Dengue in Latin America – A unique situation
Dengue in Latin America – A unique situation?
Jaime R. Torres R.
Tropical Medicine Institute, Infectious Diseases Section, Universidad Central de Venezuela, Caracas, Apartado 47019, Caracas 1041-A
e-mail addresses: torresj@; carlos@
Overview
Although known to cause large outbreaks in the Caribbean since the first half of the XVII century, and continental epidemics or true pandemics along all XIX and XX centuries, dengue virus was isolated for the first time in the Americas in 1942. 1,2 The first large epidemic of dengue hemorrhagic fever (DHF) in the region occurred in Cuba in 1981, with 24,000 cases of DHF and 10,000 cases of dengue shock sindrome (DSS) and 158 deaths reported during a 3-month period. 1,2,3,4 In 1986 and 1987 massive outbreaks of dengue fever (DF) were reported in Brazil. 5,6 Subsequent serologic investigations in the same country estimated almost 4 million cases of DF compared with the clinically estimated 1 million.6 In 1988 an outbreak of DF was reported at 1700 m above sea level in Guerrero State, Mexico.7 In 1990 almost one fourth of the 300,000 population of Iquitos, Peru, contracted DF8 and in the same year 3,108 cases of DHF with 78 deaths were reported in Venezuela.9 The last available regional figures, corresponding to the year 2001, indicate the occurrence of 610,625 cases of infection, 15,376 of which were DHF/DSS, with 92 deaths. Several Latin American countries report the concurrent circulation of all four serotypes of the virus. 1
Dengue virus infection is without doubt the most common arthropod-borne disease worldwide in terms of morbidity (en terminos de mortalidad seria malaria) rates with an increasing incidence in the tropical regions of Central and South America.
The widespread distribution and rising incidence of dengue virus infections is related to a wider distribution of A. aegypti and to the increase of population density in many large urban areas. Lack of effective programs to contain the vector, and deterioration of the urban environment are responsible.2,4 However, the reason for the change in Latin America from simple DF epidemics to a severe hemorrhagic disease, often associated with shock, DHF/DSS, is not fully understood. 2,4
Furthermore, increased air travel and hence the spread of the mosquito vector and viremic patients almost certainly facilitates the spread of DF. 10 In the United States, of the 143 persons with laboratory-diagnosed dengue reported to the CDC between 1997 and 1998, a travel history within the 2 weeks before illness, could be collected in 122 persons, indicating that infections probably were acquired in the Caribbean islands (61 cases), Asia (30), Central America (23), South America (4), Africa (3), and the Pacific islands (1). 11
During the last decade, the spread of dengue fever was most dramatic in virtually all Latin American and Caribbean countries infested with Aedes aegypti. A sharp upward trend in the number of cases reported each year, from over 250,000 in the early 1990s to more than 600,000 by the end of the century, has been observed.2 Furthermore, serological surveys suggest the occurrence of millions of such infections.12 In the period between 1968 and 1980 only 60 cases of DHF from 5 countries, were reported in the entire region. However, after its emergence in Cuba in 198113, epidemics or sporadic cases of dengue hemorrhagic fever (DHF) have been reported in at least 25 countries in the Americas.14 Since 1989, when a large epidemic with 2,500 cases of DHF occurred, Venezuela has reported large numbers of DHF cases every year, and in 1995 the country recorded the largest regional outbreak with almost 30,000 dengue cases and 5,000 DHF cases. Although dengue viruses serotypes 1, 2, and 4 were isolated during this epidemic, dengue-2 was by large the predominant serotype.15
Regional Epidemiology
Today dengue and sometimes hemorrhagic dengue affects most of the American continent and several islands of the Caribbean. According to the Pan American Organization of Health (PAHO), dengue transmission has increased significantly in our region in the last the 2 decades (Figure 1). The incidence of the disease in the area has shown cyclic peaks and troughs as of 1980. 1,4,16 The epidemic that happened in Cuba determined the high peak in 1981 (344. 203 cases corresponded to Cuba). The seven-fold reduction (around 50,000 cases) in the incidence of dengue observed immediately after such year must be attributed to the rapid eradication of dengue in Cuba. It is plausible to assume that the alarm caused by this epidemic prompted the adoption of vector control measures in the other countries during the following years to 1981. 16
Overall, between 1995 and 1997, the region experienced an annual increase in DF incidence rate of +12% and +35%, respectively, with a simultaneous increase in DHF incidence rate of +61.87%. Martinica, Trinidad/Tobago, and Cuba experienced a +100% annual increase in DHF incidence rate, followed by Venezuela and Puerto Rico with +73.33% and +61.29%, respectively. 1,16,17
By the year 2000, twenty-seven countries of Central and South America, and the Caribbean, reported dengue transmission, of them, 17 registered cases of hemorrhagic dengue, and 10 registered deaths by DHF. The most affected subregion was South America, and the hardest hit countries Brazil, Ecuador, Colombia, Paraguay, and Venezuela (Table 1). 1,16 More worrisome and remarkable is the trend in dengue hemorrhagic fever incidence that has been observed in the region during the last decade. Since the onset of the epidemic in Cuba in 1981, the incidence of the DHF/DSS remained at negligible levels during 7 years until it suddenly rose again in 1989, due to the second large epidemic of DHF/DSS that this time occurred in Venezuela. Following that year, the number of cases of hemorrhagic dengue reported has been significant, with moderate yearly variations, except for an unusual increase in 1997 (11,645 cases). These variations and the lack of correspondence between the incidence of dengue fever and dengue hemorrhagic fever (See Figure 1) could be due to the intense active monitoring of DHF, as opposite to the passive monitoring normally used for classic dengue.
It must be noted that every 3 to 4 years a reduction in the incidence is immediately followed by 2 or 3 years of increase in the number of reported patients. However, the new peaks of incidence are always higher than those observed in the previous cycle. In the last decade the maximum peaks of incidence were observed in 1987 (134,390 cases), 1991 (157,340 cases), 1995 (284,476 cases) and 1997 (387,459 cases) with an evident tendency to increase. 1,17
The 7 years of low DHF incidence seen between 1982 and 1988 could be related to the absence of virulent strains in the area, as the strain causing the Cuban epidemic in 1981 probably did not circulate in the other countries of the region once the epidemic subsided.15 Recent evidence indicates that since 1989 at least 4 countries of the region (Venezuela, Brazil, Mexico and Colombia), have isolated viral strains of Southeast Asian origin, potentially associated with epidemics of hemorrhagic dengue.16 Is indeed around those years that the incidence of DHF/DSS in the Americas began to steadily increase, until in 2001, when it reached a high of 15,376 DHF/DSS cases out of 610,625 dengue reports in the region. Whereas these numbers are obviously affected by underreporting, they do indicate that dengue and hemorrhagic dengue constitutes an important health problem in the Americas.
Factors such as the unavailability of diagnostic facilities in some countries or delay in the diagnosis, inefficient control programs, as well as deficient epidemiological and entomological surveillance systems, may all play a role in increasing the magnitude of the problem in the area.
In general, relevant risk factors for the occurrence of dengue in a given region are included among the so called macrodeterminants, which in Latin America have been defined as:5, 6-8
-Population growth: The percentage of urban population and the expansion of megacities (10,000,000 of inhabitants or more), are on the increase. It has been estimated that by the year 2020 urban population in Latin America will be about 80% (from 42% in 1954), and by the year 2030 close to 50 % of the population will live in megacities.9,17
The incorporation of more land for food production and the negative impact of indiscriminate deforestation, in combination with a trend towards global warming often creates the conditions for the emergency of vector-borne diseases such as dengue.
-Inadequate and unplanned urbanization: which is almost always accompanied by lacking or inappropriate availability of water for consumption, as well as by an inadequate disposition of liquid and solid residues, poor housing conditions and the presence of abundant vectors. In Latin America this factor is of vital importance due to the constant migration flux from the countryside to the cities in pursuit of better work opportunities and living conditions, supposedly offered by the latter. 9,17
-Migrations: It has been calculated that around 500,000,000 of people cross national borders every year around the world. The reasons for such migrations are varied and go from tourism (425,000,000), that generally entails a lesser health risk, to displacesment by armed conflicts (30,000,000 ) and legal or illegal immigration of workers ( around 70 000 000 ,almost all from Third World countries). In the Americas, the actual impact of migration as a risk factor for the occurrence of dengue, remains to be assessed.10,11.
-Air travels: Along with migrations, the marked increase of aerial trips favors the traffic of dengue virus between endemic areas and other areas free of the disease, due to the arrival of people during the incubation period of the disease (the viremia period might be prolonged and the virus can be detected in blood from two days before the initiation of symptoms to eight days after) and subsequent risk of infection of local mosquitoes, with the consequent development of epidemics. This situation is exemplify by the recent reemergence of dengue fever in Eastern Isle, in Chile.1
-Global warming: many scientists believe that global warming disurbs a delicate equilibrium thus contributingto new epidemics of dengue fever as well as malaria, yellow fever, etc. however, vector borne diseases have a extremely complex ecology and available data is not conclusive regarding the potential role of global warming on diseases such as dengue. Despite the undeniable potentially negative impact of climatic factors on the emergence or reemergence of diseases, the increase of dengue transmission in a given geographic area seems to be rather multifactorial with public health deficiencies, and not climate, playing a key role. This is clearly illustrated by the recent transmission pattern of dengue in the U.S.A./Mexico border.12 In 1995, the Mexican state of Tamaulipas, registered 4,479 cases of dengue, 2,361 of them occurred in Reynosa, a Mexican city contiguous to the city of Hidalgo, in Texas, where only 7 native cases were registered. Whereas these 2 cities have equal climate and ecological conditions, and their population is largely similar in origin, sanitary living conditions and income of the population are markedly different. 12
-Poor sanitary conditions: The main factors directly or indirectly influencing the magnitude of dengue transmission appears to be the low socioeconomic level and poor sanitary conditions of the population. While the other ecological, geographic or climatic factors already mentioned may also play a role, it is clear that underneath almost all the factors favoring emergence of dengue are the consequences of negative human activity, and the social inequalities characteristic of our world today.9,13
-Deterioration of the Public Health Infrastructure: Also contributing to worsen an already bleak situation is the decaying of most regional public health systems and as a consequence of this, of the efficiency of Aedes aegypti control programs, as well as an ineffectual and obsolete sanitary legislation. Besides, due to economic constraints that most Latin American countries face, the health authorities have privileged contingency activities to combat epidemics over prevention measures to avoid them to initiate.
-Introduction of new, more complex secondary vectors: A potential additional risk, is the introduction in the region of Aedes albopictus, an efficient dengue vector in Southeast Asia reported in the continent for the first time in 1985, in the U.S.A.18 This vector has been also detected in several Latin American countries (Mexico, Honduras, Guatemala, Cuba, Dominican Republic, Brazil and Bolivia), although its presence has not yet has been related to the increase in dengue transmission. Of note, Aedes albopictus may act both as an urban and rural vector, is not obligated anthropophilic as A. aegypti and sometimes displaces the latter from its habitat.
An unique epidemiological situation was experienced in Cuba, where two epidemics of DF and DHF occurred 15 years apart, after a period of complete absence of transmission.16,19 The unusual severity of both epidemics could be related to the convergence of several factors, among them: a) both epidemics were produced by the dengue 2 serotype; b) the exposed population involved about 5,000,000 people previously infected during 1977-1978 by the dengue 1 serotype and were therefore at risk of a developing FHD/SCD due to a secondary infection with the dengue 2 serotype. This dengue 1/dengue 2 sequence of infection has been more frequently incriminated in the epidemics of DHF/DSS.19,20 ; c) the estimated index of houses infected with the vector in the affected urban centers was higher than 70% in 1981 and 40% in 1997, which created the conditions for a true epidemic explosion17; d) finally, the dengue 2 strain isolated in the 1981 Cuban epidemic was closely related genetically to a strain originating from Southeast Asia that had not circulated previously in the region, 21 which stopped circulating in the area immediately afterwards. Similar strains were only recognized again one decade later. In fact, another Asian strain, although different from the one involved in 1981, was also isolated during the 1997 outbreak.17,19
At the present time (table 1) the 4 serotypes of dengue virus circulate regularly in the Americas, and at least 14 countries reported the simultaneous presence of more than one serotype in the population Additionally, dengue virus 3 was recently reintroduced in the region after 17 years of complete absence.1 In the year 2001, six countries (Dominican Republic, Ecuador, Panama, Peru, and Venezuela) documented the simultaneous circulation of the 4 dengue virus serotypes. Therefore, the number of countries where more than one viral serotype circulates has steadily increased, which favors the occurrence of more cases of secondary infections, and consequently, increase the risk of DHF/DSS.
Is clinical expression of the disease in the region any different?
In contrast with observations from Asian countries, where DHF is almost completely restricted to young children, in the Americas older age groups are widely involved.6,19,22,23,24,25,26.27,28,29 For example, during the Venezuelan outbreak of 1989, about one third of the deaths were among patients over 14 years of age, while in the 1997 Cuban outbreak, all of the deaths were among adults.22 More over, in Puerto Rico, in 1990-91 the reported mean age of the patients was 38 years23, and during the 1981 Cuban outbreak of DHF/DSS, the frequency of DHF/DSS was higher among female adults.22 Of note, an increase in the percentage of DHF cases in individuals over 15 years of age has been noticed in Malaysia and the Philippines during recent years30; however, young children continue to be the age group predominantly affected.29,30
Many potential factors may influence the type and severity of disease arising out of any epidemic of dengue.23 The host immune response appears to be a major factor. Sequential infection with different dengue viral serotypes in the presence of non-neutralizing antibodies has been strongly incriminated in the occurrence of DHF/DSS22,23,24, and cases of DHF/DSS are seldom documented in patients with primary infection.25,26,27,28 Individual factors, such as age, sex, genetic background, and underlying diseases, may also play a role.22,24,25,28
Severity of the dengue virus infection appears to be influenced by race. For instance, white individuals in Cuba were affected more significantly than blacks and mulattos by FHD/SCD in both recent outbreaks. 17,19,22 Unlike most Latin American countries, Cuba has a predominance of whites, blacks and mulattos in its population, and lack Amerindians or mestizos, since native population was completely exterminated during colonial time.
As epidemics progress, some Latin American countries have recorded a significant steady increase in the proportion of total cases presenting as DHF or DHF/DSS, and in case-fatality rates for both DF and DHF/DSS. 31 Such increases has been explained by the fact that a part of the population of antibodies against a dengue virus serotype raised after natural prior primary infections react with "neutralization" determinants found on a different serotype. These heterotypic antibodies do not prevent a secondary dengue infection, but serve to down-regulate the disease to mild illness or symptomless infections. Nevertheless, a subpopulation of the new viral serotype that replicates in the hosts immune to the preceding serotype may escape heterotypic neutralization. When inoculated into a new host immune to the prior serotype, these viruses are free to interact with the more abundant infection-enhancing antibodies, thus producing severe disease. 31
Adults seem less likely than children to suffer from DSS. Indeed, in a retrospective study of 108 adult Malaysians with DHF, the overall morbidity was significant (29.4%) but the case fatality rate remained low (2.0%). The lowest platelet level occurred on day 6 of the fever. Hyponatremia was observed in 46.8% of the cases. 32
Some clinical manifestations of dengue in adults differ from those usually described in children. For instance, hepatomegaly is found in only 10.5% of adults, as compared to more than 70% in children.33,34
Unlike children, many adults with dengue show severe bleeding of GI, or of other sites, preceding the shock, which may be severe enough to cause death.35,36 Liver necrosis may be severe and has been observed in fatal cases among children and adults, both in primary and in secondary infections. 23,24,37
Of note, about 10% of 97 Venezuelan adults with dengue recently studied by us (Torres JR, et al. unpublished data) developed acute acalculous cholecystitis (AAC), according to clinical and ultrasonographic criteria. The latter included: enlarged gallbladder with thickened wall (( 6 mm) and pericholecystic fluid appearing as a halo, tenderness to palpation with the ultrasound probe, or the presence of a diffuse, homogeneous, non-shadowing, medium level echogenicity within the gallbladder lumen, were all considered "positive" findings.38 Whereas patients AAC exhibited a statistically significant increase in the level of peripheral blood leukocytes, clinical outcome appears not to differ from that of patients without AAC in terms of length of clinical interval prior to admission and hospitalization, or the occurrence of other life-threatening complications. Details of our findings on this newly recognized condition, will be discussed elsewhere.
Only scattered reports exist in the medical literature on the pathological and clinical implications of AAC complicating adults with DHF. 40,41,42,43 However, recent data in children with DHF suggests that a gall bladder wall thickening ≥ 5 mm on ultrasonography correlates with a higher risk of hypovolemic shock,39
The relatively common occurrence of dengue virus infection among adults in the region allows for the recognition of some complications of the disease harder to be noticed in affected children. This is the case of the recent description by us of acute bilateral parotitis.43 More over, clinical experience continues to accumulate on the impact of coinfection with dengue virus and other endemic agents present in the area, such as Paracoccidioides braziliensis, Histoplasma capsulatum, Leishmania spp, etc.2
In conclusion, DHF/DSS continues to occur in the Americas in a significant number of adults, but it is not clear whether this relates with the genetic background of the populations, epidemiological events, or else, with other unknown factors.
Regional health Impact and perspectives for control
Little information exists on the impact of dengue in the region in terms of disease burden. Based on the experience in Puerto Rico, using disability-adjusted life years (DALYs) as a means of assessing the economic impact of dengue, dengue was found to cause the loss of an average of 658 DALYs per year per million population.43 It has been estimated that the loss to dengue is similar to the losses per million population in the Latin American and Caribbean region attributed to any of the following diseases or disease clusters: the childhood cluster (polio, measles, pertussis, diphtheria, tetanus), meningitis, hepatitis, or malaria. The loss is also of the same order of magnitude as any one of the following: tuberculosis, sexually transmitted diseases (excluding human immunodeficiency virus), tropical cluster (e.g., Chagas' disease, leishmaniasis), or intestinal helminths.42 These results suggest that when resources for research and control are allocated regionally, dengue should be given a priority equal to many other infectious diseases that are generally considered more important.
The current situation of DF and DHF in the region remains alarming and since most of the factors conditioning the emergency of dengue do not have real possibilities to disappear in the short term, perspectives for its control appear unrealistic. As availability of an effective vaccine against dengue is still remote, the only practical alternative for the control of the disease at the present time is by means of costly programs aimed to reduce the presence, and if possible, eradicate the vector from heavily infested urban areas. 44
Indeed, in the 1950s and 1960s PAHO lead an initially successful continental campaign aimed to avoid the risk of urban yellow fever through the eradication of Aedes aegypti, Unfortunately, less than twenty years later, distribution of the vector in the region was basically similar to that observed before the campaign. 2, 12, 16
The application of vector control methods, including source reduction, use of chemical larvicides and adulticides and of biological control agents is hampered by weak programs capacity, the absence of well-defined indicators and program targets, and poor understanding of efficacy and cost-effectiveness of control measures, particularly in terms of reducing transmission. Major epidemiological and operational research challenges are a better understanding of virus transmission dynamics and the identification of transmission thresholds. 45
A key factor to be considered in any control program requiring a strong social participation component is "behavior change". As in other parts of the word, dengue prevention and control programs in the Americas have traditionally relied upon educational approaches, on the premise that knowledge would lead to behavior change.12, 16 However, experience with this and similar programs, such as HIV and diarrheal diseases prevention and control, have demonstrated that a poor correlation exists between knowledge improvement and behavior change. Hence, emphasis must be shifted to the development of behavior change interventions. For this purpose, ministries of health and the communities, need to develop stronger links both among themselves and with other key partners, in order to achieve a sustainable reduction in the risk of infection and burden of disease.
PAHO reported that in 1995, only about US$ 104,000,000 were spent in dengue control activities in the Americas. 44 This amount is clearly insufficient for that purpose. Therefore, unless significantly larger resources are allocated and more aggressive and effective vector control measures carried out, the countries of the region will continue to face repeated epidemics of dengue, and as a consequence, an increased danger of DHF epidemics.
References
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Table 1. Dengue cases reported in the Americas, according to country, type of disease and when available, serotype of the virus isolated. PAHO, 2000-2001
|Country |DF and/or DHF incidence 2000 |DF and/or DHF incidence 2001 |
| |(Jan. 1-Dec.31, 2000) |(reported from Jan. 1-Dec. 31, 2001) |
|Argentina |1,700 DF cases |11 DF cases |
|Bolivia |73 DF cases |31 DF cases |
| |Serotypes 1 and 2 |Serotype 1 |
|Brazil |210,289 cases, including 40 DHF cases |390,701 DF cases, including 675 DHF cases |
| |Serotypes 1 and 2 |Serotypes 1, 2 and 3 |
|Colombia |10,934 cases, including 803 DHF cases |17,732 DF cases, including 1,739 DHF cases |
| | |Serotypes 2 and 4 |
|Costa Rica |2,313 DF cases |9,007 DF cases, inlcuding 34 DHF cases |
| | |Serotype 2 |
|Cuba |0 cases |1,303 DF cases |
|Dominican Republic |3,310 cases, including 55 DHF cases |719 DF cases, including 4 DHF cases |
| |Serotypes 1, 2, 3 and 4 | |
|Ecuador |21,031 DF cases |10,919 cases, including 55 DHF cases |
| |Serotypes 1, 2, 3 and 4 |Serotypes 2 and 3 |
|El Salvador |2,898 cases, including 324 DHF cases |594 DF cases, including 8 DHF cases |
| |Serotype 2 |Serotype 2 |
|Guatemala |8,750 cases, including 42 DHF cases |4,274 DF cases, including 4 DHF cases |
| |Serotype 2 |Serotypes 2 and 4 |
|Haiti |No data is available. |No data available |
|Honduras |13,350 cases, including 296 DHF cases |8,953 DF cases, including 421 DHF cases |
|Mexico |2,186 cases, including 34 DHF cases |5,900 DF cases, including 191 DHF cases |
| |Serotypes 1, 2 and 3 | |
|Nicaragua |6,220 cases, including 507 DHF cases |666 DF cases, including 81 DHF cases |
| |Serotypes 2 and 4 |Serotypes 2 and 3 |
|Panama |253 cases, including 2 DHF cases |1,431 DF cases, inclduing 7 DHF cases |
| |Serotypes 1, 2, 3 and 4 | |
|Paraguay |24,282 DF cases |38 DF cases |
| |Serotype 1 |Serotypes 1 and 2 |
|Peru |2,912 DF cases |22,847 DF cases, including 251 DHF cases |
| |Serotypes 1 and 2 |Serotypes 1, 2, 3 and 4 |
|Puerto Rico |2,267 DF cases |5,233 DF cases, including 36 DHF cases |
| |Serotypes 1, 2 and 3 |Serotypes 2 and 3 |
|Venezuela |20,771 cases, including 2,154 DHF cases |82,036 DF cases, including 6,417 DHF cases |
| |Serotypes 1, 2, 3 and 4 |Serotypes 1,2, 3 and 4 |
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