Clinicians’ views and expectations of human microbiome science on asthma and its translations

Abstract

Human microbiome science examines the microbiota that live in and on the human body and their role in human health. This paper examines clinicians’ views and expectations of microbiome science in asthma care. Drawing on qualitative interviews with 10 clinicians in Canada, we explore their perspectives for insights into translation of human microbiome science. The emphasis on novelty in much microbiome scholarship, we suggest, does not account fully for the ways in which microbiome science translations may be taken up in multiple ways that are both disruptive to and continuous with contemporary biomedicine. We suggest that clinicians drew on scientific discourses of “evidence” and “facts” as a form of boundary work to re-establish a separation between western biomedicine and alternative health practitioners, and clinical expertise and lay knowledge. We conclude with a discussion of human microbiome science and the emergence of post-Pasteurian modes of health in western biomedicine.

Keywords:

• Human microbiome
• clinician expectations
• translation
• asthma
• boundary work
• post-Pasteurian

Introduction

Human microbiome science is a relatively new and growing field examining the microbiota that live in and on the human body and their role in human health. Researchers are examining the microbiota in various parts of the body (e.g. gut, mouth, vagina, and lungs) to understand how microbes interact with human physiology and influence health. The scope of applied microbiome research is broad and increasing. For example, scientists are examining the role of the microbiota in asthma (Arrieta et al. 2015), cystic fibrosis (Maughan et al. 2012), and vaginal health (Albert et al. 2015; Chaban et al. 2014). Researchers are also studying more fundamental questions related to the microbiome such as its stability over time (Costello et al. 2009; Lozupone et al. 2012) and the transmission of microbiota among people living in close proximity (i.e. horizontal transmission) as well as across generations (i.e. vertical transmission) (Schwarz et al. 2008; van Opstal and Bordenstein 2015).

For proponents, there is little doubt that human microbiome research is the next great frontier in the molecular life sciences and that it will lead to many new clinical applications (Blaser et al. 2013). Some commentators consider microbiome research to be the “second human genome project” with its focus on the interactions between microbial and human genomes and the expectation that microbiome research will deliver the many clinical benefits that the first human genome project failed to do (Cho and Blaser 2012). The therapeutic promise of new applications, in part, has encouraged financial investment in various jurisdictions and the development of national and international networks organized around the human microbiome. In 2007 the National Institutes of Health in the USA began the 5-year Human Microbiome Project (HMP) with the aim of surveying and cataloguing microbial genome sequences in the microbiomes of healthy adults (Proctor 2011). Also in 2007, a meeting of international scholars working on the human microbiome was held in Rockville, MD to discuss the establishment of an international network of microbiome scholars. From this meeting the International Human Microbiome Consortium was established by Australia, Canada, China, the EU, Singapore and the USA.¹ Since then, the Canadian Institutes for Health Research in Canada has invested over $17 million on microbiome research.² In 2016, following the HMP, the USA proposed a further investment of $121 million in the National Microbiome Initiative (Reardon 2016).

Translation scholarship tells us that the movement of microbiome findings from the laboratory to the clinic involves material and immaterial shifts (Lewis, Hughes, and Atkinson 2014) and movement across different social worlds (Fujimura 1996). The social world of the clinic – that is, the meanings, perspectives and commitments of clinicians – differ from that of research scientists in the laboratory. Clinicians are key social actors in the translation process and thus examining their expectations of microbiome science not only provides conceptual and practical insights on translation, but also sheds light on the current social and cultural context of biomedicine into which microbial applications will be situated. To date, no research has examined clinicians working at the “coal face”, to borrow from Pickersgill (2011), of patient care and their views of human microbiome research. The current paper addresses this gap by exploring clinicians’ views and expectations of microbiome science in asthma care. Drawing on in-depth, semi-structured interviews with clinicians, we explore their expectations of human microbiome science for what it might tell us not only about microbiome translations, but also about broader biomedical preoccupations and new modes of health from changing human-microbe relations.

Clinicians in this study expressed both high and low expectations of human microbiome translations and situated their discussions of microbiome interventions in relation to the hygiene hypothesis and clinical use of antibiotics. In these discussions, some clinicians suggested a model of the body that is holistic and intelligent which stands in contrast to the conventional biomedical model of the mechanistic body. Interviewees spoke about microbes as both mutualists (i.e. necessary for human health) and pathogens, consistent with a post-Pasteurian view (Paxson 2008, 2014). A post-Pasteurian view recognizes that some bacteria are “good” (i.e. mutualists) and others “bad” (i.e. pathogens). In this nuanced view, the work of good bacteria is harnessed to help control the harmful effects of bad bacteria (Paxson 2008, 2014). Paxson (2014) makes explicit that a post-Pasteurian view is not an anti-Pasteurian one. That is, a post-Pasteurian view recognizes that some microbes are harmful and it is only because of the success of Pasteurianism in managing pathogens that a post-Pasteurian view can exist. Post-Pasteurianism is aligned with a microbiopolitics that aims to categorize and evaluate microbes and govern human behavior in order to manage this more complex view of human-microbe relations (Paxson 2008, 2014).

Throughout most interviews, clinicians spoke about microbiome research on asthma as providing scientific “evidence” and “facts” in support of the health-promoting role of microorganisms. We suggest that clinicians’ emphasis on scientific evidence and facts not only demonstrates that western medicine has increasingly come to rely on the biological sciences (i.e. “bio”-medicine) (Clarke et al. 2003), but that clinicians are engaging in a form of boundary work (Gieryn 1983) or discursive boundary making (Kerr, Cunningham-Burley, and Amos 1997) in response to potential disruptions associated with microbiome science translations. Examining the role of scientists in distinguishing between “science” and “non-science”, Gieryn (1983) defines the “boundary-work of scientists [as] their attribution of selected characteristics to the institution of science (i.e. to its practitioners, methods, stock of knowledge, values and work organization) for purposes of constructing a social boundary that distinguishes some intellectual activities as ‘non-science’.” (782, italics in original). Kerr, Cunningham-Burley, and Amos (1997) draw on Gieryn’s (1983) and Gilbert and Mulkay’s (1984) work to examine how new genetics professionals draw boundaries to maintain cognitive authority and participate in debates regarding the social implications of the new genetics. They refer to these activities as discursive boundary making (Kerr, Cunningham-Burley, and Amos 1997). While Gieryn’s concept of boundary work applies to practices, Kerr et al.’s description of discursive boundary making deals with discourse and interactional phenomena. Together, these concepts provide a strong foundation for our analysis in this paper as they capture both material and discursive aspects of how boundaries between social groups are made and re-made. Two sites of disruption suggested by interviewees in our study include: boundaries between patients and clinicians and boundaries between western biomedicine and alternative health approaches. First, with lay publics learning about human microbiome science and patients increasingly seeking out their own health knowledge, clinicians can reassert the boundary between their expertise and patients’ non-expertise through scientific discourses emphasizing evidence and facts. Second, while human microbiome science is relatively new, alternative health approaches have a longer history of recognizing the benefits of microbes in human health (Sangodeyi 2014). In this context, clinicians drew on scientific evidence of human-microbe interactions in health to provide epistemological authority and set biomedicine apart from these alternative approaches.

The translation of microbiome research into clinical care is of great interest to scholars, funding agencies, and lay publics. In this paper, we examine one specific group of social actors in the translation process, practicing clinicians, to better understand shifts and continuities in clinical care and discourse associated with microbiome translations in the context of asthma. We demonstrate that clinicians discussed microbiome findings in terms of both high and low expectations and mobilized discourses of “scientific evidence” and “fact” as a form of boundary work to delimit western biomedicine from alternative health approaches. Moreover, microbiome findings were discussed in relation to the hygiene hypothesis and concerns regarding antibiotic use suggesting the emergence of post-Pasteurian modes of health.

Biomedical translation circuits and expectations

Translation of scientific findings into clinical practice is a complex process involving multiple social actors, regulations, technologies, and knowledges (Lewis, Hughes, and Atkinson 2014). While conventional approaches to translation view it as the uni-directional or bi-directional movement of some stable entity or phenomena from one field (e.g. the laboratory) to another (e.g. the clinic), Lewis, Hughes, and Atkinson (2014) argue that this view of translation fails to capture the complexities and instabilities of the translation process. They argue that translation involves both material movement and conceptual transformations as phenomena from one domain are made sense of and integrated in another domain (Lewis, Hughes, and Atkinson 2014). Moreover, the process of translation may also transform the “thing” itself that is being translated. As Lewis, Hughes, and Atkinson (2014) contend, translation does not simply happen, it is made to happen, and clinicians are critical to this process.

With the emphasis on translation in science and biomedicine and its increasing normative weight in determining funding priorities, high expectations in emerging promissory scientific fields, like human microbiome science, are increasingly important. For example, post-genomic scientists have been shown to take seriously an ethics of translation – that is, to have a sense of social responsibility – regarding their research (Ackerman et al. 2017). Yet how this research is translated for the benefit of the “public” is a complex and, at times, ambiguous process given the disciplinary range of the scientists conducting post-genomic research. Different disciplines use different techniques and technologies, and have different conventions and standards for knowledge production. These differences play a critical role in making certain kinds of translations possible and others not (Ackerman et al. 2017). The field of microbiome science is also made up of disparate disciplines with differing epistemological and ontological commitments, providing a context that may contribute to uncertain futures for microbial translations. Human microbiome science is, no doubt, viewed by its proponents as a field holding great promissory potential. The large financial investments to fund this research, backed by the legitimating weight of national organizations in countries around the world (Sangodeyi 2014) support a vision of the future in which microbial treatments and interventions will play a significant role in maintaining and managing human health and disease. These high expectations for microbiome science (whether justified or not) have a hand in shaping future clinical applications.

As scholars in the sociology of expectations argue, high expectations of science and biotechnologies function to bring new technologies and scientific advancements into being (Borup et al. 2006; Brown and Michael 2003). In other words, expectations are conceptualized less as personal or cognitive phenomena, and more as social actants tied to material and non-material phenomena that are critical to enacting particular futures (Martin, Brown, and Kraft 2008). Expectations, viewed this way, may be more significant when practical applications have yet to be developed in an emerging area of science (Brown and Michael 2003). In some areas of scientific development, low expectations may also play an important role in guiding the direction of innovative scientific fields (Fitzgerald 2014; Pickersgill 2011; Tutton 2011). Examining the translation of neuroscientific findings on personality disorder into the clinic, Pickersgill (2011) demonstrated how neuroscientists and clinicians emphasized the ontological complexities of personality disorders and had ambivalent expectations of clinical futures for neuroscience. Clinicians used low expectations of developing clinical applications to manage the expectations of patients. While emerging neuroscience provides a new view of personality disorder as located in the brain and produced neuroscientists as new experts in this field, the scientists themselves emphasized the challenges of translating scientific findings to clinical treatments for a complex condition such as personality disorder (Pickersgill 2011). Thus, both high and low expectations for innovative scientific fields act to bring about particular futures for these fields. Expectations or concerns from the clinic may have a hand in shaping the particular direction and futures of scientific work just as science and its attendant techniques and technologies can shape and influence clinical practice. Even before clinical applications are available, how clinicians view microbiome research and their expectations about possible clinical implications provides insight into the translation process and attendant conceptual and material changes.

Human microbiome science and the Microbial Body 2.0

While much of the current popular and scholarly writing on human microbiome science frames it as highly novel and ground breaking, Sangodeyi (2014) argues in his history of the emergence of the Microbial Body that its current iteration – that is, the twenty-first century version supported by such projects as the HMP- is in fact version 2.0. Various groups throughout the twentieth century extolled the virtues of mutualistic bacteria and their role in human health. These early post-Pasteurians included scientists (e.g. intestinal bacteriologists and gnotobiologists), clinicians (e.g. dentists), and others (e.g. counter-culturalists and feminists) who were largely marginalized and ignored by those in science and medicine who held the dominant Pasteurian view of microbes (i.e. microbes are viewed primarily as pathogens). What is different in the twenty-first century, according to Sangodeyi (2014) is that the voices of groups supporting a post-Pasteurian view of microbes today carry tremendous authority and weight (e.g. the National Institutes of Health and the National Research Council). In addition to these new and powerful supporters, the emergence of the Microbial Body 2.0 was made possible by the taking up of ecological theory and discourse in various fields of science and the development of new molecular technologies, namely metagenomics (first used to study soil science). Sangodeyi’s (2014) intervention into the dominant view espousing the novelty of human microbiome science is significant, we suggest, for at least two reasons. First, an over-emphasis on novelty in new scientific “discoveries” promotes the idea that scientific discoveries occur ex nihilo; that is, free from the social, political, economic, and technological conditions that make them possible. Second, this kind of fetishization of the novel, by which we mean the erasure of the social, political, and economic conditions that make the emergence of a phenomenon possible, can lead to assumptions about the phenomenon that are not grounded in empirical details. Being mindful of the historical- and social-situatedness of the Microbial Body 2.0, we review some of the key scholarship shaping the field of human microbiome science.

Much of the social sciences and humanities literature, thus far, has focused on examining rhetorical strategies and/or metaphors used in microbiome science, and reflections on potential ethical, legal and social issues associated with microbiome research. Social scientists and philosophers contend that metaphors in microbiome research suggest a significant shift in ideas about the individual, human species, and health and illness (Juengst 2009; Juengst and Huss 2009; Nerlich and Hellsten 2009). Metagenomics, or the study of the entire complement of microbial genomes (Qin et al. 2010), views the human body, and specific sites such as the gut and mouth, as naturally occurring “environments” or “ecological systems” for microbes. In other words, the human body is viewed as composed of numerous interacting ecological systems (Blaser 2006). Viewing the genomes of a community of microbes as a single metagenome destabilizes long-held categories in the biological sciences, such as the “individual organism” since conventional ideas of the individual organism are of an autonomous cell or group of cells that share the same genome (Dupré and O’Malley 2007). Microbiome scientists theorize that the human genome co-evolved – and continues to co-evolve – with the microbial genome disrupting a long-held view of the human being as a single, genetically autonomous species (Juengst 2009). Lastly, ecological metaphors and discourse may lead to shifting ideas of health and illness as health comes to be understood as a state of ecological “balance” and illness as a state of “imbalance” (Juengst 2009). Conventional ontological conceptualizations of disease that view it as separate from the human host are challenged by views in which disease is not a foreign intruder, but overall system disruption (Juengst 2009).

Scholars have also examined social, ethical and legal issues related to human microbiome science. This body of scholarship has dealt with questions of privacy and confidentiality regarding microbial samples, legal questions of ownership, and commercialization of microbiome research (Chuong et al. 2017; Hawkins and O’Doherty 2011; Rhodes, Gligorov, and Schwab 2013; Slashinski et al. 2012). Scientists suggest that a person’s microbiome is unique and may act as a “fingerprint” opening up the possibility of personal identification by one’s microbial sample (Franzosa et al. 2015). This raises ethical concerns regarding anonymity and confidentiality in human microbiome research thus attendant safeguards may be necessary (Hawkins and O’Doherty 2011). In addition, microbiome research adds greater complexity to questions of ownership and property of biological samples since it involves material that is both human and microbial, and must be retrieved from people. Matters of property and ownership of human body tissue depend on the relationship between the person and their tissue (Charo 2006). If the microbiome is considered to be part of the person’s body (i.e. an “organ” as some microbiome scientists suggest), then questions of ownership fall under the ambiguous rules and laws that govern human bodily property (Schwab et al. 2013). Moreover, as clinical applications are developed from human microbiome research, the potential for commercial profit is significant, raising questions of who might have rights to some of these profits (Schwab et al. 2013; Slashinski et al. 2012). In summary, current social sciences and humanities scholarship suggests that human microbiome science will have significant and far-reaching effects on biomedical practice, both practically (e.g. new treatments and diagnostics, collection of microbial samples, etc.) and conceptually (e.g. new understandings of health and illness).

Background and methods

An important area of human microbiome research involves investigating the association between the gut microbiota and asthma. Asthma continues to be a highly prevalent chronic airway condition in the global North for which there is currently no cure. Microbiome researchers have identified in humans a causal link between the abundant presence of 4 gut microbial strains and asthma (Arrieta et al. 2015). Children who had lower relative abundance of the bacteria Lachnospira, Veillonella, Faecalibacterium, and Rothia owing to gut microbial disruption were shown to be at greater risk for developing asthma (Arrieta et al. 2015). In other words, these bacteria were critical to the developing immune system and protected against developing asthma. Disruptions of the gut microbiota, for example through exposure to antibiotics during a “critical window” period (i.e. the first 100 days of life), were associated with risk of long-term adverse health effects. Researchers argue that their findings have important implications for clinical practice including the potential for microbial therapies to protect against the development of asthma and other immune hypersensitivities, such as eczema (Arrieta et al. 2015). While clinical applications have not yet been developed from these findings, the authors contend that this research is highly promising and contributes to understanding the gut microbiome’s role in developing a healthy immune system.

The data for this paper were generated as part of a larger study examining the relationship between the gut microbiota and asthma, and the lived experiences of people with asthma. Given the lack of research conducted with clinicians and microbiome research, we sought to address this gap by conducting an exploratory, qualitative study with clinicians in Canada. The clinicians interviewed offer a diverse range of perspectives of non-specialist practitioners and provide early insights into clinical views of human microbiome science in relation to broader social and clinical concerns. By clinicians we refer to physicians and nurses who are responsible for providing healthcare services to people living with asthma. None of our participants identified as scientists or conducted research on the human microbiome. We conducted semi-structured interviews with 10 clinicians (7 physicians and 3 nurses) who treat people with asthma, to examine their expectations of microbiome science and their views regarding translation of these findings into clinical practice. Participants were recruited through national organizations for physicians and nurses, and through researchers’ professional networks using a purposive sampling strategy with the aim of gaining a diverse sample of practicing clinicians from across Canada. Interviews were conducted by JH from May 2015 to October 2015. The 10 participants were from three provinces: Ontario, Manitoba, and Saskatchewan. They ranged in clinical experience from junior clinicians who had recently graduated, to clinicians who had been practicing for over 30 years. Although none were respirologists, most had practices with high rates of asthma cases and several were considered to be leaders in their field in airway conditions. The clinicians were diverse practitioners ranging from emergency room and neonatal intensive care nurses to family physicians, paediatricians and general hospital physicians. Since, at the time of the interviews, the research on a causal relationship between gut microbiota and asthma had just been published, participants were given a one-page summary of the recent findings on the microbiome and asthma (Arrieta et al. 2015) to review prior to, or during the interview. Each interview lasted from 30 to 60 min and was audio-recorded with the participant’s permission. Participants were asked broad and open-ended questions about their thoughts on the recent findings, how they thought the findings might influence their practice, and any issues they thought might arise from the application of microbiome research in their practice. Ethics approval was received from the Research Ethics Board at the University of Guelph.

Data analysis followed an iterative process moving between interview transcripts and the literature. All interviews were transcribed and coded using NVivo 10. Guided by constructionist epistemology we did not treat clinicians’ accounts to be reflections of an objective reality, but rather as insights into socio-cultural and discursive contexts within which microbiome science will be entangled. We do not suggest that the expectations and views expressed by our interviewees are necessarily indications of how things will occur in the future; instead, we consider their speculations to be indicative of the current context of, and preoccupations in, biomedical practice that may be relevant as microbial interventions are developed. Moreover, what clinicians had to say about microbiome science and its translations provide insights into potential shifts, disruptions, and as we show, continuities with biomedical practice and discourse. In our analysis we focused on interview excerpts that discussed microbiome findings and translation in relation to clinical practice and concerns, and analysed these excerpts for what they might suggest about broader social and clinical issues.

Cautious optimism

When clinicians in this study spoke about microbiome research and future treatments they did so in terms that expressed both high and low expectations. In particular, they were optimistic about the potential of microbiome science in broad terms and much more cautious when speaking about specific treatments for asthma. Clinicians described the future possibilities for microbiome science by using words such as, “phenomenal”, “fascinating” and “thought provoking”. P6, a family physician, suggested that the current asthma findings are only “the tip of the proverbial iceberg in terms of what’s coming” and described microbiome science as the “Wild West”, evoking images of a new frontier ripe with possibility, but also potential hazards:

This is like the Wild West, this is like the very beginning of something that has a, just a dramatic and huge future potential to it. So to me this is very exciting to see what is going to come out of this.

While specific applications for asthma are not yet available, clinicians envisioned many possibilities for future diagnostics and treatments in their practice. These included: early screening of infant gut microbiota during the critical window period to detect absence of protective microbial strains and intervening with microbial treatments; the potential to adjust the microbiota of patients outside of the critical window period to treat asthma and immune hypersensitivities; and to optimize the microbiota of pregnant women to potentially populate the newborn’s gut with health promoting bacteria. One physician, P2, spoke about the potential for the administration of the protective bacteria to act as “vaccinations” against asthma in the future. Set within a backdrop of clinical concerns regarding current asthma treatment adherence (Bender et al. 1998), clinicians expressed high expectations of the potential for microbiome research to offer asthma prevention and immune system treatment.

High expectations were tempered by low expectations regarding when these applications might actually become available and when the findings might be clinically actionable. P2 described changes in clinical practice as “excruciatingly slow.” He, and others interviewed, spoke about clinical practice as largely based on following guidelines similar to an “algorithm” that organized how they do their work. All the clinicians agreed that any changes to their clinical practice would require much more clinical evidence and changes to clinical guidelines. A paediatrician, P10, explained that the microbiome results would need to be “solidified as fact, or truth, by medical research” and “proven in the literature” before she would make any changes to her clinical practice. While microbial interventions to prevent asthma are not yet available, protecting against gut microbial dysbiosis by minimizing antibiotic exposure is currently possible. However, for this paediatrician, the potential benefits of minimizing antibiotic use in very young children are weighed against the relatively high risk of these children being harmed by bacterial infection.

Several clinicians spoke about low expectations of microbiome science as offering a means by which to manage patient concerns of their own microbial health. Similar to other fields of innovative science (Pickersgill 2011), clinicians in this study felt they had to help their patients understand the current limits of microbiome science. While clinicians were hesitant to initiate discussions of the microbiome with their patients, all agreed that if their patients brought up the subject they would be happy to discuss the implications of microbiome research on asthma. As P1, a family physician, explained:

I can imagine, new moms reading this [i.e. the findings summary], or new parents, new anybody with a child, reading this, and saying “oh, okay, so what if I were to try and read about those four markers, try and get exposure to them”. I don’t know how they’d do that, but it won’t be contained within the context of somebody who’s already thought it through thinking this is the way that we should implement this. It’s not going to go that way. So I think we’ll be playing catch up trying to manage what people will end up wanting to do based on the information which would be, you know, if someone reads this they’ll think, “well let’s just make sure I have lots of those four things so my baby will be healthier”, and “How am I gonna get them? Well I don’t know if I’ll call the number on the screen and get something to swallow or if I will try and make sure that I don’t have antibiotics, or if I will actually tell my doctor I will not accept antibiotics for my, uh, whatever the hundred day window is”. And that could lead to problems. That could lead to dangerous outcomes.

Clinicians anticipated having to manage the expectations and actions of patients who will have read or heard about microbiome effects on health. A paediatrician, P10, envisioned microbiome research as becoming a “more regular discussion in clinical practice” and “becoming specifically part of the spiel about choosing antibiotics or not.” While it may be some time before specific microbial applications are developed, it may not be long, if it is not already happening, before discussions about microbiome interventions and antibiotics become a common part of the discussion between clinicians and patients.

Hygiene hypothesis and the holistic body

Several clinicians discussed the microbiome findings in relation to the older hygiene hypothesis which suggests mutualistic relations between microbes and humans. They spoke about the positive association between the presence of certain bacterial strains and a healthy immune system as a contemporary, and more specific, iteration of the decades old hygiene hypothesis or “cleanliness model,” as P6 described it. He remembered attending a conference several years earlier and hearing a leading paediatrician and immunologist speak about asthma and hygiene:

And he was talking about the cleanliness model, I mean this observation that there was, you know, … sort of the sterility thing or whatever, um, and so that the observation has been out there for some time but of course nobody could make a causal link or anything. It’s just that, you know, we observed this, this is something we observed. And so this led to, obviously, a lot of speculation.

P4, a family physician who works extensively with patients who have respiratory disorders, also connected microbiome findings with the hygiene hypothesis:

I mean the whole hygiene hypothesis, over whether it’s good to have natural immunity develop versus too much fixing of the environment and fixing with injections in terms of causing asthma. There’s never really been a good theory for this other than just the, sort of what turns on the TH1 versus the TH2 system, the causality and therefore asthma. And the microbiome as a possible link to that makes some good sense.

Among the clinicians interviewed who spoke about the hygiene hypothesis there were different views on what is meant by “hygiene.” P6, for example, seemed to apply a narrow definition whereby hygiene was understood as cleanliness related to personal and domestic practices. On the other hand, P4 discussed the hygiene hypothesis in relation to “fixing the environment” or “fixing with drugs,” suggesting a broader definition of hygiene not necessarily limited to individual cleanliness practices. Fox (1997) recognized this dual understanding of hygiene – i.e. narrower and broader – in his ethnography of the surgical theater and its “circuits of hygiene.” Hygienic practices referred both to specific practices enacted to ensure sterility and cleanliness, and to broader practices aimed at overall health of the patient (Fox 1997).

The hygiene hypothesis was first introduced by Strachan, an epidemiologist, in the late 1980s. He proposed that the increased rates of people with immune hypersensitive conditions such as asthma, hay fever, and eczema were associated with a decrease in cross-contamination and unhygienic living conditions (Strachan 1989). He postulated that decrease in family size, increased standards of cleanliness, and greater use of household cleaning products were leading to people living in “too clean” conditions. More recently, Rook and colleagues have argued for abandoning the term “hygiene hypothesis” in favor of the “Old Friends Mechanism” (Bloomfield et al. 2016; Rook 2012, 2013). According to these scholars, the hygiene hypothesis – which focuses on domestic cleanliness and lifestyle changes – fails to capture the broader evolutionary scope of microbial effects on human immunoregulation. “The Old Friends (OF) Mechanism was proposed by Rook in 2003 and argues that the vital microbial exposures are not colds, measles and other childhood infections (the crowd infections), but rather microbes already present during primate evolution and in hunter-gatherer times when the human immune system was evolving” (Bloomfield et al. 2016: 216). As Rook and colleagues argue, the term “hygiene” is misleading because much of the lay public understands it as limited to personal and domestic practices such as hand washing and cleaning the home. Moreover, they argue that the hygiene hypothesis is potentially dangerous because these hygiene practices remain important to avoid contracting infectious diseases so eliminating them because they are viewed as the cause of illness is dangerous.

Notwithstanding the very important differences between the hygiene hypothesis and the OF mechanism, what both offer is a reorientation of microbes vis-à-vis humans such that they are considered not only pathogens, but also mutualists. In fact, Rook’s choice to refer to microbes as “Old Friends” could not make this reorientation any clearer. Moreover, Rook and colleagues’ critique of the hygiene hypothesis for being misleading also emphasizes the complex relations between microbes and humans by pointing out the still very real threat of infectious microbes and the importance of managing their threat through various hygiene practices. Rook’s OF mechanism exemplifies a post-Pasteurian view in that it recognizes the importance of maintaining practices that protect against pathogenic microorganisms together with the health-promoting role of mutualistic microbes. The bringing together of the hygiene hypothesis with microbiome research that is establishing a “causal link” elevates in epistemological status a view that was once considered to be “observation” and “speculation” (P6). As P6 went on to explain, prior to microbiome research, the clinical advice might have been limited to, “everyone needs to take their child to the farm and let them roll around in the mud”.

Recognizing the health benefits of bacteria and the negative effects of an overly sterile living environment also suggested alternative models of bodies and health for some clinicians. In a clinical context, this shift in models of bodies was again spoken about less as novel and more as a reassertion of older models of bodies in clinical care. P6 described microbiome findings as acting as a reminder of a “holistic” view of bodies and health that is too often displaced by a more mechanistic view in clinical practice:

The microbiota, yeah the gut microbiota, like I’ve done some work with functional medicine, I mean, it used to be called “holistic” or “anti-aging” medicine. It’s gone through iterations as far as names, but the idea that, to try and look at the body from the inside out on an individual basis rather than looking at each person from the top down … . So um, I think the message is that what we learn in microbiology and what we learn in first-year medicine about all these connections seem to get forgotten so easily once we start in practice and it’s all, “here’s a pill for this, here’s a pill for that.”

A holistic view of bodies, one that P6 suggests is supported by microbiome research and taught in microbiology, conceptualizes the body as an inter-connected, dynamic system rather than a static collection of parts. This holistic view of bodies and mutualistic relations with bacteria challenged and put tension on biomedical discourses that assert a mechanistic view of bodies (i.e. bodies are made up of separable parts and the role of medicine is to “fix” the “broken part”) (Armstrong and Armstrong 2010) and that support a Pasteurian view of microbes.

Some clinicians also spoke about mutualistic microbes in human health in relation to alternative approaches to health. In interviews, clinicians intimated tensions between western biomedicine and these alternative approaches. For example, P4 spoke about naturopathic doctors as directly challenging his treatment regimen for people with asthma:

I already have enough naturopathic physicians telling people to stop their [asthma] medication because they’re steroids and they’re bad for you, that I don’t want to have another, ah, I know what does work for asthma. I know what does not work for asthma.

And P6:

I don’t know if you’re what I call “green people”, hippie, uh, “tree hugger”, kind of, “go back to nature” people, they’re claiming that they’re doing this already in terms of, you know, like, they’re not living in a sterile environment … . So [now] we’re learning some of these things scientifically.

The concerns expressed by these clinicians suggest that microbiome findings and translations may add to challenges clinicians experience with patient adherence to treatment regimens – that is, add tensions to patient-clinician relations – and disrupt the boundary between western biomedicine and alternative health approaches and biomedicine’s authority. If alternative health practitioners have been arguing against living in a too-sterile environment for some time and western biomedicine is coming to recognize this now, the two approaches may not be as different as previously thought and biomedicine’s slower recognition of the importance of microbes may position alternative approaches, for some patients, as superior. Clinicians who mentioned these concerns addressed these challenges by distinguishing the microbiome findings from alternative medicine and “hippies” by speaking of the scientific evidence that microbiome findings offer. They pointed out that recognizing the role of mutualistic bacteria and a holistic view of bodies in biomedicine is based on microbiome findings with the implication that scientific research offers valid evidence. For clinicians, microbiome findings hold different and superior epistemological status than anecdotal, or non-scientific, evidence which many associate with alternative fields of medicine. Clinicians’ assertion of scientific evidence as unique to microbiome findings and its epistemological authority, we suggest, demonstrates a form of boundary work to re-establish a boundary and hierarchy between western biomedicine and alternative health approaches.

Antibiotic use and the intelligent body

Clinicians also discussed the findings of a causal association between gut microbial dysbiosis and the development of asthma in relation to antibiotic use for bacterial infections. Concerns regarding the liberal use of antibiotics and the evolution of antibiotic-resistant bacteria, or “superbugs”, have led many experts to advocate for more judicious use of antibiotics in humans and animals (Cully 2014). The current rhetoric on antibiotic-resistant bugs draws on military metaphors, such as an “arms race”, to describe the state of affairs regarding drug resistant bacteria and human health (Hede 2014). It frames concerns regarding antibiotic use as an urgent and life-threatening battle in which we are racing against the speed at which bacteria mutate and develop antibiotic resistance. P8, a paediatric nurse working in a neonatal intensive care unit, spoke about current tensions and challenges with antibiotic treatment:

When antibiotics first came out, they thought it was going to cure the world and everything and now we’re getting into all these superbugs and we’re having to make stronger and stronger and bigger and better antibiotics [be]cause half of them don’t work all the time … That resistant list is growing.

Other clinicians spoke about challenges with patients not complying with completion of a full cycle of antibiotics, potentially contributing to the development of antibiotic resistant bacteria. These concerns are well established with public health organizations, such as the Public Health Agency of Canada³ and the Centers for Disease Control and Protection in the USA⁴ cautioning physicians about the rise in antibiotic and antimicrobial resistance. Moreover, the WHO considers antimicrobial resistance as a growing threat to global public health.⁵

Currently, administering antibiotics involves weighing the risk of harm to the individual patient from the bacterial infection against the risk to society of the development of antibiotic-resistant bacteria. However, as P1, a family physician, explained microbiome findings may introduce a new risk consideration regarding antibiotic use:

So usually that decision about antibiotics is based on how, like, the actual condition that you’re trying to treat in the moment, how sick they are, and what [are] the chances that they’ll get better without antibiotics meaning that it’s viral, and what’s the chances that they won’t, and how close are they to care if they get worse in the next hour or two. Can they get to the emergency room? How comfortable are the parents in understanding, in noticing signs? How possible is it for someone to have close monitoring in their certain situation, their social environment? And then you’re also balancing that with the risk of resistance. So, you don’t want to give extra antibiotics, and you don’t want to give extra antibiotics for the sake of the actual child [be]cause they all have side effects and you don’t want to have extra antibiotics for the sake of society at large. And you don’t want to use drugs when you don’t need to use drugs [be]cause that’s a cost we don’t need to incur. Um, so all of those things go into the normal, what we call the normal, the current decisions on antibiotics. But now we’re adding another thing to that and that another thing might be quite an important thing. And it’s going to be something that people on different sides of the table will have different, weighing it in different amounts in their head. Because it will be more about the acute, “are they going to die right now?” [for physicians]. And [parents of young children] will be more about, “but I want them to be healthy when they’re 30 and not have asthma when they’re trying to play soccer 10 years from now.” And, um, they both are important, but they’ll be differently important to different people at the table.

In the context of risk assessment, this physician suggests that microbiome applications may introduce a new consideration concerning the risk to the individual patient of harm in the present versus the risk of adverse health effects in the future. Current risk calculation regarding antibiotic use involves weighing risks in the present versus the future, and risks of acute versus chronic illness. As P1’s quote demonstrates, risk calculations by clinicians are complex and context-dependent in which different social actors – patients and clinicians – may have different views and priorities. P1 suggests that microbiome research may add to this complexity by introducing a new dimension; that is, time, with considerations of present versus future health. She suggests that in weighing the risks of acute versus chronic illness, clinicians may prioritize the former while parents of young children may prioritize the latter. How these tensions and trade-offs between clinicians and parents are resolved will be influenced at least in part by the extent to which clinicians are viewed as an authority.

Microbiome findings introduce into clinical practice the importance of different kinds of bacteria and the need to balance the presence of “good” bacteria with that of “bad” bacteria. As P8, a paediatric nurse explained, this requires clinical tools to identify different bacteria and to treat them accordingly. Antibiotics, she explains, are too blunt in this regard:

So how do they differentiate between, ok, this child is being plagued with a good bacteria as opposed to a bad one making him sick? … You would need a specimen to test. And then try to get a kid to cough up crap from their lungs [laughs] … Well that’s it. The antibiotics can’t differentiate between good and bad, so they kill off everything.

P8 and other clinicians suggested that microbiome research increases the complexity of clinical concerns regarding antibiotics. In addition to the concern of contributing to an increase in the number of antibiotic-resistant bacteria (i.e. a detrimental effect on the treatment of pathogenic bacteria), clinicians must also consider the harmful effects of antibiotics killing mutualistic bacteria and disrupting microbial balance.

Discussion of different types of bacteria and the need to differentiate between these different types also elicited from one physician, P6, a view of the body that is intelligent and able to identify pathogen from mutualist:

And the best things to fight bacteria aren’t [his emphasis] antibiotics. The best things to fight bacteria are actually your body’s own immune system … . it’s hard to imagine, uh, like the change that your body will undergo when your immune system isn’t present to mediate. And being aware of that so that we’re not killing anything. We’re allowing the body to work or we’re interfering with the body’s ability to work.

The kind of body envisioned is an intelligent body working through its immune system to distinguish between pathogenic and mutualistic bacteria. This view of the body, like the holistic body discussed earlier, challenges a mechanistic view of the body. Unlike a static mechanistic body, a holistic and intelligent body is dynamic and responsive and antibiotics may interfere with its functioning. Moreover, P6’s reference to “allowing the body to work” suggests a post-Pasteurian view in which the body can harness the effects of mutualistic microbes to mitigate the harmful effects of pathogenic microbes.

Discussion and conclusion

Translations of human microbiome science are often associated with significant novelty and high expectations of clinical impact; however, the clinicians interviewed in this study described a much more complex picture than this. They spoke about microbiome translations with both high and low expectations and situated new findings within existing biomedical discourses, theories, relations, and practices. Clinicians drew on scientific discourses of “evidence”, “truth,” and “facts” to differentiate microbiome findings from existing theories on hygiene and mutualistic microbes (i.e. hygiene hypothesis, or OF mechanism), their expert knowledge from patients’ lay knowledge of microbiome interventions, and to distinguish biomedicine from alternative health approaches. We suggest that this demonstrates a form of boundary work or boundary making by clinicians to re-establish a separation from, and authority over, both patients and alternative health practitioners. By drawing on the epistemological superiority of scientific evidence and fact over anecdotes and observation, clinicians are able to mark a boundary that sets their adoption of new views on microbes from their patients and other health paradigms. This boundary making supports a complex, multi-modal, and multi-directional view of translation by demonstrating that movement of scientific findings may also disrupt boundaries and demarcations between various social actors and groups. In addition, the expansion of microbes to be viewed as both mutualist and pathogen in relation to human health is consistent with the dual poles of “promise” and “peril” associated with bacteria in a post-Pasteurian paradigm (Paxson 2008; Paxson and Helmreich 2014). We examine this further in the remainder of the discussion and conclusion.

We suggest that microbiome translations and clinicians’ discourses demonstrate the emergence of a post-Pasteurian view in the clinic. In suggesting this, we are cautious of contributing to what Helmreich (2015) has termed “microbiomania” in much popular and scientific writing, and mindful of Sangodeyi’s (2014) history of the microbial body that predates the current excitement around the human microbiome and the figure of the Microbial Body. Thus, we situate the emergence of post-Pasteurianism in the clinic within the continuities, as well as disruptions, that may be associated with microbiome translations. In the remaining paragraphs, we want to consider several implications of a post-Pasteurian view in western biomedicine. Since the nineteenth century, the dominant model of disease in western biomedicine assumes that disease is a “real” entity that exists separate from the person. Disease is viewed as a “predator” attacking the human host, and clinical care is aimed at targeting the disease agent. This model is consistent with Pasteurian germ theory in which microbes are of clinical concern primarily as disease-causing pathogens (Juengst and Huss 2009; Latour 1988). Central to a Pasteurian paradigm in the clinic is the view that human-microbe relations are largely antagonistic. While gut microbes have long been understood to play an essential role in human digestion (Sangodeyi 2014), when bacteria are the targets of clinical action the aim has primarily been to eliminate them through the administration of antibiotics in order to treat and/or avoid infection. Suggesting that a post-Pasteurian view is emerging in the clinic is not to suggest that a Pasteurian one has been replaced. Both co-exist with concerns regarding bacterial infection remaining an important concern in clinical care alongside an emergent post-Pasteurian view. As clinicians interviewed made clear, control of bacterial infection remains a key area of clinical concern and is particularly challenging for specialists working with newborns and very young children.

A post-Pasteurian approach in the clinic, however, foregrounds the mutualistic role of bacteria in human health, and multiplies the ways in which clinicians may intervene. Treatment or intervention, then, is not limited to eradicating microbes but may involve promoting the presence and activity of certain microbes. Microbes may be the target of clinical intervention with the aim of encouraging their growth and shifting their relative abundance within their particular microbial community. This raises a second important feature of a post-Pasteurian paradigm; that is, the recognition of the importance of microbial communities and maintaining “balance” among the various bacterial strains in these communities. Not only is the presence or absence of individual microbes important, but so too is their relative balance within their particular ecological system and the interactions between microbial communities and their human host. A post-Pasteurian paradigm complicates the current primary clinical response to microbes of treating them primarily as pathogenic parasites and administering antibiotics. A third feature of a post-Pasteurian paradigm is recognition of the role of microbes in enhancing, or optimizing, life and health. Optimizing life and health is a key aim of biopolitical strategies in the contemporary global North. With microbes viewed as agents in optimizing human health, strategies aimed at preserving and/or encouraging the survival of microorganisms may be enacted at both the policy and individual levels.

Translations of human microbiome science and The Microbial Body 2.0 (Sangodeyi 2014) offer a new view of bodies and disease that seems promising for those wary of a reductionistic view of bodies and disease that tends to emphasize individual risk, responsibility, and surveillance rather than a broader ecological approach. If we take seriously the ecological view encouraged by the current iteration of the microbial body, interventions to address illness/imbalance in individuals must also be considered for various levels of the ecological system. And, as Ackerman et al. (2017) demonstrate, translational ethics and considerations must be made not only at the end stages, after the science has been “done”, but early and throughout the research process since decisions made at these earlier stages have a hand in determining what kinds of translations are even possible.

Acknowledgements

We would like to thank the Discourse, Science, Publics research group at the University of Guelph as well as the anonymous reviewers for helpful comments on previous versions of the paper. We also thank Mackenzie Seasons for help in transcribing the interviews with clinicians.

Disclosure statement

No potential conflict of interest was reported by the authors.

ORCID

Kieran O’Doherty http://orcid.org/0000-0002-9242-2061

Additional information

Funding

This work was supported by Canadian Institutes of Health Research.

Notes

1. http://www.human-microbiome.org/index.php?id=27, accessed April 13, 2017.

2. http://www.cihr-irsc.gc.ca/e/48470.html, accessed May 14, 2017.

3. http://www.phac-aspc.gc.ca/cphorsphc-respcacsp/2013/resistance-eng.php, accessed November 14, 2016.

4. https://www.cdc.gov/drugresistance/, accessed November 14, 2016.

5. http://www.who.int/mediacentre/factsheets/fs194/en/, accessed November 14, 2016.