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The Four Epidemiological Stages in the Global Evolution of Inflammatory

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The Four Epidemiological Stages in the Global Evolution of Inflammatory PERSPECTIVES the next is a result of human influence: the factors that contribute to these transitions The four epidemiological stages in include industrialization, urbanization and westernization of society10. the global evolution of inflammatory By combining epidemiological principles with temporal prevalence trends, a fourth bowel disease stage can be postulated: Prevalence Equilibrium, the countervailing force Gilaad G. Kaplan and Joseph W. Windsor between the increasing mortality of an ageing IBD population and the incidence Abstract | Inflammatory bowel disease (IBD) is a global disease; its evolution can be of IBD (Fig. 1). Prevalence Equilibrium stratified into four epidemiological stages: Emergence, Acceleration in Incidence, represents a future epidemiological stage Compounding Prevalence and Prevalence Equilibrium. In 2020, developing that has yet to materialize but provides the framework for predicting the future global countries are in the Emergence stage, newly industrialized countries are in the burden of IBD. Understanding the changing Acceleration in Incidence stage, and Western regions are in the Compounding epidemiological patterns is critical to Prevalence stage. Western regions will eventually transition to the Prevalence provide clues to the pathogenesis of disease Equilibrium stage, in which the accelerating prevalence levels off as the IBD and to support health-care systems in population ages and possibly as a result of an unexpected rise in mortality during addressing the rising global burden. the COVID-19 pandemic. Mitigating the global burden of IBD will require In this Perspective, we provide evidence of the epidemiological stages of IBD using concerted efforts in disease prevention and health- care delivery innovations that real- world data from different regions across respond to changing demographics of the global IBD population. In this the globe. We show how postulating a fourth Perspective, we summarize the global epidemiology of IBD and use these data to stage in IBD evolution provides a theoretical stratify disease evolution into four epidemiological stages. framework for predicting the future burden of disease. A glossary of relevant terms and new terminology introduced herein The journey from a few sporadic cases transition proposed by Omran was the Age is detailed in BOx 1, and a video abstract of inflammatory bowel disease (IBD) of Degenerative and Human-Influenced and interactive map are available online to millions of people with IBD is a Diseases that arises in industrialized (see Related links). 250- year path beginning with the industrial and urbanized societies6. Mortality is revolution1. The distribution of IBD was dominated by non-communicable diseases, Stage one: Emergence of IBD initially thought to be bound by ethnicity the occurrence of which is influenced by In many ways, the evolution of IBD parallels and geography — predominantly affecting environmental pressures such as nutrition the evolution of biological species; thus, people of Western European descent2. and lifestyle behaviours6. This final stage we take a cue from the father of evolution, By the end of the twentieth century, these is a proposed anthropological explanation Charles Darwin, who had a surprising boundaries had been shattered with the for the rise in chronic inflammatory connection to the emergence of IBD himself. disease recorded on every populated conditions7. In a 2018 editorial, Kedia and On 27 December 1831, Darwin embarked continent of the globe3,4. Whereas Ahuja postulated that IBD is an example of on a 5-year journey from England to the the incidence of IBD in the Western Omran’s final stage8. coast of South America, across southern world increased in the twentieth century, The evolution of IBD occurs within Australia, around the Horn of Africa and the incidence began to increase in newly Omran’s Degenerative and Human- back to England. Only 18 months of this industrialized countries at the turn of the Influenced Diseases age and has occurred journey was on water; the rest of the time, twenty- first century4. across three distinct epidemiological stages Darwin explored foreign lands and made In 1971, Omran proposed the (Fig. 1): Emergence, Acceleration in Incidence observations that formed the basis of the Epidemiologic Transition Theory to explain and Compounding Prevalence. Emergence theory of evolution. In 1859, his seminal human population growth via predominant is represented by sporadic case reports of book On The Origin of Species By Means drivers of mortality5. The pre-industrial IBD2. Acceleration in Incidence is a tipping of Natural Selection was published, which society was labelled the Age of Pestilence point whereby incidence steadily increases revolutionized our understanding of and Famine, in which populations were over several decades, although prevalence biology11. Throughout his adult life, Darwin limited by epidemic outbreaks, deprivation remains low3. Compounding Prevalence was plagued — even while writing his most and wars. The Age of Receding Pandemics reflects a steady increase in the population famous book — with undiagnosed, chronic, reflects a reduction in mortality crises and living with IBD, despite stabilization or gastrointestinal symptoms (for example, a greater burden of endemic diseases (for even a decline in incidence9. The transition abdominal pain, vomiting, ulcerations example, malaria and tuberculosis). The final from one stage in the evolution of IBD to in the mouth, eczema and peripheral 56 | JANUARY 2021 | VOLUME 18 www.nature.com/nrgastro PERSPECTIVES Western world Prevalence Incidence 1750 1950 2000 2020 2050? Newly industrialized countries 1950 2000 2020 Developing countries 2000 2020 Burden of disease Burden Emergence Acceleration in Incidence Compounding Prevalence Prevalence Equilibrium Epidemiological stages Fig. 1 | Four epidemiological stages of IBD evolution. The changing pattern in the incidence (orange) and prevalence (blue) of inflammatory bowel disease (IBD) across the four the stages of IBD evolution. Developing countries are in the Emergence stage, during which sporadic cases of IBD are docu- mented. Newly industrialized countries are in the Acceleration in Incidence stage, during which incidence rises and prevalence is relatively low. Countries of the Western world are in the stage of Compounding Prevalence, during which incidence is stable, but prevalence is rising steeply. The slope of the prevalence increase will level off with the transition to the Prevalence Equilibrium stage, which represents the opposing force between an ageing IBD population and the incidence of IBD. neuropathy)12. Initially, it was believed that non- infectious, gastrointestinal disease was Awareness of ulcerative colitis he had contracted Chagas disease in South in 1859 by British physician Samuel Wilks expanded during the early twentieth America, but this has been challenged on — the same year that Darwin published century; additionally, an inflammatory the basis that he experienced coexisting his book while possibly affected by the disorder outside the colon was beginning eye and skin inflammation suggestive of yet- unrecognized Crohn’s disease15. On the to be recognized. Wilks’s original case an underlying diagnosis of Crohn’s disease heels of Wilks’s classification, several case report in 1859 (later understood to be a — a diagnosis that was unheard of during reports were published in Europe and the case of Crohn’s disease) described ileal Darwin’s lifetime (1809–1882)12. USA, including a case series from William inflammation15. T. Kennedy Dalziel reported The first stage in the evolution of IBD — Hale White in 1888 that introduced the term a surgical case series in 1913 that described Emergence — occurred in North America ulcerative colitis into the medical lexicon16. chronic inflammation of the terminal and Western Europe following the advent With the formal naming of ulcerative colitis, ileum19. Finally, the landmark 1932 paper by of the industrial revolution. James Watt the Western world became rooted in the first Crohn et al. on regional ileitis fundamentally modified the steam engine in 1764, which stage of IBD evolution17. entrenched two distinct gastrointestinal triggered the industrial revolution that led By the early 1900s, awareness of ulcerative chronic inflammatory diseases under the to fundamental societal shifts involving colitis was mounting with the transition paradigm of IBD and established Crohn’s manufacturing, urbanization, agriculture from sporadic case reports to regularly disease as clinically distinct from ulcerative and transportation. In this milieu, IBD recognizable diagnoses. In 1909, the Royal colitis20. By the 1950s, ulcerative colitis emerged in the Western world, starting as a Society of Medicine assembled a symposium and Crohn’s disease were established in the handful of case studies published at the end in London, England, to address the surge in Western world, which was then in the process of the eighteenth century to taking root as the number of cases of ulcerative colitis. The of shifting to the second epidemiological a new affliction of health2. Matthew Baillie, physicians at the symposium reviewed stage in the evolution of IBD. in his 1793 publication Morbid Anatomy the 317 documented cases of ulcerative By contrast, recognition of IBD in the first of Some of the Most Important Parts of the colitis that had been collected from seven half of the twentieth century in developing Human Body, reported among the earliest
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