The July issue of Perspectives in Public Health (published by the Royal Society of Public Health) takes an objective view of ongoing research showing that the hygiene hypothesis – the idea that allergies are the price we are paying for our “modern obsession with cleanliness” – is a misleading misnomer. Not only does it undermine attitudes to hygiene at a time when antibiotic resistance threatens our ability to treat infections, it also hinders the search for ways to reverse the recent dramatic rise in allergies and other chronic inflammatory diseases. These conclusions and the underlying data are set out in this issue, in a review which summarises the consensus findings of six experts who presented at a joint conference organised by the Royal Society for Public Health and the International Scientific Forum on Home Hygiene in February 2016, together with articles from other contributors.
Whilst the primary function of our immune system is to protect us from infection, equally the system must tolerate non-harmful agents, which we also constantly encounter in our daily lives, many of which may be helpful to our health. For the development of immune tolerance, it is believed that the immune system requires exposure to certain microbes and even intestinal worms (collectively referred to as “Old Friends”) that evolved together with humans during primate evolution in hunter gatherer times when the immune system was evolving. Failure to develop the right ‘type’ of immune tolerance may lead to inappropriate responses to otherwise harmless agents such as pollen and foods, etc., causing allergic reactions; it can also attack our own body tissues causing diseases such as multiple sclerosis and type 1 diabetes.
The Old Friends mechanism was proposed by Graham Rook in 2003 as an alternative to the hygiene hypothesis, proposed in 1989 by David Strachan. Professor Rook, one of the review authors, states that “although Strachan’s idea about the importance of human:microbe interactions was essentially correct, the original hygiene hypothesis that the vital exposures were infections such as colds, influenza, measles and similar childhood illnesses is unlikely. Common childhood infections are not believed to have existed in early human populations when our immune system was evolving”.
Although the Old Friends are still there, our bodies are less exposed to them due to a range of changes which have occurred over the last 200 years. These include sanitation and clean water supplies (which have cut us off from Old Friends as well as harmful microbes), changes in lifestyle, rapid urbanization, altered diet and excessive antibiotic use, all of which have had profound effects on the human microbiome (the millions of microbes which live on or in our bodies), leading to failure of immunotolerance and increased risk of allergic and other inflammatory diseases. In a special article, Professors Tobias Rees and Martin Blaser explore the concept that, in the future, the benefits of antibiotics will need to be weighed not just in terms of their life-saving properties, but also their possible adverse effects on the human microbiome and immune health.
Review author Professor Sally Bloomfield says, “there is no good evidence that hygiene, as the public understands it, is responsible for the loss of vital microbial exposures. If our day-to-day hygiene and cleanliness habits contribute, their role is likely to be small relative to other factors. Modern homes, however clean they appear, are “teeming with microbes” which come from the people and domestic animals living there, the food they eat, together with input from the local outdoor environment – and circulate constantly via hands, surfaces, etc. It is quite probable that the microbial (and intestinal worm) content of modern urban homes has altered, but not because of home and personal cleanliness, but because, prior to the 1800s, people lived in predominantly rural surroundings and had different diets and no antibiotics. As a result, we now interact with a very different and less diverse mix of microbes”.
In tackling the issue of allergies and chronic inflammatory diseases, US Professor William Parker argues against traditional therapeutic approaches. He says, ”currently held views that drug discovery and development offer effective solutions to these diseases which are products of modern society, are deeply flawed – not only is this approach expensive, it is about treating disease without addressing underlying causes”.
If allergic diseases are not the price we have to pay for protection against infection, this is good news. However, if we are to maximise protection against infection whilst at the same time sustaining exposure to our Old Friends, we need to actively pursue three things:
- Review author Elizabeth Scott says, ”we need to adopt smarter approaches to hygiene than the ‘scrupulous cleanliness’ approach advocated by Florence Nightingale. Hygiene is more than ‘keeping our home spotlessly clean’”. Professor Scott and another review author, Professor Sally Bloomfield, say, “Good hygiene is based on knowing how harmful microbes are transmitted around the home and other environments, and targeting hygiene practices in the places and at the times that matter to prevent these microbes from spreading, most particularly times associated with activities such as food, respiratory, hand and toilet hygiene”.
- Recent studies suggest that strategies to restore interaction with our Old Friends, such as natural childbirth, healthier diets, reduced antibiotic prescribing and increased outdoor exposure, could reverse trends in inflammatory diseases. Professor Fergus Shanahan is optimistic but cautions: “much further work is needed to evaluate this”.
- To take advantage of new perspectives, we must first change public, public health and professional perceptions. The consensus of the review authors is that “the term hygiene hypothesis is a misleading and dangerous misnomer which must be abandoned in favour of a more appropriate term such as the Old Friends Mechanism. Continuing publicity given to this misnomer, and the notions which it sustains, are undermining public confidence in hygiene as a means to prevent infection”.
Review author Dr Rosalind Stanwell-Smith says, “having enjoyed the benefits of sanitation, clean water and food, antibiotics and vaccines over the last century, we face the possibility that antibiotic resistance may rob us of the ability to treat infection”. Agencies working to tackle antibiotic resistance clearly recognise that “every infection prevented is less antibiotics used”. The importance of hygiene in the home and in everyday life is also being driven by increasing numbers of people at increased risk of infection living in the community, and the increasing amount of healthcare being delivered in out-of-hospital settings. The 2015 Ebola outbreak also serves as a reminder that hygiene is the first line of defence during the early critical period of an outbreak or other emergency situations before mass measures such as vaccination become available.
In a guest editorial, Professor Sally Bloomfield concludes:
Microbiome science shows us that our microbiome constitutes an organ, as essential to health, as our liver and kidneys. To tackle diseases related to immune dysfunction, and infectious diseases, in future, we are all, health agencies and the public alike, going to have to view our microbial world very differently.