Keywords
bronchial asthma, hand washing, hygienic hypothesis, shower taking
bronchial asthma, hand washing, hygienic hypothesis, shower taking
Asthma is an important cause of quality of life impairment1,2, complications in long-term corticosteroid therapy3,4, increased health care utilization5 and mortality1. For instance, a recent study by Jia and colleagues1 demonstrated that the loss of the quality-adjusted life expectancy was 7.0 years for people with asthma compared to those without asthma. The prevalence of asthma has considerably increased during the twentieth century in both Western and Eastern Europe. For instance, in the UK, the rate of children consulting for asthma showed an eightfold increase from 1955/6 to 1991/2, and the rate of adults showed a three to fourfold increase6. Although from the mid-1990s the incidence of asthma stabilized or even somewhat decreased in Western societies6, this has not been true in Russia’s case. The Ministry of Healthcare of the Russian Federation reported an increase of asthma prevalence from 0.62% to 0.82% during the period from 2000 to 20087.
Multiple factors have been shown to be associated with an increased risk of asthma. Allergy in parents and genetic factors8–10, bronchitis or pneumonia in infancy8, viral infections11, air pollution12, insufficient aerobic exercise13, obesity14, and special dietary patterns15 have all been associated with an increased asthma risk. At the same time, growing up or living in rural settings has been consistently shown to be associated with a reduced risk of asthma and allergies9,16,17. A study of 13,889 Belarusian children confirmed earlier findings in Western populations of the protective effects of rural settings, pet ownership and the presence of siblings on the risk of asthma development18. The latter findings underlie the hygiene hypothesis, which postulates that infections and unhygienic contact may confer protection against the development of allergic illnesses16,17.
Adult-onset asthma and allergies appear to be highly prevalent in contemporary Russia. The official epidemiologic data do not show the real prevalence and incidence of asthma due to poor diagnostics at ambulatory centers and imperfect statistical service. However, even the official statistics showed an increase of adult-onset asthma incidence from 0.048% to 0.060% in 2008 compared to 20027. In a recent Swedish study, the incidence rate of adult-onset asthma (defined as “physician-diagnosed” asthma with onset at or after 16 years of age) was 2.3%19. In the Russian Federation, the prevalence of adult-onset allergy and asthma appeared to increase after the boundaries of the country were opened in the 1990s, and many Russian citizens visited European countries and adopted European life-styles, including daily showers and frequent hand washing.
No previous studies on the effects of hygienic habits on the risk of adult-onset asthma could be identified. Here the results of a pilot investigation of hygienic habits in asthmatic patients are presented. The findings presented here were discovered as part of a larger investigation on the evaluation of neurological complications of chronic asthma medications with a special attention to steroid myopathy20. Therefore, only two short questions concerning hygienic habits were added to the study protocol. Nevertheless, the findings of excessive hand washing and shower taking in asthmatic patients were significant in comparison with controls, and, therefore suggest excessive hygiene as a risk factor in asthma development in adults.
The design of the present study was reviewed and approved by the administration of the Municipal Ambulatory Medical Service N124 of Moscow Health Care Department.
Patients with bronchial asthma attending the Municipal Ambulatory Medical Service N124 of the Moscow Health Care Department were invited to participate in the study. The inclusion criteria for patients with asthma were: 1) recent consultation in the Pulmonology department, which confirmed that the patient suffered bronchial asthma; 2) asthma onset over the age of 20. The exclusion criteria were: 1) age younger than 20 and older than 85 years; 2) serious concomitant diseases. The first control group included patients attending the medical service due to non-allergic diseases (i.e., arterial hypertension, diabetes mellitus, etc.) or subjects who visited the medical center for prophylactic examination. In addition, we included patients with autoimmune diseases (sarcoidosis, pulmonary fibrosis, etc.) who received steroids, as the primary aim of our main study was the evaluation of symptoms of steroid myopathy. Patients with autoimmune diseases constituted the second control group. An age of 75 years or over, emergency cases and severe conditions were exclusion criteria for patients of control groups.
It was explained to all patients that the examination did not concern the medical management of their disease and was conducted as a part of scientific research. The methods of the examination were explained to all patients, and 23 asthmatic patients, 24 controls and 12 patients with autoimmune diseases gave a verbal informed consent to participate in the study as is customary in Russia.
We asked patients and healthy subjects to complete a two item questionnaire by choosing one of four possible responses. The first item contained the following question: ‘How often do you take shower or bath?’ The optional responses were: 1) twice per week or less; 2) 3 – 4 times per week; 3) once per day; 4) twice per day. The second item was: ‘How often do you wash hands?’ The optional responses were: 1) once per day or less; 2) 2 – 3 times per day; 3) 4 – 6 times per day; 4) 7 times and more per day. Responses demonstrating infrequent hygienic behaviors were evaluated as 1 point, and excessive hygienic behaviors (e.g., taking showers twice per day and hand washing over 7 times per day) were evaluated as 4 points, whilst intermediate habits ranged from 2 to 3 points.
All analyses were performed using SPSS software for windows (SPSS 17.0, Chicago, IL, USA).
Group characteristics were compared by ANOVA with a post hoc Bonferroni multiple comparisons correction. The distribution of hand washing and shower taking frequency in the three groups were compared by Pearson χ2-tests. Mann-Whitney tests were used for comparing mean scores on the hygienic habits questionnaire.
Patient characteristics and statistics are presented in Table 1. The mean age of asthma onset was 43.4±12.8 years old in our patient group (range 21 – 71 years old). Patients of the first control group visited the medical service due to diabetes mellitus, arterial hypertension, myelopathy, gastritis, pancreatitis, dorsopathy and coronary disease. The autoimmune disease control group included patients with sarcoidosis, pulmonary fibrosis, chronic inflammatory demyelinating polyneuropathy and rheumatoid arthritis.
Abbreviations: ADG, autoimmune disease group; AH, arterial hypertension; CD, coronary disease; CIDP, chronic inflammatory demyelinating disease; DM, diabetes mellitus; Do, dorsopathy; Ga, gastritis; My, myelopathy; NS, not significant; Pa, pancreatitis; Pro, prophylactical examination; PulmFibr, pulmonary fibrosis; RA, rheumatoid arthritis.
The asthma and both control groups did not show significant differences in age, education, height or weight. The asthma patients (mean age = 56 ± 13 years) were older in comparison with the autoimmune disease group (44 ± 15 years). In addition, the asthma patients were significantly shorter (mean height = 168 ± 10 cm) in comparison with the patients with autoimmune disease (177 ± 7 cm). Although, there was a larger proportion of females in the asthma group, this was not significant.
Asthma patients significantly differed in hygienic habits from both control groups (Table 2). At the same time no differences in hygienic habits between the two control groups were found.
Nine of the 23 asthmatic patients reported taking showers twice per day, whereas only two patients with the autoimmune disease, and none in the non-autoimmune controls reported taking showers twice per day. Although 4 patients with asthma reported rare shower taking (twice per week or less), the same four patients reported excessive hand washing (7 or more times per day). When both control groups were combined together, asthma patients showed significantly higher shower taking scores (2.87 ± 1.14) in comparison with controls (2.11 ± 0.95; z=-2.59, p=0.01).
Sixteen (69.6%) asthmatic patients reported very frequent hand washing (7 or more times per day), whereas only 2 of the 24 (8.3%) patients without allergic or immune diseases and 2 of 12 (16.7%) patients with autoimmune diseases reported very frequent hand washing habits. When the two control groups were combined together, asthmatic patients showed significantly higher hand washing scores (3.61 ± 0.72) in comparison with controls (2.69 ± 0.75; z=-4.64, p < 0.001).
When only males or only females were included in the analysis, the distribution of shower taking frequency did not reach significance. However, the distribution of hand washing frequency was still significantly higher in asthmatic patients in comparison with the combined control group in males [χ2 = 13.0, p=0.005] and females [χ2 = 8.7, p=0.013].
These results support the hypothesis that excessive hygiene may underlie the high prevalence of allergic diseases in the contemporary world. Here it was found that excessive hygiene is significantly associated with adult-onset bronchial asthma. Interestingly, it was found that excessively frequent hand washing was more strongly related to bronchial asthma in comparison with shower taking. In contrast, non-allergic autoimmune diseases did not show associations with hygienic habits in this pilot study.
Investigations of the effects of infectious diseases on the risk of allergy development show an inverse and frequency dependent relationship: the more infections subjects have encountered as assessed by positive serology, the lower the observed prevalence of atopy, allergic rhinitis and asthma17. Many epidemiologic studies suggest that ‘microbial deprivation’ considerably contributes to the etiology of allergy and asthma21.
A range of recent pediatric studies demonstrated that intestinal microbiota imbalances in infants are associated with the development of asthma and allergies in children over the age of three22,23. Higher counts of Lactobacilli, Bifidobacteria and Enterococci in stool samples were characteristic for non-allergic children, whereas an increased number of Clostridia were typical for children who developed allergies22. Collectively, these studies demonstrated the importance of gut microbial community as a correlate of the development of atopy23. Many studies have demonstrated the effectiveness of probiotic treatment for reducing atopic eczema in children, though studies of probiotic effects on asthma symptoms are limited24. In addition, a regular intake of probiotics was consistently shown to reduce respiratory symptoms of the common cold in both schoolchildren25 and adult26 cohorts.
Overall, the negative effects of excessive hygiene in this patient cohort may be explained by an insufficient microbial load (brought about through excessive hygienic habits) and, therefore, abnormal functioning of the immune system in asthmatic patients. Insufficient immune system stimulation in infants has consistently been recognized as an important contributor to allergy development in previous studies22–24. These results provide evidence that excessive hygiene, perhaps mediated through microbial deprivation, is associated with adult-onset asthma as well.
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Competing Interests: No competing interests were disclosed.
Competing Interests: No competing interests were disclosed.
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