Review of the malaria epidemiology and trends in Zambia

Abstract

A comprehensive desk review of malaria trends was conducted between 2000-2010 in Zambia to study malaria epidemiology and trends to guide strategies and approaches for effective malaria control. This review considered data from the National Health Information Management System, Malaria Surveys and Programme Review reports and analyzed malaria in-patient cases and deaths in relation to intervention coverage for all ages. Data showed three distinct epidemiological strata after a notable malaria reduction (66%) in in-patient cases and deaths, particularly between 2000-2008. These changes occurred following the (re-)introduction and expansion of indoor residual spraying up to 90% coverage, scale-up of coverage of long-lasting insecticide-treated nets in household from 50% to 70%, and artemisin-based combination therapy nationwide. However, malaria cases and deaths re-surged, increasing in 2009-2010 in the northern-eastern parts of Zambia. Delays in the disbursement of funds affected the implementation of interventions, which resulted in resurgence of cases and deaths. In spite of a decline in malaria disease burden over the past decade in Zambia, a reversal in impact is notable in the year 2009-2010, signifying that control gains are fragile and must be sustained toeliminate malaria.

1. Introduction

Analysis of the epidemiological changes of any disease should be the starting point to guide prioritization of interventions. For this reason, the present review analyzed malaria trends and implications on disease prevention and control in Zambia, a land-locked country with approximately 13.6 million people, 61% of which live in rural areas and 39% in urban[1]. Malaria is endemic throughout the country though it has the greatest influence on rural areas. Plasmodium falciparum is responsible for most of the disease, including its severe form, and it is transmitted by Anopheles gambiae (An. gambiae) complex and Anopheles funestus (An. funestus)[2],[3]. The malaria season follows the rainfall patterns in Zambia; thus, mosquito population starts to increase soon after the rains start in September-November, and malaria peaks in April-May and falls off in June-July when the rains stop.

Over the past 10 years, Zambia has implemented malaria control at various times with different effects depending on the available resources[4],[5]. Also, during the 20 years before 1999, much of the emphasis on malaria control in Zambia was focused on treatment, with little efforts placed on prevention. The introduction and scale-up of prevention interventions such as indoor residual spraying (IRS), intermittent preventive treatment in pregnancy and insecticide-treated nets (ITNs) had a significant impact on the reduction of malaria, particularly from 2000 to 2008[6]. This impact has been demonstrated by a change in the epidemiology of malaria, which necessitates an accurate understanding to guide interventions. Over-looking these basic principles may have inevitable negative economic and social consequences[7],[8].

We reviewed nationally representative data from various sources: routine Health Information System, population based malaria surveys[9]–[11] and reports from the Ministry of Health and Roll Back Malaria partners, Central Statistics Census 2010 and national programme reviews such as Annual Statistical Health Bulletins[12]–[13], and the Zambia Malaria Program Review 2010 report[14]. These documents provided malaria trends and data on vectors, parasites, malaria in-patient cases and deaths in children under the age of 5 years and for all ages; household coverage with long lasting insecticidal nets (LLINs), IRS and the first-line treatment with artemether lumefantrine between 2000 and 2010.

2. Analysis

2.1. Drug efficacy studies

In the period 1995-2000, the National Malaria Control Programme conducted 28 efficacy studies in vivo involving 19 chloroquine and 9 sulfadoxine pyrimethamine (SP) in 6 sentinel sites based on a 14-day WHO protocol[15]. These studies showed approximately 50% chloroquine treatment failure and 5.5% SP failure[15]. As a result, Zambia revised its national treatment policy for uncomplicated malaria in 2003, changing from chloroquine which had been used since 1960 to an artemisinin combination therapy using artemether lumefantrine as the first line drug, while quinine which has remained efficacious served as a second line medicine to treat severe cases[16],[17].

Between 2000-2010, 12 therapeutic efficacy studies had been conducted; 5 on artemether lumefantrine, 1 on cortesiane, 2 on SP-artesunate and 4 on SP (Table 1). These studies reported 98%-100% efficacy-adequate clinical and parasitological responses in both 14 and 28-day protocols (Table 1).

Table 1. Therapeutic efficacy tests of antimalarial medicines conducted in different malaria epidemiological zones in Zambia from 2000 to 2008.

Year	Drug	Sample	Numberof sites	Protocol (d)	Age group (months)	ACPR range (%)	Epidemiological zones
2000	ND	ND	ND	ND	ND	ND	ND
2003	AL	183	3	14	6-59	98.0-100.0	I, II
2003	SP	222	4	14	6-59	68.0-92.0	II, III
2003	SP-art	227	4	14	12-60	91.0-100.0	II, III
2004	SP-art	126	2	28	12-60	90.2	II, III
2004	SP	124	2	28	12-60	73.3	II, III
2004	AL	287	5	28	12-60	100.0	II, III
2005	AL	282	5	28	12-60	98.0-100.0	I, III
2005	Cortesiane	91	5	28	12-60	100.0	I, III
2005	SP	242	5	28	12-60	69.0-82.0	I, III
2006	AL	324	5	28	12-60	97.0-100.0	I, II, III
2006	SP	344	5	28	12-60	77.0	I, II, III
2008a	AL	10	1	28	12-60	100.0	I

AL: artemether lumefantrine; SP: sulphadoxine pyrimethamine; SP-art: sulphadoxine-pyrimethamine-artesunate; ACPR: adequate clinical and parasitological response; ND: not tested; I=Low transmission zone; II=Low-Medium transmission zone; III=Medium-High transmission zone.

a: The study in 2008 was conducted for 3 months during the high transmission season; however, after screening 1 378 patients, only 10 were found to be positive.

2.2. Malaria vectors

Anopheles gambiae sensu stricto (An. gambiae s.s.), Anopheles arabiensis (An. arabiensis) and An. funestus are the main malaria vectors in Zambia[18]. An. gambiae s.s. and An. funestus predominate in the wetter northern part of the country, whilst An. arabiensis predominates in the drier southern region[18]. The presence of potential secondary vectors Anopheles rufipes, Anopheles squamosus and Anopheles coustani has been reported[18]. More recent studies have described the presence of Anopheles nili, Anopheles funestus-like, Anopheles rivulorum within the An. funestus group[18].

Vector susceptibility studies conducted in 2000 in three provinces (Copperbelt, Luapula and Lusaka provinces) showed 100% malaria vector susceptibility to dichloro-diphenyl-trichloroethane (DDT), deltamethrin, malathion and propoxur based on a WHO 1992 protocol[18]. However, 10 years after scaling-up vector control interventions, insecticide resistance to pyrethroids (deltamethrin, lambdacyhalothrin and permethrin) and DDT were detected in An. gambiae s.l., An. funestus s.s. and other malaria vectors. More resistance has been reported from areas with IRS than those with LLINs[18]. Resistance mutation has been detected in areas showing cross resistance between pyrethroids and DDT[18]. Pyrethroids,, deltamethrin, lambda-cyhalothrin and permethrin, have been used for mosquito net impregnation in Zambia since 2001, when ITNs were introduced. LLINs used in Zambia are pre-treated with deltamethrin. DDT, deltamethrin, lambdacyhalothrin and alphacypermethrin have been used for IRS following the re-introduction of the intervention through public-private collaboration[19].

2.3. Malaria trends in 2000-2010

A total of 3 783 deaths in children younger than 5 years were reported in 2007 compared to a baseline of 5 498 in 2001[20],[21]. In-patient malaria cases and deaths started to decline steadily from 2003 to 2004 after the introduction of accelerated malaria control activities in those years. The trend continued steadily to reach a significant decline in 2008 (Figure 1). The pattern of decline of in-patient malaria cases and deaths was the same in all age groups. Child mortality had been declining rapidly during the same time period (2001-2008)[20],[21]. Population surveys showed a year-to-year similar pattern of decline of 1-59 month child mortality and in-patient malaria child deaths from 2001 to 2008[20],[21]. The decline of in-patient malaria cases and deaths was similar across provinces during 2001-2008, except in the eastern province where in-patient malaria cases declined only by 30%[20],[21].

Figure 1. In-patient malaria cases and deaths in children under 5 years old when interventions were introduced (ITNs, LLINs and ACTs) or re-introduced (IRS and RDTs) between 2001 and 2010 in Zambia.

ITNs: insecticide-treated nets; LLINS: long-lasting insecticide-treated nets; ACTs: artemisin-based combination therapies; IRS: indoor residual spraying; RDTs: rapid diagnostic tests.

In 2006, three years after acceleration of control activities, the national average malaria parasitemia was 23% in children under 5 years old. Although the average malaria parasitemia rate baseline before 2003 was unknown for comparisons with the 2006 average parasitemia, the figure represents a moderate level of transmission when compared to other high-burden African countries[20],[21]. The nationwide malaria survey in 2006 referred to earlier shows that parasitemia was the highest in the eastern half of the country, with many areas having over 40% of parasitaemia.

2.4. Malaria resurgence in 2009-2010

Three distinct epidemiological zones were classified in the survey from 2009 to 2010 (Figure 2). Compared to Zone I with very low transmission in Lusaka province, malaria resurgence was especially notable in the moderate to high transmission Zone III (Table 2) in the eastern, northern, and Luapula provinces. Malaria in-patient and out-patient cases continued to decline in the low to moderate transmission Zone II in central, north-western, western, southern and Copperbelt provinces (Tables 2 and 3). The resurgence in eastern province continued in 2010 as reflected in both in-patient and out-patient malaria cases. The Copperbelt province experienced resurgence malaria in 2009-2010, and this was much more pronounced in out-patient cases than in-patient malaria cases and deaths. Complicated cases and deaths were affected slightly probably due to better access to treatment of malaria. In contrast, the central, western, and southern part of the country did not experience large-scale resurgence of malaria. As of 2006, the prevalence of parasitemia in children under 5 years old was 15%-40% in the eastern provinces and 5%-15% in the central and western provinces.

Figure 2. Map of three malaria strata (transmission) zones.

Table 2. Malaria stratification in Zambia in 2010.

Zone	Parasite prevalence (%)a	Annual parasite prevalence (%)	Other determinants	Number of districts	Populationper zone
I	<1	1.9	Urban and peri-urban	4	2 198 996
II	2-14	9.6	Urban and rural	41	6 421 205
III	>15	16.1	Rural	27	4 426 307
Total				72	13 046 508

^a: prevalence in children under five.

Table 3. Malaria interventions and implementation approaches in Zambia based on the stratification in 2010.

Zone	LLINs	IRS	IPTp	Diagnosisa	Treatment	IEC/BCC	Surveillance
I	Targeted, used in response to focal cases	Targeted use in response to focal cases	None; Rely on case identify, diagnose and treat	Universal diagnosis for suspected malaria	Treat promptly with the 1st line drug ACT	Sensitize community to reduced malaria and local action	Strengthen surveillance procedures, mapping, follow-up investigate
II	Achieve, sustain universal coverage of sleeping spaces (rural)	Achieve, sustain high IRS coverage in target areas (urban)	Applicable; Strengthen diagnosis, case management for fever during pregnancy	Universal diagnosis for suspected malaria	Treat promptly with the 1st line drug ACT	Ensure high ITN use; IRS acceptance; sensitize community to reduced malaria	Strengthen reporting, records, mapping, follow-up
III	Achieve, sustain universal coverage of sleeping spaces (urban)	Achieve, sustain high IRS coverage in target areas (urban)	Applicable	Universal diagnosis for suspected malaria	Treat promptly with the 1st line drug ACT	Ensure high ITN use; IRS acceptance; prompt presentation for fever illness	Strengthen surveillance procedures (reporting and feedback) at facilities; track intervention coverage, parasite and anemia prevalence

^a: Diagnosis was done by either microscopy or rapid diagnostic tests (RDTs). IEC/BCC: information education and communication/behavioural change and communication. LLINs: long-lasting insecticide-treated nets; IRS: indoor residual spraying; IPTp; intermittent preventive treatment in pregnancy; ACT: artemisin-based combination therapy; ITN: insecticide-treated net.

2.5. New malaria stratification in Zambia

Based on recent malaria parasite prevalence in children and surveys from 2008 to 2010, different trends in the three zones have emerged: Zone I with very low transmission in Lusaka province, characterized by parasite prevalence of less than 1% in children under 5 years old; Zone II with low to moderate stable transmission of parasite prevalence of 2%-14% in children under 5 years old; Zone III with moderate to high transmission of more than 15% parasite prevalence in children under 5 years old (Table 2). Prior to 2000, malaria stratification was based on the rural and urban division: rural riverine and basins of Zambezi, Kafue and Luangwa rivers, with stable and perennial transmission; rural plateau and highlands with virtually no malaria, and the urban and peri-urban areas with unstable malaria[22]. Parasite surveys showed the rural parts of the country to have hyper- to holo-endemicity with parasite prevalence rates ranging from 50% to 100% in the 2-9 age group, urban areas to have hypo- to meso-endemicity with parasite prevalence rates ranging from 5% to 50% in the 2-9 age group and lower level of parasite prevalence of less than 5%[22].

Following this early stratification and the Mapping Malaria Risk in Africa project in 1998, no other malaria stratification has been undertaken[23]. Based on the new evidence and stratification, interventions and implementation approaches were defined as shown in Tables 2 and 3.

3. Discussion

The present review of the epidemiology of malaria in Zambia has identified declining trends on malaria cases and deaths. It was observed that in the early years of malaria control from 1970s to late 1990s, malaria burden was increasing and the disease was endemic across the country. However, a substantial 66% decline in in-patient cases and deaths occurred in 2000-2008 following the introduction of multiple interventions. A malaria upsurge occurred in 2009-2010 when vector control interventions were disrupted following delays in the disbursement of funds. Three epidemiological zones were identified to describe the range of disease burden from very low to high transmission. Appropriate epidemiological information is an integral part of effective malaria control[24],[25].

Several socio-economic factors contributed to the increase in malaria burden across the country in the 1970s. These were largely due to economic down turn-following a fall in copper prices in the international market which resulted in budget cuts for malaria control and the discontinuation of IRS. Zambia's economy depended heavily on copper mining and there was over-reliance on curative services, which was adversely affected by the significant decline in efficacy of chloroquine, the first line anti-malarial medicine during that period; chloroquine treatment failure increased from 0% to 50%, which was above the WHO recommended 25% cut-off point for policy change to other antimalarial medicines.

The substantial decline in malaria cases recorded between 2000-2008 is attributed to multiple factors. These factors include evidence-based planning informed by operational research, use of WHO-recommended strategies, interventions and increased technical and financial support from partner's[25]. External financial support grew considerably from under USD 10 million in 2003 to USD 41 million by 2008. Major funding came from the Global Fund to fight HIV/AIDs, tuberculosis and malaria, USAID, Malaria Control and Evaluation Partnership at PATH funded by Bill and Melinda Gates Foundation, the World Bank (in 2005) and US-PMI initiated in 2007[25]. Global health funding also increased from about 17.8 billion USD dollars in 2006 to 23.9 billion USD in 2008 among development assistance including Bill and Melinda Gates Foundation and the Global Fund[26].

The substantial funding over this period in Zambia facilitated expansion of intervention coverage and utilization of malaria services with LLINs, IRS, RDTs and ACTs[27], which have excellent clinical and parasitological efficacy and limited gametocidal effect thereby curtailing transmission. By 2008, approximately 65% of households had at least one LLIN compared to baseline of less than 10% in 2000 as reported in the WHO 2008 World malaria report. Similarly, 47% of residents were protected by IRS in 2008 compared to less than 5% in 2000. Cumulatively, nearly 6 million LLINs had been distributed nationwide since the introduction of mass distribution in 2005, which increased the number of people protected from malaria by LLINs. Nationwide mass distribution of LLINs has reversed the disproportionately heavy burden of malaria in rural areas in Zambia.

Malaria cases and deaths in the entire eastern half of Zambia (eastern, Luapula, and northern provinces) had increased in 2009-2010, but western provinces did not have similar incidents. Delayed disbursements of funds led to reduced procurements of preventive commodities like LLINs, coupled with wear and tear of the nets quicker than expected and loss of insecticidal effect of the LLINs possibly contributed to this malaria comeback. Although malaria made a comeback in many parts of Zambia in 2009-2010, the overall impact of control efforts on the disease remained substantial during the year 2010 when compared to 2000. In 2010, more household members in the rural areas were reported to sleep under an ITN than in urban areas, a finding which has important implications given that the burden of malaria was generally higher in rural than in urban setting in the past (1970s-1990s). The provision of new LLINs to replace the old ones in 2009 may have contributed to less resurgence in the western part of the country. Insufficient LLINs coverage, declining physical integrity (wear and tear) of LLINs, declining insecticide efficacy of the mosquito nets, insecticide resistance reported both in An. gambiae s.l. and An. funestus to pyrethroids and DDT and anti-malarial immunity due to decreasing transmission, may have contributed to the resurgence in 2009-2010 in Eastern part of Zambia.

The epidemiological strata reported in this review can be a guide to the national malaria control programme to prioritize interventions in the 2011-2015 National Malaria Strategic Plan. According to the newly adopted strategic orientation, areas with very low transmission of parasite (lower than 1%) in under-fives will be targeted for strengthened surveillance (including case investigations), universal diagnosis and prompt treatment. Targeted use of IRS and LLINs to respond to focal malaria cases supported by community mobilization and sensitizations will create awareness on the changing malaria epidemiological patterns. On the other hand, the strategy prioritized for moderate to high transmission strata of above 15% prevalence in the population, such as population in the eastern and northern parts of Zambia and those above 5 years old, should be improved with high IRS and LLIN coverage of sleeping spaces or at least one LLIN per two persons in a household. Also, universal diagnosis of suspected malaria cases, prompt treatment with ACTs and, strengthened surveillance should be carried out. In conclusion, documentation of malaria epidemiology is vital as it can strengthen the capabilities national malaria programme to re-orient strategies and interventions towards improved malaria control. This review serves to stimulate documentation on malaria epidemiology and to enhance evidence-based malaria control and pre-elimination strategies and interventions.

Comments

Background

Epidemiological changes in malaria have been reported in Zambia. These changes include malaria mortality, morbidity, malaria parasite prevalence; vector and parasite responses to insecticides and antimalarial medicines. However, there appears to be no systematic, comprehensive analysis of these changes in the period of the analysis to guide choice of cost-effective, efficient interventions.

Research frontiers

The analysis tracked malaria epidemiological trends in Zambia. Understanding of these trends is extremely vital not only for Zambia but also for the region and world over, given that this knowledge has direct implications on effective malaria planning for impact.

Related reports

Information on malaria epidemiology in Zambia and other countries was reported in different areas. Related reports include the Demographic and Health Surveys, Indicator Surveys and routine malaria information system, and national reports. These data need to be collated, synthesized, and analyzed to maximize its value for decision making.

Innovations and breakthroughs

In this epidemiological malaria review, experts analysed various disciplines including medicines, malaria programme management, epidemiologists, entomologists, parasitologists, etc., providing a unique analysis and a clear understanding of the epidemiology of malaria based on nationally representative data. This information helps to suggest practical effective methods of malaria control to assure the efficancy of the interventions.

Applications

The analysis observed important trends and changes in malaria epidemiology, malaria burden over time. A possible stratification was described to facilitate judicious and effective use of resources for malaria control.

Peer review

WHO has been regarded malaria eradication as one of biggest tropical diseases, plasmodium spread and antimalarial drugs resistance, have raised serious challenges for WHO, African governments, financial department and scientists. This paper reviews a decade-long, continent-across antimalarial cooperation projects, which was foundation supported by the WHO and Zambian Ministry of health, summarizes malaria prevention and control progress during the past ten years, with the emphasis on the efforts taken in the undeveloped areas. Widely combined with the early works of the difficulties they have encountered before, this paper reports the implementations of the prevention and treatment measures by local government, with prospects for future work including new methods as well as challenges. Especially in the last two years of this project, the authors find the revival trend of malaria in some areas, warning people of the heavy responsibilities of malaria prevention and control. Financial, scientific& technological supporting projects must be performed at international level, to achieve the purpose of the eradication of malaria. This is a comprehensive review that brings out relevant, practical knowledge on malaria control.