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Short Research Article

Hygienic habits are a risk factor for adult-onset asthma

[version 1; peer review: 2 not approved]
PUBLISHED 06 Mar 2013
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Abstract

Multiple etiologies have been shown to contribute to asthma development, with excessive hygiene and microbial deprivation being one of the strongest risk factors for asthma onset in pediatric populations. The present study evaluated the contribution of hygienic habits in the development of adult-onset asthma. Twenty three adult-onset asthma patients (age of onset ranged from 21 to 71 years old) and 36 controls were asked to respond to a questionnaire concerning their frequency of shower taking and hand washing. Nine of the 23 (39.1%) asthmatic patients reported taking showers twice per day, compared to 2 controls (5.6%; χ2 = 15.4, p=0.017). In addition, sixteen (69.6%) of the asthmatic patients reported very frequent hand washing (≥ 7 times per day), whereas only 6 (16.7%) controls reported less frequent (2 – 6 times per day) hand washing habits. These data confirm that excessive hygienic habits are associated with the development of adult-onset asthma.

Keywords

bronchial asthma, hand washing, hygienic hypothesis, shower taking

Introduction

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 factors810, 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.

Methods

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

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.

Hygienic questionnaire

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.

Statistical analysis

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.

Results

Group characteristics

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.

Table 1. Group characteristics*.

CharacteristicsAsthma patients
(n=23)
Controls
(n=24)
Autoimmune
disease control group
(n=12)
Statistics
Males/Females12/1117/710/2NS
Diagnosis (n)Asthma (23)DM(8), AH(5),
Pro(3), My(2),
Ga(3), Pa(1),
Do(1), CD(1)
Sarcoidosis(7),
PulmFibr(3),
CIDP(1), RA(1)
-
Age (years)56.0±13.050.8±14.243.9±15.3F=2.98, p=0.059
Asthma>ADG
Education (years)14.7±2.414.6±3.013.8±2.4NS
Height (sm)167.6±10.3173.4±10.0177.1±6.7F=5.01, p=0.010
Asthma<ADG
Weight (kg)76.7±19.582.2±16.088.0±18.7NS
Age of asthma
onset (years)
43.4±12.8---

*Means and standard deviations are presented where appropriate.

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.

Distribution of hygienic habits in asthma and control groups

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.

Table 2. Distribution of responses of asthma patients and controls to the hygienic questionnaire.

Question 1: How often do you take shower or bath?
Twice
per week or less
(1 point)
3–4 times
per week
(2 points)
Once
per day
(3 points)
Twice
per day
(4 points)
Asthma patients
(n=23)
4469
Controls
(n=24)
95100
Autoimmune disease
control group (n=12)
3522
Question 2: How often do you wash hands?
Once per
day or less
(1 point)
2 – 3 times
per day
(2 points)
4 – 6 times
per day
(3 points)
≥ 7 times
per day
(4 points)
Asthma patients10616
Controls01194
Autoimmune disease
group (n=12)
0642

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].

Discussion

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 studies2224. These results provide evidence that excessive hygiene, perhaps mediated through microbial deprivation, is associated with adult-onset asthma as well.

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Polunina AG. Hygienic habits are a risk factor for adult-onset asthma [version 1; peer review: 2 not approved]. F1000Research 2013, 2:80 (https://doi.org/10.12688/f1000research.2-80.v1)
NOTE: If applicable, it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Open Peer Review

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Key to Reviewer Statuses VIEW
ApprovedThe paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approvedFundamental flaws in the paper seriously undermine the findings and conclusions
Version 1
VERSION 1
PUBLISHED 06 Mar 2013
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Reviewer Report 27 Mar 2013
Paul Licciardi, Allergy and Immune Disorders Group, Murdoch Children Research Institute, Melbourne, Australia 
Not Approved
VIEWS 23
The manuscript by Polunina assesses the negative association of hand washing and shower taking with the development of asthma in adults. The premise for this work is based on the hygiene hypothesis where reduced microbial exposures in early life can ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Licciardi P. Reviewer Report For: Hygienic habits are a risk factor for adult-onset asthma [version 1; peer review: 2 not approved]. F1000Research 2013, 2:80 (https://doi.org/10.5256/f1000research.313.r870)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
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Reviewer Report 22 Mar 2013
Dina Czeresnia, Escola Nacional de Saúde Pública, Fundação Oswaldo Cruz, Rio de Janeiro, Brazil 
Not Approved
VIEWS 25
The article aims to evaluate a causal association between hygiene habits (washing hands and taking showers) and the onset of asthma in adults. 

In the introduction, the author justifies this option by using the hygienic hypothesis theory, which according to her ... Continue reading
CITE
CITE
HOW TO CITE THIS REPORT
Czeresnia D. Reviewer Report For: Hygienic habits are a risk factor for adult-onset asthma [version 1; peer review: 2 not approved]. F1000Research 2013, 2:80 (https://doi.org/10.5256/f1000research.313.r858)
NOTE: it is important to ensure the information in square brackets after the title is included in all citations of this article.
  • Author Response 23 Mar 2013
    Anna Polunina, Municipal Ambulatory Medical Service N124, Moscow Health Care Department, Russian Federation
    23 Mar 2013
    Author Response
    1) The hygienic hypothesis of allergies is yet the hypothesis but not the theory or completely clear scientific conception. Although, the association between the demographic characteristics of the populations and ... Continue reading
COMMENTS ON THIS REPORT
  • Author Response 23 Mar 2013
    Anna Polunina, Municipal Ambulatory Medical Service N124, Moscow Health Care Department, Russian Federation
    23 Mar 2013
    Author Response
    1) The hygienic hypothesis of allergies is yet the hypothesis but not the theory or completely clear scientific conception. Although, the association between the demographic characteristics of the populations and ... Continue reading

Comments on this article Comments (0)

Version 1
VERSION 1 PUBLISHED 06 Mar 2013
Comment
Alongside their report, reviewers assign a status to the article:
Approved - the paper is scientifically sound in its current form and only minor, if any, improvements are suggested
Approved with reservations - A number of small changes, sometimes more significant revisions are required to address specific details and improve the papers academic merit.
Not approved - fundamental flaws in the paper seriously undermine the findings and conclusions
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