Running Head: METACOGNITIONS AND MOTOR FLUCTUATIONS

Thinking about motor fluctuations: an examination of metacognitions in Parkinson’s

disease

Word count: XXXX

March 2015

Bruce A. Fernie, PsychDKing’s College London, Institute of Psychiatry

Department of Psychology, London, UKCASCAID, South London & Maudsley NHS Foundation Trust

London, UK

Marcantonio M Spada, PhDLondon South Bank University, London, UK

K Ray Chaudhuri, MDKing’s College and NPF Centre of Excellence, Kings College Hospital NHS

Foundation TrustLondon, UK

Lisa Klingelhoefer, MDKing’s College Hospital NHS Foundation Trust

London, UK

Richard G Brown, PhDKing’s College London, Institute of Psychiatry

Department of Psychology, London, UK

AcknowledgementsAuthors BAF and RGB receive salary support from the National Institute for Health Research (NIHR) Mental Health Biomedical Research Centre and Dementia Research Unit at South London and Maudsley NHS Foundation Trust and King’s College London. KRC is supported in part by NIHR CRN salary. The views expressed are those of the authors and not necessarily those of the NHS, the NIHR, or the Department of Health.

Author NotesCorrespondence should be addressed to: Bruce Alexis Fernie, Department of Psychology, Institute of Psychiatry, King’s College London, Henry Wellcome

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Running Head: METACOGNITIONS AND MOTOR FLUCTUATIONS

Building, De Crespigny Park, London, SE5 8AF, United Kingdom. Tel. +44 (0)7779 300 427, fax +44 (0)20 7848 5310, e-mail bruce.fernie@kcl.ac.uk

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Running Head: METACOGNITIONS AND MOTOR FLUCTUATIONS

AbstractObjective: Motor fluctuations (characterized by a sudden increase in symptom

intensity) are common side effects after treatment of Parkinson’s disease (PD) with

dopaminergic medication. A proportion of these people find motor fluctuations highly

distressing. This study aimed to identify metacognitions associated with cognitive and

attentional responses to these experiences. Methods: Ten individuals with PD who

experience motor fluctuations were interviewed for this study using an adapted

metacognitive profiling schedule. Participants were asked about their metacognitions,

and the cognitive processes and attentional strategies activated in response to a

distressing off-period. Results: The interviews identified metacognitions pertaining to

conceptual thinking about symptoms and symptom focus that may be relevant to levels

of distress experienced during an off-period. Conclusion: Metacognitive therapy offers

a framework for understanding how metacognitions may influence off-period distress.

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Running Head: METACOGNITIONS AND MOTOR FLUCTUATIONS

1. Introduction

Parkinson’s disease (PD) is the second most common neurodegenerative disorder after

Alzheimer’s disease. A recent systematic review and meta-analysis revealed a

population prevalence of approximately 250 per 100,000, but this increases to more

than one in a hundred in those over the age of 70 (Pringsheim, Jette, Frolkis, & Steeves,

2014). PD is defined by a constellation of motor symptoms including slowness in the

initiation and execution of movement, reduced movement amplitude, tremor and

stiffness, leading to progressive disability affecting mobility and fine motor control,

balance, swallowing and speech. PD is also associated with a wide range of non-motor

symptoms, although their pattern and severity can vary more widely. These can include

cognitive impairment, anxiety, depression, psychosis, pain, autonomic dysfunction,

sleep problems, and fatigue (Chaudhuri, Healy, & Schapira, 2006). Such symptoms

have been shown to have a greater impact on health related quality of life than the

motor symptoms (Hinnell, Hurt, Landau, Brown, & Samuel, 2012; Martinez-Martin,

2011).

In the first few years of the disease, effective management of the motor

symptoms is offered by the use of dopaminergic medication such as levodopa or

dopamine agonists. With progression of the disease, however, such drugs become less

effective, and complications can emerge with long-term use. The most commonly used

drug, levodopa, is associated with the emergence of fluctuations in symptoms over the

course of the day. These periods of symptom worsening (off-periods) can happen at the

end of a dose before the next tablet (‘wearing off’), or less predictably with the dose

stopping working unexpectedly, or may not work at all (Jankovic, 2005). Apart from a

worsening of the motor symptoms, many patients report the emergence or exacerbation

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Running Head: METACOGNITIONS AND MOTOR FLUCTUATIONS

of non-motor symptoms during these off-periods (Jankovic, 2005) including depression

and anxiety, as well as pain, fatigue, and other symptoms.

Off-periods can be a significant source of distress for patients. Some of this may

reflect from a physiological response to variations in brain dopamine during the off-

period, or a reaction to unpleasant symptoms such as pain, fatigue, or immobility.

Another potential psychological factor is the role of metacognitions. This psychological

construct refers to higher order ‘thinking about thinking’. Specifically, in the context of

mental health, it refers to explicit beliefs held by an individual about the value of the

specific cognitive (thinking) processes (such as worry and rumination) and attentional

strategies. Metacognitions can be positive (e.g. ‘worry helps me prepare’) or negative

(e.g. ‘my worry is uncontrollable’). Evidence suggests that both types of beliefs can

result in the activation and persistence of worry and ruminative thinking (Papageorgiou

& Wells, 2002; Wells, 1999) because the goals of these cognitive processes is often a

reduction in distress, which is seldom achieved. In PD, metacognitive style has

previously been shown to be associated with psychological distress (Allott, Wells,

Morrison, & Walker, 2005), while a recent study demonstrated that general

metacognitions concerning a patients’ beliefs about uncontrollability and danger were

found to be significantly related distress reported during off-periods (Brown & Fernie,

2014).

We report here a small proof-of-concept, mixed-methods study aimed to: (1)

determine whether patients express metacognitions specifically related to their

individual off-period experiences, (2) characterize those metacognitions, and (3)

examine whether they might be meaningfully related to psychological distress in

relation to current models. The existence of potentially maladaptive metacognitions

associated with off-periods and off-period symptoms, even in some patients, would

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support the exploration of novel tailored treatment approaches to help manage off-

period distress.

2. Method

2.1. Participants

Ten participants with PD (six males; mean age 59.2 years, SD 7.0 years, range 48 to 71

years) reporting motor fluctuations were recruited from movement disorders services at

King’s College Hospital NHS Foundation Trust and Lewisham University Hospital,

London. The mean number of years since PD diagnosis was 9.6 (SD 5.2; range 3 to 20).

All but one participant self-identified as White-British.

Eligibility criteria were: (1) a clinical confirmed diagnosis of idiopathic PD; (2)

current use of dopaminergic medication; (3) the presence of off-periods for at least 25%

of the day on average; (4) recent evidence of significant psychological distress (not

specifically related to off-periods); (5) understanding written and spoken English; (6)

able to provide informed consent. 13 patients who met inclusion criteria following case

note review were invited to participate. Those who agreed were seen in their own home

or at the research site (to their preference) for assessment after providing signed

consent.

2.2. Materials

2.2.1. Case note screening measures

Potential participants were first identified from a case note review by a member of the

clinical team. The presence of recent motor fluctuations was indicated by the

Movement Disorders Society Unified Parkinson’s Disease Rating Scale Part IV (MDS-

UPDRS; Goetz et al., 2007). Recent psychological distress was indicated by the

Hospital Anxiety and Depression Scale (HADS; Zigmond & Snaith, 1983) with a score

of seven or more on the depression or anxiety subscale.

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2.2.2. Depression and anxiety

For the included participants, the 9-item Patient Health Questionnaire (PHQ 9;

Kroenke, Spitzer, & Williams, 2001) provided a measure of depression severity over

the preceding two weeks. The scale taps into the Diagnostic and Statistical Manual IV-

R (DSM-IV-R; American Psychiatric Association & Association, 1994) criteria for

Major Depressive Disorder. The Parkinson’s Anxiety Scale (PAS) is a 12-item scale

measuring avoidance behaviour, and persistent and episodic anxiety over the past four

weeks, and shows good psychometric properties (Leentjens et al., 2014). PAS factors

can be totalled to provide a global anxiety score.

2.2.3. Worry, rumination, and metacognitions

A 5-item version of the Penn State Worry Question (bPSWQ; Topper, Emmelkamp,

Watkins, & Ehring, 2014) was used to assess participants’ level of worry, and a 5-item

version of the Ruminative Response Scale (bRRS; Topper et al., 2014) was used to

measure participants’ tendency to respond to negative events with rumination. Despite

being brief, both scales have good psychometric properties (Topper et al., 2014)

although they have not been used previously in PD. Finally, the 17-item

Metacognitions about Symptom Control Scale (MaSCS) was used to assess general

levels of positive and negative metacognitions pertaining to both worry and rumination

about symptoms and symptom focused attention (Fernie, Maher-Edwards, Murphy,

Nikcevic, & Spada, 2014).

2.2.4. Eliciting metacognitive about off-periods

The Metacognitive Profiling interview template (Wells, 2002) is a non-quantitative tool

devised as an aid to clinical assessment to elicit positive and negative metacognitions

and related components that an individual may hold. In this study, the interview was

adapted to focus on cognitive processes and attentional strategies activated during an

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off-period. Participants were asked to recall a particular recent off-period that they

found difficult or distressing. They were asked to describe both their chain of thoughts

and focus of attention (i.e. was it on their thoughts, feelings, or symptoms, on the

situation or something else?) during this off-period. They were then asked about the

advantages and disadvantages of these cognitive processes and attentional strategies, as

well as the goal they were attempting to achieve by utilising them and how they would

know that this had been achieved (i.e. the stop signal).

2.4. Data analysis

All interviews were conducted by the author BAF and transcribed before further

analysis. Author BAF (a clinician and researcher in the field of metacognitions and PD)

reviewed the transcribed material and identified a pool of probable metacognitions.

These were subsequently reviewed by authors RGB (an expert in PD) and MMS (an

expert in metacognitions) to identify the final set reported here (Table 2). We did not

undertake a formal qualitative analysis of this small dataset, but take the opportunity to

identify and describe individual variability and possible common themes.

Finally, scatterplots were used to explore and illustrate any potential relationship

between positive and negative metacognitions as measured by the MaSCS and

depression (PHQ-9) and anxiety (PAS).

3.0 Results

3. 1 Nature of metacognitions

All participants were able to recollect a recent difficult or distressing off-period

experience. Table 2 shows all elicited metacognitions classified as positive or negative,

and related to conceptual thinking about symptoms (CTS) or symptom focussed

attention (SF). Nine participants described positive CTS metacognitions and four SF

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metacognitions. The most common theme of the positive CTS metacognitions

concerned beliefs about controlling or coping better with symptoms including motor

fluctuations (#1,3,4,6,7,9,10) with one participant taking it as a signifier of strength of

character (#2). Positive SF metacognitions again related to beliefs about better control

over symptoms but less consistently than for CTS (#7,10).

Seven participants described negative CTS metacognitions and seven reported

them about SF. Negative metacognitions about CTS concerned a negative impact on

emotional and/or physical state (#2,4,7,8). One participant noted the inability to control

the thoughts (#5) and one a negative impact on concentration (#9). Negative SF

metacognitions pertained to an increased awareness of symptoms leading to an increase

in their severity (#2), a worsening of mood (#3,7,9), and a restriction of activities (#10).

One participant’s negative SF metacognition related to the risk of believing they were

experiencing an off-period when they were not (#7).

It is notable that some participants held both positive and negative

metacognitive beliefs, even on the same subject. For example, for CTS, participant #7

felt that thinking about symptoms allowed him to “identify … and do something about

them” but also a belief that “dwelling [on them] allows symptoms to develop and

seemingly get worse”. Similarly, participant #9 felt that thinking about symptoms

provided a “sort of mental picture of what you’re going and what might happen” but at

the same time making it “very difficult to concentrate”. For SF, participant #7 felt that

focussing on symptoms “…deals with the situation and it stops symptoms, or you get

the symptoms to stop sooner” but also believed that “I may think I am going into an off-

period… when I am not.” While participant #10 believed that “By focussing on your

symptoms, you’ll do your best to control them.” but also that “The more I focus [on

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symptoms], the more I feel I cannot do things”. Such apparently contradictory beliefs

may result in further distress as a consequence of cognitive dissonance.

All but two participants were unable to identify goals or stop signals (i.e. cues

that indicated that CTS or SF had been successful and therefore could stop) for CTS or

SF. The remaining two participants (#1, 9) had goals and stop signals that related to

shortening the duration of an off-period.

3.2 Relationship between metacognitions and distress

The planned sample size was not intended to enable a quantitative test of the

relationship between metacognitions and distress. Nevertheless, it is possible to discern

interpretable relationships between the quantitative scores on the MaSCS (which

measured trait metacognitions pertaining to thinking about PD symptoms and symptom

focussed attention) and measures of depression (PHQ-9) and anxiety (PAS). Figure 1

shows scatterplots of emotional distress and level of trait metacognitions for the

participants. These data indicate a possible positive relationship with higher levels of

depression tending to be associated with higher levels of both positive and negative

metacognitions, with a similar, but perhaps less clear relationship for anxiety.

4. Discussion

This small study employed a convenience sample of patients attending a movement

disorder service. It was intended to explore whether patients with PD express

conceptually meaningful and interpretable metacognitions about off-periods. All 10

participants were able to recall a recent off-period that they found difficult or

distressing in some way, and were able to describe at least one thought identified as

metacognitive. The same individual revealed both positive and negative

metacognitions, sometimes concurrently. Furthermore, the results suggested, as found

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elsewhere (e.g. Papageorgiou & Wells, 2002; Wells, 1999), that the tendency to hold

positive or negative metacognitions is associated with greater levels of depression and

anxiety.

A conceptual model for understanding the role of metacognition in depression

and anxiety is provided by the Cognitive Attention Syndrome (CAS) which forms the

central framework for a psychological approach called Metacognitive Therapy (MCT;

Wells, 2011). The CAS is characterised by metacognitions that initially activate (and

subsequently maintain) maladaptive metacognitive control strategies (i.e. cognitive

processes and attentional strategies such as worry, rumination, and symptom focus).

These are hypothesized to result in persistent or recurrent psychological distress.

According to MCT, the presence of positive metacognitions indicates that an

individual believes that metacognitive control strategies confer an advantage. For

example, if one believes thinking about symptoms helps their management, then it is

more likely that the experience of an off-period will lead to CTS (conceptual thinking

about symptoms). CTS in turn would lead to the activation of negative metacognitions

such as ‘it is impossible not to think about symptoms once I have started’, which

confers the idea that attempts to stop CTS would be futile, or ‘thinking about my

symptoms could make them worse’, which may result in increased distress.

As described, we observed examples of individuals holding both positive and

negative beliefs about the consequences of thinking about or focussing attention on

problems during the off-period. While this may appear paradoxical, such conflicting

metacognitions are not unusual (e.g. Fernie & Spada, 2008; Maher-Edwards, Fernie,

Murphy, Nikcevic, & Spada, 2012; Spada, Giustina, Rolandi, Fernie, & Caselli,

2014). According to MCT, an individual processes their experiences and the world

around them in one of two distinct modes: ‘object-mode’ and ‘metacognitive-mode’.

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In object-mode an individual sees their own thoughts as facts that accurately represent

reality. While in metacognitive-mode, an individual views their thoughts as

hypotheses that are merely transient mental events (Wells, 2011). In object-mode, the

presence of contradictory metacognitions is likely to result in distress as a

consequence of cognitive dissonance. Such a mode of processing may result in

effortful, and ultimately unsuccessful, strategies to control thinking.

However, in metacognitive mode the presence of contradictory metacognitions would

viewed as competing hypotheses and are unlikely to result in a strong sense of

cognitive dissonance.

If metacognitions characterise part of a patient’s way of thinking about the

motor fluctuations and associated symptoms, what are the implications for

management? In other conditions such as Chronic Fatigue Syndrome (CFS), reduction

in symptom focus has been shown to mediate treatment outcomes (Moss-Morris,

Sharon, Tobin, & Baldi, 2005). Metacognitions that serve to maintain symptom

focussing in PD may lead to an increase in awareness of off-period symptoms or the

threat of such symptoms as a patient starts to wear-off. This in turn may trigger

conceptual thinking about the symptoms (worry and rumination) and so worsen

psychological distress.

The results from this study, alongside those from Brown and Fernie (2014),

suggest that metacognitions may play an role in determining or maintaining the levels

of distress experienced by individuals with PD during an off-period. From a

therapeutic perspective, these findings suggest that further research that evaluates the

impact of therapeutic techniques and interventions such as those offered by MCT on

levels of off-period distress is warranted.

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This study is subject to limitations and, as a result, its findings must be

considered with caution. Results were obtained from a small sample of individuals

with PD. The interviews and measures used were all retrospective, meaning that

results may reflect rationalizations of cognitive, attentional, and emotional

experiences. Collection of real-time data on the relationship between worry,

rumination, distress and off-periods would offer the opportunity for more detailed

assessment and causal modelling. The use of a structured interview template, while

maximizing the opportunity to elicit examples of metacognitions, may also have

introduced bias, both in terms of participant responses and investigator evaluation.

Despite these limitations, we believe this study provides further evidence of a

potential role for metacognitions in chronic health conditions generally and PD

specifically.

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Table 1: Participant characteristics

Measure Mean (SD; range)

PHQ 9 12.7 (3.7; 7 to 18)

PAS 23.2 (9.2; 5 to 38)

bRRS 12.8 (2.9; 8 to 17)

bPSWQ 15.7 (5.0; 7 to 22)

MaSCS – Positive metacognitions 23 (5.8; 13 to 35)

MaSCS – Negative metacognitions 19.2 (4.5; 13 to 28)

Note. PHQ 9 = Patient Health Questionnaire 9; PAS = Parkinson’s Anxiety Scale;

bRRS = brief Ruminative Response Scale; bPSWQ = brief Penn State Worry

Questionnaire; MaSCS = Metacognitions about Symptom Control Scale; n=10.

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Figure 1: Scatterplots of metacognitive and emotional factors

Note. MaSCS = Metacognitions about Symptom Control Scale; PHQ 9 = Patient

Health Questionnaire 9; PAS = Parkinson’s Anxiety Scale; n=10.

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Table 2: Metacognitions about CTS and SF Related to Distressing Off-periods in PD

Conceptual Thinking about Symptoms (CTS) Symptom Focussing (SF)Participant Positive metacognitions Negative metacognitions Positive metacognitions Negative metacognitions1 “You manage them [symptoms]

much better if you think about them and you can remember how it’s likely to last…”

“[Thinking about symptoms]… helps you to concentrate… rather than be distracted by the things [symptoms].”

“[Thinking about symptoms] makes you feel more in control.”

None identified. None identified. None identified.

2 “A strong-willed person probably gets through it [by thinking about symptoms] in a better fashion than a weaker person.”

“[Thinking about symptoms] make it [symptoms and emotions] worse.”

None identified. “[Focussing on symptoms]… make [the symptoms] worse.”

3 “[By thinking about symptoms] I can figure out how to get over the problem of symptoms.”

None identified. None identified. “… it [focussing on symptoms] makes me feel low… and start worrying about things.”

4 “Sometimes I can cope with it better [off-period symptoms] if I’ve thought about it.”

“It [thinking about symptoms] could make me feel worse.”

“I might decide to do [a task] regardless.”

None identified.

5 None identified. “… it is impossible not to think about my symptoms [during an off-period].”

None identified. None identified.

6 “[Thinking about the potential implications of symptoms] makes me try and control the situation as much as I possibly can, risk management.”

“… thinking about the symptoms would make the whole thing more stressful.”

None identified. “it [focussing on symptoms] highlights the idea that Parkinson’s is an unwelcome guest.”

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Conceptual Thinking about Symptoms (CTS) Symptom Focussing (SF)Participant Positive metacognitions Negative metacognitions Positive metacognitions Negative metacognitions

“Thinking, analysing… to get over them so I can control them.”

“I learn to manage things… [by thinking about my symptoms]”

7 “If you identify what the symptoms are… [you can be]… doing something about them.”

“… thinking about your symptoms… [connects you]… to Parkinson’s.”

“…. sometimes dwelling [on symptoms] allows the symptoms to develop and seemingly become worse.”

“… it [focussing on symptoms] deals with the situation and it stops symptoms or you get the symptoms to stop sooner.”

“[By focussing on symptoms] I may think I am going into an off-period… when I am not.”

8 None identified. “I don’t think it [thinking about symptoms] helps with your frame of mind.”

None identified. “… it [focussing on symptoms] might affect my mood.”

9 “[When thinking about symptoms]… there are certain advantages in sort of having a mental picture of where you’re going and what might happen.”

“[When thinking about symptoms…] it’s very difficult to concentrate.”

None identified. “… to focus on my symptoms would be in an indication to become obsessed by them.”

10 “… it [thinking about symptoms] helps me cope with it [Parkinson’s disease].”

None identified. “By focussing on your symptoms, you’ll do your best to control them.”

“The more I focus [on symptoms], the more I feel I cannot do things.”

Note. CTS = Conceptual thinking about symptoms; SF = Symptom focus.

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