Epidemiology of malaria in a village in the Rufiji River Delta, Tanzania: declining transmission over 25 years revealed by different parasitological metrics

Anna Färnert, Victor Yman, Manijeh Vafa Homann, Grace Wandell, Leah Mhoja, Marita Johansson, Salome Jesaja, Johanna Sandlund, Kazuyuki Tanabe, Ulf Hammar, Matteo Bottai, Zulfiqarali G Premji, Anders Björkman, Ingegerd Rooth, Anna Färnert, Victor Yman, Manijeh Vafa Homann, Grace Wandell, Leah Mhoja, Marita Johansson, Salome Jesaja, Johanna Sandlund, Kazuyuki Tanabe, Ulf Hammar, Matteo Bottai, Zulfiqarali G Premji, Anders Björkman, Ingegerd Rooth

Abstract

Background: Assessments of the epidemiology of malaria over time are needed to understand changes in transmission and guide control and elimination strategies.

Methods: A longitudinal population study was established in 1985 in Nyamisati village in the Rufiji River Delta, Tanzania. A physician and research team lived in the village 1984-2000. Parasite prevalence by microscopy and two PCR methods, spleen rates and haemoglobin levels were measured in repeated cross-sectional surveys between 1985 and 2010. Passive surveillance of malaria cases was maintained until end 1999. Bed nets were distributed after the surveys 1993, 1999 and 2010.

Results: In 1985, overall parasite prevalence by microscopy was 70% (90% in children ages two to nine years). The prevalence decreased gradually by microscopy (38.9% 1994, 26.7% 1999) and msp2-PCR (58.7% 1994, 44.8% 1999), whereas real-time PCR prevalence remained higher throughout the 1990s (69.4% 1994, 64.8% 1999). In 2010, parasite prevalence was 17.8% by real-time PCR and 16.3% by msp2-PCR, and estimated to 4.8% by microscopy. Spleen rates in children ages two to nine years decreased earlier than parasite prevalence, from >75 to 42% in the 1980s, to nil during the 1990s. The prevalence of severe and moderate anaemia decreased from 41.1 to 13.1%. No deaths at the time of acute malaria were recorded when the research team lived in the village.

Conclusions: A marked decline in malaria transmission was observed over 25 years. The decrease was detected after the arrival of the research team and continued gradually both before and after distribution of bed nets. Spleen rates and microscopy identified early changes when transmission was still intense, whereas real-time PCR was a more sensitive metric when transmission was reduced. The study provides historical data on malaria within a closely monitored rural village and contributes to the understanding of changing epidemiology in sub-Saharan Africa.

Figures

Figure 1
Figure 1
Location of Nyamisati village, Tanzania A) Location of Nyamisati within the Rufiji District, Tanzania; B) Google Earth map showing Nyamisati in the Rufiji River Delta.
Figure 2
Figure 2
Parasite prevalence in Nyamisati 1985–2010 including all ages, by microscopy and two PCR methods (msp2genotyping PCR and real-time species-specific PCR). The parasite prevalence by msp2-PCR for 1986 and 1993 as well as microscopy for 2010 were estimated from slide and msp2-PCR data, respectively, using the prevalence estimation tool developed by Okell et al. [26] (as indicated by *).
Figure 3
Figure 3
Parasite prevalence and spleen rates in children aged two to nine years in repeated cross-sectional surveys in 1985–2010. Parasite prevalence was assessed by microscopy, real-time PCR, and msp2-PCR. ITNs were distributed in October 1993-April 1994 (n = 300) and in 1999 after the survey (n = 900); LLINs were distributed after the survey 2010 (n = 1,000) (as indicated by arrows). The data from 1986–1988 are available only as published data, spleen rates are available for individual years, whereas parasite prevalence by microscopy is only available as pooled data.
Figure 4
Figure 4
Age patterns of parasite prevalence by microscopy, real-time PCR, andmsp2-PCR A) overall and B) in asymptomatic individuals in 1994, 1999 and 2010.
Figure 5
Figure 5
Proportion of Nyamisati population with mild, moderate and severe anaemia at cross-sectional surveys, classified according to age and sex-specific WHO criteria[[27]].
Figure 6
Figure 6
Clinical episodes of malaria. A) Number of clinical episodes of malaria diagnosed each month in 1993–1999 at the Nyamisati Health Clinic (bars) and rainfall patterns (solid line) averaged from data from the nearest meteorological stations of Utete, Kingupira, Kilwa Masoko, and Dar es Salaam International Airport, provided by the Tanzania Meteorological Agency; B) Incidence rate of clinical malaria by age over three observation periods 1986–1988, 1993–1995, and 1998–1999 (no data available 2010); C) Parasite densities in febrile malaria episodes over years.

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