The allergy epidemics: 1870-2010
2015; Elsevier BV; Volume: 136; Issue: 1 Linguagem: Inglês
10.1016/j.jaci.2015.03.048
ISSN1097-6825
Autores Tópico(s)Asthma and respiratory diseases
ResumoBefore the first description of hay fever in 1870, there was very little awareness of allergic disease, which is actually similar to the situation in prehygiene villages in Africa today. The best explanation for the appearance and subsequent increase in hay fever at that time is the combination of hygiene and increased pollen secondary to changes in agriculture. However, it is important to remember that the major changes in hygiene in Northern Europe and the United States were complete by 1920. Asthma in children did not start to increase until 1960, but by 1990, it had clearly increased to epidemic numbers in all countries where children had adopted an indoor lifestyle. There are many features of the move indoors that could have played a role; these include increased sensitization to indoor allergens, diet, and decreased physical activity, as well as the effects of prolonged periods of shallow breathing. Since 1990, there has been a remarkable increase in food allergy, which has now reached epidemic numbers. Peanut has played a major role in the food epidemic, and there is increasing evidence that sensitization to peanut can occur through the skin. This suggests the possibility that changes in lifestyle in the last 20 years could have influenced the permeability of the skin. Overall, the important conclusion is that sequential changes in lifestyle have led to increases in different forms of allergic disease. Equally, it is clear that the consequences of hygiene, indoor entertainment, and changes in diet or physical activity have never been predicted. Before the first description of hay fever in 1870, there was very little awareness of allergic disease, which is actually similar to the situation in prehygiene villages in Africa today. The best explanation for the appearance and subsequent increase in hay fever at that time is the combination of hygiene and increased pollen secondary to changes in agriculture. However, it is important to remember that the major changes in hygiene in Northern Europe and the United States were complete by 1920. Asthma in children did not start to increase until 1960, but by 1990, it had clearly increased to epidemic numbers in all countries where children had adopted an indoor lifestyle. There are many features of the move indoors that could have played a role; these include increased sensitization to indoor allergens, diet, and decreased physical activity, as well as the effects of prolonged periods of shallow breathing. Since 1990, there has been a remarkable increase in food allergy, which has now reached epidemic numbers. Peanut has played a major role in the food epidemic, and there is increasing evidence that sensitization to peanut can occur through the skin. This suggests the possibility that changes in lifestyle in the last 20 years could have influenced the permeability of the skin. Overall, the important conclusion is that sequential changes in lifestyle have led to increases in different forms of allergic disease. Equally, it is clear that the consequences of hygiene, indoor entertainment, and changes in diet or physical activity have never been predicted. Information for Category 1 CME CreditCredit can now be obtained, free for a limited time, by reading the review articles in this issue. Please note the following instructions.Method of Physician Participation in Learning Process: The core material for these activities can be read in this issue of the Journal or online at the JACI Web site: www.jacionline.org. The accompanying tests may only be submitted online at www.jacionline.org. Fax or other copies will not be accepted.Date of Original Release: July 2015. Credit may be obtained for these courses until June 30, 2016.Copyright Statement: Copyright © 2015-2016. All rights reserved.Overall Purpose/Goal: To provide excellent reviews on key aspects of allergic disease to those who research, treat, or manage allergic disease.Target Audience: Physicians and researchers within the field of allergic disease.Accreditation/Provider Statements and Credit Designation: The American Academy of Allergy, Asthma & Immunology (AAAAI) is accredited by the Accreditation Council for Continuing Medical Education (ACCME) to provide continuing medical education for physicians. The AAAAI designates this journal-based CME activity for a maximum of 1 AMA PRA Category 1 Credit™. Physicians should claim only the credit commensurate with the extent of their participation in the activity.List of Design Committee Members: Thomas A. E. Platts-Mills, MD, PhD, FRSDisclosure of Significant Relationships with Relevant CommercialCompanies/Organizations: T. A. E. Platts-Mills has received research support from the National Institute of Allergy and Infectious Diseases, has received consulting fees and royalties from Thermo Fisher, and has received travel support from Merck.Activity Objectives1.To trace the onset and progression of asthma and allergies from 1870-2010 and, in particular, its relation to improvements in public hygiene.2.To understand the major theories behind the epidemic increase in asthma since 1960 and the supporting evidence for this increase.3.To review the relevant environmental and lifestyle changes that might be associated with the increasing prevalence of allergic disease.Recognition of Commercial Support: This CME activity has not received external commercial support.List of CME Exam Authors: Niti S. Agarwal, MD, Gina Coscia, MD, and Rachel L. Miller, MD.Disclosure of Significant Relationships with Relevant CommercialCompanies/Organizations: The exam authors disclosed no relevant financial relationships.The human race has come to dominate its environment so completely that any analysis of the increase or appearance of a disease has to take changes in our lifestyle into account. In the case of allergic disease changes in our environment, diet, water quality, and personal behavior over the last 150 years have played a dominant role in the specificity of these diseases, as well as in prevalence and severity. The first thing to address is when “the epidemic” started and how much the increase in different allergic diseases has occurred separately. It should be noted that some or most previous reviews have implied that the increase in allergic disease has been unimodal, but actually, that has never been a tenable analysis. Not only have increases occurred or are currently occurring at different times in different countries, but also hay fever, asthma, and peanut allergy have had strikingly different time courses both in Europe and North America.Occasional descriptions of allergic disease occurred in antiquity, such as the suggestion that one of the pharaohs died of anaphylaxis after a bee sting.1Bergmann K. Ring J. History of allergy in antiquity.in: History of allergy. Karger, Unionville (CT)2014Google Scholar The first convincing description of hay fever was by John Bostock, who described his own symptoms in 1828. The first investigations of hay fever were published in the 1870s by Blackley,2Blackley C.H. Experiments and researches on the causes of nature of catarrhus aestivas. Balliere, London1873Google Scholar who studied grass pollen in the United Kingdom, and Wyman,3Wyman M. Autumnal catarrh (hay fever). Huro & Houghton, Cambridge (MA)1872Google Scholar who studied ragweed pollen in the United States. At that stage, the only recognized allergic disease was hay fever, and reports of an increase came from Germany, as well as the United Kingdom and United States. It is important to recognize that there were no clear reports of an increase in pediatric asthma until 1970. Furthermore, the current “epidemic” of food allergy does not appear to have started until after 1990.This review will attempt to evaluate both the evidence for those increases and the changes that have occurred in lifestyle that could have contributed to sequential increases in different allergic diseases.The hay fever epidemicIn 1982, Lady Simon, with a startling level of confidence about her facts, asked the author of this review, “Why did hay fever start in 1870?”4Platts-Mills T. Local production of IgG, IgA and IgE antibodies to pollen allergen in patients with hay fever [PhD thesis]. London University, London (UK)1983: 163Google Scholar She then explained that her father had symptoms of allergic rhinitis and conjunctivitis in Germany in June of 1875, but after several years of symptoms, he could not find a physician who was aware of the condition. By 1890, he knew a group of such patients, but none of them had symptoms before 1870. Blackley2Blackley C.H. Experiments and researches on the causes of nature of catarrhus aestivas. Balliere, London1873Google Scholar started studying the disease in Manchester, United Kingdom, in the 1860s, but his studies, including skin tests and challenge tests with grass pollen out of season, were primarily performed on himself (Fig 1). By 1900, the disease was well recognized and sufficiently severe for 2 developments.1.Sites at which patients with hay fever could go during the season to avoid exposure to pollen were identified, and thus the island of Heligoland in the North Sea was kept free of grass pollen, and Bretton Woods Resort in New Hampshire was recognized as a retreat from the ragweed season by the United States Hay Fever Association (Fig 1).5Mitman G. Hay fever holiday: health, leisure, and place in gilded-age America.Bull Hist Med. 2003; 77: 600-635Crossref PubMed Scopus (43) Google Scholar2.The earliest investigations of the effects of injections of pollen extract were carried out with the objective of establishing immunity against pollen toxin. Those experiments were published by Dunbar6Dunbar W. The present state of knowledge of hay fever.J Hyg (Lond). 1913; 13: 105-148Crossref PubMed Scopus (46) Google Scholar in Germany and most significantly by Noon7Noon L. Prophylactic innoculation for hay fever.Lancet. 1911; i: 1572Abstract Scopus (1110) Google Scholar in the United Kingdom.The question to address is what happened in the second half of the 19th century that could have contributed to the appearance and progressive increase in seasonal allergic rhinitis. It seems likely that changes in both airborne pollen and public hygiene contributed. In England major changes in agriculture followed the reform of the corn laws in 1847.8Briggs A. The making of modern England 1783-1867: the age of improvement. Routledge, New York (NY)1959: 314Google Scholar That reform allowed the import of cheap wheat from Odessa in the Ukraine with the result that much of English farm land lay fallow.9deWaal E. The hare with amber eyes. Picador, Farrr, Straus and Giroux, New York (NY)2010Google Scholar Between 1850 and 1880, dairy herds increased, and Italian rye grass (Lolium perenne) was introduced, which pollinated more heavily than any of the traditional grasses.10Johnson P. Marsh D.G. ‘Isoallergens’ from rye grass pollen.Nature. 1965; 206: 935-937Crossref PubMed Scopus (98) Google Scholar, 11Davies R. Grass pollen counts: London 1961-1980.Clin Allergy. 1982; 12: 511-512Google Scholar In the United States the progressive increase in arable farming is thought to have increased the growth of ragweed. Certainly ragweed became the most import cause of seasonal rhinitis in the United States.3Wyman M. Autumnal catarrh (hay fever). Huro & Houghton, Cambridge (MA)1872Google Scholar, 12King T. Norman P. Isolation studies of allergens from ragweed pollen.Biochemistry. 1962; 1: 709Crossref PubMed Scopus (106) Google ScholarMajor changes in public hygiene started during the 19th century. Given the fact that the Greeks and Romans understood the need for clean water supplies, it is difficult to believe that London in 1854 and Chicago as late as 1890 were collecting “drinking water” from the same site that was used to discharge untreated sewage (Table I).13Johnson S.B. The ghost map. Riverhead Books, London (UK)2006Google Scholar, 14Reynolds A. Hazen A. The water-supply of Chicago: its source and sanitary aspects.Public Health Pap Rep. 1893; 19: 146-151PubMed Google Scholar The critical studies that led to the acceptance of the relationship between sewage and enteric disease were carried out by John Snow in London, starting with the evidence about the Soho pump and cholera and following this with epidemiologic comparison in 1854 of typhoid cases among populations who obtained their water from the London River compared with those whose water came from farther up the river (Fig 2).13Johnson S.B. The ghost map. Riverhead Books, London (UK)2006Google Scholar, 15Hempel S. John Snow.Lancet. 2013; 381: 1269-1270Abstract Full Text Full Text PDF PubMed Scopus (16) Google Scholar However, as late as 1880, there was still only limited acceptance of the germ theory of disease, even among physicians. Indeed, in 1881, President James Garfield was “murdered” by his physicians, who repeatedly probed a nonfatal gunshot wound using nonsterile instruments and fingers.16Millard C. Destiny of the republic. A tale of madness, medicine, and the murder of a president. Doubleday, New York (NY)2011Google Scholar Starting in 1892, the city of Chicago reversed the course of the Chicago River so that sewage flowed into the Mississippi rather than into Lake Michigan, which was the source of drinking water.14Reynolds A. Hazen A. The water-supply of Chicago: its source and sanitary aspects.Public Health Pap Rep. 1893; 19: 146-151PubMed Google ScholarTable IThe essence of hygiene: What elements are likely to be relevant to the onset of allergic disease?Primary measuresClean water•Complete separation of sources of drinking water from the discharge of untreated sewage•Water chlorinationUncontaminated food•Separation of untreated sewage from farming, including strict enforcement of restrictions on defecation in fields•Strict enforcement of abattoir regulationsHelminth eradication•Wearing shoes—control of hookworm•Water and food control—Ascaris species•No swimming in contaminated water—schistosomiasis•Regular (annual) anti-helminth treatmentSecondary elements Decreased exposure to farm animals—decreased diversity of bacterial exposure Decreased exposure to older siblings caused by small family sizes with resulting decreased transmissible infections (exposure in day care might have the opposite effect) Decreased exposure to soil bacteria Open table in a new tab Fig 2A, London water supplies in 1854 used by John Snow as evidence that typhoid and cholera were spread through the water. B, Typhoid fever deaths in Chicago in 1892, which were controlled by extending the water intake into the lake and pumping 407 million gallons per day from the Chicago River into the Mississippi. Fig 2, A: Robert W. Mylne. Map of the contours of London and its environs, showing the districts and areas supplied by the nine metropolitan water companies, published for the author by Edward Stanford, Charing Cross, London; published by Waterlow and Sons, 1856. Accessed at: http://www.ph.ucla.edu/epi/snow/watermap1856/watermap_1856.html. Fig 2, B: From the Annual report of the department of health of the city of Chicago for the year ended December 31, 1894. Department of Health, City of Chicago; 1895 (public domain).View Large Image Figure ViewerDownload Hi-res image Download (PPT)By 1920, chlorination of water was widespread, and all the major cities in the United States had clean water, with the result that typhoid and cholera became rare. If you look at New York City, you could argue that the critical changes in hygiene were complete by 1920 (Table II). In keeping with that, allergy became more common, and by 1946, ragweed-induced hay fever was such a severe problem in New York that the city council initiated a ragweed eradication campaign (Table II).174000 Acres that breed sneezes, target in City's hay fever war. New York Times. June 3, 1949.Google Scholar, 18Walzer M. Siegel B.B. The effectiveness of the ragweed eradication campaigns in New York City; a 9-year study; 1946-1954.J Allergy. 1956; 27: 113-126Abstract Full Text PDF PubMed Scopus (9) Google ScholarTable IIAllergic diseases in New York City1900Shoes universalSources of clean water identified1920Helminths and malaria eradicated on Staten IslandWater chlorination complete in New York City1924Last abattoir closedHorses becoming less common1932-1950Allergic disease increases up to 10% to 13%1946Ragweed eradication campaign started in Manhattan because of the severity of hay fever in the city1982Asthma was rated the number 1 medical problem of the city, but this was reversed because of the explosion of HIV during the year1996“Emerging epidemic of asthma” in New York schools; 200 of 1100 students in East Harlem on treatment (see the New York Times, September 29, 1996)1997Mayor Giuliani declares war on rats in New York City Open table in a new tab Equally, in London Dr Frankland's allergy clinic had hundreds of patients in the 1950s, and he and Dr Augustin carried out the first controlled trial of immunotherapy for grass pollen hay fever.19Frankland A. Augustin R. Prophylaxis of summer hay fever and asthma: controlled trial comparing crude grass pollen extracts with isolated main component.Lancet. 1954; 266: 1055-1057Abstract PubMed Scopus (230) Google Scholar In fact, the increase in allergic disease was already obvious when Dr Swineford was appointed professor of allergy and rheumatology at the University of Virginia in 1935. He had been called back from doing pathology research in Vienna to “help deal with the allergy epidemic,” and he opened the first subspecialty clinic in the Medical School in 1936.20Swineford Jr., O. Asthma and hay fever. Charles C Thomas, Springfield (IL)1971Google ScholarThe epidemic increase of asthma among children: 1960-2000For further information, see Table III. Before 1960, most pediatrics textbooks did not regard asthma as common, let alone epidemic. During the 1960s, there were occasional reports that asthma appeared to be becoming more common, but the first convincing publication came in 1969. Smith et al21Smith J.M. Disney M.E. Williams J.D. Goels Z.A. Clinical significance of skin reactions to mite extracts in children with asthma.BMJ. 1969; 2: 723-726Crossref PubMed Scopus (98) Google Scholar carried out a population-based study on schoolchildren in Birmingham, United Kingdom, which demonstrated a sharp increase in asthma between 1958 and 1968. In addition, they reported that many of the children with asthma had positive skin test responses to dust mites. Over the next few years, reports on the increasing prevalence of asthma came from several countries but predominantly from countries in which dust mites were the dominant allergen. Thus increases were reported from Australia, New Zealand, and Japan, as well as the United Kingdom.21Smith J.M. Disney M.E. Williams J.D. Goels Z.A. Clinical significance of skin reactions to mite extracts in children with asthma.BMJ. 1969; 2: 723-726Crossref PubMed Scopus (98) Google Scholar, 22Clarke C.W. Aldons P.M. The nature of asthma in Brisbane.Clin Allergy. 1979; 9: 147-152Crossref PubMed Scopus (11) Google Scholar, 23Miyamoto T. Johansson S.G. Ito K. Horiuchi Y. Atopic allergy in Japanese subjects: studies primarily with radioallergosorbent test.J Allergy Clin Immunol. 1974; 53: 9-19Abstract Full Text PDF PubMed Scopus (57) Google Scholar Indeed, by the 1980s, it was possible to argue that increasing growth of dust mites in houses was an important cause of the increase in asthma.24Platts-Mills T.A.E. Mitchell E.B. Tovey E.R. Chapman M.D. Wilkins S.R. Airborne allergen exposure, allergen avoidance and bronchial hyperreactivity.in: Kay A.B. Austen K.F. Lichtenstein L.M. Asthma: physiology, immunopharmacology and treatment, Third International Symposium. Academic Press, London1984: 297-314Google Scholar, 25Platts-Mills T.A. Tovey E.R. Mitchell E.B. Moszoro H. Nock P. Wilkins S.R. Reduction of bronchial hyperreactivity during prolonged allergen avoidance.Lancet. 1982; 2: 675-678Abstract PubMed Scopus (561) Google Scholar That argument was helped by the fact that homes in the United Kingdom, Australia, and New Zealand had become warmer and tighter and had more carpets. In turn, this was thought to have provided improved conditions for the growth of dust mites and for the accumulation of debris from dust mite growth.26Tovey E.R. Chapman M.D. Wells C.W. Platts-Mills T.A. The distribution of dust mite allergen in the houses of patients with asthma.Am Rev Respir Dis. 1981; 124: 630-635PubMed Google Scholar However, it is important to recognize that a large part of the reason for wanting homes warmer and less drafty was because of the increase in indoor entertainment.Table IIIChanges that have been suggested as explanations for the progressive increase in pediatric asthma, 1955-2000I. Increased number of immunizations in early childhood and possible changes in vaccinesII. Progressive increase in the use of broad-spectrum antibioticsIII. Use of paracetamol to treat fever in childhood, which replaced aspirin, after identification of Reyes syndrome in 1979IV. Changes that occurred either because of or in parallel with the introduction and increase in indoor entertainment: primarily television programs for children, 1955 onwardA.Decreased play outdoors with consequent decrease in exposure to bacteria and decreased physical activityB.Progressive increase in body mass index among childrenC.Changes in homes to increase comfort, including decreased ventilation, increased carpeting and furnishing, and increased temperatureD.Changes in breathing patterns while watching television, including decrease in sigh ratesV. Increased exposure to indoor allergens secondary to less time outdoors and higher quantities indoors Open table in a new tab Although it is well known today that asthma has increased in all Western countries, it might be forgotten that this did not become clear until 1990. In that year, data on asthma among recruits to the Finnish and Swedish armies came out, showing a progressive increase over 20 years.27Haahtela T. Lindholm H. Bjorksten F. Koskenvuo K. Laitinen L.A. Prevalence of asthma in Finnish young men.BMJ. 1990; 301: 266-268Crossref PubMed Scopus (227) Google Scholar, 28Braback L. Hjern A. Rasmussen F. Trends in asthma, allergic rhinitis and eczema among Swedish conscripts from farming and non-farming environments. A nationwide study over three decades.Clin Exp Allergy. 2004; 34: 38-43Crossref PubMed Scopus (134) Google Scholar However, in large parts of Sweden, the dominant allergens associated with asthma are those associated with cats or dogs.29Erwin E.A. Ronmark E. Wickens K. Perzanowski M.S. Barry D. Lundback B. et al.Contribution of dust mite and cat specific IgE to total IgE: relevance to asthma prevalence.J Allergy Clin Immunol. 2007; 119: 359-365Abstract Full Text Full Text PDF PubMed Scopus (70) Google Scholar, 30Ronmark E. Bjerg A. Perzanowski M. Platts-Mills T. Lundback B. Major increase in allergic sensitization in schoolchildren from 1996 to 2006 in northern Sweden.J Allergy Clin Immunol. 2009; 124 (e1-15): 357-363Abstract Full Text Full Text PDF PubMed Scopus (139) Google Scholar In addition, evidence was accumulating that cockroach was a major allergen related to asthma among African Americans living in poverty in the United States.31Hulett A. Dockhorn R. House dust, mite (D. farinae) and cockroach allergy in a Midwestern population.Ann Allergy Asthma Immunol. 1979; 43: 160-165Google Scholar, 32Gelber L.E. Seltzer L.H. Bouzoukis J.K. Pollart S.M. Chapman M.D. Platts-Mills T.A. Sensitization and exposure to indoor allergens as risk factors for asthma among patients presenting to hospital.Am Rev Respir Dis. 1993; 147: 573-578Crossref PubMed Scopus (466) Google Scholar, 33Rosenstreich D.L. Eggleston P. Kattan M. Baker D. Slavin R.G. Gergen P. et al.The role of cockroach allergy and exposure to cockroach allergen in causing morbidity among inner-city children with asthma.N Engl J Med. 1997; 336: 1356-1363Crossref PubMed Scopus (1180) Google Scholar By 1995, it was accepted that both the prevalence and hospitalization for asthma had increased among children living in climates or living conditions in which several different allergens dominated both exposure and sensitization.34Anderson H. Gupta R. Strachan D. Limb E. 50 years of asthma: UK trends from 1955 to 2004.Thorax. 2007; 62: 85-90Crossref PubMed Scopus (187) Google Scholar, 35Crater D.D. Heise S. Perzanowski M. Herbert R. Morse C.G. Hulsey T.C. et al.Asthma hospitalization trends in Charleston, South Carolina, 1956 to 1997: twenty-fold increase among black children during a 30-year period.Pediatrics. 2001; 108: E97Crossref PubMed Scopus (53) Google Scholar, 36Mitchell E. International trends in hospital admission rates for asthma.Arch Dis Child. 1985; 60: 376-378Crossref PubMed Scopus (160) Google Scholar At this point, it became very difficult to argue that the increase had occurred simply because of an increase in allergens in homes because there was no reason to think that dust mite, cockroach, cat, and Alternaria species had all increased in parallel. It is important to recognize that the best evidence about the role of allergens in asthma came between 1970 and 1980, with convincing demonstrations that chronic allergen exposure could make a major contribution to nonspecific bronchial hyperreactivity (BHR).24Platts-Mills T.A.E. Mitchell E.B. Tovey E.R. Chapman M.D. Wilkins S.R. Airborne allergen exposure, allergen avoidance and bronchial hyperreactivity.in: Kay A.B. Austen K.F. Lichtenstein L.M. Asthma: physiology, immunopharmacology and treatment, Third International Symposium. Academic Press, London1984: 297-314Google Scholar, 37Altounyan R.E.C. Changes in histamine and atropine responsiveness as a guide to diagnosis and evaluation of therapy in obstructive airways disease.in: Pepys J. Frankland A.W. Disodium chromoglycate in allergic airways disease. Butterworth, London (UK)1970Google Scholar, 38Kerrebijn K. Endogenous factors in childhood CNSLD: methodological aspects in population studies. Royal Van Gorcum, Assen (The Netherlands)1970: 38-48Google Scholar, 39Cockcroft D. Ruffin R. Dolovich J. Hargreave F. Allergen-induced increase in non-allergic bronchial reactivity.Allergy. 1977; 7: 503-513Google ScholarAny attempt to explain the increase in pediatric asthma has to deal with the progressive nature of the increase. Although major changes were present by 1980, the increase continued for at least 2 more decades. Although there is evidence for many different aspects of the increase in asthma prevalence and severity, most of these arguments cannot explain either the time course or the scale of the increase (Fig 3).27Haahtela T. Lindholm H. Bjorksten F. Koskenvuo K. Laitinen L.A. Prevalence of asthma in Finnish young men.BMJ. 1990; 301: 266-268Crossref PubMed Scopus (227) Google Scholar, 34Anderson H. Gupta R. Strachan D. Limb E. 50 years of asthma: UK trends from 1955 to 2004.Thorax. 2007; 62: 85-90Crossref PubMed Scopus (187) Google Scholar, 35Crater D.D. Heise S. Perzanowski M. Herbert R. Morse C.G. Hulsey T.C. et al.Asthma hospitalization trends in Charleston, South Carolina, 1956 to 1997: twenty-fold increase among black children during a 30-year period.Pediatrics. 2001; 108: E97Crossref PubMed Scopus (53) Google Scholar, 36Mitchell E. International trends in hospital admission rates for asthma.Arch Dis Child. 1985; 60: 376-378Crossref PubMed Scopus (160) Google Scholar A typical example is the change from aspirin to paracetamol in 1979 after the identification of Reyes syndrome. This change might well have contributed to the severity of asthma but did not occur until halfway through the increase.40Shaheen S. Newson R. Ring S. Rose-Zerilli M. Holloway J. Henderson A. Prenatal and infant acetaminophen exposure, antioxidant gene polymorphisms, and childhood asthma.J Allergy Clin Immunol. 2010; 126: 1141-1148.e7Abstract Full Text Full Text PDF PubMed Scopus (43) Google Scholar In most studies asthmatic children were found to be allergic to 1 or more of the common perennial allergens. In Australia Peat and Woolcock reported detailed studies on the “modifiable risk factors for asthma,” including diet and immunization, and they concluded that dust mite allergy was the most important of these factors.41Peat J.K. Tovey E. Mellis C.M. Leeder S.R. Woolcock A.J. Importance of house dust mite and Alternaria allergens in childhood asthma: an epidemiological study in two climatic regions of Australia.Clin Exp Allergy. 1993; 23: 812-820Crossref PubMed Scopus (244) Google Scholar, 42Peat J.K. Li J. Reversing the trend: reducing the prevalence of asthma.J Allergy Clin Immunol. 1999; 103: 1-10Abstract Full Text Full Text PDF PubMed Scopus (166) Google ScholarFig 3Published data on the increase in hospitalizations of children and young adults caused by asthma in 4 countries during the 20th century: A, asthmatic patients in the United Kingdom34Anderson H. Gupta R. Strachan D. Limb E. 50 years of asthma: UK trends from 1955 to 2004.Thorax. 2007; 62: 85-90Crossref PubMed Scopus (187) Google Scholar; B, asthmatic children at the Medical College of South Carolina35Crater D.D. Heise S. Perzanowski M. Herbert R. Morse C.G. Hulsey T.C. et al.Asthma hospitalization trends in Charleston, South Carolina, 1956 to 1997: twenty-fold increase among black children during a 30-year period.Pediatrics. 2001; 108: E97Crossref PubMed Scopus (
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