Background

For the period of written history, and probably long before it, the nature of human habitation and the man-made environment has influenced the presence or absence of malaria transmission [1, 2]. In recent decades there has been renewed interest in this association [3,4,5,6] driven by awareness that better general standards of living and of housing tend to mitigate against malaria transmission. Here, the relationship between housing and living environment and the disappearance of malaria in a historical example in England and a recent example in Sri Lanka is discussed.

The disappearance of malaria from England

English wetlands, much of them southern coastal salt marsh, which had been highly malarious since at least late medieval times [7], became effectively malaria-free in the first decades of the 20th Century [8]. Between 1917 and 1926, as malaria-infected soldiers returned from the First World War, malarial infections re-appeared among local inhabitants across these same areas of England [8]. However, no further transmission took place. Even though the malaria vector mosquitoes (e.g.,. Anopheles atroparvus and Anopheles plumbeus [9]) were clearly still present and competent to generate new cases from introduced ones, the previously malarious regions of England had apparently become incapable of sustained malaria transmission.

How could this be? The answer, James [8] argued, lay to a large extent in two transformations. One was that by the early 20th Century the anti-malarial drug, quinine, had become widely affordable and available in England. The other lay in the quality of the human living environment, and above all of human dwellings. James describes it thus. In contrast to dwellings of “straw or stones or mud bricks, without windows or means of introducing light and ventilation….invariably infested with anopheles mosquitoes…In England… “civilising” social influences…particularly during the last seventy years (i.e. since about 1860) … (have resulted in) houses (that) are better lighted and ventilated; they have windows and are less damp; they have floors and are provided with ceilings shutting off the bedrooms from the rafters of the roof, they are more open and less crowded and are more frequently painted and whitewashed on the inside than they used to be. These changes, as well as more cleanly conditions in the home generally, have made the houses much less liable to harbour anopheles mosquitoes and have broken, to a considerable extent, the close association between those mosquitoes and man which existed when living conditions were primitive. Undoubtedly this disassociation has contributed materially towards the reduction of malaria.” The idea that James espoused as a major component to the disappearance of malaria from England was not the total elimination of the vector mosquitoes (important as their numerical reduction would have been through drainage of wetland [10]) but the sufficient reduction in contact between these mosquitoes and their human hosts through decent housing. Reduction in human and Anopheles contact had also occurred through increase in the cattle population as diversionary hosts to the mosquitoes [10].

Principles of malaria transmission and the human living environment

James’ ideas are well supported by the theoretical principles of malaria transmission. Pioneered by Ronald Ross [11] they were formulated by George Macdonald [12,13,14] in terms that, although subject to ongoing analysis and modification, are still broadly accepted. A central concept presented by Macdonald is that of the “basic reproduction number for malaria”—the number of new cases resulting from each existing case of malaria—now designated R0, is given in what is widely known as a Ross/Macdonald equation [14]. In such an equation (e.g., Box 1) R0 is, among other factors, a function of ‘M’, the number of adult female malaria vector mosquitoes in a defined locality, and of ‘a’, their daily biting rate upon humans. Reducing either or both M and a reduces R0. Because R0 is proportional to a2 (Box 1), anything that reduces a, the daily rate at which vector mosquitoes take a human blood meal, is particularly powerful in reducing the value of R0. Improved house-type construction that is secure against mosquito entry reduces a. It is likely that there are other malaria transmission-reducing effects that result from those types of housing that resist entry by mosquitoes. These include their impact upon mosquito egg-laying rates due to the lower frequency of blood meals. Recent analysis indicates that such effects on M (Box 1) could also significantly reduce R0 [15]. Improvements in housing are, therefore, as James proposed, likely to have contributed greatly to the reduction leading to disappearance of indigenous malaria transmission in England.

The termination of autochthonous malaria transmission in Sri Lanka

When the malaria R0 is reduced to a stable value below 1, irrespective of the cause, then malaria incidence can be expected to decline continuously and exponentially. These expectations are well met by the recorded cases of malaria in Sri Lanka for most of the period from 2001 to 2012 (Fig. 1) [16, 17] (Fig. 2). In 2013 no indigenously acquired case of malaria was recorded in Sri Lanka. There have been none since [17,18,19] except for a recent case acquired by infection from a foreign migrant [20].

Fig. 1
figure 1

Recorded cases of indigenously transmitted malaria in Sri Lanka, 1967 to 2020 (Source: Anti Malaria Campaign, Ministry of Health, Sri Lanka) (AMC: Anti-malaria Campaign; RBM: Roll Back Malaria). logarithmic scale blue lines; arithmetic scale red lines

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Fig. 2
figure 2

Panel 1 R ratios calculated from recorded cases for each year from 1995 to 2013. R ratio is below 1 for the years 2001 to 2007 and again for the years 2011 and 2012. In the years 2008 and 2009 there were two local outbreaks of malaria leading to the island wide R rising to 1 or above for the years 2008 to 2010. Panel 2 Recorded yearly number of cases (orange) and yearly cases calculated for R = 0.911 (blue) for period 2001 to 2013

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