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The hygiene hypothesis: identifying microbial friends and protecting against microbial enemies Sally Bloomfield Perspectives in Public Health 2013 133: 301 DOI: 10.1177/1757913913506642 The online version of this article can be found at: http://rsh.sagepub.com/content/133/6/301
Published by: http://www.sagepublications.com
On behalf of:
Royal Society for Public Health
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>> Version of Record - Nov 8, 2013 What is This?
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CURRENT TOPICS & OPINIONS
The hygiene hypothesis: identifying microbial friends and protecting against microbial enemies We frequently read about how we have ‘become too clean for our own good’ – but is this really true? What is meant by this anyway? And, more importantly, what are the implications for hygiene and public health? This issue has been reviewed in a recent report by the International Scientific Forum on Home Hygiene (IFH).1,2 Sally Bloomfield, Chairman of the International Scientific Forum on Home Hygiene and Visiting Professor, London School of Hygiene and Tropical Medicine, takes a closer look at the discussion. The hygiene hypothesis dates back to 1989, when Strachan proposed that a lower incidence of infection in early childhood could be an explanation for the rapid 20th century rise in allergic diseases. Over the last decade, researchers have recognised that the concept of a link between microbial exposure and allergy is probably correct, but the idea that children who have more infections are less likely to develop allergies is wide of the mark. Their other finding, which highlights the growing importance of this issue, is that the concept applies to a much broader range of chronic inflammatory diseases (CIDs) such as type 1 diabetes and multiple sclerosis, and also some types of depression and cancer. In 2003, Graham Rook proposed the ‘Old Friends’ hypothesis, which seems to offer a more rational explanation. He argues that the vital exposures are not colds, influenza, measles and other common childhood infections which have evolved relatively recently over the last 10,000 years, but rather the microbes already present over 2 million years ago in hunter-gatherer times when the human immune system was developing. His argument is that we have become so dependent on our ‘Old Friends’ that our immune systems cannot function properly without them.
What sort of microbes do we need and when? Rook suggests that our ‘Old Friends’ are most likely to include the following: •E nvironmental species which inhabit our indoor and outdoor environments; •T he normal microbiota of the human skin, gut and respiratory tract, and that of the animals we live with; •A nd organisms such as hepatitis A virus and helminths (worms) which establish chronic infections or carrier states, and that need to be tolerated.
For allergic disease, it seems that the most important times for exposure are early in development, during pregnancy and the first few days or months of infancy, and this exposure needs to be maintained over a significant period. This fits with evidence that Caesarean section may be associated with an increased tendency to develop allergies, while breastfeeding for 6 months or more can be protective. What we do not know is the extent to which exposures need to be maintained during childhood and adult life and whether these diseases could be contained or reversed by ongoing exposure. There is some evidence for this, but much more research is required to better understand.
Are other factors involved?
It now seems clear that the risk of allergic and other CIDs also depends on factors such as changes in diet, pollution, physical activity, obesity, socio-economic factors and stress. Genetic predisposition is also an influencing factor, which could explain why exposure to we do not all suffer from these these microbes diseases. We all still get some is vital because microbial exposure, which for some is sufficient, for others not. they interact For these people, allergies and with regulatory other CIDs may be triggered, systems when these other factors cause further immune dysregulation.
Studies now show how exposure to these microbes is vital because they interact with regulatory systems which keep our immune systems in balance. Without this our immune systems may react inappropriately, sometimes overreacting and causing asthma and hay fever, and sometimes attacking our own tissues and causing autoimmune diseases such as multiple sclerosis. Increasingly, it seems that diversity of exposure to these microbes is key to building a well-regulated immune system.
What has caused the problem and why now? Since allergies and other CIDs are largely diseases of the last 100 years or so, the obvious assumption is that the ‘hygiene revolution’ of the last 200 years is a, or the root, cause. During this time, we saw radical improvements in sanitation,
Copyright © Royal Society for Public Health 2013 November 2013 Vol 133 No 6 l Perspectives in Public Health 301 SAGE Publications Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013 ISSN 1757-9139 DOI: 10.1177/1757913913506642
CURRENT TOPICS & OPINIONS The key point may be that the microbial content of modern urban homes has altered, not because of home and personal hygiene habits, but because mostly our homes now interact with urban environments. We also have different diets and lifestyles, which will affect the nature of our gut, skin and respiratory microbiota. This means that we now interact with an altogether different and less diverse mix of microbes relative to earlier generations, which were largely rural.
cleaner food and water, the clean-up of city streets and a decline in diseases through reduced exposure to infectious disease agents. However, if Rook’s hypothesis is correct, the likely explanation is that although these changes are important, it is because they have also inadvertently reduced exposure to our ‘Old Friends’, which occupy the same habitats. It is also possible that antibiotic usage, which is known to reduce the diversity of gut microbiota, is involved but again we need to know more. Of all the trends that might explain our declining ‘Old Friends’ exposure, one of the weakest is the idea that we have become too clean in our own homes. If home and personal cleanliness contributes, their role is likely to be small. The idea that we could create a ‘sterile’ home through excessive cleanliness is implausible: as fast as they are removed by cleaning, the microbes are being replaced via dust and air from outdoors, by microbes constantly shed from the human body and our pets and from the foods brought into our homes.
How could we tackle the problem of allergies and other CIDs?
more sport and other outdoor activities. It could mean persuading local authorities that green spaces in urban areas have a direct physiological action on our immune system. Rook et al.3 and others argue that because urban societies have lost contact with many of the categories of ‘Old Friends’, we are now more dependent on exposure to the microbiota of other family members, animals and the outdoor environment. This is supported by the consistent evidence of a protective effect from growing up on a farm.
The importance of hygiene At the same time, concerns about allergies and other CIDs have been increasing, as have concerns about infectious disease. Infectious gastrointestinal, respiratory and other diseases circulating in the community continue to exert a heavy toll on health and prosperity. This is being driven mainly by the growing immunocompromised population living and being cared for in the community and in the home. Increasingly, healthcare is delivered at home. Preventing global pandemics and reducing the spread of antibiotic resistance are global priorities, and hygiene is a key cornerstone of containing these threats.
Ultimately, the question is what measures could we use to reverse the trend? Various therapeutic approaches are being investigated, as yet at an early stage. Using probiotic drinks or foods to reintroduce key microbes to our bodies is Can we address both issues an obvious approach, but further work is at the same time? required to identify which ‘Old Friends’ Indications are that we can, but to do are truly friendly – and safe. this, we will have to persuade people to Encouraging lifestyle changes to view their microbial world very differently. increase exposure to ‘Old Friends’ is a The big challenge is to dispel misconchallenge, but needs more robust ceptions and change attitudes and evidence of real health benefits. Changes understanding. Because the terms which could be beneficial range from ‘hygiene’ and ‘cleanliness’ are used interencouraging natural childbirth, sustained changeably, to many people ‘being too breastfeeding clean’ implies the need to and physical be less particular about interaction hygiene. The public are The public are between siblings constantly confused by constantly confused to designing and headlines such as those by headlines . . . running our shown in the image which which alternately tell alternately tell us of the homes to ensure us of the benefits, more interaction benefits, then warn us of then warn us of harm harm from microbes. We with our environment, or have to promote the idea from microbes encouraging that protecting against
302 Perspectives in Public Health l November 2013 Vol 133 No 6 Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013
CURRENT TOPICS & OPINIONS infectious diseases is not about how clean our homes look, or how often we shower, or how we smell. It is what we do at the times when it matters to stop the spread of germs like washing our hands after visiting the toilet, decontaminating the chopping board after preparing raw poultry or good respiratory hygiene to prevent spread of cold and flu germs. This is the basis for a more rational approach to home hygiene, developed by the International Scientific Forum on Home Hygiene (IFH), known as ‘targeted hygiene’. This involves simply knowing what the critical points and times in the chain of infection transmission are (the hands, hand and food contact surfaces, cleaning utensils, etc.) and targeting hygiene measures at these points at the right time to block the ongoing spread of pathogens, while being more relaxed about general visible cleanliness. The basis of the IFH approach is that it seeks to protect against infection while
sustaining normal exposure to human, animal and environmental microbes, which means that it addresses both health issues. Using this approach, the IFH has developed a range of guidelines, training resources and fact sheets which can be found on the IFH website.4 Whatever the solution to these issues, one thing is clear. It is time we
recognised that using home and personal cleanliness as a scapegoat for a problem that has a much more complicated set of causes is both unjustified and ill advised, since it is diverting effort and attention from finding the true causes and workable solutions.
References 1. Stanwell-Smith R, Bloomfield SF, Rook GA. The Hygiene Hypothesis and Its Implications for Home Hygiene, Lifestyle and Public Health. International Scientific Forum on Home Hygiene, 2012. Available online at: http://www.ifhhomehygiene.com/best-practice-review/ hygiene-hypothesis-and-its-implications-homehygiene-lifestyle-and-public-0 (Last accessed 4th September 2013). 2. Bloomfield SF, Stanwell-Smith R, Rook GA. The Hygiene Hypothesis and Its Implications for Home Hygiene, Lifestyle and Public Health: Summary. International Scientific Forum on
Home Hygiene, 2012. Available online at: http:// www.ifh-homehygiene.org/best-practice-review/ hygiene-hypothesis-and-its-implications-homehygiene-lifestyle-and-public (Last accessed 4th September 2013). 3. Rook GAW, Lowry CA, Raison CL. Microbial ‘Old Friends’, immunoregulation and stress resilience. Evolution, Medicine, & Pubic Health 2013, (1): pp. 46-64. 4. IFH. Home Hygiene. Available online at: www.ifhhomehygiene.org (Last accessed 4th September 2013).
November 2013 Vol 133 No 6 l Perspectives in Public Health 303 Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013
The hygiene hypothesis: identifying microbial friends and protecting against microbial enemies Sally Bloomfield Perspectives in Public Health 2013 133: 301 DOI: 10.1177/1757913913506642 The online version of this article can be found at: http://rsh.sagepub.com/content/133/6/301
Published by: http://www.sagepublications.com
On behalf of:
Royal Society for Public Health
Additional services and information for Perspectives in Public Health can be found at: Email Alerts: http://rsh.sagepub.com/cgi/alerts Subscriptions: http://rsh.sagepub.com/subscriptions Reprints: http://www.sagepub.com/journalsReprints.nav Permissions: http://www.sagepub.com/journalsPermissions.nav
>> Version of Record - Nov 8, 2013 What is This?
Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013
CURRENT TOPICS & OPINIONS
The hygiene hypothesis: identifying microbial friends and protecting against microbial enemies We frequently read about how we have ‘become too clean for our own good’ – but is this really true? What is meant by this anyway? And, more importantly, what are the implications for hygiene and public health? This issue has been reviewed in a recent report by the International Scientific Forum on Home Hygiene (IFH).1,2 Sally Bloomfield, Chairman of the International Scientific Forum on Home Hygiene and Visiting Professor, London School of Hygiene and Tropical Medicine, takes a closer look at the discussion. The hygiene hypothesis dates back to 1989, when Strachan proposed that a lower incidence of infection in early childhood could be an explanation for the rapid 20th century rise in allergic diseases. Over the last decade, researchers have recognised that the concept of a link between microbial exposure and allergy is probably correct, but the idea that children who have more infections are less likely to develop allergies is wide of the mark. Their other finding, which highlights the growing importance of this issue, is that the concept applies to a much broader range of chronic inflammatory diseases (CIDs) such as type 1 diabetes and multiple sclerosis, and also some types of depression and cancer. In 2003, Graham Rook proposed the ‘Old Friends’ hypothesis, which seems to offer a more rational explanation. He argues that the vital exposures are not colds, influenza, measles and other common childhood infections which have evolved relatively recently over the last 10,000 years, but rather the microbes already present over 2 million years ago in hunter-gatherer times when the human immune system was developing. His argument is that we have become so dependent on our ‘Old Friends’ that our immune systems cannot function properly without them.
What sort of microbes do we need and when? Rook suggests that our ‘Old Friends’ are most likely to include the following: •E nvironmental species which inhabit our indoor and outdoor environments; •T he normal microbiota of the human skin, gut and respiratory tract, and that of the animals we live with; •A nd organisms such as hepatitis A virus and helminths (worms) which establish chronic infections or carrier states, and that need to be tolerated.
For allergic disease, it seems that the most important times for exposure are early in development, during pregnancy and the first few days or months of infancy, and this exposure needs to be maintained over a significant period. This fits with evidence that Caesarean section may be associated with an increased tendency to develop allergies, while breastfeeding for 6 months or more can be protective. What we do not know is the extent to which exposures need to be maintained during childhood and adult life and whether these diseases could be contained or reversed by ongoing exposure. There is some evidence for this, but much more research is required to better understand.
Are other factors involved?
It now seems clear that the risk of allergic and other CIDs also depends on factors such as changes in diet, pollution, physical activity, obesity, socio-economic factors and stress. Genetic predisposition is also an influencing factor, which could explain why exposure to we do not all suffer from these these microbes diseases. We all still get some is vital because microbial exposure, which for some is sufficient, for others not. they interact For these people, allergies and with regulatory other CIDs may be triggered, systems when these other factors cause further immune dysregulation.
Studies now show how exposure to these microbes is vital because they interact with regulatory systems which keep our immune systems in balance. Without this our immune systems may react inappropriately, sometimes overreacting and causing asthma and hay fever, and sometimes attacking our own tissues and causing autoimmune diseases such as multiple sclerosis. Increasingly, it seems that diversity of exposure to these microbes is key to building a well-regulated immune system.
What has caused the problem and why now? Since allergies and other CIDs are largely diseases of the last 100 years or so, the obvious assumption is that the ‘hygiene revolution’ of the last 200 years is a, or the root, cause. During this time, we saw radical improvements in sanitation,
Copyright © Royal Society for Public Health 2013 November 2013 Vol 133 No 6 l Perspectives in Public Health 301 SAGE Publications Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013 ISSN 1757-9139 DOI: 10.1177/1757913913506642
CURRENT TOPICS & OPINIONS The key point may be that the microbial content of modern urban homes has altered, not because of home and personal hygiene habits, but because mostly our homes now interact with urban environments. We also have different diets and lifestyles, which will affect the nature of our gut, skin and respiratory microbiota. This means that we now interact with an altogether different and less diverse mix of microbes relative to earlier generations, which were largely rural.
cleaner food and water, the clean-up of city streets and a decline in diseases through reduced exposure to infectious disease agents. However, if Rook’s hypothesis is correct, the likely explanation is that although these changes are important, it is because they have also inadvertently reduced exposure to our ‘Old Friends’, which occupy the same habitats. It is also possible that antibiotic usage, which is known to reduce the diversity of gut microbiota, is involved but again we need to know more. Of all the trends that might explain our declining ‘Old Friends’ exposure, one of the weakest is the idea that we have become too clean in our own homes. If home and personal cleanliness contributes, their role is likely to be small. The idea that we could create a ‘sterile’ home through excessive cleanliness is implausible: as fast as they are removed by cleaning, the microbes are being replaced via dust and air from outdoors, by microbes constantly shed from the human body and our pets and from the foods brought into our homes.
How could we tackle the problem of allergies and other CIDs?
more sport and other outdoor activities. It could mean persuading local authorities that green spaces in urban areas have a direct physiological action on our immune system. Rook et al.3 and others argue that because urban societies have lost contact with many of the categories of ‘Old Friends’, we are now more dependent on exposure to the microbiota of other family members, animals and the outdoor environment. This is supported by the consistent evidence of a protective effect from growing up on a farm.
The importance of hygiene At the same time, concerns about allergies and other CIDs have been increasing, as have concerns about infectious disease. Infectious gastrointestinal, respiratory and other diseases circulating in the community continue to exert a heavy toll on health and prosperity. This is being driven mainly by the growing immunocompromised population living and being cared for in the community and in the home. Increasingly, healthcare is delivered at home. Preventing global pandemics and reducing the spread of antibiotic resistance are global priorities, and hygiene is a key cornerstone of containing these threats.
Ultimately, the question is what measures could we use to reverse the trend? Various therapeutic approaches are being investigated, as yet at an early stage. Using probiotic drinks or foods to reintroduce key microbes to our bodies is Can we address both issues an obvious approach, but further work is at the same time? required to identify which ‘Old Friends’ Indications are that we can, but to do are truly friendly – and safe. this, we will have to persuade people to Encouraging lifestyle changes to view their microbial world very differently. increase exposure to ‘Old Friends’ is a The big challenge is to dispel misconchallenge, but needs more robust ceptions and change attitudes and evidence of real health benefits. Changes understanding. Because the terms which could be beneficial range from ‘hygiene’ and ‘cleanliness’ are used interencouraging natural childbirth, sustained changeably, to many people ‘being too breastfeeding clean’ implies the need to and physical be less particular about interaction hygiene. The public are The public are between siblings constantly confused by constantly confused to designing and headlines such as those by headlines . . . running our shown in the image which which alternately tell alternately tell us of the homes to ensure us of the benefits, more interaction benefits, then warn us of then warn us of harm harm from microbes. We with our environment, or have to promote the idea from microbes encouraging that protecting against
302 Perspectives in Public Health l November 2013 Vol 133 No 6 Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013
CURRENT TOPICS & OPINIONS infectious diseases is not about how clean our homes look, or how often we shower, or how we smell. It is what we do at the times when it matters to stop the spread of germs like washing our hands after visiting the toilet, decontaminating the chopping board after preparing raw poultry or good respiratory hygiene to prevent spread of cold and flu germs. This is the basis for a more rational approach to home hygiene, developed by the International Scientific Forum on Home Hygiene (IFH), known as ‘targeted hygiene’. This involves simply knowing what the critical points and times in the chain of infection transmission are (the hands, hand and food contact surfaces, cleaning utensils, etc.) and targeting hygiene measures at these points at the right time to block the ongoing spread of pathogens, while being more relaxed about general visible cleanliness. The basis of the IFH approach is that it seeks to protect against infection while
sustaining normal exposure to human, animal and environmental microbes, which means that it addresses both health issues. Using this approach, the IFH has developed a range of guidelines, training resources and fact sheets which can be found on the IFH website.4 Whatever the solution to these issues, one thing is clear. It is time we
recognised that using home and personal cleanliness as a scapegoat for a problem that has a much more complicated set of causes is both unjustified and ill advised, since it is diverting effort and attention from finding the true causes and workable solutions.
References 1. Stanwell-Smith R, Bloomfield SF, Rook GA. The Hygiene Hypothesis and Its Implications for Home Hygiene, Lifestyle and Public Health. International Scientific Forum on Home Hygiene, 2012. Available online at: http://www.ifhhomehygiene.com/best-practice-review/ hygiene-hypothesis-and-its-implications-homehygiene-lifestyle-and-public-0 (Last accessed 4th September 2013). 2. Bloomfield SF, Stanwell-Smith R, Rook GA. The Hygiene Hypothesis and Its Implications for Home Hygiene, Lifestyle and Public Health: Summary. International Scientific Forum on
Home Hygiene, 2012. Available online at: http:// www.ifh-homehygiene.org/best-practice-review/ hygiene-hypothesis-and-its-implications-homehygiene-lifestyle-and-public (Last accessed 4th September 2013). 3. Rook GAW, Lowry CA, Raison CL. Microbial ‘Old Friends’, immunoregulation and stress resilience. Evolution, Medicine, & Pubic Health 2013, (1): pp. 46-64. 4. IFH. Home Hygiene. Available online at: www.ifhhomehygiene.org (Last accessed 4th September 2013).
November 2013 Vol 133 No 6 l Perspectives in Public Health 303 Downloaded from rsh.sagepub.com at St Petersburg State University on December 10, 2013
