Category Archives: Malaria

General Principles of Zoonotic Landscape Epidemiology

Zoonoses, pathogens with animal reservoirs, exist as part of a complex system of interactions between animal reservoirs, vectors, ecological factors and human interaction. Landscape epidemiology has existed as a field of study since Russian epidemiologist E.N. Pavlovsky coined the term and laid the groundwork in the 1960s. Landscape epidemiology is in essence the study of environmental foci of zoonotic disease, what Pavlovsky called a nidas. Many of the variables have been identified and studied in individual pathogen systems.

Each system seems so complex and unique that it can be easy to think that they each exist as separate entities with little to do with each other. It is necessary to develop some general principles to both see the bigger picture, and guide research and response to less studied and newly discovered pathogens. Lambin et al. set out to do just that by doing a meta-analysis of eight regional case studies of zoonotic diseases in Europe and East Africa: West Nile Virus in Senegal, Tick-borne Encephalitis in Latvia, Sandfly abundance (leishmaniasis vector) in the French Pyrenees, Rift Valley Fever in Senegal, West Nile Virus hosts in Camargue, Rodent-borne Puumala hantavirus in Belgium, human cases of Lyme borreliosis in Belgium, and risk of malaria re-emergence in Camargue. Obviously, as indicated, not all of these studies look at all factors involved in landscape epidemiology so validation is not solely based on the number of case studies that support each principle.

The ten proposed principles by Lambin et al are shown graphically below where they fit into the system of variables.

Graphical representation of the landscape determinants of disease transmission. The numbers refer to the ten propositions formulated in this paper. Lambin et al. International Journal of Health Geographics 2010 9:54   doi:10.1186/1476-072X-9-54
Graphical representation of the landscape determinants of disease transmission. The numbers refer to the ten propositions formulated in this paper.
Lambin et al. International Journal of Health Geographics 2010 9:54 doi:10.1186/1476-072X-9-54

Proposed general principles (Lambin et al, 2010):

  1. Landscape attributes may influence the level of transmission of an infection” This proposal is found in all case species. Features of the landscape influence vector and host distribution across the region of study. Distribution and type of water (fresh, brackish, or salt water) is a common landscape feature that influences density of insect vectors.
  2. Spatial variations in disease risk depend not only on the presence and area of critical habitats but also on their spatial configuration“.   The sheer size of the critical area is not the only or necessarily the most important characteristic to determine risk in an area. Some vectors like ticks thrive along border zones between ecosystems, like edges between woodland and grasslands.
  3. Disease risk depends on the connectivity of habitats for vectors and hosts” Creating contact zones or contiguous zones that create linked areas are also important. The spatial configuration can create corridors for disease persistence in harsh landscapes. Type and connectivity of  vegetation is as important as terrain for vector habitats. Connectivity between suitable habitat for rodents and insects allows the disease to spread from one patch to the next amplifying the pathogen to a level that increases risks of human transmission. Connections between patches of critical habitats allows for recolonization after local extinction.
  4. The landscape is a proxy for specific associations of reservoir hosts and vectors linked with the emergence of multi-host disease.” Their principle could be better fleshed out; their primary evidence coming from West Nile Virus (WNV). Like other multi-host pathogens, WNV has some hosts that are much more important than others for transmission across wide regions. In WNV migratory birds are a key to understanding its spread and epidemic dynamics. WNV is also an example of a disease with different proxies and amplification hosts in different regions of the world.
  5. To understand ecological factors influencing spatial variations of disease risk, one needs to take into account the pathways of pathogen transmission between vectors, hosts, and the physical environment.” Vector-borne diseases require direct contact between humans and the vector. For other zoonoses like hantavirus contact between humans and animal hosts can be via aerosols of material with rodent feces or dust containing rodent remains. For example, people have contracted hantavirus by vacuuming up rodent remains in homes. When estimating risk of transmission to humans, abiotic (non-living) environmental conditions that can preserve or transmit to humans have to be considered. Climate and moisture content of the soil are common abiotic factors to be concerned about. Additional support for this principle comes from the role of the rodent burrow system on plague (Yersinia pestis) hosts and vectors.
  6. The emergence and distribution of infection through time and space is controlled by different factors acting at multiple scales” In their discussion of this principle, they focus on human interaction with the environment and particularly urbanization altering disease risk. They note that climate change and natural environmental change do not account for all emerging and re-emerging disease but the activities of humans including urbanization and ecological change like deforestation. Ben-Ari et al‘s study on plague and climate change also looks at the many factors at all levels from micro to macro scales effect the abundance and likelihood of transmission of the plague.

    Plague cycle including hosts and vectors with abiotic influences
    Plague cycle including hosts and vectors with abiotic influences (Ben-Ari et al, 2011).
  7. Landscape and meteorological factors control not just the emergence but also the spatial concentration and spatial diffusion of infection risk” This principle just adjusts the previous principles to take account of primarily rainfall by looking at temporary ponds or wetlands. This particularly affects mosquito abundance, but as the graphic above demonstrates also effects soil moisture.
  8. Spatial variation in disease risk depends not only on land cover but also on land use, via the probability of contact between, on one hand, human hosts and, on the other hand, infectious vectors, animal hosts or their infected habitats” Land use has been long known to affect mosquito abundance and disease transmission. Clearing land for settlements or agriculture always increases standing water in ditches, tire ruts, railroad ditches, animal troughs, incomplete building projects, and due to loss of water absorbing vegetation. A century of malaria research and management has focused on land use and the elimination of standing water.  Mature water management programs for cultivation or flood control can also alter vector abundance and human contact rates. For example flooding fields to grow rice not only provides habitat for mosquito production but also brings people into the fields to cultivate increasing contact rates. Irrigation canals would have a similar effect.
  9. The relationship between land use and the probability of contact between vectors and animal hosts and human hosts is influenced by land ownership” In Lambin et al, they looked at the contact rates between public (state) land and private ownership. In these studies state ownership increased access to forestland over private ownership.By the same token, state ownership could also prevent deforestation and urbanization by preserving the wilderness or reserving the land for other uses. Forest age and maturity also varies significantly between state forests and private land.
  10. Human behaviour is a crucial controlling factor of vector-human contacts, and of infection.”  Humans bring themselves into contact with vectors by risky behavior and can control exposure vectors and infections. Obviously, vaccination is one of the controlling factors of infection, although many zoonotic infections have either no or poor vaccines. Occupational and recreational exposure to vectors often explains gender difference in infection rates.

In conclusion these principles begin to mark out the three sides of a zoonotic triangle: biology of pathogen, vector and host; ecological system where they exist; and human behavior and ecological interaction. Human behavior including land use and constructed environments is as important as the other two sides of the triangle. Humans are not passive victims or collateral damage.


Lambin, E. F., Tran, A., Vanwambeke, S. O., Linard, C., & Soti, V. (2010). Pathogenic landscapes: Interactions between land, people, disease vectors, and their animal hosts. International Journal of Health Geographics, 9(1), 54. doi:10.1186/1476-072X-9-54 [open access]

Ben-Ari T, Neerinckx S, Gage KL, Kreppel K, Laudisoit A, et al. (2011) Plague and Climate: Scales Matter. PLoS Pathog 7(9): e1002160. doi:10.1371/journal.ppat.1002160

Dr Seuss Does Malaria

NEWSMAP, United States Military, 8 Nov. 1943

This Malaria map was illustrated by Theodor Seuss Geisel, better known as Dr. Seuss, during World War II to educate young GIs. According to the Naval Department Library, this map was printed on the back of a Newsmap (two sided poster) that showed the five war fronts in 1943: Russia, Italy, “air offensive”, southwest Pacific and Burma.

The text as transcribed by the Navy Department Library reads:

THIS IS ANN…..she drinks blood!

Her full name is Anopheles Mosquito and she’s dying to meet you. Her trade is dishing out MALARIA! If you’ll take a look at the map below you can see where she hangs out.

She can knock you flat so you’re no good to your country, your outfit or yourself. You’ve got the dope, the nets and stuff to lick her if you will USE IT.

Use a little horse sense and you can lick Ann. Get sloppy and careless about her and she’ll bat you down just as surely as a bomb, a bullet or a shell.

This text is taken from a booklet done by Theodor Geisel to train soldiers or sailors during the war. Cartoon educational materials were probably fairly effective. Newspaper cartoons were very popular at the time and the average GI was very young. Many (if not most) of these soldiers/sailors dropped out of school, often in grade school, to work during the Great Depression so educational materials had to be targeted at a lower reading level that modern military materials.

Since this is now a 60+ year old government publication, I will assume that its public domain. I found this at the Young Dipterists website. “What to do about Ann” was apparently a header on each page after the first page. I’ve tried to reproduce it as well as I could. The site appears to be missing the last page(s) since the last page has a “turn the page”.

Mapping Malaria in Anglo-Saxon England

Guthlac at Croyland in the marshes of the Wash.

England once looked very different. Much of southern Britain was marshland for most of the island’s occupied history. These bogs, fens, and marshes ensured that areas of virtual wilderness persisted  from before Roman Britain through the Norman period and beyond. Despite the difficulties of using fenlands, these areas were not only occupied throughout the Anglo-Saxon period, but important centers like Croyland, Bardney, and Ely eventually developed in the marsh.

The largest fenland region was known as ‘the Wash’.  This low-lying region drained four rivers into  a square bay of the North Sea that forms the corner between Lincolnshire and Norfolk. In Anglo-Saxon times, this tidal marsh and bog was a vast border region between the region of Lindsey and East Anglia.  Places like Croyland and Ely were islands in the wetlands.  The eighth century Life of Guthlac describes the environment of Croyland when Guthlac arrived:

There is in the Midland district of Britain a most dismal fen of immense size, which begins at the banks of the river Granta not far from the camp which is called Gronte (Cambridge) and stretches from the south as far north as the sea. It a very long tract, now consisting of marshes, now of bogs, sometimes with black waters overhung by fog, sometimes studded with woodland islands and traversed by the windings of tortuous streams. (Hill, 1981:11 cited in Gowland & Western, 2011).

These marshes are ideal for malaria, but evidence of malaria in Anglo-Saxon England has been lacking. It is supposed that malaria would have been brought to Britain with the Romans (1). Unfortunately, there is no evidence that I know of that malaria became endemic in Roman Britain much less lasted into the early medieval (Anglo-Saxon) period. It has also been speculated that ‘spring fever’ (lecten adl) found in Anglo-Saxon leechbooks is the spring manifestation of tertian malaria (1) caused by Plasmodium vivax. This would fit the pattern of malaria in cool or cold climates like that found in Finland discussed in a recent post. Indoor transmission in Anglo-Saxon earthen floored, open structured wooden homes with thatched roofs would be an ideal way to concentrate malaria in a thinly populated marsh.  (Without chimneys homes had to open enough to allow smoke to escape from a central hearth.)

Incidence of Malaria in England, 1840-1910 (2)

It has long been known that Britain can environmentally support endemic malaria. Malaria was fairly wide-spread in 19th century Britain when it was first mapped (figure to left) (2). The upper black area on the map includes much of ‘the Wash’. However, proof of malaria is more tenuous for the medieval period.  Together with the unhealthy reputation of the brackish marshlands there is at least enough evidence to suggest that endemic malaria reached back into the late medieval period.

Malaria went by a variety of local names before the early modern period. Malaria-like fevers are mentioned in literature from Geoffrey Chaucer to William Shakespeare (2, 3). Terminology for malaria was not settled upon the Italian ‘malaria’ until the early modern period. Before then, it went by a variety of terms the most universal being ‘ague’, meaning the shakes, and sometimes  ‘fever and ague’ referring to the cyclic breaking of a fever.

Gowland and Western (2011) took a new approach to finding evidence of malaria in Anglo-Saxon England (400-1100 AD) (4). Malaria caused by Plasmodium vivax causes chronic hemolytic anemia that may result in cribra orbitalia due to expansion of the bone marrow in the cranium. Gowland and Western correlated the presence of cribra orbitalia in Anglo-Saxon skeletal remains with the presence of the malarial vector Anopheles atroparavus and reports of ‘ague’ in 19th century England.

The Anglo-Saxon cemeteries used in their study are mapped in the figure below on the left. Note that not many cemeteries are located near the modern coastline of ‘the Wash’. This area would have likely been too wet for settlement.

Anglo-Saxon cemeteries (4)
Map of A. atroparvus with 19th century "ague" records. (4)

Gowland and Western  determined areas capable of sustaining malaria by mapping the presence of A. atroparvus from a 1900 AD British Museum survey (shown above on the right) (4).  The darker the shading the more reports of mosquitoes. This survey was reported to not have been systematic, so they augmented it with 19th century ‘ague’ reports (triangles).  There are some notable areas with high levels of mosquitoes that lack ague reports. This map was use to determine malarial regions for correlation with either cribra orbitalia or the poor nutrition control enamel hypoplasia. It also roughly correlates with the 1840-1910 malaria incidence in the color map above by Kuhn et al (2).

An inverse distance map showing A. atroparus incidence vs. hot and cold spots for cribra orbitalia. (4)

In this last map, malarial areas are plotted with hot and cold spots for cribra orbitalia.  Purple and blue areas on the map indicate the highest areas of A. atroparvus in 1900, while red and orange circles indicate the cribra orbitalia ‘hot’ spots. Areas of cribra orbitalia correlate very well with malarial areas around the Wash.  Cribra orbitalia ‘cold’ spots (blue circles) correlate with areas of low A. atroparvus. They found no correlation between enamel hypoplasia with either ‘malarial’ or ‘non-malarial’ areas (4).

If this cribra orbitalia is due to malaria, it is likely an underestimate of the amount of malaria in the English wetlands. Cribra orbitalia forms in children so it will not indicate adults who contract malaria. Communities like Ely, Croyland and Peterborough were large monasteries who probably drew many into the marsh as adults.

Confirmation of malaria in Anglo-Saxon England will have to wait for molecular evidence, but this skeletal evidence strengthens the hypothesis that it was endemic in early medieval Britain. It also should be informative for the areas to concentrate efforts to find molecular evidence.


(1) Cameron, M.L. (1993, repr. 2006) Anglo-Saxon Medicine. Cambridge University Press.

(2) Kuhn, K., Campbell-Lendrum, D., Armstrong, B., & Davies, C. (2003). Malaria in Britain: Past, present, and future Proceedings of the National Academy of Sciences, 100 (17), 9997-10001 DOI: 10.1073/pnas.1233687100

(3) Reiter P (2000). From Shakespeare to Defoe: malaria in England in the Little Ice Age. Emerging infectious diseases, 6 (1), 1-11 PMID: 10653562

(4) Gowland RL, & Western AG (2011). Morbidity in the marshes: Using spatial epidemiology to investigate skeletal evidence for malaria in Anglo-Saxon England (AD 410-1050). American journal of physical anthropology PMID: 22183814

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