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The role of improved housing and living environments in malaria control and elimination

Abstract

Malaria risk and endemicity is often associated with the nature of human habitation and living environment. The disappearance of malaria from regions where it had been endemic for centuries, such as coastal areas of southern England, has been attributed, at least in part, to improvement in the quality of housing. Moreover, indigenous malaria transmission ceased throughout England without the necessity to eliminate the vector mosquitoes. The principles of malaria transmission, as formulated following the thinking of the pioneers of malaria epidemiology, Ronald Ross and George Macdonald, show how this may happen. Malaria ceases to be sustainable where its reproduction number, R0, the number of new cases generated on average for each existing case of malaria, falls below 1. In the terms of a Ross/Macdonald analysis the reduced contact between humans and blood-feeding mosquitoes that is achieved through housing that is secure against mosquito entry can have a powerful effect in reducing malaria R0. The island of Sri Lanka, where malaria had been endemic probably for centuries previously, has reported no indigenous cases of malaria since 2012. The disappearance of malaria from Sri Lanka followed an effective attack upon malaria transmission by the Sri Lanka Anti Malaria Campaign. The targeted and enhanced efforts of this campaign launched in 1999, drove the malaria R0 below 1 for most of the period up to 2012, leading to a nearly continuous decline in malaria cases until their extinction. The decades leading up to the launch of these efforts were ones of general improvement of living environment and notably in the quality of housing stock. Studies in the late 1980s had shown that quality of housing in a highly malarious district of Sri Lanka was a strong determinant of malaria risk. Through its effects on malaria R0, improved housing is likely to have facilitated the malaria control and cessation of indigenous malaria transmission in Sri Lanka and that it will help reduce the risk of the re-introduction of malaria to the island.

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
figure1

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

Fig. 2
figure2

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

Availability of data and materials

Not applicable.

Abbreviations

R0:

Reproduction number

M:

Number of adult female malaria vector mosquitoes in a defined locality

a:

Daily mosquito biting rate upon humans

References

  1. 1.

    Boyd MF. Malariology. Philadelphia: WB Saunders; 1949.

    Google Scholar 

  2. 2.

    Carter R, Mendis KN. Evolutionary and historical aspects of the burden of malaria. Clin Microbiol Rev. 2002;15:564–94.

    Article  Google Scholar 

  3. 3.

    Tusting LS, Willey B, Lines J. Building malaria out: improving health in the home. Malar J. 2016;15:320.

    Article  Google Scholar 

  4. 4.

    Tatem AJ, Gething PW, Smith DI, Hay SI. Urbanization and the global malaria recession. Malar J. 2013;12:133.

    Article  Google Scholar 

  5. 5.

    Wang S-Q, Li Y-C, Zhang Z-M, Wang G-Z, Hu X-M, Qualls WA, et al. Prevention measures and socioeconomic development result in a decrease in malaria in Hainan, China. Malar J. 2014;13:362.

    CAS  Article  Google Scholar 

  6. 6.

    Rek JC, Alegana V, Arinaitwe E, Cameron E, Kamya MR, Katureebe A, et al. Rapid improvements to rural Ugandan housing and their association with malaria from intense to reduced: a cohort study. Lancet Planet Health. 2018;2:e83–94.

    Article  Google Scholar 

  7. 7.

    Dobson MJ. Malaria in England: a geographical and historical perspective. Parassitologia. 1994;36:35–60.

    CAS  Google Scholar 

  8. 8.

    James SP. The disappearance of malaria from England. Proc R Soc Med. 1929;23:71–87.

    CAS  Google Scholar 

  9. 9.

    Shute PG. Indigenous P. vivax malaria in London believed to have been transmitted by Anopheles plumbeus. Mon Bull Minist Health Public Health Lab Serv. 1954;13:48–51.

    CAS  Google Scholar 

  10. 10.

    Kuhn KG, Campbell-Lendrum DH, Armstrong B, David CR. Malaria in Britain: past, present, and future. Proc Natl Acad Sci USA. 2003;100:9997–10001.

    CAS  Article  Google Scholar 

  11. 11.

    Ross R. The prevention of malaria. London: John Murray; 1911.

    Google Scholar 

  12. 12.

    Macdonald G. The analysis of equilibrium in malaria. Trop Dis Bull. 1952;49:813–1129.

    CAS  Google Scholar 

  13. 13.

    Macdonald G. The epidemiology and control of malaria. London: Oxford University Press; 1957.

    Google Scholar 

  14. 14.

    Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, Macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8:e1002588.

    CAS  Article  Google Scholar 

  15. 15.

    Brady OJ, Godfray HCJ, Tatem AJ, Gething PW, Cohen JM, McKenzie FE, et al. Adult vector control, mosquito ecology and malaria transmission. Int Health. 2015;7:121–9.

    Article  Google Scholar 

  16. 16.

    Karunaweera ND, Galappaththy GNL, Wirth DF. On the road to eliminate malaria in Sri Lanka: lessons from history, challenges, gaps in knowledge and research needs. Malar J. 2014;13:59.

    Article  Google Scholar 

  17. 17.

    Wijesundere DA, Ramasamy R. Analysis of historical trends and recent elimination of malaria from Sri Lanka and its applicability to malaria control in other countries. Front Public Health. 2017;5:212.

    Article  Google Scholar 

  18. 18.

    Sri Lanka free of malaria. Case study. New Delhi: World Health Organization, Regional Office for South-East Asia; 2017.

    Google Scholar 

  19. 19.

    Premaratne R, Wickremasinghe R, Ranaweera D, Kumudu WM, Gunasekera AW, Hevawitharana M, et al. Technical and operational underpinnings of malaria elimination from Sri Lanka. Malar J. 2019;18:256.

    Article  Google Scholar 

  20. 20.

    Karunasena VM, Marasinghe M, Koo C, Amarasinghe S, Senaratne AS, Hasantha R, et al. The first introduced malaria case reported from Sri Lanka after elimination: implications for preventing re-introduction of malaria in recently eliminated countries. Malar J. 2019;18:210.

    Article  Google Scholar 

  21. 21.

    Housing and Sustainable Urban Development in Sri Lanka. National Report for the Third United Nations Conference on Human Settlements Habitat III. 2015. http://habitat3.org/wp-content/uploads/Sri-Lanka-%EF%BC%88Final-in-English%EF%BC%89.pdf.

  22. 22.

    Gamage-Mendis AC, Carter R, Mendis C, De Zoysa APK, Herath PRJ, Mendis KN. Clustering of malaria infections within an endemic population: risk of malaria associated with the type of housing construction. Am J Trop Med Hyg. 1991;45:77–85.

    CAS  Article  Google Scholar 

  23. 23.

    Gunawardena DM, Wickremasinghe AR, Muthuwatta L, Weerasingha S, Rajakaruna J, Senanayaka T, et al. Malaria risk factors in an endemic region of Sri Lanka, and the impact and cost implications of risk factor-based interventions. Am J Trop Med Hyg. 1998;58:533–42.

    CAS  Article  Google Scholar 

  24. 24.

    Premaratne R, Ortega L, Jankan N, Mendis KN. Malaria elimination in Sri Lanka: what it would take to reach the goal. WHO South-East Asia J Public Health. 2014;3:85–9.

    Article  Google Scholar 

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Acknowledgements

We thank Kamini Mendis, David L. Smith and Geoffrey Pasvol for their insightful comments and advice.

Funding

NDK is supported by the National Institute of Allergy and Infectious Diseases of the National Institutes of Health under Award Number U01AI136033. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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RC was the major contributor in synthesis of the theories behind the article. Both authors contributed to researching the context of the article and to writing the manuscript. Both authors read and approved the final manuscript.

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Correspondence to Nadira D. Karunaweera.

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Carter, R., Karunaweera, N.D. The role of improved housing and living environments in malaria control and elimination. Malar J 19, 385 (2020). https://doi.org/10.1186/s12936-020-03450-y

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Keywords

  • Malaria transmission
  • Malaria control
  • Malaria elimination
  • Housing
  • Ross/Macdonald equations
  • Reproduction number
  • Sri Lanka
  • Living environment
  • Socio-economic development