Abstract
This paper considers how the full range of human experience may catalyze a placebo response. The placebo effect has been characterized as something to control in clinical research, something to cultivate in clinical practice and something present in all healing encounters. We examine domains in which the term ‘placebo’ is used in discourse: clinical research, clinical practice, media representations of treatment efficacy and lay interpretations of placebo—an underresearched topic. We briefly review major theoretical frameworks proposed to explain the placebo effect: classical conditioning, expectancy, the therapeutic relationship and sociocultural ‘meaning.’ As a corrective to what we see as an overemphasis on conscious cognitive approaches to understanding placebo, we reorient the discussion to argue that direct embodied experience may take precedence over meaning-making in the healing encounter. As an example, we examine the neurobiology of rehearsing or visualizing wellness as a mode of directly (performatively) producing an outcome often dismissed as a ‘placebo response.’ Given body/mind/emotional resonance, we suggest that the placebo response is an evolutionarily adaptive trait and part of healing mechanisms operating across many levels—from genetic and cellular to social and cultural.
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Notes
The flip side of the ‘placebo effect’ has been referred to as the ‘nocebo effect.’ This term has been used in a number of ways to indicate the negative effects associated with ostensibly ‘inert’ treatments in practice and research (Barsky et al. 2002; Benedetti et al. 2007; Bootzin and Bailey 2005; Caspi 2002; Hahn 1999; Helman 2001). Bootzin and Bailey (2005) observe that “the fact that placebos and nocebos elicit a pattern of reactions in symptom relief and side effects that is similar to that produced by the medication or intervention to which they are being compared means that mechanisms of action for either specific or nonspecific effects must be able to account for the complex patterning of results” (p. 873). Clearly, understanding nocebo effects may be at least as complicated as understanding placebo effects. While it is beyond the scope of this paper to examine nocebo effects, we view this as an important future direction for research.
Although there is a well-developed literature on the cognitive unconscious—including implicit perception, learning and thought (Kihlstrom 1987, 1996)—the vast majority of the literature on the placebo effect (with the exception of work on a conditioned placebo response) privileges a state of conscious awareness on the part of the patient in its explanations of the placebo effect.
Bootzin and Caspi (2002) offer another useful way of framing this issue. Specifically, their definition of ‘placebo response’—a patient’s positive (placebo) or negative (nocebo) response to treatment (broadly construed) stemming from the ‘incidental’ or ‘preliminary’ therapeutic elements—vis-à-vis those treatment responses specifically attributable to ‘defining or characteristic elements’ intended to be “causally responsible for the outcome” (see also Caspi 2003).
This schema suggests the need to deconstruct the notion of healing intent. Most simply put, one practitioner’s placebo may be another’s ‘active’ treatment. Within biomedicine, take the example of diagnosis itself. While the healing intent underlying physicians’ diagnosis has not been systematically studied, Brody and Waters (1980) argue that the diagnostic process itself is a powerful therapeutic tool—especially for behavioral problems for which diagnosis provides an explanatory system that gives meaning to otherwise unexplainable suffering and symptoms. Further research is needed on what elements practitioners (biomedical, as well as complementary and alternative) consider ‘active’ vs. incidental. While randomized controlled trials (RCTs) narrowly define the ‘active’ treatment according to the biomedical paradigm of disease (and treatment) specificity—thus relegating everything else to the category of ‘nonspecific’ or ‘incidental’—it is not clear whether practitioners themselves would agree with this distinction.
While the notion of a placebo-controlled clinical trial was created to help health-care providers decide between pharmaceutical treatments, it has become an increasingly thorny and politicized issue. The U.S. Food and Drug Administration (FDA), which regulates and approves pharmaceuticals for the lucrative U.S. drug market, privileges evidence from placebo-controlled clinical trials. There is increasing pressure from the World Medical Association’s Declaration of Helsinki for pharmaceutical companies to use active controls (often the current standard of care) whenever a condition has a ‘proven therapy’ (http://www.wma.net/e/policy/b3.htm). To cut costs, more rapidly recruit naïve subjects and avoid having to offer subjects expensive, gold-standard therapies during or following trials, pharmaceutical companies seek out patient populations (frequently Third World, underprivileged and underserved patient populations) that are willing to submit to placebo-controlled clinical trials because they do not have access to standard-of-care treatments. Pharmaceutical companies have thus found it more cost-effective to run clinical trials overseas (Shah 2006). Critics argue that placebo-controlled trials are examples of the pharmaceutical companies’ “stacking the deck” in their favor: “Why risk trying to be better than something…when all you need to show is that you are better than nothing?” (p. 33).
With respect to complementary and alternative medicine (CAM) therapies and procedures, the National Institutes of Health (NIH) frequently demands that clinical trials of all kinds of therapies be placebo-controlled. Conflicts between researchers and funding/regulating agencies arise as to what, precisely, is the active element of a CAM therapy and how to design a study with an appropriate placebo arm. Bootzin (personal communication) argues that the concept of placebo—as it is used in clinical trials—is limited to testing a specific mechanism of action and tells us little about the overall therapeutic effectiveness of a given intervention. In fact, some critics argue that the FDA and NIH have become more concerned with mechanism than with outcome (Kaptchuk 1998).
Ader (2000) similarly observes that the notion that “real” drug effects can be parsed out in clinical trials is a gross oversimplification. “Drug effects can only be evaluated in vivo… There are no ‘real’ drug effects outside of those observed in a behaving organism.” He argues that “we have no a priori right to assume that placebo effects and drug effects are additive. It may be more reasonable to hypothesize that they interact in complex ways that have not been studied in any systematic manner.”
A recent meta-analysis of all clinical trials on four ‘new-generation’ antidepressants, which used data obtained from the FDA through the Freedom of Information Act, found that these drugs provide only slight, if any, statistical benefit (and did not reach clinical significance) over placebo in mild to moderate depression (Kirsch et al. 2008; Mayor 2008). Furthermore, while these antidepressants appear to provide somewhat more benefit to those with the most severe depression, this is due more to a decrease in the placebo response among the most severely depressed than to an increase in the drug response.
According to some researchers, CAMs, which operate within novel paradigms that are responsive to patient individuality on the level of diagnosis and treatment, may be particularly well positioned for activating the placebo effect in clinical practice (Kaptchuk 2002). This has created a conundrum in which the efficacy of CAM therapies may be rendered ‘just’ placebo effects (Bausell 2007; Beyerstein 2001; Shang et al. 2005). Bootzin and Caspi (2002) argue that this ‘placebo problem’ in CAM is not insignificant:
If indeed the incidental elements of CAM are those that account for its effectiveness, then health care providers need not necessarily be skilled in any of the CAM techniques but rather should be trained to activate the placebo effect/healing system pathways. However, if the therapeutic relationship enhances rather than substitutes for the treatment…then all practitioners need to be trained to activate healing pathways. (p. 125)
To be fair, the ENHANCE study was not a placebo-controlled clinical trial, but a study of the combination drug (Zetia and Zocor) versus Zocor alone (Kastelein John et al. 2008). Nevertheless, the idea persists that Zetia was just “an expensive placebo” circulated in the media, especially on Internet blogs (http://www.forbes.com/2008/04/04/schering-merck-vytorin-biz-healthcare-cx_mh_0404floor.html?boxes=custom). Another example is the dramatic drop in sales of Quaker Oats following the media attention to a flawed study indicating that oat bran had no cholesterol-lowering effect (Bausell 1990; Lehman 1990; Swain et al. 1990).
This broadcast came out while we were working on the early drafts of this paper. We authors were pleased to find this broadcast a remarkably robust media treatment of this topic, which touched on many of the issues we cover here. It can be found online at: http://www.wnyc.org/shows/radiolab/episodes/2007/05/18.
Unfortunately, says Benedetti (2008), our internal pharmacy “sometimes does not work”—that is, while the placebo effect (in this case, the stimulation of our endogenous production of a therapeutic substance) is “incredibly powerful, it’s rarely consistent. It’s hard to predict who’s going to get a placebo effect under what circumstances.”
Inadvertently conditioned ‘nocebo’ effects are also well documented. A well-known example is that of conditioned nausea among chemotherapy patients, in which up to one-third of patients “become profoundly nauseated when encountering a previously neutral stimulus that has now become associated with the chemotherapy, such as meeting the infusion nurse outside the hospital or entering a room painted the same color as the infusion room” (Barsky et al. 2002, p. 624).
The concept of “placebo” is a biomedical construction. When we use nonbiomedical or cross-cultural examples in this paper, readers may wonder whether we are implying that these are examples of ‘sham’ healing. Of course, we are not. We use these examples to illustrate oft-overlooked aspects of healing, a number of which have been disparagingly referred to as ‘placebo effects’ in biomedical literature.
Elsewhere, Bootzin and Caspi (2002) have identified other “preliminary elements of treatment”—such as the decision to seek treatment in the first place, as well as the diagnostic process (including testing and diagnosis)—that may also set in motion certain expectations on the part of the patient and that may, in turn, trigger a shift in patient practice and/or the body’s homeostatic healing response. These elements may be located prior to the clinician-patient relationship on this same ‘cognitive’ trajectory.
Moerman (2002a, p. 121) argues that each time a patient takes a pill, he or she “recalls” the entire medical experience. We must stress that the connection goes beyond the patient’s cognitive connection with a past medical experience. In fact, the pill is a metonym (part representing the whole) for all of biomedical technology. Each time the patient takes the pill, he or she indexes the technological and symbolic power of biomedicine.
The feelings associated with apple pie may able be associated with the mammalian attraction to safe and sweet foods.
Examples include culturally specific manifestations such as ‘sore neck syndrome’ among Khmer refugees (Hinton et al. 2001), as well as biomedicalized manifestations such as PTSD and anxiety attacks.
We thank the reviewers for bringing our attention to Frenkel’s (2008) recently published phenomenological account of the placebo effect. Although we disagree with Frenkel’s wholesale disregard of expectancy theory and his contention that placebo responses are better referred to as “meaning responses,” we appreciate his application of Merleau-Ponty’s (1962) notion of ‘motor intentionality’ to this topic. Bringing in Dreyfus’s (1999) work on ‘absorbed coping’ and his own concept of ‘affordances of healing,’ Frenkel (2008) constructs a compelling argument for the “sentient body, capable of responding to the world without having to invoke any reflexive activity” (p. 70).
Like ‘classical conditioning’ models, both Frankel (2008) and Ader’s (1997, 2000) frameworks suggest that the body ‘learns’ from past experience. However, an embodiment paradigm differs from conditioning in that it operates on multiple senses engaged in the world rather than relying on the direct pairing (and later withdrawal) of an unconditioned stimulus with a conditioned stimulus to stimulate the desired therapeutic effect.
Strictly speaking, we are operating outside the domain of the placebo effect, as the perlocutionary force of performance—which, by definition does something—cannot be considered ‘inert.’
In contexts of collective intervention, such as surgery and ritual, collective efficacy, that is, “a group's shared belief in its conjoint capabilities to organize and execute the courses of action required to produce given levels of attainments,” may also catalyze a positive feedback loop to maximize both the performance of team members and the patient’s placebo response, thus enhancing the overall therapeutic effect (Bandura 1997, p. 477).
When an individual observes an action of another, the mirror neuron system (discovered in macaque monkeys and indirectly proven to exist in humans) activates as if the individual were performing the action him- or herself. The mirror neuron system can also be triggered—although to a lesser degree—by audio stimulation (that is, hearing a sound that represents a particular action such as the ripping of a sheet of paper) or by observing a ‘goal’ of which the action is implicit (for example, seeing a basketball go through a hoop). In a study of the translation of verbal stimulus into neural networks, for example, Pulvermuller (2001) found topographic differences in the brain activity between subjects who listened to action verbs related to leg-related activities (such as “walking,” which stimulated cortical leg areas of the brain) and subjects who listened to face-related action verbs (such as “talking,” which stimulated cortical areas related to the motor representation of the face and mouth).
The mirror neuron system appears to come into play in interpersonal emotions such as empathy, as well. For example, when an individual observes another person in pain or disgust, mirror neurons track that emotional experience in the observer’s brain. Rizzolatti et al. (2006) suggest that this process bypasses consciousness and provides a “direct mapping of sensory information onto motor structures that would produce the experience of that emotion in the observer.” What these studies indicate is that audio and visual stimuli can influence the body’s neural networks, affecting physical performance as well as emotional experience.
Mirror neurons (or some structure similar to them) may have implications for anthropology that have yet to be explored. For instance, internalization of cultural knowledge may be the work of mirror neurons constructing neurological pathways based on the observation, sensation, emotion and practice of cultural schemas. It may be that habitus and the internalization of culture are the result of mirror neurons building up neural pathways from childhood. Furthermore, mirror neurons may help us better understand biocultural feedback loops, including the way that the external world shapes our internal world (by building up neural pathways based on observation, sensory input, emotion and practice) and, conversely, the way our internal world (given structure and coherence by a lifetime of neural pathways) affects our external world (manifesting these pathways externally through action).
Although there is strong evidence that expectancy-induced placebo analgesia is the result of endogenous opioid production, Benedetti et al. (2005) posit that positive expectations may also affect other body systems that can help individuals better tolerate pain by decreasing anxiety, increasing positive emotions and activating reward systems.
Lakoff (2007) cites studies indicating that depression trials result in placebo response rates of 15 to 70 percent, with verum (or study drug) response rates of 30 to 70 percent, although Benedetti et al. (2005) stress that “significant short-term placebo response rates are in contrast to continuation studies that demonstrate a significant advantage of maintenance medication over continued placebo treatment in preventing relapse and recurrence” (p. 10396). Given the complexity of the phenomenon labeled ‘depression’ and the many confounds of clinical studies of depression therapies, including that research subjects are often veterans of depression, depression treatments and drug trials, Benedetti and colleagues argue that there is a “complex interaction between mechanisms mediating expectation and conditioning effects for a given antidepressant and the heterogeneity of the depressed patient population under study” (p. 10396).
The best-known mechanisms are those that involve the antioxidant nutrients (vitamins C and E, glutathione) and enzymes such as the superoxide dismutases, which require copper, manganese or selenium as cofactor (Maggini et al. 2007). These are just a few of the many mechanisms that essentially “heal” cells damaged by ROS.
A pluralistic health-care environment provides individuals (and those caring for them) with therapeutic options (with regard to diagnoses that ‘make sense,’ reduce stigma or accomplish social goals, as well as with treatment options), a sense of agency in the therapeutic process and opportunities for holding out hope (Frank 1973; Good et al. 1990; Nichter and Quintero 1996). Through the proliferation of pluralistic medicine, opportunities for catalyzing a placebo response by triggers to the mind, body and senses are multiplied. Further, in the current Western context, patients are choosing to use multiple health-care systems interactively.
Although placebos and placebo arms are tools at the foundation of clinical research, a number of prominent scholars of this topic have noted that the placebo effect has been treated as a “nuisance factor”—that is, something to be controlled, minimized or, at the very least, tolerated—in clinical research (Ader 2000; Benedetti 2008; Enck et al. 2008; Kaptchuk 2002; Walach and Jonas 2004).
Whole-systems research (WSR) aims to investigate the efficacy of complex health-care systems (such as homeopathy, naturopathy or traditional Chinese medicine and, ultimately, biomedicine) in a way that is consistent with their philosophical underpinnings and real-world practice (including diagnosis, therapeutic intervention and outcome assessment). WSR looks beyond the specific efficacy of an intervention to consider the contribution of indirect (‘placebo’) effects and larger ‘whole-person’ shifts on overall well-being. A key issue central to carrying out WSR is the need for research designs that are tailored to best understanding the intact system (Ritenbaugh et al. 2003; Verhoef et al. 2005).
We acknowledge that the term ‘placebo’ has specific utility in pharmaceutical trials, in order to establish the safety and specific efficacy of pharmaceutical therapies. There, the term plays a functional design role, helping to account for other sources of variance in outcome, including the natural course of the disease and random variation. While we concede that the term placebo continue to be used within this narrow focus, we reiterate the call for further research and critique into the problematic nature of placebo-controlled clinical trials (see Shah 2006). One informant in India told M.N., when he asked whether she was concerned that the medication she received in a clinical trial would not work (was a placebo), “Of course it works! It must work! No one would spend this kind of money [to outfit and run the clinic housing the study] if it didn’t work!”
For example, Fabrega (1997b) argues that the earliest forms of sickness (that is, “the behavioral expressions of disease and injury” [p. ix]), emerging in family-level foragers, were short-term and generally acute; healing was fairly unelaborated, as sick persons were self-treated or treated by family members, with the goal being a quick return to productivity or death. In contrast to the contemporary industry of sickness and healing, Fabrega (1997a) stresses that evolutionarily early healing “did not prolong dependence or sickness, nor could it be said to have caused conditions of sickness and dependence” (p. 43).
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Acknowledgments
The writing of this paper was partially supported by NIH/NCCAM Grant T32AT001287-06. J.J.T. is a predoctoral fellow; M.N. and C.R. are faculty. Some of the research cited in this paper was supported by NSF Grant DDIG 0718313, received by M.N. and J.J.T.
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Thompson, J.J., Ritenbaugh, C. & Nichter, M. Reconsidering the Placebo Response from a Broad Anthropological Perspective. Cult Med Psychiatry 33, 112–152 (2009). https://doi.org/10.1007/s11013-008-9122-2
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DOI: https://doi.org/10.1007/s11013-008-9122-2