Inflammatory bowel disease and the hygiene hypothesis: an argument for the role of helminths

Abstract

The hygiene hypothesis [ 1 , 2 ] argues that in developed nations the lack of childhood exposure to infectious pathogens, parasites, and symbiotic microorganisms increases susceptibility to allergy and other chronic diseases in adulthood. A modified hygiene hypothesis, (‘the old friends hypothesis’ proposed by G. A. Rook [ 3 ]) excludes childhood diseases as a requisite factor and focuses on organisms such as lactobacilli, a variety of saprophytic mycobacteria and helminthic parasites that are tolerated by the immune system and are absent from the pathogen load of developed nations. The exposure to these ubiquitous agents is postulated to help in the development of the T regulatory response that when absent in industrialized nations results later in the manifestation of allergies and an array of autoimmune diseases such as inflammatory bowel disease, multiple sclerosis, and Type 1 diabetes [ 3 ]. To evaluate this hypothesis, I will examine the pattern of human diseases using a model of epidemiological transition modified from A. R. Omran’s [ 4 – 7 ] original formulation. The epidemiological transition provides a means of understanding the changing relationship between humans, pathogens and other disease insults from the Paleolithic period to the present [ 8 ]. The adaptation of hominid populations in the Paleolithic created a disease ecology that minimized the impact of infectious disease but exposed the foragers to many saprophytic mycobacteria in the soil and decaying plant matter. The shift to agriculture about 10,000 years ago heralded the first epidemiological transition characterized by the continued exposure to helminths and saprophytic environmental organisms, plus the emergence of additional infectious and nutritional diseases that continue to the present. The acceleration of urbanization and social inequality increases the spread of infectious disease. Within the last century, some populations have undergone the second epidemiological transition in which public health measures, improved nutrition and medicine resulted indeclines in infectious disease and a rise in non-infectious, chronic and degenerative diseases. This phase with the control of infectious disease and the development of a sanitized water supply and sewer system has played a role in the modified hygiene or ‘old friends’ hypothesis. It is a period in which ‘cleanliness’ [ 9 ] removes us from contact with ‘dirt’ [ 10 , 11 ].