Potential influence of climate variability on dengue incidence registered in a western pediatric Hospital of Venezuela, AD Herrera

Tags: dengue cases, dengue, Venezuela, PLoS Neglected Tropical Diseases, incidence, dengue incidence, El Ni, dengue fever, increase, dengue viruses, Emerging Infectious Diseases, International Journal of Environmental Health Research, climate variability, Travel Health, Lancet Infectious Diseases, Salud Publica de Mexico, Revista Panamericana de Salud Publica, International Health, dengue transmission, REFERENCES Barrera, European Congress, climate changes, Tropical Medicine, Climatological variables, Environmental Health Perspectives, Memorias do Instituto Oswaldo Cruz, Mediterranean Conference, global climate change, Chiaravalloti Neto, Tropical Medicine & International Health, climatic variables, Universidad Centro-Occidental Lisandro Alvarado, Los Andes University, Luis Razetti Medical School, Caracas, Venezuela, Barquisimeto, Venezuela, Central University of Venezuela, pediatric Hospital, Trujillo, Venezuela 3 Public Health Division, Hospital Agustin Zubillaga, temperature, climatic variability, microclimatic conditions, The Department of Epidemiology, epidemiological data, weekly basis, mosquito development
Content: Tropical Biomedicine 27(2): 280­286 (2010)
Potential influence of climate variability on dengue incidence registered in a western pediatric Hospital of Venezuela
Aura D. Herrera-Martinez1* and Alfonso J. Rodrнguez-Morales2,3 1 Pediatric Hospital Agustin Zubillaga, Universidad Centro-Occidental Lisandro Alvarado, Barquisimeto, Venezuela 2 Experimental Institute JWT, Los Andes University, Trujillo, Venezuela 3 Public Health Division, Luis Razetti Medical School, Central University of Venezuela, Caracas, Venezuela * Corresponding author email: [email protected] Received 21 November 2009; received in revised form 23 March 2010; accepted 26 April 2010
Abstract. Climate Change and variability is affecting human health and disease direct or indirectly through many mechanisms. Dengue is one those diseases that is strongly influenced by climate variability. In this study we assess potential associations between macroclimatic variation and dengue cases in a western pediatric hospital of Venezuela in an eight-year period. Between 2001 and 2008, 7,523 cases of dengue were reported in the Hospital Agustin Zubillaga, Barquisimeto, Venezuela. Climatic periods marked a difference of 23.15% in the mean incidence of cases, from El Niсo weeks (-14.16% of cases below the mean incidence) to La Niсa months (+8.99% of cases above it) (p=0.0001). Linear regression showed significantly higher dengue incidence with lower values of Oceanic Niсo Index (ONI) (El Niсo periods) and lower dengue incidence with higher values of ONI (La Niсa periods) (p=0.0002). As has been shown herein, climate variability is an important element influencing the dengue epidemiology in Venezuela. However, it is necessary to extend these studies in this and other countries in the region, because these models can be applied for surveillance as well for prediction of dengue.
INTRODUCTION Dengue fever is one of the most important viral diseases in the world. Dengue viruses are among the most widely distributed and significant arthropod-borne viruses (Arboviruses) affecting humans. Their predominant mosquito vector, Aedes aegypti, is endemic at most of the tropical and subtropical regions of the world. There, they can cause seasonal epidemics of varying populational size (Johansson et al., 2009). Global emergence and resurgence of dengue can be attributed to multiple factors including urbanization, transportation and changes in human migration and behavior, resulting in dengue increase as the second most important vector-borne disease, after
malaria, in terms of human morbidity and mortality (Gubler, 1998; Mackenzie et al., 2004). It has been estimated that each year 50 to 100 million people suffer from dengue and that two-fifths of the human population are at risk. Geographical distribution of dengue and the potential occurrence of lifethreatening dengue hemorrhagic fever (DHF) have expanded dramatically in recent decades (Guzman & Kouri, 2002). Part of this disease expansion is due to societal changes such as population growth, urbanization, transport development and changing habitats and behavior that can increase the risk of disease (Patz et al., 2000; Guzman & Kouri, 2002; Hales et al., 2002; Brunkard et al., 2008).
These complex interacting factors can be also influenced by climate, as the ecological niches of the vector, Ae. aegypti, can be favoured and then its population able to transmit disease can increase significantly. Different studies have implied that cold temperature can limits its lifecycle, then acting as an influencing factor on its distribution (Beebe et al., 2009). Then increases in temperature, as well global warming, can potentially increase mosquito populations and dengue incidence (Reiter, 1996; Hsieh & Chen, 2009). This has been particularly influenced in South America by the El Niсo Southern Oscillation (ENSO) phenomena. This climatic anomaly consisted of a periodic change in the atmosphere and ocean conditions in the tropical Pacific region. It is manifested in the atmosphere by changes in pressure and in the ocean by warming or cooling of water surface at the tropical Eastern Pacific Ocean. El Niсo is the name given to the period when water in that region is warmer than normal (means) while La Niсa is the period when is colder than normal (Brunkard et al., 2008). In countries with tropical temperatures, such as Venezuela, this has been previously reported (Rifakis et al., 2005). However, given the incidence of dengue, its increase and its multiple consequences in this as in other Latin American countries, particularly due to several epidemics of DHF since 1989 (Barrera et al., 2000), surveillance and studies reporting on the potential influence of climate variability on dengue incidence are of utmost importance. For these reasons in this study we assess potential associations between macroclimatic variation and dengue cases in a western pediatric hospital of Venezuela in an eight-year period. MATERIALS AND METHODS Pediatric Hospital Agustin Zubillaga, Barquisimeto, Lara state, Western Venezuela, is a pediatric hospital of the Lara
state (the main). The Department of Epidemiology is in charge of surveillance and laboratory confirmatory follow-up of all patients suspected with dengue. This is registered in a weekly basis. For this study, the epidemiological data was constituted by all the weekly records of confirmed dengue cases in children (<18 y-old) from the epidemiological records were collected for the period 2001-2008. Diagnosis was initially clinically made and then serologically (ELISA) and virologically (viral isolation) confirmed by the reference public health laboratory system, according to the national control program for dengue fever of the Ministry of Health. The climatic data was based on one global macroclimatic index, the Oceanic Niсo Index (ONI), classifying the climatic periods according to National Oceanographic and Atmospheric Administration (NOAA, USA) classification, and months were categorized as El Niсo, Neutral and La Niсa to establish differences in the dengue incidence according those periods. Statistical analysis Descriptive statistics were generated for the epidemiological and climatic data (means, standard deviations, SD). Qualitative and quantitative comparisons were made for climatic periods. Linear regression models were used for determining potential associations. Statistical significance was defined as p <0.05. Statistical analyses were performed on GraphPad Prism v.4.0®. RESULTS During the study period (2001-2008) 7,523 cases of dengue were diagnosed and reported. The mean number of dengue cases per year was 940±353 (±SD), while the mean number of dengue cases per week was 18±11 (range 0-68 cases/week). These weekly variations generated different endemic levels for the year 2008. In this year 5 weeks were located at epidemics level compared with the
previous 7 years, which allowed to build the weekly endemic levels (0+DE [blue], 0 [pink] and 0-DE [green]) (Figure 1). During the considered climatic periods a net difference of 23.15% was observed in the mean incidence of cases, from El Niсo weeks (-14.16% of cases below the mean incidence) to La Niсa months (+8.99% of cases above the mean incidence) (2=31.15; p=0.0001) (Figure 2). Linear regressions between the ONI index and the dengue incidence showed a significant association. With higher values of ONI (above 0, El Niсo periods) lower incidence of dengue was observed and with lower values of ONI (below 0, La Niсa periods) higher incidence of dengue was observed (r2=0.032; F=13.79; p=0.0002) (Figure 3). DISCUSSION El Niсo Southern Oscillation (ENSO) is considered a periodic change in the atmosphere and ocean of the tropical Pacific region, manifested in the atmosphere by changes in pressure and in the ocean by warming or cooling of sea surface at the tropical Eastern Pacific Ocean. Two main phases constituted the phenomena of ENSO, El Niсo, the period
when water in that region is warmer than the means (of the temperature during the previous period) while La Niсa is the period when the water is colder than the means (of the temperature during the previous period). These periods could be measured by the Oceanic Niсo Index (ONI), positives values indicate El Niсo phase and negative values La Niсa phase. Usefulness of this index in the context of climate variability impact on dengue has been previously reported by us (Rifakis et al., 2005). We found that the highest case increase was significantly associated with La Niсa. Linear regression models found a statistically significant association between dengue fever and rainfall abnormalities in Caracas (p=0.0319), as well with temperatures (p=0.0001) (Rifakis et al., 2005). Results in the current study evidenced associations between climatic conditions and dengue epidemiology in Barquisimeto, Venezuela, which was reflected with a higher number of dengue cases in the pediatric hospital of the region when La Niсa period was predominant. This would be explained by the existence of environmental conditions influenced by that macroClimatic Change favorable for Ae. aegypti reproduction, particularly in the context of urban climatic change (Sutherst, 2004). La Niсa in this region of Venezuela
Figure 1. Endemic levels for dengue fever at the Pediatric Hospital, 2008 (endemic levels were calculated with the last previous 7 years, 0+DE [blue], 0 [pink] and 0-DE [green]) 282
Figure 2. Difference in the mean incidence of cases, from El Niсo and La Niсa months and weeks Figure 3. Linear regression between ONI and dengue incidence variations in the Pediatric Hospital, Barquisimeto, Venezuela, 2001-2008 283
influenced microclimatic conditions such as increase in the rainfall, humidity and lowering temperatures. This increase the collections of water at any type of waterholding container in urban settings (tree holes or leave as well man-made cisterns, discarded bottles and tires, tree holes or leave as well man-made cisterns, discarded bottles and tires), which are suitable for disposal of eggs of A. aegypti, then making those favorable conditions for more breeding habitats for the mosquito, then increasing the available population to vector dengue viruses. Man-made habitats are abundant near urban populations, where food supply (human blood) for gravid female mosquitoes is also plentiful. In these environments, climatic variables such as temperature, humidity, and precipitation during La Niсa in Barquisimeto significantly influence mosquito development and survivorship (Watts et al., 1987). From those climatic variables, temperature is crucial. It affects the rate of development in different mosquito life stages, as well as dengue viral development (Thu et al., 1998). Different studies have shown that mosquito survival rates are temperature dependent. Additionally, humidity and in general the presence of water is necessary for egg laying and hatching and for larval survivorship, and relative humidity affects adult mosquito mortality. Herein we have found that changes in microclimatic conditions at those urban niches where Ae. aegypti can develop, can be affected by changes in macroclimatic conditions such as global climate change and global climate variability. Several studies have predicted that global climate change could increase the incidence of dengue epidemics (Phillips, 2008). An empirical model of worldwide dengue distribution, reported that annual average vapor pressure (a measure of humidity) was the single climate factor that best predicted dengue fever distribution. They also found that if humidity remained at 1990 levels into the next century, a projected 3.5 billion people would be at
risk of dengue infection in 2085, but if humidity increases as projected by the Intergovernmental Panel on Climate Change, 5.2 billion people would be at risk (Hales et al., 2002; Schwartz et al., 2008). Studies in Puerto Rico have concluded that year-to-year variability in dengue cases is positively related to temperature, but only weakly associated with local rainfall and an index of El Nino Southern Oscillation (ENSO) (Jury, 2008), however in our study we found a significant association with the ONI, an index of ENSO. In Mexico a study showed that dengue incidence increases 2.6% one week after every 1 degree Celsius increase in weekly maximum temperature and increased 1.9% two weeks after every 1 cm increase in weekly precipitation (Guzman & Kouri, 2002; Hales et al., 2002). We have previously reported in Venezuela significant associations between dengue epidemiology and climatic variability (Rifakis et al., 2005). In these studies the ENSO cold phase, La Niсa, has been linked to an increased incidence of disease, as occurred in our current study, explained by higher precipitations means as well for a favorable temperatures for vector and transmission. These results linking potential impacts of climate variability with dengue epidemiology should be considered in public health policies, particularly those focused on surveillance, forecast and prediction of disease. In Sгo Paulo, Brazil, research experiences have found that the relation between climatic factors, vector and disease can be employed in planning and undertaking dengue surveillance and control activities (Dibo et al., 2008). In fact, that relationship allows the use of climate information for early detection of epidemics. This will allow more effective prevention strategies than currently exist (Depradine & Lovell, 2004). Despite the limitations of our study (e.g. lack of local temperature, rainfall and humidity data), results show that in this 8year study more than 14% of reduction of disease mean incidence is observed during
El Niсo (dry season), and with La Niсa (wet season) almost 9% of increase is observed. Furthermore, is necessary to extend the deepness of these studies in this and other countries in the region, because these models can be applied to surveillance data for predicting trends in dengue incidence. Acknowledgements. This work was previously presented in part as a poster at the 6th European Congress on Tropical Medicine and International Health and 1st Mediterranean Conference on Migration and Travel Health. Verona, Italy. September 6-10, 2009. Poster No. 4.4-016. REFERENCES Barrera, R., Delgado, N., Jimenez, M., Villalobos, I. & Romero, I. (2000). Stratification of a hyperendemic city in hemorrhagic dengue. Revista Panamericana de Salud Publica 8: 225­233. Beebe, N.W., Cooper, R.D., Mottram, P. & Sweeney, A.W. (2009). Australia's Dengue Risk Driven by Human Adaptation to Climate Change. PLoS Neglected Tropical Diseases 3: e429. Brunkard, J.M., Cifuentes, E. & Rothenberg, S.J. (2008). Assessing the roles of temperature, precipitation, and ENSO in dengue re-emergence on the TexasMexico border region. Salud Publica de Mexico 50: 227­234. Depradine, C. & Lovell, E. (2004). Climatological variables and the incidence of dengue fever in Barbados. International Journal of environmental health Research 14: 429­441. Dibo, M.R., Chierotti, A.P., Ferrari, M.S., Mendonca, A.L. & Chiaravalloti Neto, F. (2008). Study of the relationship between Aedes (Stegomyia) aegypti egg and adult densities, dengue fever and climate in Mirassol, state of Sao Paulo, Brazil. Memorias do Instituto Oswaldo Cruz 103: 554­560.
Gubler, D.J. (1998). Resurgent vector-borne diseases as a global health problem. Emerging infectious diseases 4: 442­ 450. Guzman, M.G. & Kouri, G. (2002). Dengue: an update. Lancet Infectious Diseases 2: 33­42. Hales, S., De Wet, N., Maindonald, J. & Woodward, A. (2002). Potential effect of population and climate changes on global distribution of dengue fever: an empirical model. Lancet 360: 830­834. Hsieh, Y.H. & Chen, C.W. (2009). Turning points, reproduction number, and impact of climatological events for multi-wave dengue outbreaks. Tropical Medicine & International Health 14: 628­638. Johansson, M.A., Dominici, F. & Glass, G.E. (2009). Local and global effects of climate on dengue transmission in Puerto Rico. PLoS Neglected Tropical Diseases 3: e382. Jury, M.R. (2008). Climate influence on dengue epidemics in Puerto Rico. International Journal of Environmental health research 18: 323­334. Mackenzie, J.S., Gubler, D.J. & Petersen, L.R. (2004). Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nature Medicine 10: S98­109. Patz, J.A., Engelberg, D. & Last, J. (2000). The effects of changing weather on public health. Annual Review of Public Health 21: 271­307. Phillips, M.L. (2008). Dengue reborn: widespread resurgence of a resilient vector. Environmental Health Perspectives 116: A382­388. Reiter, P. (1996). Global warming and mosquito-borne disease in USA. Lancet 348: 622.
Rifakis, P., Gonзalves, N., Omaсa, W., Manso, M., Espidel, A., Intingaro, A., Hernбndez, O. & Rodrнguez-Morales, A.J. (2005). Asociaciуn entre las Variaciones Climбticas y los Casos de Dengue en un Hospital de Caracas, Venezuela, 1998-2004. Revista Peruana de Medicina Experimental y Salud Publica 22: 183­190. Schwartz, E., Weld, L.H., Wilder-Smith, A., Von Sonnenburg, F., Keystone, J.S., Kain, K.C., Torresi, J. & Freedman, D.O. (2008). Seasonality, annual trends, and characteristics of dengue among ill returned travelers, 1997-2006. Emerging Infectious Diseases 14: 1081­1088. Sutherst, R.W. (2004). Global change and human vulnerability to vector-borne diseases. Clinical Microbiology Reviews 17: 136­173.
Thu, H.M., Aye, K.M. & Thein, S. (1998). The effect of temperature and humidity on dengue virus propagation in Aedes aegypti mosquitos. Southeast Asian Journal of Tropical Medicine and Public Health 29: 280­284. Torres, J.R. & Castro, J. (2007). The health and economic impact of dengue in Latin America. Cadernos de Saude Publica 23 Suppl 1 S23­31. Watts, D.M., Burke, D.S., Harrison, B.A., Whitmire, R.E. & Nisalak, A. (1987). Effect of temperature on the vector efficiency of Aedes aegypti for dengue 2 virus. American Journal of Tropical Medicine and Hygiene 36: 143­152.

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