Clustered local transmission and asymptomatic Plasmodium falciparum and Plasmodium vivax malaria infections in a recently emerged, hypoendemic Peruvian Amazon community

Abstract

Background: There is a low incidence of malaria in Iquitos, Peru, suburbs detected by passive case-detection. This low incidence might be attributable to infections clustered in some households/regions and/or undetected asymptomatic infections.

Methods: Passive case-detection (PCD) during the malaria season (February-July) and an active case-detection (ACD) community-wide survey (March) surveyed 1,907 persons. Each month, April-July, 100-metre at-risk zones were defined by location of Plasmodium falciparum infections in the previous month. Longitudinal ACD and PCD (ACP+PCD) occurred within at-risk zones, where 137 houses (573 persons) were randomly selected as sentinels, each with one month of weekly active sampling. Entomological captures were conducted in the sentinel houses.

Results: The PCD incidence was 0.03 P. falciparum and 0.22 Plasmodium vivax infections/person/malaria-season. However, the ACD+PCD prevalence was 0.13 and 0.39, respectively. One explanation for this 4.33 and 1.77-fold increase, respectively, was infection clustering within at-risk zones and contiguous households. Clustering makes PCD, generalized to the entire population, artificially low. Another attributable-factor was that only 41% and 24% of the P. falciparum and P. vivax infections were associated with fever and 80% of the asymptomatic infections had low-density or absent parasitaemias the following week. After accounting for asymptomatic infections, a 2.6-fold increase in ACD+PCD versus PCD was attributable to clustered transmission in at-risk zones.

Conclusion: Even in low transmission, there are frequent highly-clustered asymptomatic infections, making PCD an inadequate measure of incidence. These findings support a strategy of concentrating ACD and insecticide campaigns in houses adjacent to houses were malaria was detected one month prior.

Figure 1

A-B: History of malaria in Peru. Before 1960, there was P. vivax, P. malariae and a very limited number of P. falciparum cases. After DDT campaigns stopped in the 1960's, malaria went from a low annual parasitaemia incidence (API = 1000*slide positive/population), limited to the northern costal regions, to a high level in 1995 (A: directly from Roberts et al[1], with permission). In 1991 P. vivax reemerged and in 1994 P. falciparum emerged in Loreto. An epidemic ensued, focused near the capital city of Loreto, Iquitos, and a hypoendemic continues (B).

Figure 2

Schema of community in the passive and active surveillance study. Zungarococha is a suburban community approximately 5 kilometres (km) from Iquitos, Peru. Zungarococha is composed of four villages: Zungarococha town (ZG, N = 1293), Puerto Almendra (PA, N = 207), Ninarumi (NR, N = 472), and Llanchama (LL, N = 142). Passive case detection occurred in the MINSA health post. Active case detection first included a community survey in March, 2003. Then, from the P. falciparum infections detected in passive case detection or the community survey, at-risk regions were defined for each month April-July, 2003, based upon the location of the month prior's P. falciparum infections. The location of these P. falciparum infections were used to determine a 100-metre radius at-risk zone for the following month. In each month of April-July 2003, 27–39 sentinel houses (approximately 150 participants/month) were selected within each at-risk zone for one month of weekly prospective visits.

Figure 3

Mean An. darlingi captured, prepared to bite/person/hour and percent of mosquitoes that were An. darlingi. Captures were conducted by mechanical aspiration from 7–11 pm (the known peak biting time), on the porch of households4. An. darlingi are known to bite in and near human households[4]. There were 10 MINSA entomologists, working in pairs, to give a total of 5 entomologic captures/night. The households were chosen from the sentinel houses in at-risk zones selected for human infection surveillance. In at-risk zones where there were more than 5 houses, 5 of the sentinel houses were randomly selected for entomologic captures. Each month, 5 at-risk zones were included, with 5 houses each, for 4 weekly captures in each house.

Figure 4

Spatial and temporal clustering of P. falciparum (Pfalc) infections within at-risk zones. Pfalc detection prompted our selection of sentinel houses within at-risk zones in the following month. There was clustering of infections (outlined in black) in the same and adjacent houses. The houses followed a general linear arrangement, with consecutive numbers being contiguous houses. Generally, the house numbers wrap around in opposite order for opposing houses located across a street. Human subjects concern prohibits display of more precise house locations. All persons with active case detection are shown (except for ZG, where, for simplicity and space constraints, the many households that were negative for Pfalc are not listed). Asterisks are passive case detections in the Health Post occurring within the sentinel houses. The index houses defining at-risk zones for the following month are shown in green font. Active sampling events are shown as a ratio. The numbers of Pfalc infected individuals detected in the household are shown as the numerator. The numbers of persons in the house participating as sentinels are shown as the denominator. There were four instances of persons living in two houses: where members were sampled within one of the two houses and reported frequently eating diner and sleeping in both houses (these are shown as dashed-house codes).