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    Map of the study areas in Iquitos. Locations of schools and study neighborhoods are marked.

  • 1

    Gubler DJ, 2004. Cities spawn epidemic dengue viruses. Nat Med 10 :129–130.

  • 2

    Gubler DJ, 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10 :100–103.

    • Search Google Scholar
    • Export Citation
  • 3

    Gubler DJ, 1998. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11 :480–496.

  • 4

    Gubler DJ, 1998. The global pandemic of dengue/dengue haemorrhagic fever: current status and prospects for the future. Ann Acad Med Singapore 27 :227–234.

    • Search Google Scholar
    • Export Citation
  • 5

    Phillips I, Need J, Escamilla J, Colán E, Sánchez S, Rodríguez M, Vásquez L, Seminario J, Betz T, da Rosa AT, 1992. First documented outbreak of dengue in the Peruvian Amazon region. Bull Pan Am Health Organ 26 :201–207.

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  • 6

    Hayes CG, Phillips IA, Callahan JD, Griebenow WF, Hyams KC, Wu SJ, Watts DM, 1996. The epidemiology of dengue virus infection among urban, jungle, and rural populations in the Amazon region of Peru. Am J Trop Med Hyg 55 :459–463.

    • Search Google Scholar
    • Export Citation
  • 7

    CDC, 1991. Dengue epidemic—Peru, 1990. MMWR Morb Mortal Wkly Rep 40 :145–147.

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    Watts DM, Porter KR, Putvatana P, Vasquez B, Calampa C, Hayes CG, Halstead SB, 1999. Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet 354 :1431–1434.

    • Search Google Scholar
    • Export Citation
  • 9

    Kochel TJ, Watts DM, Halstead SB, Hayes CG, Espinoza A, Felices V, Caceda R, Bautista CT, Montoya Y, Douglas S, Russell KL, 2002. Effect of dengue-1 antibodies on American dengue-2 viral infection and dengue haemorrhagic fever. Lancet 360 :310–312.

    • Search Google Scholar
    • Export Citation
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    Gubler DJ, 1989. Surveillance for dengue and dengue hemorrhagic fever. Bull Pan Am Health Organ 23 :397–404.

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    Rigau-Perez JG, Gubler DJ, 1997. Surveillance for dengue and dengue hemorrhagic fever. Gubler DJ, Kuno G, editors. Dengue and Dengue Hemorrhagic Fever. London, UK: CAB International, 405–423.

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    Morrison AC, Gray K, Getis A, Astete H, Sihuincha M, Focks D, Watts D, Stancil JD, Olson JG, Blair P, Scott TW, 2004. Temporal and geographic patterns of Aedes aegypti (Diptera: Culicidae) production in Iquitos, Peru. J Med Entomol 41 :1123–1142.

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  • 13

    Morrison AC, Zielinski-Gutierrez E, Scott TW, Rosenberg R, 2008. Defining challenges and proposing solutions for control of the virus vector Aedes aegypti. PLoS Med 5 :e68.

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  • 14

    Getis A, Morrison AC, Gray K, Scott TW, 2003. Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru. Am J Trop Med Hyg 69 :494–505.

    • Search Google Scholar
    • Export Citation
  • 15

    Mangada MM, Endy TP, Nisalak A, Chunsuttiwat S, Vaughn DW, Libraty DH, Green S, Ennis FA, Rothman AL, 2002. Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai school children. J Infect Dis 185 :1697–1703.

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  • 16

    Endy TP, Nisalak A, Chunsuttitwat S, Vaughn DW, Green S, Ennis FA, Rothman AL, Libraty DH, 2004. Relationship of preexisting dengue virus (DV) neutralizing antibody levels to viremia and severity of disease in a prospective cohort study of DV infection in Thailand. J Infect Dis 189 :990–1000.

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  • 17

    Laoprasopwattana K, Libraty DH, Endy TP, Nisalak A, Chunsuttiwat S, Vaughn DW, Reed G, Ennis FA, Rothman AL, Green S, 2005. Dengue Virus (DV) enhancing antibody activity in preillness plasma does not predict subsequent disease severity or viremia in secondary DV infection. J Infect Dis 192 :510–519.

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  • 18

    Vaughn DW, Green S, Kalayanarooj S, Innis BL, Nimmannitya S, Suntayakorn S, Endy TP, Raengsakulrach B, Rothman AL, Ennis FA, Nisalak A, 2000. Dengue viremia titer, antibody response pattern, and virus serotype correlate with disease severity. J Infect Dis 181 :2–9.

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  • 19

    Endy TP, Nisalak A, Chunsuttiwat S, Libraty DH, Green S, Rothman AL, Vaughn DW, Ennis FA, 2002. Spatial and temporal circulation of dengue virus serotypes: a prospective study of primary school children in Kamphaeng Phet, Thailand. Am J Epidemiol 156 :52–59.

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  • 20

    Endy TP, Chunsuttiwat S, Nisalak A, Libraty DH, Green S, Rothman AL, Vaughn DW, Ennis FA, 2002. Epidemiology of inapparent and symptomatic acute dengue virus infection: a prospective study of primary school children in Kamphaeng Phet, Thailand. Am J Epidemiol 156 :40–51.

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  • 21

    Aguilar PV, Greene IP, Coffey LL, Medina G, Moncayo AC, Anishchenko M, Ludwig GV, Turell MJ, O’Guinn ML, Lee J, Tesh RB, Watts DM, Russell KL, Hice C, Yanoviak S, Morrison AC, Klein TA, Dohm DJ, Guzman H, Travassos da Rosa APA, Guevara C, Kochel T, Olson J, Cabezas C, Weaver SC, 2004. Endemic Venezuelan equine encephalitis in northern Peru. Emerg Infect Dis 10 :880–888.

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    Morrison AC, Astete H, Chapilliquen F, Ramirez-Prada C, Diaz G, Getis A, Gray K, Scott TW, 2004. Evaluation of a sampling methodology for rapid assessment of Aedes aegypti infestation levels in Iquitos, Peru. J Med Entomol 41 :502–510.

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    Schneider JR, Morrison AC, Astete H, Scott TW, Wilson ML, 2004. Adult size and distribution of Aedes aegypti (Diptera: Culicidae) associated with larval habitats in Iquitos, Peru. J Med Entomol 41 :634–642.

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    Comach G, Blair PJ, Sierra G, Guzman D, Soler M, Quintana MC, Bracho-Labadie M, Camacho D, Russell KL, Olson JG, Kochel TJ, 2008. Dengue virus infections in a cohort of schoolchildren from Maracay, Venezuela: a 2-year prospective study. Vector Borne Zoonotic Dis. doi: 10.1089/vbz.2007.0213.

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Comparison of Two Active Surveillance Programs for the Detection of Clinical Dengue Cases in Iquitos, Peru

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  • 1 US Naval Medical Research Center Detachment, Lima and Iquitos, Peru; Department of Entomology, University of California, Davis, California; Hospital de Apoyo, DISA-Loreto, Iquitos, Peru

Endemic dengue transmission has been documented in the Amazonian city of Iquitos, Peru, since the early 1990s. To better understand the epidemiology of dengue transmission in Iquitos, we established multiple active surveillance systems to detect symptomatic infections. Here we compare the efficacy of distinct community-based (door to door) and school absenteeism–based febrile surveillance strategies in detecting active cases of dengue. Febrile episodes were detected by both systems with equal rapidity after disease onset. However, during the period that both programs were running simultaneously in 2004, a higher number of febrile cases in general (4.52/100 versus 1.64/100 person-years) and dengue cases specifically (2.35/100 versus 1.29/100 person-years) were detected in school-aged children through the community-based surveillance program. Similar results were obtained by direct comparison of 435 participants concurrently enrolled in both programs (P < 0.005). We conclude that, in Iquitos, community-based door-to-door surveillance is a more efficient and sensitive design for detecting active dengue cases than programs based on school absenteeism.

INTRODUCTION

Dengue virus is the causative agent of dengue fever and more severe disease manifestations including dengue shock syndrome (DSS) and dengue hemorrhagic fever (DHF). According to WHO estimates, 50–100 million people are infected with dengue virus annually and > 2 billion more are at risk of infection.14 Four serotypes have been identified, all capable of inducing serious illness, particularly in context of secondary infections. In northeastern Peru, dengue virus (DV) transmission has been documented consistently since 1990, beginning with an epidemic of dengue-1 transmission.57 In 1995, American strains of dengue-2 were introduced into the region,8 followed by the more recent emergence of dengue-3 during 2001 as the dominant strain in Iquitos. Despite a large number of secondary infections with a heterologous serotype, DHF has rarely been documented in Iquitos.8,9 Although severe, life-threatening disease is not as common in the region as in other parts of Latin America or Southeast Asia, the large number of debilitating dengue fever cases imposes a heavy burden on the local health system.

Timely and sensitive febrile surveillance programs are the cornerstones of dengue prevention and control programs.10,11 For these programs, national dengue prevention efforts typically rely on passive surveillance, either clinic or hospital based. In contrast, active surveillance strategies must be used in the context of comprehensive longitudinal field studies needed to fill many of the knowledge gaps in dengue epidemiology. For example, such programs are important components of studies examining the relationship between dengue virus transmission patterns and their quantitative relationship to Aedes aegypti population densities.1214 Furthermore, active surveillance theoretically captures fever cases earlier than hospital- or clinic-based programs, enabling detailed immunologic15 and pathogenesis studies, including studies of antibody-dependent enhancement16,17 and variation in DV serotype virulence.18 In addition, inapparent to symptomatic infection ratios are far more reliably calculated from active surveillance programs,19,20 increasing our understanding of pathogenicity associated with specific DV strains and different human populations. Therefore, research using active surveillance will enhance dengue prevention programs through the development of locally adaptable tools and strategies that account for ecologic and epidemiologic differences among sites where DV are transmitted.13

Since 1999, Iquitos has been the site of a series of prospective cohort studies to investigate dengue epidemiology and vector biology. A component of these studies has been the rapid identification and capture of fever cases to characterize dengue disease in the city. To achieve this objective, we implemented two distinct active surveillance systems. The first was established in Iquitos public schools, monitoring school absenteeism among the students. The second was a community-based program, consisting of door-to-door febrile surveillance in study neighborhoods. In this report, we compare the sensitivity and efficiency of the two programs for detecting symptomatic DV infections, including direct comparison of active dengue infection detection among students participating in both surveillance systems concurrently.

MATERIALS AND METHODS

Study site.

The study site has been described in detail elsewhere.6,12,2123 Briefly, Iquitos (3°43 46 S, 73°14 48 W) is a city of ~350,000 residents, located in the northeastern section of Peru, at the confluence of the Itaya, Nanay, and Amazon Rivers. The climate is tropical, with an annual average daily temperature of 27°C and average annual precipitation of 290.3 cm.

Active febrile surveillance programs.

Two distinct active surveillance programs were established in Iquitos, both in tandem with separate longitudinal cohorts established in the context of dengue transmission and vector surveillance studies. Both studies were reviewed and approved by the US Naval Medical Research Detachment Center, University of California—Davis, and Peruvian National Institutes of Health Institutional Review Boards.

First, 4,160 school-aged children (ages 5–17 years; 75% between ages 6 and 12 years), along with members of their families, from a geographically stratified selection of Iquitos (Figure 1) were enrolled into a longitudinal cohort and monitored from January 1999 to August 200312 (ACM, unpublished data). Participant blood samples were collected every 6–9 months and assayed for serotype-specific DV antibody status by plaque reduction neutralization assay (PRNT), according to previously described methods.24 A subset of 1,100 children per year attending any of 29 public schools in the city were recruited from the larger longitudinal cohort into a school-based febrile surveillance program in May 2000. Children were monitored in school daily between April and December each year and during vacation periods (January–March) once per week at their homes. Each year, new children from the larger cohort study were recruited to replace participants who dropped out of the study, changed to night sessions, or changed schools. In August 2003, the larger cohort study ended, but we continued to follow the subset of students enrolled in the school-based study. To bring the cohort number to 1,100 during the final year of the school-based study, additional participants were recruited from households of existing participants and from a second 2004 cohort study described below. During the 4.5-year course of the project, a total of 1,859 participants were enrolled. Ten phlebotomists monitored two to three schools daily each to verify the attendance of the students enrolled in the study. If a child was absent from school, a home visit was made to determine whether the absence was because of febrile illness (≥ 38°C).

A second longitudinal cohort study was established in 24 geographically stratified city blocks (Figure 1), incorporating 2,415 participants from ~800 households and 5,000 residents from April 2004 through December 2005. These blocks were selected based on the residences of participants in the previously established school-based surveillance program. In addition to the longitudinal cohort study, all 5,000 neighborhood residents were invited to participate in a door-to-door febrile illness surveillance program. Health workers (10 phlebotomists in total) visited each residence three times per week to determine whether anyone in the household currently had a febrile illness. Although the school-based and community-based surveillance programs were established independently, students living in study neighborhoods and attending study schools were eligible to concurrently participate in both studies.

On identification of a febrile person in either surveillance program, written informed consent was obtained from adult participants and from the parents of participants younger than 18 years of age, and assent was obtained from participating children. Acute blood samples were drawn at the time of case identification, followed by a convalescent blood sample 14–21 days later. In addition, daily medical exams and tourniquet tests were performed, starting on the day of illness detection and continuing until 2 days after defervescence. Acute-phase samples were inoculated onto C6/36 cells for virus isolation,25 whereas both acute- and convalescent-phase samples were assayed for dengue-specific IgM antibodies by antibody-capture ELISA.26,27 Active dengue cases were identified by viral isolation, IgM serology (elevated IgM antibody titers [> 1:400] in the acute sample, convalescent sample, or both), or a 4-fold rise in IgG antibody titers between acute and convalescent samples.

Statistical analyses.

Groups were compared using Pearson’s χ2 test, performed in the R statistical package, version 2.8 (R Development Core Team, Vienna, Austria).

RESULTS

In the 9 months (April 2004–December 2004) that the two programs were operated concurrently, 10 phlebotomists monitored 1,135 students (99.5%, 5–17 years of age) in the school-based surveillance, and 10 phlebotomists monitored 4,850 residents (0–98 years of age) in the community-based surveillance (Table 1). Among the residents of study neighborhoods, 1,537 (31.7%) were school aged (5–17 years), most of whom were not included in the school absenteeism–based program. In total, 14 febrile cases (12.3 cases/1,000 participants; 1.64/100 person-years) were detected in the school-based program, and 110 cases (22.7 cases/1,000 participants, or 3.35/100 person-years) were detected in the community-based program (Table 1). Among school-aged participants in the community, 48 febrile cases were detected (31.2/1,000 participants, or 4.52/100 person-years), a significantly higher ratio than in the school-based system (χ2 = 10.88, P < 0.001). Of the 14 febrile cases detected in the school-based program, 11 were determined to be dengue infections, including 1 by isolation (dengue 3), 9 by IgM serology, and 1 by IgG seroconversion, for 9.7 cases/1,000 participants (1.29/100 person-years). By comparison, in the community, 56 of 110 febrile cases were diagnosed as acute dengue infections; 14 were identified by virus isolation (all dengue 3), 31 were identified by IgM serology, and 11 were identified by 4-fold rise in IgG titers between acute and convalescent samples. Overall for community members, there were 11.5 symptomatic dengue cases per 1,000 participants (1.71/100 person-years), whereas among community-based school-aged participants, there were 16.3 cases per 1,000 participants (2.35/100 person-years). As expected, proportions of non-primary (secondary and tertiary) to primary infection, based on IgM/IgG ratios,28 were higher among adults than children (91% versus 63%; P < 0.05). However, the proportion of secondary and tertiary infections among children in the community cohort (61%) was quite consistent with the results for children detected in the school cohort (64%). Where paired longitudinal cohort samples bookending the study period were available, PRNT analysis largely corroborated the IgM/ IgG results (84.2% agreement).

During the 10 months these programs were simultaneously in operation, 435 participants were concurrently enrolled in both the school-based surveillance and the community-based surveillance programs. Among these 435 participants, febrile cases were more commonly detected in the community-based program than in the school-based program (25 and 6 cases, respectively; χ2 = 10.8, P = 0.001), as were dengue cases in particular (15 and 4 cases, respectively; χ2 = 5.38, P = 0.02). These numbers include two dengue-positive children detected on the same day by both methods, who were thus included in both tallies. It was observed that some children attended school even while febrile; their illnesses were reported by their parents during door-to-door surveillance and were not detected in school.

In the community-based program for the 10 months included in this report, 65.1% of febrile cases were detected on or before the second day of illness (Table 1), and 89.9% were detected by the third day (median: 2 days post-disease onset). In the school-based program, 46.2% of febrile cases were detected on or before the second day of illness and 69.2% before the third day (median: 3 days). This difference in date-of-capture was not statistically significant (P = 0.18). Furthermore, over the entire course of the school-based study (2000–2004), date of case detection (68.4% by second day of disease; 88.9% by third day; median: 2 days) was nearly identical to that of the community-based program.

DISCUSSION

Active surveillance strategies are important components of dengue transmission and pathogenesis studies. School-based surveillance was effective in capturing dengue cases in Kamphaeng Phet, Thailand, where febrile episodes were monitored through student absenteeism and visits to the school nurse.19,20 In addition to school-based studies, active surveillance strategies include self-reporting of enrolled cohort members to study health facilities2931 and work-absence monitoring among factory workers.32 To our knowledge, our study represents the first report of a door-to-door community-based febrile patient capture system for dengue. Despite the need for efficient and sensitive active surveillance systems in advancing our understanding of dengue epidemiology, the relative efficacies of distinct active surveillance strategies have not been directly compared. We found that community-based surveillance provided a viable alternative to school-based surveillance. In our hands, the community-based program captured 2-fold more fever and symptomatic dengue infections relative to study population size than the school-based system while monitoring five times as many people using the same number of personnel and the same amount of resources. We found that in many cases, febrile children did attend school, and their illnesses were detected only when reported by a parent during the home visit. Additionally, community-based surveillance allowed us to identify symptomatic dengue cases in all age groups and was not solely limited to school-aged children.

Several factors, including the research objective, site-specific dengue epidemiology, and cultural characteristics of the study population, will help determine the type of active surveillance system to implement. For example, there are striking differences between Iquitos and the aforementioned Kamphaeng Phet study site. In Kamphaeng Phet, the inapparent to symptomatic dengue infection ratio was low,20 indicating sensitive capture of febrile patients and perhaps more severe disease manifestations. In our cohort, the inapparent to symptomatic dengue infection ratio was ~3:1 during the 10 months of study and even higher during other periods (ACM and TJK, unpublished data). Additionally, Iquitos is an urban city with a much higher population density than the rural villages included in the Kamphaeng Phet study. In Iquitos, students often attended schools away from their neighborhoods (both private and public) or did not attend school at all, both adults and children show clinical manifestations of disease, migration rates by naive individuals from non-endemic riverine communities into the city are high, and DV transmission is more sporadic than the hyperendemic transmission of all four dengue serotypes observed in Kamphaeng Phet. Based on these characteristics, in Iquitos, community-based surveillance has a number of advantages over school-based surveillance.

It should be noted that the two surveillance programs described in this report did not operate entirely independently. Thus, although febrile students were typically enrolled into the program through which they were first detected, phlebotomists from the two programs were occasionally in contact with each other with information regarding a participant’s health, perhaps biasing enrollment into one program or the other. When possible, we noted when febrile children were detected by both programs. There was not a great deal of overlap between the two systems, however, because in many cases febrile children did attend school. Not all children absent from school were detected during household visits, pointing to some limitations of our community-based surveillance. It is possible that febrile cases were missed because of the lack of daily monitoring. Interestingly, daily monitoring of school absence did not constitute an advantage over thrice-weekly home visits in rapidity of case detection, because febrile cases were detected in very similar time frames.

School-based surveillance was not without its advantages. For example, school-based surveillance provided a study population with residences spread across a wider geographic range, representing more city blocks and neighborhoods of Iquitos than our community-based design (Figure 1). In contrast, the community-based program was limited to 24 city blocks. The community-based study was, however, a component of efficacy trials for an integrated vector control intervention (ACM, TWS, and TJK, unpublished results), and the exhaustive sampling of randomly selected city blocks provided a legitimate population sample for the direct evaluation of the intervention strategy. Thus, although the basic research question, site-specific dengue epidemiology, and cultural characteristics of the study population will determine the choice of the active surveillance strategy implemented, based on our results, community-based surveillance should be considered as a viable methodology.

Table 1

Summary of results from school absenteeism–based and community-based febrile surveillance programs

Table 1
Figure 1.
Figure 1.

Map of the study areas in Iquitos. Locations of schools and study neighborhoods are marked.

Citation: The American Journal of Tropical Medicine and Hygiene Am J Trop Med Hyg 80, 4; 10.4269/ajtmh.2009.80.656

*

Address correspondence to Tadeusz J. Kochel, 3230 Lima Pl, Washington, DC 20521-3230. E-mail: tad.kochel@med.navy.mil

Authors’ addresses: Claudio Rocha, Brett M. Forshey, Patrick J. Blair, James G. Olson, Jeffrey D. Stancil, and Tadeusz J. Kochel, Naval Medical Research Center Detachment, 3230 Lima Pl, Washington, DC 20521-3230, Tel: (51-1) 614-4141. Amy C. Morrison and Thomas W. Scott, Department of Entomology, University of California, 1 Shields Ave., Davis, CA 95616-8584, Tel: 530-754-4196. Moises Sihuincha, Hospital de Apoyo, Av. Cornejo Portugal 1710, Iquitos, Loreto, Peru, Tel: (51-65) 265-731.

Financial support: This study was funded by the US Department of Defense Military Infectious Diseases Research Program, Work Unit 62787_870_S_B0001.

Disclaimer: The views expressed in this article are those of the author and do not necessarily reflect the official policy or position of the Department of the Navy, Department of Defense, or the US Government. Study protocols were approved by the Naval Medical Research Center Institutional Review Boards (NMRC2001.0008 and NMRC2003.0008) in compliance with all Federal regulations governing the protection of human subjects. Claudio Rocha, Amy C. Morrison, Patrick J. Blair, James G. Olson, Jeffrey D. Stancil, and Tadeusz J. Kochel are military service members or employees of the US Government. This work was prepared as part of their official duties. Title 17 U.S.C. § 105 provides that “Copyright protection under this title is not available for any work of the United States Government.” Title 17 U.S.C. § 101 defines a US Government work as a work prepared by a military service members or employees of the US Government as part of those person’s official duties.

REFERENCES

  • 1

    Gubler DJ, 2004. Cities spawn epidemic dengue viruses. Nat Med 10 :129–130.

  • 2

    Gubler DJ, 2002. Epidemic dengue/dengue hemorrhagic fever as a public health, social and economic problem in the 21st century. Trends Microbiol 10 :100–103.

    • Search Google Scholar
    • Export Citation
  • 3

    Gubler DJ, 1998. Dengue and dengue hemorrhagic fever. Clin Microbiol Rev 11 :480–496.

  • 4

    Gubler DJ, 1998. The global pandemic of dengue/dengue haemorrhagic fever: current status and prospects for the future. Ann Acad Med Singapore 27 :227–234.

    • Search Google Scholar
    • Export Citation
  • 5

    Phillips I, Need J, Escamilla J, Colán E, Sánchez S, Rodríguez M, Vásquez L, Seminario J, Betz T, da Rosa AT, 1992. First documented outbreak of dengue in the Peruvian Amazon region. Bull Pan Am Health Organ 26 :201–207.

    • Search Google Scholar
    • Export Citation
  • 6

    Hayes CG, Phillips IA, Callahan JD, Griebenow WF, Hyams KC, Wu SJ, Watts DM, 1996. The epidemiology of dengue virus infection among urban, jungle, and rural populations in the Amazon region of Peru. Am J Trop Med Hyg 55 :459–463.

    • Search Google Scholar
    • Export Citation
  • 7

    CDC, 1991. Dengue epidemic—Peru, 1990. MMWR Morb Mortal Wkly Rep 40 :145–147.

  • 8

    Watts DM, Porter KR, Putvatana P, Vasquez B, Calampa C, Hayes CG, Halstead SB, 1999. Failure of secondary infection with American genotype dengue 2 to cause dengue haemorrhagic fever. Lancet 354 :1431–1434.

    • Search Google Scholar
    • Export Citation
  • 9

    Kochel TJ, Watts DM, Halstead SB, Hayes CG, Espinoza A, Felices V, Caceda R, Bautista CT, Montoya Y, Douglas S, Russell KL, 2002. Effect of dengue-1 antibodies on American dengue-2 viral infection and dengue haemorrhagic fever. Lancet 360 :310–312.

    • Search Google Scholar
    • Export Citation
  • 10

    Gubler DJ, 1989. Surveillance for dengue and dengue hemorrhagic fever. Bull Pan Am Health Organ 23 :397–404.

  • 11

    Rigau-Perez JG, Gubler DJ, 1997. Surveillance for dengue and dengue hemorrhagic fever. Gubler DJ, Kuno G, editors. Dengue and Dengue Hemorrhagic Fever. London, UK: CAB International, 405–423.

  • 12

    Morrison AC, Gray K, Getis A, Astete H, Sihuincha M, Focks D, Watts D, Stancil JD, Olson JG, Blair P, Scott TW, 2004. Temporal and geographic patterns of Aedes aegypti (Diptera: Culicidae) production in Iquitos, Peru. J Med Entomol 41 :1123–1142.

    • Search Google Scholar
    • Export Citation
  • 13

    Morrison AC, Zielinski-Gutierrez E, Scott TW, Rosenberg R, 2008. Defining challenges and proposing solutions for control of the virus vector Aedes aegypti. PLoS Med 5 :e68.

    • Search Google Scholar
    • Export Citation
  • 14

    Getis A, Morrison AC, Gray K, Scott TW, 2003. Characteristics of the spatial pattern of the dengue vector, Aedes aegypti, in Iquitos, Peru. Am J Trop Med Hyg 69 :494–505.

    • Search Google Scholar
    • Export Citation
  • 15

    Mangada MM, Endy TP, Nisalak A, Chunsuttiwat S, Vaughn DW, Libraty DH, Green S, Ennis FA, Rothman AL, 2002. Dengue-specific T cell responses in peripheral blood mononuclear cells obtained prior to secondary dengue virus infections in Thai school children. J Infect Dis 185 :1697–1703.

    • Search Google Scholar
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