number of cases between weeks 36 to 44. The number of cases ranged from 2–25.
Seasonal frequency of dengue cases
While the highest number of cases were reported in the middle to latter parts of the years, reflecting the typical rain season, Fig 4 shows that, overall, number of cases were also highest in the years with less rainfall, that is 2013, 2018 and 2020.
The total number of dengue cases in the wet seasons (June to December) and dry seasons (January to May) over the reporting period were 1741 and 458, respectively, indicating that the highest number of cases were reported in the wet season. However, within specific years, there was deviation to this general pattern. A comparable number of dengue cases were recorded across both seasons in 2014 and 2019. In 2012, a significantly higher number of cases were reported in the dry season compared to the wet season (Fig 5). In the wet season in 2015, only one case was recorded while all other years had 20+ cases reported.
In each year, less than 50 dengue cases were noted in the dry season except in 2012, 2014, 2018, and 2019 in which there were 69–117 reported cases. The cases for each year in the wet season exceeded 75 except in 2015, in which 1 case was reported. In 2015, the lowest total cases of dengue (7) were recorded, coinciding with the third lowest annual rainfall (1074 mm). In 2016, the second lowest total dengue cases (76) were reported and the fourth lowest annual rainfall (1104 mm). While, generally, the total number of cases was higher in the wet season, in 2020, the highest total dengue cases were recorded, coinciding with the lowest annual rainfall (897 mm) over the period 2010–2020 (Table 2).
Increased reported dengue cases were observed following periods of prolonged rainfall, i.e., consistent rainfall over one- to two-week period, even during the dry season. For example, following prolonged rainfall in weeks 1–2 in 2017 (dry season), the recorded dengue cases were 10 at the end of week 2. In 2018, following prolonged rainfall in weeks 4–5, 10 dengue cases were reported in week 6 compared to lower numbers in the dry season weeks following low or no rainfall. In some years, a relatively high number of cases were also observed in the first six weeks of the year, which is in the dry season. Within that period, 42 cases were recorded in 2012, 35 in 2014, 23 in 2018, and 16 in 2019 (Fig 6).
Statistical relationship between rainfall and dengue cases
Table 3 shows the results of statistical analysis testing the relationship between rainfall and dengue cases in Grenada. With each unit decrease in rainfall between the category 271–300 mm and 1–30 mm, the incidence rate ratio (likelihood) of dengue cases decreased by a factor of .108 (89.2%). This difference was also statistically significant (p = .031). A statistically significant relationship was not found for differences in dengue cases with unit decrease in rainfall between 271–300 mm and 31-60mm. The likelihood of dengue cases was lowest with unit decrease in rainfall between 271–300 to 150–180 mm.
A statistically significant relationship was not found between dengue cases and rainfall with temperature included as a covariate. There were also minimal changes in the incidence rate ratio (Exp B) values. Nonetheless, there was a 4.4% increased likelihood of dengue cases at 26 Celsius compared to 27–28 Celsius. Table 4 shows the parameter estimates from the regression analysis.
Discussion
This study was conducted to determine the pattern of dengue cases across seasons and the relationship between dengue cases and rainfall in Grenada. A weak but significant relationship was found between rainfall and dengue with a greater likelihood of cases with increasing rainfall. With each unit decrease in rainfall between the category 271–300 mm and 1–30 mm, the incidence rate ratio (likelihood) of dengue cases decreased by a factor of .108 (89.2%). The findings of a weak correlation that is statistically significant means that rainfall influences the incidence of dengue cases although other factors may also be important determinants of cases. Grenada has two defined seasons- the wet season from June to December and the dry season from January to May. Generally, a higher number of cases were reported in the months typical of the wet season within respective years. In some years, higher numbers of cases were also recorded with lower rainfall and during the typical dry season. Typically, an increase in dengue cases was noted following prolonged rainfall. The patterns suggest that dengue cases are likely to peak, even during dryer years,—but with sporadic heavy rainfall. In some years, the meteorological data did not show excessively higher rainfall during the typical rain season months.
When temperature was added as a covariate, there was a slight increase in the effect of rainfall on dengue cases. Temperature adjustment favors mosquito reproduction. In suitable conditions, female mosquitoes lay approximately 100 eggs which develop into mature adults in about 3–4 days [21]. While literature shows the tendency of increasing mosquito population with warmer temperature, this study found a greater likelihood of dengue cases in cooler temperature. Further studies should be conducted to explain this outcome and its uniqueness to Grenada.
The absence of a dengue vaccine highlights the need for interventions to control mosquito population [22]. Vector control interventions should target both the elimination of breeding sites and adult mosquitoes. Building homes with white-washed interior walls, installation of door and window screens and burning powders such as pyrethrum can help to control mosquito habitation and reproduction in buildings and in communities environs [23]. Drainage of aquatic habitat, vegetation clearance, and modification of river boundaries are also effective strategies to reduce mosquito population [23].
Other factors may explain the pattern of reported dengue cases in Grenada. The first COVID-19 case was reported in March 2020, resulting in an immediate island-wide lockdown from March to May and with continuing lockdowns and restrictions on movement throughout the year. Vector control interventions were disrupted during the lockdown period. In addition to lack of control measures, the restricted movement and rainfall may have provided favorable conditions for the surge in dengue cases, particularly in the latter half of that year.
In 2014–2015, there was a chikungunya outbreak in Grenada which led to the implementation of rigorous vector control measures. The first case of chikungunya in the country was recorded in July 2014 with the onset of the outbreak coinciding with the rainy season which runs from June to December [24]. In that year, at least 60 percent of the Grenadian population was estimated to have been affected, with the virus spreading rapidly within 3 months of the first recorded case on the island [25]. With both dengue and chikungunya cases rising, the Vector Control Unit in the Ministry of Health needed to implement aggressive measures to control the mosquito population. The reported dengue cases in the following year 2015, compared to 2020, showed a vast difference. In 2015, following vector control interventions in 2014, only 7 dengue cases were recorded which was 78 times lower than the number of cases recorded in 2020 when measures were restricted. This difference is suggestive of the importance of the role of the Vector Control Unit in the management of dengue. The sharp increase in dengue cases in 2020 may also be explained by the introduction of testing at the General Hospital from October 2020 [26]. Fig 1 shows the increase in dengue cases in the latter part of the year. It was noted that in other years, an increase in the number of reported cases did not necessarily coincide with increased rainfall. Two factors may explain high number of cases in the drier years—frequent sporadic heavy rainfall and poor water storage practices in dry season. In a study done in Grenada and published in 2005, it was found that there was a lack of knowledge of the relationship between mosquitoes, human behavior and the transmission of dengue [27]. Public education can have significant positive influence on behaviors and attitudes.
Several communities in Grenada are located near to or immersed in forested areas, close to water bodies, dumps/garbage collection sites, or have derelict buildings and vehicles, etc. which environments provide suitable natural breeding habitats for mosquitoes. Micro-habitats, created in urban areas, in particular, also encourage high mosquito density and disease transmission [28]. Communities that are characterized by these environments should be primary targets for mosquito control interventions. In the Caribbean region, events of heavy rainfall may occur repeatedly in the same year, increasing the risk of epidemics of new and emerging VBZD [29]. The occurrence of adverse events, such as hurricanes and storms, poor infrastructure and population mobility also influence mosquito population and dengue transmission [13,30–32]. The relationship between population mobility, relative to space/distance and time, and the implications for dengue and other infectious diseases transmission need to be better studied, particularly, within the context of Caribbean societies.
Rainfall data was collected at the Maurice Bishop International Airport Meteorological Office located in the south of the island. The southern part of the island is typically drier than other parts of the island and the mountainous central areas. This means that the rainfall data is not necessarily reflective of the situation across the island, and this may also have implications for understanding the relationship between rainfall and dengue cases in the various communities. The recent introduction of weather monitoring sub-stations across the island in 2020 can enhance capacity to monitor the impacts of weather on infectious disease outbreaks and transmission at the local level.
The Global Climate Models (GCMs) suggest that the annual mean rainfall would drop by 2% by the mid-2020s [33]. The Regional Climate Models (RCM) project that by the end of the 21st century, the Caribbean region, specifically the southern and central basin, would be warmer and drier, with a decrease in rainfall by 25–30% and it is projected that drying conditions would occur between May to October [27]. The impact of weather variability on dengue and other VBZD will need to be monitored to better understand the public health implications for Caribbean people. Further studies are also needed to better understand the relationship between transmission of VBZD and other environmental and socio-economic factors.
Three interventions may be of critical importance for the management of dengue in Grenada. Firstly, the application of the precautionary principle during both wet and dry seasons. Swei et al. found that land use patterns had strong influence on caseloads, accounting for about 26% of all VBZD [34]. In the Grenada context, community sanitation, settlement density, and water management in the natural and built environments may be worth addressing in comprehensive national prevention programs. The settlement of water must be controlled despite indications from studies of possible washout and mortality of larvae during periods of prolonged and high rainfall [17]. Thirdly, while some communities have already been categorized as high-risk for dengue based on mosquito population/larval density, attention should also be given to the distribution of other mediating factors, particularly of a socio-economic nature. This approach may lead to identification of other at-risk communities for targeting disease prevention programs.
Conclusion
The findings from this study show the relationship between dengue cases and rainfall in Grenada during the period 2010–2020. This study shows a weak but statistically significant relationship between dengue cases and rainfall. Temperature contributed to slightly higher incidence of dengue with unit change in rainfall. The total dengue cases reported in the wet season was generally higher in comparison to the dry season. However, the data also shows that rainfall was not consistently higher during the typical rainy season months. It was noted that higher precipitation does not absolutely result in an increase in dengue cases which is suggestive of other factors influencing cases in Grenada. Two factors may explain the high number of cases in the drier years: frequent sporadic heavy rainfall and poor water storage practices. Reporting can be influenced by surveillance, based on the Ministry’s capacity, public sensitization and motivation to report, or actual increase in cases in the specific year. Nonetheless, the analysis highlights the importance for the Ministry of Health’s to implement all-year programs to address dengue. Further studies are also needed to identify and understand other factors influencing VBZD in Grenada.
Supporting information
S1 Data. Combined meteorological and dengue data file.
https://doi.org/10.1371/journal.pclm.0000122.s001
(XLSX)
Acknowledgments
The authors extend thanks to the Ministry of Health in Grenada for providing the data on dengue cases and the Meteorological Office at the Maurice Bishop International Airport in Grenada for providing the rainfall and temperature data. Special thanks is also extended to Mr. Imi Chitterman for assisting with the data analysis.
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