Population Changes: Magnitude, Mobility, and Disease Transfer

The human population of the earth took the whole of its existence until 1800 to build to 1 billion. By 2000 it had exceeded 6 billion, more than doubling in the twentieth century alone. In 1800, the time taken to navigate the globe by sailing ship was about a year. Today, no two cities served by commercial aircraft are more than a couple of days apart. Since this is less than most disease incubation times, infected people can travel undetected—a concern noted from the early days of commercial air travel. Within developed countries, the rate of individual circulation (in terms of average distances travelled) has increased 1,000-fold in the last 200 years. While the processes of population growth and geographical churn have been at work for the whole of human history, it is in the last two centuries that the momentum of change has gathered increasing pace. As described in Section 2.1, McMichael (2004) recognizes four separate stages. (i) Early human settlements from c.5,000 to c.10,000 years ago enabled enzootic pathogens to enter Homo sapiens populations. Some of these encounters led to the emergence of many of today’s textbook infections: influenza, tuberculosis, cholera, typhoid, smallpox, measles, malaria, and many others. (ii) Eurasian military and commercial contacts c.1,500 to c.3,000 years ago with swapping of dominant infections between the Mediterranean and Chinese civilizations. As described in Section 2.2, the plagues and pestilences of classical Greece and Rome date from this period. (iii) European exploration and imperialism from c.1500 with the transoceanic spread of often lethal infectious diseases. The impact on the Americas, on Australasia, and on remote island populations is well known; ships’ crews and passengers were the devastating vectors. (iv) The fourth great transition is today’s globalization, acting through demographic change and accelerating levels of contacts between the different parts of the world to facilitate disease emergence, re-emergence, and spatial transfer. Global warming, the destabilization of environments, the unparalleled movement of peoples rapidly across the globe through air transport, are all part of an evolving host–microbe relationship (cf. Section 1.3.1).

Disease Changes: Microbial and Vector Adaptation

In this and the next four chapters, we examine five change agents which have facilitated the emergence and re-emergence of infectious human diseases. Each agent—microbial and genetic adaptation, technology and industry, changes in host populations, environmental and ecological change, and war as a disease amplifier—has underpinned over the centuries both the appearance of new diseases and the waxing and waning of familiar infections. As shown in Figure II.1, the agents are not independent and commonly interact in complex ways to facilitate microbe emergence and re-emergence at different times and in different geographical locations. Accordingly, we also explore these interactions in our account. We begin here with microbial and vector adaptation. Disease microbes are in a continuous state of evolution, responding and adapting to the challenges and opportunities afforded by their hosts and their environments (Morse 1995). New pathogens are evolving, old pathogens are developing enhanced virulence and new clinical expressions, and susceptible pathogens are acquiring resistance to antimicrobial agents. In parallel, the environmental tolerance bands of both old and new pathogens are also changing (Cohen 1998). Not only are disease microbes in a continuous state of evolution. So, too, are the arthropod vectors that transmit many human pathogens. In the second half of the twentieth century, many of these vectors have developed tolerance to an expanding range of insecticides, larvicides, pupicides, and other chemical agents used in their control (World Health Organization 1992c). Against this background, our examination of microbial change and vector adaptation is structured around the three interlinked themes shown in Figure 4.1. We begin in Section 4.2 by examining the issue of natural variation in pathogens and illustrate this with special reference to the emergence and spread of novel subtypes of influenza A virus. We then examine the topic of selective pressure and genetic change in the context of the man-made problems of pathogen resistance to antimicrobials (Section 4.3) and vector resistance to insecticides (Section 4.4). The processes of microbial change and vector adaptation are not intrinsically geographical but they take place within, and are inextricably linked to, specific geographical environments. This gives a strong geographical emphasis to our discussion.

The Geographical Matrix

A historical–geographical exploration of disease emergence is confronted by a series of fundamental questions: Which diseases have emerged? When? And where? For some high-profile diseases, such as Legionnaires’ disease, Ebola viral disease, and severe acute respiratory syndrome (SARS), the first recognized outbreaks are well documented in the scientific literature and the space–time coordinates of these early events can be fixed with a high degree of certainty. But, for some other diseases—especially those that, over the decades, have periodically resurfaced as significant public health problems—the times and places of their rise to prominence can be harder to specify. Accordingly, in this chapter we undertake a content analysis of three major epidemiological sources to identify patterns in the recognition and recording of communicable diseases of public health significance in the twentieth and early twenty-first centuries. Our analysis begins, in Section 3.2, with an examination of global and world regional patterns of communicable disease surveillance as documented in the annual statistical reports of the League of Nations/World Health Organization, 1923–83. In Section 3.3, we turn to the US Centers for Disease Control and Prevention’s (CDC’s) landmark publication Morbidity and Mortality Weekly Report (MMWR) to identify ‘headline trends’ in the national and international coverage of communicable diseases, 1952–2005. Finally, in Section 3.4, the inventory of epidemic assistance investigations (Epi-Aids) undertaken by CDC’s Epidemic Intelligence Service (EIS), 1946– 2005, provides a unique series of insights from the front line of epidemic investigative research. Informed by the evidence presented in these sections, Section 3.5 concludes by specifying the regional–thematic matrix of diseases for analysis in Chapters 4–9. The systematic international recording of information about morbidity and mortality from disease begins with the Health Organization of the League of Nations, established in the aftermath of the Great War. The first meeting of the Health Committee of the Health Section of the League took place in August 1921 to consider ‘the question of organising means of more rapid interchange of epidemiological information’ (Health Section of the League of Nations 1922: 3).

Controlling Re-emerging and Newly Emerging Diseases

As earlier chapters in this book have shown, cyclically re-emerging old plagues and newly emerging scourges are, because of their multifactorial ecology, likely to be the enduring experience of the human race. And so, in this concluding chapter, we look at some of the broad ideas which lie behind disease control and which might be used to mitigate the impact of new or re-emerging infections. Linked to surveillance systems, quarantine and vaccination are currently the front-line approaches, and we discuss these in Sections 11.2 and 11.3. The chapter is concluded in Section 11.4 with an assessment of the twenty-first- century context within which containment of newly emerging and re-emerging diseases is likely to occur. It is helpful to consider control strategies for communicable diseases by setting them within a modelling framework. A basic susceptible–infective– removed (SIR) epidemic model was described in Section 10.2.1. As shown in Figure 11.1, protection against the spread of infection can be undertaken at two points. The first method, (i), is to interrupt the mixing of infectives and susceptibles with protective spatial barriers. This may take the form of isolating an individual or a community, or of restricting the geographical movements of infected individuals by quarantine; another approach is by locating populations in supposedly safe areas. The historical use of quarantine in protecting communities against the plague and other diseases is considered in Section 11.2. For animal populations, there exists a third possibility: the creation of a disease-free buffer zone by the wholesale evacuation of areas or by the destruction of those infected. The second method, (ii), is to short-circuit the route from susceptibles to removed by the establishment of immunity through some variant of immunization. Vaccination as a control strategy is discussed in Section 11.3. Potential control strategies are illustrated schematically in Figure 11.2. In the two maps, infected areas have been shaded, while disease-free areas have been left blank. In Figure 11.2A, the disease-free areas need to be protected by isolation.

Temporal Trends in Disease Emergence and Re-emergence: World Regions, 1850–2006

In Chapters 4–8, we have examined a series of processes that, often working in combination, have served to precipitate the emergence and re-emergence of infectious and parasitic disease agents in the human population. In this chapter, we conclude our survey with an analysis of temporal trends in disease emergence and re-emergence since 1850. The discussion is informed by long-term shifts in the underlying causes of mortality encapsulated in Omran’s model of epidemiological transition (Section 1.4.1), paying particular attention to the manner in which sample infectious and parasitic diseases have waxed and waned at a variety of geographical scales from the global to the local over the last ∼150 years. Our choice of examples strikes a balance between coverage of geographical regions and epidemiological environments, and coverage of important diseases that we have not so far examined in detail. Our consideration is structured by geographical scale: (1) At the global level, we discuss three major human diseases that have undergone phases of rapid global expansion since 1850—plague, cholera, and HIV/AIDS (Section 9.2). (2) At the regional level, we examine twentieth-century trends in general infectious disease mortality in the advanced economies of Europe, North America, and the South Pacific, 1901–75, before looking at time sequences for sample emerging (Ebola–Marburg) and cyclically re-emerging (meningococcal) diseases in sub-Saharan Africa (Section 9.3). (3) At the national level, we use Hall’s (1993) data to establish the main trends in morbidity due to infectious diseases in Australia, 1917–91 (Section 9.4). (4) At the local level, we extend our examination of long-term disease trends in London, described for the pre-1850 period in Section 2.4, into the late twentieth century (Section 9.5). The chapter is concluded in Section 9.6. In this section, we examine long-term trends in three major human infectious diseases that have undergone phases of global expansion in the last 150 years: plague (Section 9.2.1); cholera (Section 9.2.2); and HIV/AIDS (Section 9.2.3).

Disease Amplifiers: Wars and Conflicts in the Post-1945 Era

The history of war is replete with examples of novel diseases that have suddenly and unexpectedly erupted into human consciousness. As we noted in Section2.2, ancient Greek historians such as Herodotus, Thucydides, and Diodorus Siculus provide classical accounts of the devastation wrought by mysterious war pestilences—diseases which, in many instances, elude classification in modern disease systems, and to which the appellation ‘antique plague’ is occasionally given (Smallman-Raynor and Cliff 2004b: 66–73). In more recent times, we saw in Table 1.7 how maladies such as the idiopathic English sweating sickness, along with venereal syphilis, typhus fever, and yellow fever, appeared— ostensibly for the first time—in association with wars of the late medieval and early modern periods. In the twentieth century, trench fever (World War I, 1914–18), scrub typhus (World War II, 1939–45), and Korean haemorrhagic fever (Korean War, 1950–3) provide further instances of the emergence phenomenon (Macpherson et al. 1922–3; Philip 1948; Gajdusek 1956). In addition to sponsoring apparently wholly new conditions, military conflict has also promoted the re-emergence of many infectious and parasitic diseases. Recent examples include African trypanosomiasis (Ugandan Civil War, 1979–86; Berrang Ford 2007), diphtheria and tuberculosis (Tajikistan Civil War, 1992–7; Keshavjee and Becerra 2000; Usmanov et al. 2000) and epidemic louse-borne typhus fever (Burundian Civil War, 1993–2005; Raoult, Ndihokubwayo, et al. 1998). Figure 8.1 illustrates schematically the sample factors that underpin the warrelated emergence and re-emergence of infectious diseases. As Price-Smith (2002: 129) observes, military conflict acts ‘as a direct disease ‘‘amplifier,’’ creating those physical conditions (poverty, famine, destruction of vital infrastructure, and large population movements) that are particularly conducive to the spread and mutation of disease’. High-level population mobility and mixing, differential patterns of disease exposure and susceptibility, the breakdown of public health infrastructure, and insanitary living conditions are all pertinent to an understanding of the (re-)emergence complex (Lederberg et al. 1992: 110–12). Additional factors also attain prominence. Within the schema of Figure 8.1, heightened exposure to the zoonotic pool has played a particularly important role in the war-related precipitation of disease emergence and re-emergence.

Technical Changes: Technology and Industry

In this chapter, we examine the second of the five overlapping drivers of disease emergence and re-emergence shown in Figure II.1—technology and industry. Technological developments have yielded immeasurable benefits to society. In the field of medicine, for example, improvements in sanitation and hygiene, along with the widespread use of vaccines and antimicrobial drugs, have served to control and prevent the spread of infectious diseases. Likewise, improvements in intensive care, surgical techniques, cancer therapy, and therapies for other conditions have led to prolonged survival and an enhanced quality of life for many millions of people. But negative effects, too, have sometimes resulted from technological developments. Not least, such developments can provide, occasionally unwittingly, supportive environments for the proliferation and spread of pathogenic micro-organisms. Following Breiman (1996), Figure 5.1 identifies several key areas to these developments. The impact of technology on food production, distribution, and processing has had a substantial effect on the spread of infectious diseases, with potential contamination occurring at all stages of production and processing. The centralization of production and the increased international sourcing of foodstuffs has also had an impact on foodborne disease activity. In addition, current methods of storing foods have resulted in the emergence of foodborne pathogens; an example is provided by outbreaks of Listeria monocytogenes. This bacterium has been found in a variety of raw foods, such as uncooked meats and vegetables, as well as in processed foods that become contaminated after processing, such as soft cheeses and cold cuts from delicatessens, in unpasteurized (raw) milk, and in foods made from unpasteurized milk. Listeria thrives in refrigerated environments and, in its presence, widespread contamination of stored refrigerated food products can occur. Legionnaires’ disease is the paradigmatic disease associated with technological innovation, with cooling towers, evaporative condensers, whirlpools, spas, and showers providing temperatures which promote the survival and proliferation of the causative bacterium, Legionella pneumophila. Municipal water systems are efficient conduits for the dissemination of pathogenic micro-organisms. While most water supplies in developed countries are effectively treated in municipal water treatment facilities, the treatment may occasionally be ineffective owing to faulty procedures or the development of resistance of an organism to routine procedures.

Disease Emergence and Re-emergence Prior to 1850

Infectious diseases have been evolving since the dawn of humankind. In Section 1.3, we noted some of the palaeopathological studies that have extended our knowledge of the occurrence of human infections back into pre-history, while recent genetic studies have indicated that the agents of diseases such as malaria (Plasmodium spp.) and leprosy (Mycobacterium leprae) first emerged in the human species many thousands of years ago (Carter and Mendis 2002; Monot et al. 2005). For the most part, however, our knowledge of the long history of disease emergence is based on the written record of earlier ages. In the present chapter, in so far as the historical evidence allows, we provide a brief and necessarily highly selective overview of disease emergence and cyclical re-emergence from the beginning of the written record to the mid-nineteenth century. McMichael (2004) identifies four great historical transitions in the relationship of humans and microbes that, since the initial advent of agriculture and livestock herding, have promoted the emergence and re-emergence diseases. These four transitions, each associated with a progressive increase in the geographical scale of operation (local → continental → intercontinental → global), are: (i) First historic transition (5,000–10,000 years ago). A local transition when early agrarian-based settlements brought humans into contact with sylvatic enzootic pathogens. As described under the ‘domestic-origins hypothesis’ in Section 1.3.2, close and prolonged exposure to domesticated animals and urban pests (for example, rodents and flies) resulted in the cross-species transmission of the ancestral agents of many modern-day human infectious diseases, including influenza, measles, smallpox, tuberculosis, and typhoid. (ii) Second historic transition (1,500–3,000 years ago). A continental-level transition fuelled by the military and trade contacts of early Eurasian civilizations which resulted in the cross-civilization transmission of infectious agents. In the wake of this historical transition, a trans- European ‘equilibration’ of infectious agents occurred and the diseases became endemic to the population. (iii) Third historic transition (200–500 years ago). An intercontinental transition associated with European expansion, resulting in the transoceanic spread of infectious agents.

Spatial Detection of (Re-)emerging Diseases

The development of models and surveillance systems to give early warning of a new or re-emerging disease is an important first step in devising control strategies to protect the public health. In this chapter, we discuss and illustrate modelling and surveillance approaches to (re-)emerging disease detection before considering in Chapter 11 what control strategies might be used to mitigate new threats. We begin by reviewing in Section 10.2.1 the generic SIR (susceptible ⇒ infected ⇒ removed) mass action models commonly used to model the spread of infectious diseases in human and many animal populations, before moving on to present a robust spatial derivative, the so-called swash–backwash model (Section 10.2.2). This model is applied in Section 10.3 to data from France, Iceland, and a small English town, Cirencester, to show, for the cyclically reemerging disease of influenza, how the model readily separates pandemic years from the normal run of influenza seasons. While it is encouraging that the model can spot pandemic years in the train of annual epidemics, influenza is an odd disease in that pandemics occur when a new strain of the causative A virus emerges to afflict the human population. To test the model further, we apply it in Section 10.4 to a set of 14 measles waves for Iceland, 1916–75, waves caused by an unchanging virus in a changing population. Our discussion of the swash–backwash model is concluded in Section 10.5, where it is shown how it can be used as part of a real-time surveillance-based earlywarning system for new disease threats. Any modelling approach to identifying newly emergent or re-emerging diseases can only be as good as the data which are supplied to the models. Accordingly, in Section 10.6, advances in surveillance methodology are outlined which have been facilitated by developments in communications technology, especially the Internet. The chapter is concluded in Section 10.7.

Environmental Changes: Ecological Modifications

Diseases originate, spread, and persist or wither, within a specific environmental context. For the entire time during which humans have lived on the earth, this environmental context has changed and, viewed from the beginning of a new millennium, all the available evidence suggests that the environment is set to change further and faster than at any other time in human history. In this chapter, we explore aspects of the changing environmental terrain in which diseases spread, and how these changes have served to promote the emergence and resurgence of infectious agents. Anthropogenic environmental changes and ecological modifications that promote the emergence and resurgence of infectious diseases are numerous and include deforestation and reforestation, road construction, agricultural development, dam building, irrigation and water control schemes, coastal zone degradation and wetland modification, mining and urbanization, and macro- and micro-climate change and variability (Morse 1995; Patz, Graczyk, et al. 2000; Patz, Daszak, et al. 2004; McMichael 2004). As Patz, Daszak, et al. (2004: 1092) observe, these changes and modifications can, in turn, provoke a ‘cascade effect’ of habitat fragmentation, ecosystem degradation, and biodiversity loss, pollution, poverty, and human migration that serve to amplify the risks of disease emergence and spread. Examples of infectious diseases that are known or suspected to be especially prone to the effects of environmental and land use change are given in Table 7.1. Of the many environmental and land use changes that can facilitate the processes of infectious disease emergence and resurgence, we have selected the five interlinked factors in Figure 7.1 for study here. We illustrate each factor with special reference to one or more examples drawn from the sample diseases and regions listed in Table 7.2. Our examples include: agricultural development and Argentine haemorrhagic fever in South America (Section 7.2); water control schemes and Rift Valley fever in Africa and the eastern Mediterranean (Section 7.3); deforestation and Nipah viral disease in the western Pacific (Section 7.4.1); reforestation and Lyme disease in North America (Section 7.4.2); climate variability and hantavirus pulmonary syndrome in North America (Section 7.5); and natural disasters and disease in North America and South-East Asia (Section 7.6).