Editor’s comments on climate change and the vectors of tropical human parasitic diseases

Dr Jillian Lenné (#1810) has provided an introduction to climate change and plant disease.

She noted the paucity of information on food crops in developing countries. This lack of evidence is partly caused by the concentration of research effort on fungal diseases of major cereal crops and the complexity of the interactions. 

A similar situation occurs with tropical diseases of humans requiring insect vectors. Mosquitoes and flies are by far the most common vectors of disease, including animal diseases which can be transmitted to humans. These are known as zoonotic diseases. 

Widespread diseases include: malaria, leishmaniasis, schistosomiasis, onchocerciasis, lymphatic filariasis, Chagas disease, African trypanosomiasis, and dengue1.

Many tropical diseases such as malaria, Chagas disease and dengue are transmitted to humans by blood sucking insects: principally: Anopheles spp., Aedes agyptiTrypanosoma cruzi and Triatoma spp.These vector-borne diseases continue to have a major impact on human health in the developing world. Each year, more than a billion people become infected and around a million people die from these diseases which are responsible for one in six cases of illness and disability worldwide2.

Malaria arguably continues to attract the most attention of all vector-borne diseases by virtue of causing the greatest global disease burden. However, others such as the virus which causes dengue are not only resurgent in some regions, but threaten a significant- proportion of the world’s population.

Climate change is very likely to favour an increase in the number of dengue cases worldwide, while many important mosquito populations that are able to transmit devastating diseases are changing in their distribution. These will be strongly affected by climatic factors such temperature, humidity, and precipitation rate. Different diseases, transmitted by different vectors, respond in different ways to changing weather and climate patterns3.

Many areas of Europe (including the UK) could become increasingly hospitable over the coming decades for mosquitoes, such as Aedes albopictus  which transmits the dengue virus. Other mosquito range expansions are likely to occur in the US and eastern Asia. If dengue and/or chikungunya are imported into these regions, there will be a considerable increase in the worldwide number of vulnerable individuals who will be affected4,5.

Disease vectors may evolve in under a decade to changes in temperature, which conflicts with many current models that assume climate change only affects their ecology, not their evolution6.

Predictions that might be affected by climate change must therefore not only take account of these uncertainties, but also allow for the migration of human populations. In addition to a warmer climate north of the equator the spread of diseases to temperate latitudes is also very likely be affected by other factors such as increased travel of humans and of domestic animals, and changes in rainfall distribution.

The mosquito is known to be extremely sensitive to temperature and rainfall. Consequently climate change represents a substantial threat to future human health, in accord with changes in the behaviour of disease carriers. It seems unquestionable that climate change will affect many, if not all, of these diseases. What is less clear, however, is the extent to which climate changes will affect the risk of infection compared to other factors, such as poverty or fragile health systems.

Malaria, it is still a threat to many people throughout the world and is a good example of the complexity of the interactions affecting disease. Although the number of new cases of malaria appears to be declining worldwide7, case numbers are still increasing in many regions for a variety of reasons such as insecticide resistance and changes in land use.

There is also some difficulty in maintaining political interest7. It is worthwhile briefly describing the natural history of malaria so that the relation of climate to its epidemiology in human society can be understood.

Only females of certain species of the Anopheles mosquito can transmit malaria. Malaria is caused by Plasmodium, a one-celled protozoan parasite, over 200 species of which can cause malaria, although only five are responsible for the disease in humans of which four are the most frequent: 

P. falciparum, P. vivax, P. ovale, and P. malariae are responsible for almost all of human malariainfections, but the distribution of Plasmodium species varies between different animals.

Vertebrate hosts simply serve as a site for the parasite to replicate asexually, whereas the sexual replication occurs in the mosquito. To act as a reservoir, the host must suffer a long term infection. P. vivax is one species noted for its ability to form a dormant stage in the liver, and cause relapses. The parasite can be dormant in the liver for days or years, causing no symptoms and remaining undetectable in blood tests.

It forms a hypnozoite ("sleeping organism"), a small form that resides in an individual liver cell. The hypnozoites allow the parasite to survive in more temperate zones, where mosquitoes bite for only part of the year. There must be thousands of individuals presently living in the EU who are hosts of this dormant stage- several of my acquaintances included. 

Birds, bats, lizards and antelopes are also hosts for malaria parasites. There are a few species of monkeys which can be infected. Cows, chimps, gorillas and humans are known to carry P. falciparum. Humans with sickle cells (abnormal erythrocytes) also act as a reservoir in a different way, perhaps more or less invisible or innocuous. Sickle cells may also have some effect in cows, chimps and gorillas.8

Some species of Plasmodium affect domestic animals and so climate changes might also affect stock welfare and productivity.

The female Anopheles, a zoophilic mosquito, picks up the parasite from infected people when bitten to obtain blood to nurture their eggs. Inside the mosquito the parasites reproduce and develop. When the mosquito bites again, the parasites contained in the salivary gland are injected into the blood of the person being bitten. Now there are sites in the British Isles where mosquitoes of the Anopheles genus breed (An. atroparvus, An. algeriensis, An. messeae,An. clavigerand An. plumbeus have been identified ).

An. messeae was formerly the main vector of malaria over a large part of European Russia. A case of Plasmodium vivax occurred in London in 1953. An. plumbeus was suspected to be the vector9

With increasing international travel and migration, it is only time before someone entering the British Isles with the parasite in their blood, or someone carrying the dormant parasite develops the disease, that the first outbreak (in our current era) will occur.

Nevertheless, it is certainly possible for other vertebrate hosts, both warm and cold-blooded, to act as a zoonotic source and spread malaria to humans. But it is thought unlikely to be occurring at an epidemiologically significant rate. Thus, asfar as is known, humans are the main source of transmission to other humans.

This probably depends on the species of plasmodium causing the infection, which is independent of the original source of human infection. For example, P. falciparum-like parasites have been identified in the faeces of western gorillas (Gorilla gorilla)10.

How climate change may affect disease prevalence has received very little attention. Almost all models are based on single diseases. So understanding how climate change affects interactions between the multiple diseases affecting most human populations is a mystery11.

We have tended to react to disease outbreaks as they occur, but we need to be more proactive. We cannot stop outbreaks of many of these diseases, but proactive risk management is less expensive (and more effective) than responding after a crisis. The challenge is not to address specific health risks owing to climate change, but to ensure sustained progress is made towards decreasing the number of deaths these diseases cause for future generations.

Conclusions

1. Disease vectors may evolve in under a decade to changes in temperature, which conflicts with many current models that assume climate change only affects their ecology, not their evolution. 

2. The continued spread of insecticide resistance, changes in land use, and difficulties in maintaining political interest will affect the distribution of insect vectors.

3. Changes in rainfall distribution will also affect the distribution and reproduction of these vectors,as mosquitoes are known to be extremely sensitive to temperature and rainfall.

4. Many areas of Europe could become increasingly hospitable for mosquitoes, e.g. Aedes albopictus that transmits the dengue virus.

5. Five species of Anopheles mosquitohave been identified in the British Isles – two of which have been recorded as transmitting Plasmodium (malaria) in Europe generally.

6. Humans are infected by five species of Plasmodium of which four are the most frequent.

7. Although cows, chimps, gorillas, humans are known, for example, to carry P. falciparum protozoa, humans are considered to be the main source of transmission of malaria to other humans. But a high proportion of these populations are burdened with multiple diseases further complicating solutions.

REFERENCES

1. Robert W. Sutherst*(2004) Global Change and Human Vulnerability to Vector-Borne Diseases Clin. Microbiol. Rev. Jan; 17(1): 136–173. doi:  10.1128/CMR.17.1.136-173.2004 PMCID: PMC321469 PMID: 14726459.

2. WHO (2014) Who day – 2014 A global brief on vector borne diseases.

3. WHO (2018) Dengue and severe dengue, 2 February.

4. Jan C Semenza Jonathan E Suk (2018) Vector-borne diseases and climate change: a European perspective  FEMS Microbiology Letters, 365, Issue 2, 1 January 2018, fnx244,https://doi.org/10.1093/femsle/fnx244.

5. Andrew K. Githeko, 1 Steve W. Lindsay, 2 Ulisses E. Confalonieri, 3 & Jonathan A. Patz (2000) Climate change and vector-borne diseases: a regional analysis. World Health Organization, Bulletin of the World Health Organization, 78 (9).

6. Paul Parham(2015)Hard Evidence: will climate change affect the spread of tropical diseases? The Conversation, February 17, 6.13am GMT.

7. Anon. (2017) A special edition of the Philosophical Transactions of the Royal Society B. Biological Sciences, 372,(1722) ed. Hillary S.

8. Boris Makanga, Patrick Yangari, Nil Rahola, Virginie Rougeron, Eric Elguero ,Larson Boundenga, Nancy Diamella Moukodoum, Alain Prince Okouga et al. (2016) Ape malaria transmission and potential for ape-to-human transfers in Africa. Proc Natl Acad Sci. USA. May 10; 113 (19): 5329–5334. Published online 2016 Apr 11. doi: 10.1073/pnas.1603008113 PMCID: PMC4868493 PMID: 27071123.

9. Snow, K (1998)European Mosquito Bulletin, 1 (1998) Distribution of Anopheles mosquitoes in the British Isles, 9-13 Journal of the European Mosquito Control Association ISSN1460-6127.  

10. Paul M. Sharp, Weimin Liu, Gerald H. Learn, Julian C. Rayner, Martine Peeters, and Beatrice H. Hahn (2011) Source of the human malaria parasite Plasmodium falciparum. PNAS September 20, 2011. 108 (38) E744-E745; https://doi.org/10.1073/pnas.1112134108.

11.Cheung, A. (2015) Hard Evidence: will climate change affect the spread of tropical diseases? Climate and Environment at Imperial, Imperial College, London, 19 February 2015.