The changing limits and incidence of malaria in Africa: 1939-2009

Abstract

Understanding the historical, temporal changes of malaria risk following control efforts in Africa provides a unique insight into what has been and might be archived towards a long-term ambition of elimination on the continent. Here, we use archived published and unpublished material combined with biological constraints on transmission accompanied by a narrative on malaria control to document the changing incidence of malaria in Africa since earliest reports pre-second World War. One result is a more informed mapped definition of the changing margins of transmission in 1939, 1959, 1979, 1999 and 2009.

FIGURE 4.1

The margins of stable P. falciparum transmission at its presumed natural extent (pre-1939). Dark grey representing no malaria risk; light grey biologically suitable transmission but population density less than 0.01 people per km²; green represents areas of unstable transmission; dark pink areas show stable transmission. Although the Western Sahara remains unrecognized by the UN, we consider here as an independent territory within Africa.The Federation of Rhodesia and Nyasaland formed a semi-autonomous state between 1954 and 1963 before it became three British governed countries of Southern Rhodesia, Northern Rhodesia and Nyasaland but throughout regarded as independent Zimbabwe, Zambia and Malawi, respectively; Eritrea and Ethiopia were officially recognized as separate nations in 1993; more recently, South Sudan and The Republic of Sudan separated in July 2011. Two small territories within the Kingdom of Morocco continue to be occupied by Spain in the North West (Ceuta) and North-East (Melilla) on the Mediterranean coastline to this day; however, we considered part of the Kingdom approximating to its Ottoman extent before 1912. The United Arab Republic of Egypt lost the Sinai Peninsula to Israeli forces during the 6-day war of 1967. This disputed territory was not fully restored to Egypt until after the partial reoccupation by President Sadat as part of the October War in 1973 and negotiated return to Egypt in 1979. We consider the Sinai Peninsula as part of UAR Egypt, and hence the African continent, throughout the entire period under review. In Libya, the Eastern coastal cities have always been regarded of unstable transmission and this intelligence has been used to indicate this area as unstable (light pink). The area of present day Namibia became a German Imperial Protectorate in 1884 and was made a South African Mandated Territory after the First World War. Until independence Namibia was referred to as German South-West Africa.The war for independence from South Africa intensified from 1973 with the international recognition of the South-West Africa People’s Organization (SWAPO) that eventually resulted in an end to South African rule in 1988 and Namibian independence in March 1990.The small territory of Walvis Bay, mid-way along the Namibian coast, was part of the Union and Republic of South Africa up to 1994, but we treat as part of the Republic of Namibia throughout all presentations of risk. AfriPOP population surfaces for each country were downloaded from www.afripop.org and re-sampled from 100 m resolution to 5km in ArcGIS 10 (ESRI, Redlands, CA, USA). These were then reclassed to identify 5×5 km grid squares that reported less than 1 person per 100 km² (population density<0.01 persons per km²). Areas that are biologically suitable for transmission but where populations are less than 0.01 km² within a contiguous area are shown in light grey in the figure. These often represent game reserves, conservation areas or deserts. Unsuitable areas for P. falciparum transmission are shown in dark grey, and based on (a), medical intelligence from Djibouti, South Africa, Namibia and Botswana has been used to define no risk (see text for details). The Kingdom of Morocco’s range of transmission intensity and risk mapped extensively by Hoeul and Donadille (1953) and Houel (1954) that mapped pre-elimination extents and the progress of elimination since 1948. These mapped ranges have been combined with the aridity mask to identify the natural extent of malaria in the Kingdom; (b) Temperature Suitability Indices generated at 1×1 km resolutions as described by Gething et al. (2011), and constructed using monthly synoptic mean, maximum, and minimum temperature records obtained from 30-arcsec (~1×1 km) spatial resolution climate surfaces (Hijmans et al., 2005) converted using spline interpolation to a continuous time series representing a mean temperature profile across an average year incorporated into a biological model of sporogyny.TSI values above zero for P. vivax are more ubiquitous across Africa suggesting transmission at higher altitudinal and wider latitudinal limits, including the highlands of Kenya, Réunion, Madagascar and Ethiopia (Gething et al., 2011), but these are harder to interpret given the absence of reported transmission in these areas even when P. vivax is prevalent in these countries and (c) areas of extreme aridity (Guerra et al., 2008) based on the enhanced vegetation index (EVI) derived from the MODerate-resolution Imaging Spectroradiometer (MODIS) sensor imagery, available at approximately 1×1 km spatial resolution (Guerra et al., 2008; Scharlemann et al., 2008). Temporal Fourier-processed, monthly EVI surfaces were used to develop 12 monthly surfaces that reclassified EVI ≤0.1 (arid) and >0.1 (non-arid) (Guerra et al., 2008). All rivers and lakes shown from single source: Global Lakes and Wetlands Database (GLWD) (Lehner and Döll, 2004).

FIGURE 4.2

Kingdom of Morocco. Annual malaria case incidence (both species) per 10,000 per annum 1928–1973 (left hand panel) and slide-confirmed P. vivax malaria 1974–2010 per 100,000 population (right hand panel). Last confirmed P. falciparum case detected in 1979. Note case incidence in 1973=1.03 per 10,000 population, 3 vivax cases detected in 2000 and 19 case in 2002, no cases detected in 2001 and 2003 and one case notified in 2004. Case data derived for 1930–1933 (Gaud, 1947); 1934–1945 (Hoeul and Donadille, 1953); 1946–1962 (Guy, 1963); 1963 and 1964 (El Aouad, 2009); 1965, 1978 and 1979 (WHO, 1992); 1966–1977, 1980–1981 and 1998 (El Aouad, 2009); 1982–1997 (WHO, 1999); 2002–2010 (WHO-Morocco, 2010). Population has been sourced for 1925–1955 (Goldewijk and Batthes, 1997); 1960–2010 (H-C au Plan, Royaume du Maroc, 2011). Intercensal growth rates used to compute non-census year population size.

FIGURE 4.3

Algeria: Annual malaria incidence per 10,000 population 1948–1954 (left hand side) and per 100,000 population 1977–2009 (right hand side). Annual malaria case data sourced from multiple sources: 1948–1953 (WHO-Algeria, 1956); 1954 (WHO, 1957); 1977–1984 (Benzerrough and Janssens, 1985); 1985–2007 (Hammadi et al., 2009); 2008–2009 (Richard Cibulskis, Personal Communication). Case data converted to annual incidence between 1948 and 1960 (Goldewijk and Batthes, 1997); 1969–1984 (CICRED, 1974) and census data for the years 1998 and 2008 from ONS, Algeria (2011). Between census years intercensal growth rates computed to estimate populations. Note no case data available for review for period 1955–1976; zero cases reported in years 1985, 1989 and 2009; Annual incidence in 2005 and 2006 was 0.003 cases per 100,000 population.

FIGURE 4.4

Tunisia. Annual malaria case incidence per 10,000 1934–1969 (left hand panel) and slide confirmed, locally acquired case incidence per 100,000 1970–1995 (right hand panel). Case data from 1935–1938 to 1955–1978 (Chadli et al., 1985); 1944–1954 (WHO-Tunisia, 1956); 1980–1995 (Mondher, 2010); No data available for review for the periods 1939–1943. Population data for whole country used to reflect national changes in incidence from 1925 to 1955 (Goldewijk and Batthes, 1997); 1966, 1975, 1984, 1994 and 2004 (National Institute of Statistics, Tunisia, 2011). Non-census years computed using annual intercensal growth rates.

FIGURE 4.5

United Arab Republic of Egypt reported malaria case incidence 1939–1953 per 10,000 (left hand side) and 1979–2004 per 100,000 (right hand side). Annual reported malaria cases sourced for 1939–1953 (WHO-Egypt, 1956); 1979 (Anon, 1981); 1986 and 1987 (WHO, 1989); 1980–1985 (EMRO-WHO, 1987); 1988 and 1991–1997 (WHO, 1999); 1989 and 1990; 1999–2002 (WHO-EMRO, 2011) and 2003 and 2004 (WHO-Egypt, 2010). National population used throughout to highlight overall changing incidence 1927, 1937, 1947, 1960, 1966, 1976, 1986, 1996, 2006 from CAPMAS, Egypt (2011). Non-census years computed using annual intercensal growth rates.

FIGURE 4.6

Cape Verde: Annual slide-confirmed malaria case incidence per 10,000 population 1934–1963 (left hand side) and annual, locally acquired, slide-confirmed case incidence per 100,000 population 1964–2010. Data sources used include 1934–1952 (De Meira, 1954); 1960–1983 (Cambournac et al., 1984); 1984–1985 and 1987–2006 (PNLP-Cape Verde, 2009); 2007–2010 (Joana Alves, personal communication). No reports available for review for the period 1953–1960. Case incidence computed for entire country per year to highlight changing national incidence and not per remaining islands at risk, denominators derived for census years 1940, 1950, 1960, 1970, 1980, 1990, 2000 and projections 2001–2010 (INE Cape Verde, 2011) and non-census years computed using intercensal growth rates. The years 1968–1972 and 1983–1986 no locally acquired cases reported.

FIGURE 4.7

São Tomé and Príncipe. Annual malaria-specific mortality per 100,000 population. Mortality data sourced from several publications: 1948–1954 (WHO São Tomé and Príncipe, 1955); 1972–1979 (Ceita, 1981); No data available for review for 1977; 2000–2009 (Teklehaimanot et al., 2009). Population data used for 1955 (WHO São Tomé and Príncipe, 1955) and 1981–2006 (Instituto Nacional de Estatistica, ST&P 2006). Non-census years computed using intercensal growth rates.

FIGURE 4.8

Mauritius. Annual malaria incidence per 10,000 population 1927–1962 (left hand side) and vivax incidence per 100,000 population 1963–2008 (right hand side). Annual malaria cases sourced from 1927–1971 (Colony of Mauritius, 1931–1972); 1940–1953 (WHO Mauritius, 1955); 1961 (WHO, 1967); 1970 and 1971 (WHO, 1971) and 1980–2008 (Communicable Disease Control Unit Mauritius, 2008). Population derived from 1927–1960 (Colony of Mauritius, 1928–1972); 1961–2008 (CSO Mauritius, 2011) and intercensal growth rates computed for non-census years to predict population between censuses. Zero indigenous cases recorded in 1966, 1967, 1969–1972, 1990, 1991, 1993–1995, 1998-2010. Last indigenous case of P. vivax malaria recorded in 1997 (Tatarsky et al., 2011).

FIGURE 4.9

Mayotte malaria case incidence per 10,000 population 1983–2010. Annual malaria case data derived for period 1984–1988 (Julvez et al., 1990a); 1983, 1989–1994 (Ali Halidi, 1995); 1995–2004 (Tchen et al., 2006); 2005 and 2006 (Solet et al., 2007) and 2007–2010 (Jean-Loius Solet, personal communication). No data available for review for the year 1997. Population for Mayotte derived from Institut National de la Statistique et des Etudes Economiques (INSEE) for the French Overseas Department, reviewed between 1985 and 1993 (INSEE, 2011a,b) and non-census years using intercensal growth rates.

FIGURE 4.10

Antananarivo Province malaria case incidence per 10,000 population 1972–1989. Annual malaria case data derived for period between 1972–1974 and 1982–1983 where data presented only as incidence (Bouma, 2003); 1975–1989(Blanchy et al., 1993) and 1981 (Tchen et al., 2006). No data available for review for the year 1983. Population for Antananarivo province derived from census bureau review of province 1975 and 1993 (Razafimanjato et al., 1997) and non-census years using intercensal growth rates. Note in 1979, chloroquine chemoprophylaxis stopped (Blanchy et al., 1993) and following rise in late 1980s DDT reintroduced in 1993. No data available for review for the province after this date.

FIGURE 4.11

Annual malaria case incidence in KwaZulu-Natal Province per 10,000 population 1974–2009. Annual Malaria Cases for KwaZulu-Natal 1974–2005 (Craig et al., 2004; Marlies Craig, unpublished data); 2006 and 2007 (DoH South Africa, 2008); 2008 and 2009 (Rajendra Maharaj, unpublished data). Population has been estimated using the 1996 population census, 20.7% of South Africa’s population lived in KwaZulu-Natal Province and intercensal growth rates between 1974 and 1991. Provincial population data for period post-1991 sourced from STATSA (2011).

FIGURE 4.12

South Africa. Annual malaria case incidence per 10,000 population 1970/1971–2008/2009. Annual malaria incidence in 1970/1971 was 0.12 per 10,000 population—not visible on the graph. Malaria case data provided for period 1970/1971–1980/1981 (DoH South Africa, 2008); 1981/1982–1995/1996 (WHO, 1999); 1996/1997–2008/2009 (WHO, 2010). Note cases reported in South Africa for periods July–June and graph shows starting July 1972 and ending June 2009; it has not been possible to define locally acquired infections from imported infections from the data available, but from 1999, the more imported infections were likely than locally acquired. No national data were available for review for the reporting year July 2009–June 2010. To compute incidence resident populations in Kwazulu-Natal, Mpumalanga and Limpopo provinces have been used (STATSA, 2011). Estimates prior to 1991 assume that 39.8% of South Africa’s total population resides in these three provinces.

FIGURE 4.13

Botswana annual slide-confirmed malaria case incidence 1928–2010 per 10,000 population. Data sources used include 1928–1938 (Bechuanaland Protectorate, 1928–1938); 1945–1953 (WHO-Bechuanaland, 1955); 1954–1960 (Bechuanaland Protectorate, 1954–1960); 1963–1973 (WHO, 2002); 1974–1984 (RBM, Southern Africa, 2002); 1985–2009 (NMCP Botswana, unpublished data, 2009). No data available for review for the years 1933, 1936, 1939–1944, 1948 and 1971. Reported cases converted to annual incidence using annual population, to reflect overall changing population sizes with time rather than population residing in risk areas. Population data from actual census years derived from MoH reports and National Census Office (Bechuanaland Protectorate, 1934 and 1963; Botswana CSO, 2002–2004; Botswana CSO, 2005) and intercensal growth rates used to compute non-census years. Annual malaria Incidence in 1928 and 1934 was 280 and 312 per 10,000, respectively, but attenuated on graph.

FIGURE 4.14

Zimbabwe: Annual malaria case incidence per 10,000 population 1980–2009. All case data combinations of slide confirmed and presumed cases. No data available for review for the years 2001–2003. Data 1980–1989 from Freeman (1995); 1990–2009 (WHO, 2010); 2000 extracted from WHO (2002). Population data used to compute incidence derived from the World Bank database (2011).

FIGURE 4.15

Kingdom of Swaziland. Annual malaria case incidence 1928/1929–2009/2010 per 10,000 populations. Total population of Swaziland used throughout to highlight changing national case incidence despite changing margins of risk. Case data derived for period 1929–1938 (Ministry of Health, Swaziland, 1930–1938); 1946–1973 (Ministry of Health, Swaziland, 1974); 1974–1982 (MoH Swaziland, 1983); other years and most recent years provided by Simon Kunene and Joe Novotny. Annual malaria incidence in 1946 was 370 per 10,000 populations. No data available for review for the years 1939–1945. Population has been sourced from several sites: 1929–1938 (Ministry of Health, Swaziland, 1930–1939); 1946, 1956 census years (Ministry of Health, Swaziland, 1948 and 1957); 1966, 1976, 1986, 1997 and 2007 (CSO, Kingdom of Swaziland, 2011). Non-census years computed using annual intercensal growth rates. Annual case reporting is July–June; therefore, graph starts July 1929 and ends June 2010.

FIGURE 4.16

Nairobi city malaria incidence per 10,000 population 1916–1969 (adapted from Mudhune et al., 2011). Annual malaria incidence in 1926 was 3649 per 10,000 populations and attenuated in graph. No data were reported in 1921–1925 and 1945. Case incidence between 1952–1964 was less than 5 per 10,000 and between 1965 and 1969 was less than 1 per 10,000. Annual malaria incidence has been sourced from several publications: 1916–1920, 1926, 1928 and 1929 (Symes, 1940); 1930–1939, 1944–1949 (Nairobi Municipality, 1930–1939 and 1946–1949); 1940–1943 (De Mello, 1947); 1950–1969 (Nairobi Municipality, 1950–1969). No data available for review for years 1921–1925. Population between 1916 and 1925 is estimated from historical prediction in 1926 (Symes, 1940) and 1928 (Mitullah, 2003); data on censused population 1929–1949 (Nairobi Municipality, 1930–1949) and 1950–1969 (Nairobi Municipality, 1950–1969). Note that malaria was a notifiable disease after 1930 through to 1969.

FIGURE 4.17

Annualized malaria-specific mortality in children aged 0–4 years old pre-1960; 1960–1989 and 1990–1999. Box plot showing median (central lines), 25%, 75% quartile ranges around the median (box width) and upper and lower limits (T) mortality estimates per 1000 children aged 0–4 years per annum (reproduced from Snow et al., 2001).

FIGURE 4.18

Niakhar, Senegal: Malaria-specific mortality per 1000 children 0–4 years 1984–2010 (adapted from Munier et al., 2009; Trape et al., 2012). Malaria defined in demographic surveillance of Naikhar population using verbal autopsies. In 1992, chloroquine resistance established; by 2000, sulphadoxine–pyrimethamine (SP) used for second-line rescue therapy; 2003 amodiaquine (AQ)+SP became first-line treatment until replaced by AQ-Artesunate in 2006; in 2008, ITN distribution went to scale.

FIGURE 4.19

Annual malaria admissions in Kericho Tea Estate population, Kenya 1966–2009 (adapted from Shanks et al., 2002; Stern et al., 2011).

FIGURE 4.20

The changing margins and stability of P. falciparum transmission (A) 1959, (B) 1979, (C) 1999 and (D) 2009. Dark grey representing no malaria risk; light grey biologically suitable transmission but population density less than 0.01 person per km²; light green unstable transmission and dark pink stable transmission. (A) 1959: The remaining focal areas of P. falciparum risk in Kingdom of Morocco as reported and mapped by Hoeul and Donadille (1953).The regions of Oran, Constantine and Algers in Algeria were under aggressive control from the mid-1940s that transitioned this area to unstable conditions by 1959 (Benzerrough and Janssens, 1985; Hammadi et al., 2009; Parrot et al., 1946). Elimination campaigns systematically reduced the margins of malaria risk in Libya with a remaining area of unstable risk in Fezzan region by 1959 (Gebreel et al., 1985). In Egypt, by 1953, no cases were recorded in the Canal Zone, Assiut, Girga, Kom Ombo, Asswan and Nubia regions (Halawani and Shawarby, 1957). The Republic of Djibouti was malaria free. The islands of Réunion and Mauritius had substantially reduced malaria incidence to render each island unstable by 1959. Use of IRS and chemoprophylaxis in Madagascar led to effective control in the highland plateau districts by 1959 (Bernard, 1954) and resulted in exceptionally low transmission and disease incidence. For South Africa, the map produced by Brink (1958) and narrative provided by Hansford (1974) have been used to constrain the margins of risk in the Transvaal area by 1959 resulting from aggressive use of DDT and providing evidence of unstable risk in the lower margins. It was felt that these control efforts were mirrored by a changing risk along the lower margins of Botswana along the Limpopo River (Franco de et al., 1984a). In Zimbabwe, similar attack phases of elimination were able to reduce case incidence in unstable transmission and provided as mapped extents by Alves and Blair (1955). Case incidence declined rapidly in the Kingdom of Swaziland though the use of DDT and stable transmission was constrained to Lubombo and Hhohho regions until 1999 (MoHSW, 1999; Simon Kunene, personal communication); the highveld was regarded as malaria free (Fontaine, 1987), and this was digitized using ARCGIS and regarded as malaria free through to 2009. (B) 1979: The Kingdom of Morocco was free from P. falciparum by 1974. By 1979, falciparum transmission had been eliminated in the northern territories of Algeria and focal risks persisted in the southern provinces with increasing stability with increasing latitude (Benzeroug and Wery, 1985). All of the Northern provinces of Tunisia were malaria free by 1968, and by 1979, all districts were falciparum free (Ambroise-Thomas et al., 1976). Libya was declared malaria free in 1973. Stable transmission in Fayoum region. Unstable transmission was likely in some parts of Egypt in 1979 at malaria suitable areas but national case incidence dropped to less than 1 in 10,000 (Hassan et al., 2003). 1979 was probably the last period when The Republic of Djibouti was regarded as malaria free. Réunion and Mauritius were declared malaria free by 1979. Elimination efforts on the islands of Cape Verde had reduced case incidence to zero in all but Santiago by the late 1960s. It is also likely that combined disease control on Mayotte resulted in a case incidence that would be regarded as unstable by 1979. Drug-based and IRS control in the highlands of Madagascar sustained unstable control through to 1979. Continued efforts to eliminate malaria in the Transvaal and KwaZulu-Natal provinces rendered increasing areas unstable and reduced the spatial extent of risk in South Africa (Craig et al., 2004; Hansford, 1974; Kleinschmidt et al., 2001). In Namibia, combined medical intelligence based on case data generated by the Ministry of Health and Social Services since the 1980s shows the regions of Khomas and Erango to have conditions that are borderline malaria free and unstable transmission with consistently low case incidence (MoHSS, 1996). The southern-most risk districts in Namibia had very few clinical cases during the early 1980s and regarded here as unstable by 1979 (MoHSS, 1996). These qualitative observations were more systematically quantified using reporting from mapped facilities over the period 2008–2009 (Snow et al., 2010b). In Zimbabwe, evidence suggests that the areas under control in 1959 remained under control rendering them unstable transmission; the cities of Harare and Bulawayo were malaria free as were highland districts (NMCP Zimbabwe, 2008). In Swaziland, case incidence data were mapped in 1983 to show that stable risks were constrained to only the areas located on the east of the country (Franco de et al., 1984b); these cases were digitized and enveloped using ARCGIS. (C) 1999: A foci of risk in Algeria on the border with Mali at Tinzaouatine continued through to 2009 (Boubidi et al., 2010). El Fayoum Governorate in Egypt remained a focal area of unstable transmission in 1999 (Hassan et al., 2003) with no autochthonous cases elsewhere in Egypt. The Republic of Djibouti witnessed a sequence of epidemics from 1988 and in areas where transmission was biologically suitable leading to the establishment of stable endemicity. Madagascar, Cape Verde (Santiago) and Mayotte witnessed resurgent risks of malaria during the late 1980s and early 1990s that returned previously unstable areas to stable transmission and high disease burden. Risks in South Africa were constrained by 1999 to areas located along the Kruger national park and borders with Zimbabwe in the Limpopo and Mpumalanga Provinces (Philip Kruger and Aaron Mbuza, personal communication) and the two northerly districts of Ingwavuma and Ubombo in KwaZulu-Natal Province (Craig et al., 2004; Kleinschmidt et al., 2001). The subregional rise in malaria risks affected Zimbabwe against a background of political crisis and it is assumed that lowveld areas previously under control in Zimbabwe returned to stable transmission by 1999 with the exceptions of malaria-free situations in Bulawayo, Harare and central highlands. (D) 2009: Since 1998, no locally acquired case has been reported from Fayoum in Egypt and now the country is malaria free although not certified about. Following efforts to control malaria in the Republic of Djibouti from 2008, case incidence was unstable (Hawa Guessod, personal communication). In Algeria, Tinzaouatine remains the only area of unstable risk by 2010. Locally acquired cases have been reported on the Cape Verdean islands of Santiago (mainly Saint Caterina and Santa Cruz) and Boa Vista in recent years but represent an unstable situation. Cases are concentrated in the northern districts of the main island of Mahoré, in Mayotte (Solet et al., 2007). Botswana reported no cases in most areas previously free of malaria by 2010; however, locally acquired cases were detected in Kweneng West and East districts between 2006 and 2008 rendering this area unstable (Ministry of Health, 2009). By 2009, malaria-free areas extended to include 14 districts in central highlands in Zimbabwe and under consolidation phase of elimination (Global Fund Zimbabwe, 2010). By 2009, case incidence in South Africa and Swaziland had dropped dramatically and case incidence by district has been used to delineate unstable and stable areas risks in Limpopo and Mpumalanga (Philip Kruger and Aaron Mbuza, personal communication; Ngomane and de Jager, 2012), unstable risks in Ingwavuma, KwaZulu-Natal (Marlies Craig and Rajendra Maharaj, personal communication) and unstable risks within the districts of Hhohho and Lubombo, with one stable endemic district of Mhlangatane, in the Kingdom of Swaziland (Kunene et al., 2011).

FIGURE 4.20

The changing margins and stability of P. falciparum transmission (A) 1959, (B) 1979, (C) 1999 and (D) 2009. Dark grey representing no malaria risk; light grey biologically suitable transmission but population density less than 0.01 person per km²; light green unstable transmission and dark pink stable transmission. (A) 1959: The remaining focal areas of P. falciparum risk in Kingdom of Morocco as reported and mapped by Hoeul and Donadille (1953).The regions of Oran, Constantine and Algers in Algeria were under aggressive control from the mid-1940s that transitioned this area to unstable conditions by 1959 (Benzerrough and Janssens, 1985; Hammadi et al., 2009; Parrot et al., 1946). Elimination campaigns systematically reduced the margins of malaria risk in Libya with a remaining area of unstable risk in Fezzan region by 1959 (Gebreel et al., 1985). In Egypt, by 1953, no cases were recorded in the Canal Zone, Assiut, Girga, Kom Ombo, Asswan and Nubia regions (Halawani and Shawarby, 1957). The Republic of Djibouti was malaria free. The islands of Réunion and Mauritius had substantially reduced malaria incidence to render each island unstable by 1959. Use of IRS and chemoprophylaxis in Madagascar led to effective control in the highland plateau districts by 1959 (Bernard, 1954) and resulted in exceptionally low transmission and disease incidence. For South Africa, the map produced by Brink (1958) and narrative provided by Hansford (1974) have been used to constrain the margins of risk in the Transvaal area by 1959 resulting from aggressive use of DDT and providing evidence of unstable risk in the lower margins. It was felt that these control efforts were mirrored by a changing risk along the lower margins of Botswana along the Limpopo River (Franco de et al., 1984a). In Zimbabwe, similar attack phases of elimination were able to reduce case incidence in unstable transmission and provided as mapped extents by Alves and Blair (1955). Case incidence declined rapidly in the Kingdom of Swaziland though the use of DDT and stable transmission was constrained to Lubombo and Hhohho regions until 1999 (MoHSW, 1999; Simon Kunene, personal communication); the highveld was regarded as malaria free (Fontaine, 1987), and this was digitized using ARCGIS and regarded as malaria free through to 2009. (B) 1979: The Kingdom of Morocco was free from P. falciparum by 1974. By 1979, falciparum transmission had been eliminated in the northern territories of Algeria and focal risks persisted in the southern provinces with increasing stability with increasing latitude (Benzeroug and Wery, 1985). All of the Northern provinces of Tunisia were malaria free by 1968, and by 1979, all districts were falciparum free (Ambroise-Thomas et al., 1976). Libya was declared malaria free in 1973. Stable transmission in Fayoum region. Unstable transmission was likely in some parts of Egypt in 1979 at malaria suitable areas but national case incidence dropped to less than 1 in 10,000 (Hassan et al., 2003). 1979 was probably the last period when The Republic of Djibouti was regarded as malaria free. Réunion and Mauritius were declared malaria free by 1979. Elimination efforts on the islands of Cape Verde had reduced case incidence to zero in all but Santiago by the late 1960s. It is also likely that combined disease control on Mayotte resulted in a case incidence that would be regarded as unstable by 1979. Drug-based and IRS control in the highlands of Madagascar sustained unstable control through to 1979. Continued efforts to eliminate malaria in the Transvaal and KwaZulu-Natal provinces rendered increasing areas unstable and reduced the spatial extent of risk in South Africa (Craig et al., 2004; Hansford, 1974; Kleinschmidt et al., 2001). In Namibia, combined medical intelligence based on case data generated by the Ministry of Health and Social Services since the 1980s shows the regions of Khomas and Erango to have conditions that are borderline malaria free and unstable transmission with consistently low case incidence (MoHSS, 1996). The southern-most risk districts in Namibia had very few clinical cases during the early 1980s and regarded here as unstable by 1979 (MoHSS, 1996). These qualitative observations were more systematically quantified using reporting from mapped facilities over the period 2008–2009 (Snow et al., 2010b). In Zimbabwe, evidence suggests that the areas under control in 1959 remained under control rendering them unstable transmission; the cities of Harare and Bulawayo were malaria free as were highland districts (NMCP Zimbabwe, 2008). In Swaziland, case incidence data were mapped in 1983 to show that stable risks were constrained to only the areas located on the east of the country (Franco de et al., 1984b); these cases were digitized and enveloped using ARCGIS. (C) 1999: A foci of risk in Algeria on the border with Mali at Tinzaouatine continued through to 2009 (Boubidi et al., 2010). El Fayoum Governorate in Egypt remained a focal area of unstable transmission in 1999 (Hassan et al., 2003) with no autochthonous cases elsewhere in Egypt. The Republic of Djibouti witnessed a sequence of epidemics from 1988 and in areas where transmission was biologically suitable leading to the establishment of stable endemicity. Madagascar, Cape Verde (Santiago) and Mayotte witnessed resurgent risks of malaria during the late 1980s and early 1990s that returned previously unstable areas to stable transmission and high disease burden. Risks in South Africa were constrained by 1999 to areas located along the Kruger national park and borders with Zimbabwe in the Limpopo and Mpumalanga Provinces (Philip Kruger and Aaron Mbuza, personal communication) and the two northerly districts of Ingwavuma and Ubombo in KwaZulu-Natal Province (Craig et al., 2004; Kleinschmidt et al., 2001). The subregional rise in malaria risks affected Zimbabwe against a background of political crisis and it is assumed that lowveld areas previously under control in Zimbabwe returned to stable transmission by 1999 with the exceptions of malaria-free situations in Bulawayo, Harare and central highlands. (D) 2009: Since 1998, no locally acquired case has been reported from Fayoum in Egypt and now the country is malaria free although not certified about. Following efforts to control malaria in the Republic of Djibouti from 2008, case incidence was unstable (Hawa Guessod, personal communication). In Algeria, Tinzaouatine remains the only area of unstable risk by 2010. Locally acquired cases have been reported on the Cape Verdean islands of Santiago (mainly Saint Caterina and Santa Cruz) and Boa Vista in recent years but represent an unstable situation. Cases are concentrated in the northern districts of the main island of Mahoré, in Mayotte (Solet et al., 2007). Botswana reported no cases in most areas previously free of malaria by 2010; however, locally acquired cases were detected in Kweneng West and East districts between 2006 and 2008 rendering this area unstable (Ministry of Health, 2009). By 2009, malaria-free areas extended to include 14 districts in central highlands in Zimbabwe and under consolidation phase of elimination (Global Fund Zimbabwe, 2010). By 2009, case incidence in South Africa and Swaziland had dropped dramatically and case incidence by district has been used to delineate unstable and stable areas risks in Limpopo and Mpumalanga (Philip Kruger and Aaron Mbuza, personal communication; Ngomane and de Jager, 2012), unstable risks in Ingwavuma, KwaZulu-Natal (Marlies Craig and Rajendra Maharaj, personal communication) and unstable risks within the districts of Hhohho and Lubombo, with one stable endemic district of Mhlangatane, in the Kingdom of Swaziland (Kunene et al., 2011).

FIGURE 4.20

The changing margins and stability of P. falciparum transmission (A) 1959, (B) 1979, (C) 1999 and (D) 2009. Dark grey representing no malaria risk; light grey biologically suitable transmission but population density less than 0.01 person per km²; light green unstable transmission and dark pink stable transmission. (A) 1959: The remaining focal areas of P. falciparum risk in Kingdom of Morocco as reported and mapped by Hoeul and Donadille (1953).The regions of Oran, Constantine and Algers in Algeria were under aggressive control from the mid-1940s that transitioned this area to unstable conditions by 1959 (Benzerrough and Janssens, 1985; Hammadi et al., 2009; Parrot et al., 1946). Elimination campaigns systematically reduced the margins of malaria risk in Libya with a remaining area of unstable risk in Fezzan region by 1959 (Gebreel et al., 1985). In Egypt, by 1953, no cases were recorded in the Canal Zone, Assiut, Girga, Kom Ombo, Asswan and Nubia regions (Halawani and Shawarby, 1957). The Republic of Djibouti was malaria free. The islands of Réunion and Mauritius had substantially reduced malaria incidence to render each island unstable by 1959. Use of IRS and chemoprophylaxis in Madagascar led to effective control in the highland plateau districts by 1959 (Bernard, 1954) and resulted in exceptionally low transmission and disease incidence. For South Africa, the map produced by Brink (1958) and narrative provided by Hansford (1974) have been used to constrain the margins of risk in the Transvaal area by 1959 resulting from aggressive use of DDT and providing evidence of unstable risk in the lower margins. It was felt that these control efforts were mirrored by a changing risk along the lower margins of Botswana along the Limpopo River (Franco de et al., 1984a). In Zimbabwe, similar attack phases of elimination were able to reduce case incidence in unstable transmission and provided as mapped extents by Alves and Blair (1955). Case incidence declined rapidly in the Kingdom of Swaziland though the use of DDT and stable transmission was constrained to Lubombo and Hhohho regions until 1999 (MoHSW, 1999; Simon Kunene, personal communication); the highveld was regarded as malaria free (Fontaine, 1987), and this was digitized using ARCGIS and regarded as malaria free through to 2009. (B) 1979: The Kingdom of Morocco was free from P. falciparum by 1974. By 1979, falciparum transmission had been eliminated in the northern territories of Algeria and focal risks persisted in the southern provinces with increasing stability with increasing latitude (Benzeroug and Wery, 1985). All of the Northern provinces of Tunisia were malaria free by 1968, and by 1979, all districts were falciparum free (Ambroise-Thomas et al., 1976). Libya was declared malaria free in 1973. Stable transmission in Fayoum region. Unstable transmission was likely in some parts of Egypt in 1979 at malaria suitable areas but national case incidence dropped to less than 1 in 10,000 (Hassan et al., 2003). 1979 was probably the last period when The Republic of Djibouti was regarded as malaria free. Réunion and Mauritius were declared malaria free by 1979. Elimination efforts on the islands of Cape Verde had reduced case incidence to zero in all but Santiago by the late 1960s. It is also likely that combined disease control on Mayotte resulted in a case incidence that would be regarded as unstable by 1979. Drug-based and IRS control in the highlands of Madagascar sustained unstable control through to 1979. Continued efforts to eliminate malaria in the Transvaal and KwaZulu-Natal provinces rendered increasing areas unstable and reduced the spatial extent of risk in South Africa (Craig et al., 2004; Hansford, 1974; Kleinschmidt et al., 2001). In Namibia, combined medical intelligence based on case data generated by the Ministry of Health and Social Services since the 1980s shows the regions of Khomas and Erango to have conditions that are borderline malaria free and unstable transmission with consistently low case incidence (MoHSS, 1996). The southern-most risk districts in Namibia had very few clinical cases during the early 1980s and regarded here as unstable by 1979 (MoHSS, 1996). These qualitative observations were more systematically quantified using reporting from mapped facilities over the period 2008–2009 (Snow et al., 2010b). In Zimbabwe, evidence suggests that the areas under control in 1959 remained under control rendering them unstable transmission; the cities of Harare and Bulawayo were malaria free as were highland districts (NMCP Zimbabwe, 2008). In Swaziland, case incidence data were mapped in 1983 to show that stable risks were constrained to only the areas located on the east of the country (Franco de et al., 1984b); these cases were digitized and enveloped using ARCGIS. (C) 1999: A foci of risk in Algeria on the border with Mali at Tinzaouatine continued through to 2009 (Boubidi et al., 2010). El Fayoum Governorate in Egypt remained a focal area of unstable transmission in 1999 (Hassan et al., 2003) with no autochthonous cases elsewhere in Egypt. The Republic of Djibouti witnessed a sequence of epidemics from 1988 and in areas where transmission was biologically suitable leading to the establishment of stable endemicity. Madagascar, Cape Verde (Santiago) and Mayotte witnessed resurgent risks of malaria during the late 1980s and early 1990s that returned previously unstable areas to stable transmission and high disease burden. Risks in South Africa were constrained by 1999 to areas located along the Kruger national park and borders with Zimbabwe in the Limpopo and Mpumalanga Provinces (Philip Kruger and Aaron Mbuza, personal communication) and the two northerly districts of Ingwavuma and Ubombo in KwaZulu-Natal Province (Craig et al., 2004; Kleinschmidt et al., 2001). The subregional rise in malaria risks affected Zimbabwe against a background of political crisis and it is assumed that lowveld areas previously under control in Zimbabwe returned to stable transmission by 1999 with the exceptions of malaria-free situations in Bulawayo, Harare and central highlands. (D) 2009: Since 1998, no locally acquired case has been reported from Fayoum in Egypt and now the country is malaria free although not certified about. Following efforts to control malaria in the Republic of Djibouti from 2008, case incidence was unstable (Hawa Guessod, personal communication). In Algeria, Tinzaouatine remains the only area of unstable risk by 2010. Locally acquired cases have been reported on the Cape Verdean islands of Santiago (mainly Saint Caterina and Santa Cruz) and Boa Vista in recent years but represent an unstable situation. Cases are concentrated in the northern districts of the main island of Mahoré, in Mayotte (Solet et al., 2007). Botswana reported no cases in most areas previously free of malaria by 2010; however, locally acquired cases were detected in Kweneng West and East districts between 2006 and 2008 rendering this area unstable (Ministry of Health, 2009). By 2009, malaria-free areas extended to include 14 districts in central highlands in Zimbabwe and under consolidation phase of elimination (Global Fund Zimbabwe, 2010). By 2009, case incidence in South Africa and Swaziland had dropped dramatically and case incidence by district has been used to delineate unstable and stable areas risks in Limpopo and Mpumalanga (Philip Kruger and Aaron Mbuza, personal communication; Ngomane and de Jager, 2012), unstable risks in Ingwavuma, KwaZulu-Natal (Marlies Craig and Rajendra Maharaj, personal communication) and unstable risks within the districts of Hhohho and Lubombo, with one stable endemic district of Mhlangatane, in the Kingdom of Swaziland (Kunene et al., 2011).

FIGURE 4.20

The changing margins and stability of P. falciparum transmission (A) 1959, (B) 1979, (C) 1999 and (D) 2009. Dark grey representing no malaria risk; light grey biologically suitable transmission but population density less than 0.01 person per km²; light green unstable transmission and dark pink stable transmission. (A) 1959: The remaining focal areas of P. falciparum risk in Kingdom of Morocco as reported and mapped by Hoeul and Donadille (1953).The regions of Oran, Constantine and Algers in Algeria were under aggressive control from the mid-1940s that transitioned this area to unstable conditions by 1959 (Benzerrough and Janssens, 1985; Hammadi et al., 2009; Parrot et al., 1946). Elimination campaigns systematically reduced the margins of malaria risk in Libya with a remaining area of unstable risk in Fezzan region by 1959 (Gebreel et al., 1985). In Egypt, by 1953, no cases were recorded in the Canal Zone, Assiut, Girga, Kom Ombo, Asswan and Nubia regions (Halawani and Shawarby, 1957). The Republic of Djibouti was malaria free. The islands of Réunion and Mauritius had substantially reduced malaria incidence to render each island unstable by 1959. Use of IRS and chemoprophylaxis in Madagascar led to effective control in the highland plateau districts by 1959 (Bernard, 1954) and resulted in exceptionally low transmission and disease incidence. For South Africa, the map produced by Brink (1958) and narrative provided by Hansford (1974) have been used to constrain the margins of risk in the Transvaal area by 1959 resulting from aggressive use of DDT and providing evidence of unstable risk in the lower margins. It was felt that these control efforts were mirrored by a changing risk along the lower margins of Botswana along the Limpopo River (Franco de et al., 1984a). In Zimbabwe, similar attack phases of elimination were able to reduce case incidence in unstable transmission and provided as mapped extents by Alves and Blair (1955). Case incidence declined rapidly in the Kingdom of Swaziland though the use of DDT and stable transmission was constrained to Lubombo and Hhohho regions until 1999 (MoHSW, 1999; Simon Kunene, personal communication); the highveld was regarded as malaria free (Fontaine, 1987), and this was digitized using ARCGIS and regarded as malaria free through to 2009. (B) 1979: The Kingdom of Morocco was free from P. falciparum by 1974. By 1979, falciparum transmission had been eliminated in the northern territories of Algeria and focal risks persisted in the southern provinces with increasing stability with increasing latitude (Benzeroug and Wery, 1985). All of the Northern provinces of Tunisia were malaria free by 1968, and by 1979, all districts were falciparum free (Ambroise-Thomas et al., 1976). Libya was declared malaria free in 1973. Stable transmission in Fayoum region. Unstable transmission was likely in some parts of Egypt in 1979 at malaria suitable areas but national case incidence dropped to less than 1 in 10,000 (Hassan et al., 2003). 1979 was probably the last period when The Republic of Djibouti was regarded as malaria free. Réunion and Mauritius were declared malaria free by 1979. Elimination efforts on the islands of Cape Verde had reduced case incidence to zero in all but Santiago by the late 1960s. It is also likely that combined disease control on Mayotte resulted in a case incidence that would be regarded as unstable by 1979. Drug-based and IRS control in the highlands of Madagascar sustained unstable control through to 1979. Continued efforts to eliminate malaria in the Transvaal and KwaZulu-Natal provinces rendered increasing areas unstable and reduced the spatial extent of risk in South Africa (Craig et al., 2004; Hansford, 1974; Kleinschmidt et al., 2001). In Namibia, combined medical intelligence based on case data generated by the Ministry of Health and Social Services since the 1980s shows the regions of Khomas and Erango to have conditions that are borderline malaria free and unstable transmission with consistently low case incidence (MoHSS, 1996). The southern-most risk districts in Namibia had very few clinical cases during the early 1980s and regarded here as unstable by 1979 (MoHSS, 1996). These qualitative observations were more systematically quantified using reporting from mapped facilities over the period 2008–2009 (Snow et al., 2010b). In Zimbabwe, evidence suggests that the areas under control in 1959 remained under control rendering them unstable transmission; the cities of Harare and Bulawayo were malaria free as were highland districts (NMCP Zimbabwe, 2008). In Swaziland, case incidence data were mapped in 1983 to show that stable risks were constrained to only the areas located on the east of the country (Franco de et al., 1984b); these cases were digitized and enveloped using ARCGIS. (C) 1999: A foci of risk in Algeria on the border with Mali at Tinzaouatine continued through to 2009 (Boubidi et al., 2010). El Fayoum Governorate in Egypt remained a focal area of unstable transmission in 1999 (Hassan et al., 2003) with no autochthonous cases elsewhere in Egypt. The Republic of Djibouti witnessed a sequence of epidemics from 1988 and in areas where transmission was biologically suitable leading to the establishment of stable endemicity. Madagascar, Cape Verde (Santiago) and Mayotte witnessed resurgent risks of malaria during the late 1980s and early 1990s that returned previously unstable areas to stable transmission and high disease burden. Risks in South Africa were constrained by 1999 to areas located along the Kruger national park and borders with Zimbabwe in the Limpopo and Mpumalanga Provinces (Philip Kruger and Aaron Mbuza, personal communication) and the two northerly districts of Ingwavuma and Ubombo in KwaZulu-Natal Province (Craig et al., 2004; Kleinschmidt et al., 2001). The subregional rise in malaria risks affected Zimbabwe against a background of political crisis and it is assumed that lowveld areas previously under control in Zimbabwe returned to stable transmission by 1999 with the exceptions of malaria-free situations in Bulawayo, Harare and central highlands. (D) 2009: Since 1998, no locally acquired case has been reported from Fayoum in Egypt and now the country is malaria free although not certified about. Following efforts to control malaria in the Republic of Djibouti from 2008, case incidence was unstable (Hawa Guessod, personal communication). In Algeria, Tinzaouatine remains the only area of unstable risk by 2010. Locally acquired cases have been reported on the Cape Verdean islands of Santiago (mainly Saint Caterina and Santa Cruz) and Boa Vista in recent years but represent an unstable situation. Cases are concentrated in the northern districts of the main island of Mahoré, in Mayotte (Solet et al., 2007). Botswana reported no cases in most areas previously free of malaria by 2010; however, locally acquired cases were detected in Kweneng West and East districts between 2006 and 2008 rendering this area unstable (Ministry of Health, 2009). By 2009, malaria-free areas extended to include 14 districts in central highlands in Zimbabwe and under consolidation phase of elimination (Global Fund Zimbabwe, 2010). By 2009, case incidence in South Africa and Swaziland had dropped dramatically and case incidence by district has been used to delineate unstable and stable areas risks in Limpopo and Mpumalanga (Philip Kruger and Aaron Mbuza, personal communication; Ngomane and de Jager, 2012), unstable risks in Ingwavuma, KwaZulu-Natal (Marlies Craig and Rajendra Maharaj, personal communication) and unstable risks within the districts of Hhohho and Lubombo, with one stable endemic district of Mhlangatane, in the Kingdom of Swaziland (Kunene et al., 2011).