The “Hygiene Hypothesis”

PERSONAL VIEW thebmj.com Ж Read rapid responses to this article at bit.ly/hygieneresponse The “hygiene hypothesis” for allergic disease is a misnomer “Biome depletion” is a better term for how immune function is undermined in industrialised societies, writes William Parker, 25 years after The BMJ published David Strachan’s seminal hypothesis publication by David Strachan in “the hygiene hypothesis.” And the reasons for Issues regarding the inaccuracy of the The BMJ in 1989 described the idea being careful about this label extend beyond the term “hygiene hypothesis” are compounded that a loss of species diversity from correct attribution of the term to its originator. because the biome depletion paradigm forms the ecosystem of the human body First and foremost, the term “hygiene hypo- a fundamental principle of modern immu- could lead to allergic disease (BMJ thesis” has become a misnomer. Biome depletion nology and can no longer be considered a A1989; 299:1259-60).1 Subsequent studies have in Western culture was indeed induced in the 20th hypothesis. So, not only is the underlying focused on exactly which species of symbionts century by the revolutionary and widespread use cause of allergy and autoimmunity unrelated might be important,2 and they have expanded of such technological advances as sewer systems to hygiene as we understand it today, but our the model beyond allergy to include autoim- and water treatment facilities. However, hygiene understanding of the cause ceased to be a mune diseases3 and cognitive disorders related today is associated much more with handwash- hypothesis some years ago. to inflammation.4 This view, now confirmed by a ing and the use of a dust More important than vast body of literature as a cornerstone of immu- mop than the availability Modern hygienic practices issues of attribution or nology, is likely to affect the discipline of cancer of a toilet and clean drink- often alleviate, not increase, inaccuracy, use of the term study in the future.5 ing water. This modern allergy—by reducing the “hygiene hypothesis” in Strachan’s view can be accurately described view of hygiene—relating levels of allergens produced by connection with dreaded as “biome depletion,” an evolutionary mismatch to personal health habits organisms such as dust mites, immune diseases gives that works in tandem with other mismatches rather than advancing cockroaches, and mould credence to the view that (for example, inflammatory diets and vitamin technology—is not a signifi- hygiene is not beneficial— D deficiency) to undermine immune function in cant factor in the increased incidence of allergic potentially undermining public health efforts industrialised societies.6 Strachan articulated disease. On the contrary, a lack of handwashing aimed at avoiding the spread of infectious dis- his quantum leap of thinking in his 1989 paper, often results in an increased incidence of flu and ease. Perhaps most importantly, the term diverts stating, “These observations do not support sug- other acute infections, many of which exacerbate attention from the intuitive solution to the prob- gestions that viral infections, particularly of the rather than mitigate allergy and autoimmunity. lem of biome depletion: biome enrichment or respiratory tract, are important precipitants of Furthermore, modern hygienic practices often restoration.11 the expression of atopy. They could, however, alleviate, not increase, allergy—by reducing the Barker’s term “hygiene hypothesis,” which he be explained if allergic diseases were prevented levels of allergens produced by organisms such as applied to a view much older than his own work, by infection in early childhood.” dust mites, cockroaches, and mould. Thus, aller- clearly deserves its place in the history books as With this statement, Strachan dismissed the gies and autoimmune diseases are not caused by part of our ongoing evolution in understand- prevailing notion that immune diseases, par- “hygiene” as people now think of it. ing the pandemics of non-infectious, immune ticularly asthma, were the results of infections. related diseases that plague industrialised soci- Instead, he suggested the seemingly bizarre eties. But the term is a complete misnomer that notion—now widely appreciated—that coloni- can deflect attention from potential solutions. sation by an organism could prevent an allergic It is time to provide the model with an appro- disease that was apparently unrelated to that priate and productive name, giving credit not organism. only to Strachan, but also to those who have Strachan’s view eventually became associated expanded the view of the model over the years to with the nickname “the hygiene hypothesis,” a include depletion of organisms that do not nec- term that had already been coined: David Barker essarily cause disease, as well as a wide range used the term more than once in 1988 to explain of autoimmune and cognitive diseases related an increasing incidence of appendicitis.7 8 Barker’s to immune dysfunction. hygiene hypothesis used the considerably older, William Parker is associate professor, Department of Surgery, and now disproved, view that hygiene led to a Duke University Medical Center, Box 2605, Durham, NC delayed exposure to infectious agents and that it 27710, USA [email protected] was the exposure to those infectious agents rela- 9 10 I thank Chantal Villeneuve of Tufts University (Veterinary tively late in life that caused immune disease. Medicine), Somerville, Massachusetts, USA; and Randal R So, Strachan’s advance was not the already Bollinger, Duke University Medical Center (Surgery), Durham, long held view that hygiene was a problem; North Carolina, USA. Competing interests: None declared. rather, he identified a loss of species diversity Provenance and peer review: Not commissioned; externally peer from the ecosystem of the human body as a prob- reviewed. lem. With this in mind, it seems appropriate to References are in the version on thebmj.com. label Strachan’s advance with a name other than Enriching his biome Cite this as: BMJ 2014;349:g5267 24 8 November 2014 | the bmj LAST WORDS NO HOLDS BARRED Margaret McCartney Pattern spotting Under my fingertips, indentations later broken by anxiety, depression, school or been repeatedly reported as from a now obsolete typewriter flit or obsessional thoughts in the late missing from home. This was against like Braille. Medicine’s recent past teens and early 20s. a backdrop of underfunded social and was typed or written by hand. Flicking Consultations are then frequent— care services, impossibly long waiting through these fading paper records like some in the emergency department, lists for counselling, and children a book, one of my jobs is to summarise some with the out-of-hours service. afraid to give evidence against their them onto a computer. And sometimes A letter from the drugs and alcohol abusers. there is a pattern. service, or a psychiatric nurse, after GPs are pattern spotters—but not Shortly after birth the baby is crying an intentional overdose. This may every such pattern indicates a child a lot, teething, unhappy. Something Half of the abused recur often. The patient may leave at risk. Electronic records disjoint illegible is prescribed from the end children had before a full assessment and then patients’ narratives across separate of a fountain pen. A couple of years not be seen until the next crisis. Self documents, each a click away. Might later, a broken bone. Someone tells misused drugs harm is rife. And after that comes this make patterns harder to spot? the doctor that the child is behaving or alcohol; a third the devastation of sexual abuse in Either way, as GPs we need named badly. DNAs—“did not attends”— had mental health childhood. social workers in our teams who we actually mean “child not brought by problems Some 1400 cases of child sex can talk to as regularly as our health the adults responsible.” abuse went unchecked in Rotherham visitors. And we need to fund health Vaccination schedules slip. from 1997 to 2013, the horrendous and social services properly, so that Frequent presentations occur with recent report details.1 Half of these the most vulnerable children always one word outcomes. The copperplate thebmj.com children had misused drugs or get the priority they need. swirls make no other comment. ̻ Baby P: The Untold alcohol; a third had mental health Margaret McCartney is a GP, Glasgow A head injury; another accident. Story, reviewed (BMJ 2014; problems; two thirds had emotional [email protected] A presentation to the emergency 349:g6643) difficulties. Almost half came from a Competing interests and references are in the department with intoxication in late Twitter home with reports of domestic abuse, version on thebmj.com. childhood. And then silence, which is ̻ @mgtmccartney and two thirds had refused to go to Cite this as: BMJ 2014;349:g6347 William E Cayley Jr practises at the Augusta Family BMJ BLOG OF THE WEEK William E Cayley Jr Medicine Clinic; teaches at the Eau Claire Family Medicine Residency; and is a professor at the University of Patient time v patient time Wisconsin, Department of Family Medicine Who are you, what do you need, and that is gathered (eg, documentation of The sick person I see 20 chats I learned the extent to which how do I figure out how to care for you? resuscitation preferences, tobacco use, minutes late, because of the patient’s primary health concern Fundamentally, those are the or marital status), or the conversation wonderful conversations was really about the health of another questions that drive every encounter and relationship building. Sometimes, with other patients, does family member. between a doctor and a patient. A Yet we are in the profession of even the most thorough gathering not care how wonderful recent article in the New England of social history leads to the same caring for the sick, and the sick Journal of Medicine calls for us to amount of essentially flat and affectless those conversations were person who I see 20 minutes late, expand the “social history” facet of note taking as reviewing a medication wishes, etc).

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