Public perception of the vegetative state/unresponsive wakefulness syndrome: a crowdsourced study

Introduction

The term vegetative state (VS) was coined in the 1970’ies to describe a condition of wakefulness without awareness following brain injury (Jennett & Plum, 1972). Patients in VS may open their eyes but exhibit only reflex behaviors during clinical examination and were therefore considered unaware of themselves and their surroundings. The word vegetative (referring to the preserved autonomous nervous system) is etymologically related to vegetable, which may evoke negative associations. Thus, in 2009, the European Task Force on Disorders of Consciousness introduced the term unresponsive wakefulness syndrome (UWS) (Laureys et al., 2010).¹ It was felt that this term lacked the pejorative connotations of vegetative state and enabled the medical community to refer to the level of consciousness “in a human way” (Von Wild et al., 2012).

Aside from the semantic peculiarities of VS/UWS, in the 2000s neuroscientists and physicians began to recognize a disturbing dilemma: Brain-injured patients who appear entirely unresponsive at the bedside may show signs of covert consciousness when examined by functional MRI (fMRI) or EEG (Schnakers et al., 2008; Bekinschtein et al., 2009; Monti et al., 2010; Bruno et al., 2011; Boly et al., 2011; Faugeras et al., 2011; Cruse et al., 2011; Casali et al., 2013; Formisano, D’Ippolito & Catani, 2013; Sitt et al., 2014; Stender et al., 2014; Di Perri et al., 2016; Edlow et al., 2017; Chennu et al., 2017; Bodien, Chatelle & Edlow, 2017; Curley et al., 2018; Engemann et al., 2018). About 15% of behaviorally unresponsive patients can participate in mental tasks by modifying their brain activity during EEG- or fMRI-based paradigms, suggesting that they are conscious and misdiagnosed (Kondziella et al., 2016). In 2015, this state of covert consciousness was termed cognitive motor dissociation (CMD) (Schiff, 2015).

Many experts prefer the term unresponsive wakefulness syndrome to avoid the negative connotations associated with vegetative state and to highlight the possibility for CMD (Gosseries et al., 2011; Machado et al., 2012; Von Wild et al., 2012; Wannez et al., 2017a; Vanhaudenhuyse et al., 2018), while others have been skeptical because the adjective unresponsive is open for ambiguous interpretations (Naccache, 2018; Giacino et al., 2018). However, the perception of VS/UWS by the public has never been examined systematically.

Here, we recruited a large global sample of lay people to evaluate public perception of the VS and UWS. Specifically, we tested the hypothesis that vegetative state and unresponsive wakefulness syndrome might have a different influence on lay people’s attitudes towards treatment withdrawal and understanding of the CMD concept. In addition, we searched Google Trends and PubMed between 2004–2018 to compare trends in the application of the two terms by lay people and academics, respectively.

Methods

Results

We recruited 1,297 participants from 32 countries (mean age 32.06 years ± SD 10.12; n = 884 for part I, n = 413 for part II), most of which were well-educated with a secular background and residing in Europe and North America. Table 2 and Fig. 1A provide epidemiological information. Raw data are provided in the online supplemental files.

More participants had heard about vegetative state (91.83%) than unresponsive wakefulness syndrome (18.56%; difference 73.27%, 95% CI 62.52 to 80.84, Chi-squared 205.11; p < 0.0001). Only few participants had not heard of either term (4.46%). A minority of participants (4.52%, from total n = 413) had personal experience of someone close to them being in VS/UWS.

Results are listed according to the pre-specified five research questions as outlined in Methods.

• Attitudes towards treatment withdrawal: vegetative state vs. unresponsive wakefulness syndrome Vegetative state-was not associated with greater likelihood of participants agreeing with treatment withdrawal (48.79%) as compared to unresponsive wakefulness syndrome (46.47%; total n = 880; relative risk 1.0520, 95% CI 0.9143 to 1.2104; p = 0.48). The average score of participants on the 7-point Likert scale (1 = “strongly agree with treatment withdrawal”, 7 = “strongly disagree”) was 2.87 ± 1.59 for vegetative state and 2.94 ± 1.63 for unresponsive wakefulness syndrome. Equivalence testing, using a small effect size (0.2), was significant, t(817.44) = 2.301, p = 0.0108, whereas the null hypothesis test was non-significant, t(817.44) =  − 0.639, p = 0.523. Based on the equivalence test and the null-hypothesis test combined, we can conclude that any difference in the effect size of vegetative state and unresponsive wakefulness syndrome on attitudes towards treatment withdrawal must be smaller than 0.2.

• Attitudes towards treatment withdrawal: oneself vs. someone else Participants did more often agree with treatment withdrawal in a hypothetical case involving themselves being in VS/UWS (32.27%) than in a case with someone else being in VS/UWS (19.20%; total n = 880; difference 18.07%, 95% CI 13.91 to 22.14, Chi-squared 70.863; p < 0.0001) (Fig. 1B).

• Attitudes towards treatment withdrawal: high vs. low degree of religiosity Compared to participants with the lowest degree of religiosity (51.92%), participants with the highest degree of religiosity (4.07%) were more likely to be undecided or against treatment withdrawal (20 of 36 religious participants vs. 113 of 459 secular participants; relative risk 1.5963, 95% CI [1.1257–2.2636]; p = 0.0087).

• Plausibility of the concept of cognitive motor dissociation Participants exposed to the term vegetative state believed that the average % of unresponsive patients with CMD was lower (median % 35, mean % 38.07 ± SD 25.15) than participants exposed to the term unresponsive wakefulness syndrome (median % 40, mean % 42.29 ± SD 26.63; total n = 880), a small but significant difference (Cohen’s d 0.164; p = 0.016) (Fig. 1C).

• Preferences for unresponsive wakefulness syndrome versus vegetative state Most participants preferred unresponsive wakefulness syndrome (60.05%), whereas a sizeable minority of respondents favored vegetative state (24.21%; difference 35.84%, 95% CI 29.36 to 41.87, Chi-squared 108.66; p < 0.0001). Sixty-five respondents (15.74%, total n = 413) were undecided (Fig. 1D).

Selected comments from participants on their preference for one term over the other can be found in Tables 3 and 4.

A search on PubMed showed a clear trend for the increasing use of unresponsive wakefulness syndrome in medical papers as compared to vegetative state. In 2012, for instance, there were 13 papers on unresponsive wakefulness syndrome compared to 103 papers on vegetative state, whereas for January–November 2018, the ratio was 62/101. In contrast, Google Trends revealed no such tendencies, but internet searches peaked around highly publicized cases in the media (Fig. 2).

Discussion

Here, we have shown that the terms vegetative state and unresponsive wakefulness syndrome have measurable effects on the way people perceive VS/UWS. Although attitudes towards treatment withdrawal appeared unchanged, people exposed to the term vegetative state were less likely to believe in CMD than people inquired about the unresponsive wakefulness syndrome. The effect was small (Cohen’s d 0.164), but this effect size is comparable to similar framing effects in psychological research (Lakens, 2013; Open Science Collaboration, 2015; Koon, Hawkins & Mayhew, 2016).

Does this effect matter for clinical routine? We believe, it does. Up to 40% of unresponsive patients are incorrectly classified as being in VS/UWS because standardized rating scales such as the Coma Recovery Scale-Revised are not widely used (Schnakers et al., 2009; Di et al., 2014; Thonnard et al., 2014; Chatelle et al., 2016; Wannez et al., 2017a; Wannez et al., 2017b; Wannez et al., 2017c; Vanhaudenhuyse et al., 2018). Moreover, an estimated 15% of patients with a clinical diagnosis of VS/UWS can follow commands by performing mental imagery tasks when examined with fMRI and/or EEG paradigms, strongly suggesting that they are indeed conscious and in a state of CMD (Schiff, 2015; Kondziella et al., 2016). This has major ethical and practical implications, including prognosis, treatment, resource allocation and end-of-life decisions (Laureys et al., 2005; Turgeon et al., 2011; Demertzi et al., 2014; Di Perri et al., 2016; Kondziella, 2017; Kondziella, 2018; Harvey et al., 2018; Faugeras et al., 2018). Careful communication about patients’ levels of consciousness and the potential for CMD seems crucial in this regard (Laureys et al., 2010; Gosseries et al., 2011; Von Wild et al., 2012).

The present data, including the comments in Table 3, suggest that the term wakefulness in UWS seems to increase the odds of associating the VS/UWS entity with awareness. Indeed, wakefulness and awareness are frequently misinterpreted (Naccache, 2018), even among caregivers (Hermann et al., 2018). It is interesting in this regard that study participants overestimated the prevalence of covert consciousness in VS/UWS by a large margin (40%). As stated earlier, data from the scientific literature suggest that the correct rate is rather around 15% (Kondziella et al., 2016). Of note, our study in which lay people were explicitly primed about CMD yielded very different results compared to a previous study on the public perception of VS/UWS in which the participants were not introduced to the concept of CMD (Gray, Knickman & Wegner, 2011). Gray and co-workers recruited 201 lay people (51% females, mean age 23 years) from train stations and public parks in Massachusetts and New York State, USA, and asked them to read a clinical vignette involving a road traffic victim whose “entire brain was destroyed, except for the one part that keeps him breathing. So, while his body is still technically alive, he will never wake up again”. Participants considered this fictive protagonist to be “more dead than dead” and with “less mental capacity than [a] dead [person]”, which the authors suggested was due to “afterlife beliefs, and the tendency to focus on the bodies of [persistent] VS patients at the expense of their minds” (Gray, Knickman & Wegner, 2011). Again, physicians and other caregivers should carefully discuss these discrepancies with patient relatives to achieve a realistic view of VS/UWS, while at the same time acknowledging that figures about the prevalence of CMD are likely to change in the future with more accurate data.

The many emotional comments from participants about vegetative state and unresponsive wakefulness syndrome also suggest that terminology matters. Both terms evoke strong opinions. Among the adjectives associated with the vegetative state were “dehumanizing”, “offensive”, “ignorant” and “pejorative”, whereas many people related unresponsive wakefulness syndrome to kindness, dignity and professionalism. Of note, however, one quarter of participants favored vegetative state because they perceived this term as less euphemistic and easier to understand. Once more, empathic communication by the attending physicians and caregivers seems essential to navigate these controversies.

Apart from the semantic effects, our results suggest that the public attitude towards treatment withdrawal in brain-injured patients is influenced by religiosity, i.e., people with a high degree of religiosity are less likely to endorse treatment withdrawal than secular individuals (Gipson, Kahane & Savulescu, 2014). This corroborates previous work and is probably because values such as the sanctity of life are more important in religious groups as compared to secular groups that tend to give greater weight to patient autonomy (Gipson, Kahane & Savulescu, 2014). Concerns related to autonomy may also explain why most participants were even more willing to endorse withdrawal of treatment in a hypothetical case involving themselves than someone else, suggesting that the former decision is easier than the latter.

An online study such as this one has limitations that should be acknowledged (Woods et al., 2015; Peer et al., 2017). First, complex clinical and ethical notions are impossible to fully implement in a survey form. Second, it should be kept in mind that for obvious reasons only a small minority of participants (<5%) stated they personally knew someone being in VS/UWS. Although their responses did not differ from that of participants in general (see online supplemental files), it is obvious that people might change attitudes when being confronted with a real case of VS/UWS. Third, our sample included a high degree of secular participants; sampling from countries with strong religious cultures would likely have resulted in more people disagreeing with treatment withdrawal. Finally, for the sake of simplicity we inquired participants about their attitudes towards treatment withdrawal which is a somewhat more ambiguous term than withdrawal of life-sustaining therapies. It might be that including practical details such as stopping artificial feeding and hydration would have yielded lower approval rates. On the positive side, this is the first systematic and (and least in part I) randomized controlled study on public perception of VS/UWS and the semantic effects of vegetative state and unresponsive wakefulness syndrome. Further, we recruited a much larger sample size than what typically can be achieved with lab-based behavioral testing or mail-based questionnaires. Lastly, although we were unable to recruit participants from Africa (and although Asian participants were underrepresented), this was a truly intercontinental sample with respondents from more than 30 countries on 5 continents, which strengthens the validity and generalizability of our results.

We also retrieved publicly available data from PubMed and Google Trends to trace the application of the terms vegetative state and unresponsive wakefulness syndrome by lay people and academics over the last 15 years. We found that unresponsive wakefulness syndrome is increasingly being used by academics but not by lay people, suggesting that the term is still not widely known in the public. (This is in line with our survey in which 4.5 times as many people had heard about vegetative state.) Instead, Google searches peaked around highly publicized patient cases in the media, most notably Terri Schiavo and Otto Warmbier. Diagnosed with a persistent VS following cardiac arrest, Terri Schiavo was the subject of a right-to-die legal case between her husband (pro treatment withdrawal) and her parents (contra), even prompting US President George W. Bush to take sides (contra). She died in March 2005, when her feeding tube was finally removed. This explains the peak in internet searches related to vegetative state as revealed in Fig. 2. Similarly, the case of Otto Warmbier is associated with a sharp increase (albeit much less intense) in search activities related to unresponsive wakefulness syndrome. Otto Warmbier was a US citizen arrested in North Korea, where he suffered a brain injury (probably due to cardiac arrest). When he returned to the US 18 months later, his physicians diagnosed ”a state of unresponsive wakefulness”, following which his parents requested the feeding tube to be removed. Warmbier died shortly after in June 2017. Thus, highly publicized media cases trigger public interest and may offer an opportunity to raise awareness for patients with VS/UWS and other disorders of consciousness.

Conclusion

VS/UWS is a condition associated with strongly polarized opinions in the public. The term vegetative state has particularly negative connotations and seems counterintuitive to the concept of CMD, which is of increasing relevance given our improved abilities to identify covert consciousness in unresponsive patients using fMRI- and EEG-based paradigms. However, simply replacing vegetative state with unresponsive wakefulness syndrome may not be entirely appropriate given that one of the four still prefer the first term over the latter. Instead, we suggest that physicians and caregivers take advantage of the controversy around the terminology and use it to explain to patient relatives the concept of CMD and its inherent diagnostic uncertainties and ethical implications. This approach might reconcile any aversions the next-of-kin might have towards one or the other term and increase their understanding of the patient’s condition. Ultimately, such an approach might also increase public awareness of patients with other disorders of consciousness than VS/UWS.

Supplemental Information