Prevalence and severity of freezing of gait in a Danish cohort of people with Parkinson’s disease

Parkinson’s disease (PD) is a widespread neurodegenerative disorder with a point prevalence in Europe ranging from 0.37-0.781% at age 60 years to 1.9-4.5% at age 80 years [1]. In Denmark, the Danish Parkinson’s Association estimates the prevalence to fall in the 0.7-0.8% range above age 60 years. Many patients develop symptoms of gait impairment and postural instability. Among these, freezing of gait (FoG), a transient feeling of the patient’s feet being nailed to the floor, resulting in inability to move forward, is particularly distressful. Typically, FoG occurs when negotiating crowded areas or during multi-tasking. FoG decreases patients’ overall mobility and increases the risk of falls, negatively impacting quality of life and ability to function in daily living. In general, FoG represents a major milestone in the symptomatic clinical progression of the disease [2].

Widely implemented clinical rating scales such as the Movement Disorder Society's Unified Parkinson’s Disease Rating Scale [3] have elements assessing FoG in both the clinician-rated motor component and the patient’s Activity of Daily Living Questionnaire. However, for a more extensive assessment of the frequency, duration and severity of FoG, other patient questionnaires such as the Freezing of Gait Questionnaire (FOGQ [4]) and the updated New Freezing of Gait Questionnaire (NFOGQ) [5] are used.

Until now, neither of these questionnaires has been translated and validated for Danish patients, despite their usefulness in subjective experiences of FoG.

The aim of this study was two-fold: Firstly, to enable Danish clinicians and researchers to gain accurate and detailed knowledge of FoG in Danish PD patients. Secondly, to assess the prevalence and severity of FoG in a Danish cohort of PD patients. The study was conducted as a two-step process: 1) We translated and adapted the NFOGQ for use among Danish patients; and 2) we distributed the translated the NFOGQ as an online survey aimed specifically at Danish PD patients.

METHODS

Translation and cultural adaptation of the NFOGQ into Danish

The NFOGQ scale comprises nine questions. Patients are asked to evaluate the presence, duration and complexity of FoG over the past month. Items are rated either 0-1 or 1-4, higher scores implying more severe FoG and more impact on daily living.

The NFOGQ was translated according to the guidelines of the World Health Organization (WHO) and the International Society of Pharmacoeconomics and Outcomes Research task force for translation and cultural adaptation [6].

Forward translations and harmonisation

The team consisted of four people (MHT, RNV, ASMA and VSH). Initially, two native Danish speakers (MHT and VSH), one fluent in English, the other bilingual, independently translated the NFOGQ from English into Danish (forward translation). Both are medical doctors and are engaged in PD research. Readability was ensured in Danish without straying from the English phrasing. Forward translations were harmonised by a third native Danish speaker, fluent in English (RNV). Harmonisation occurred independently of the English original. The harmonised forward translation was translated back into English (back translation) by a fourth person (ASMA). The back-translated English version was compared to the original by MHT and VSH. Changes were made to the Danish version to ensure equivalence between the Danish and English versions.

The final step consisted of piloting the questionnaire on two patients with PD in person.

Self-reported survey of freezing of gait in Danish patients with Parkinson’s disease

Patients were recruited directly through the Department of Neurology at Aarhus University Hospital, Denmark, or through advertisement through the Danish Parkinson Association. Respondents were given written information about the study, names of and information about the primary investigators and information regarding storage of responses and management of data. Written information specified that participation was voluntary and that consent could be withdrawn at any time by contacting an investigator. Advertising emphasised that anyone with a diagnosis of PD could reply.

The finalised translation of the questionnaire was entered as an online survey using RedCap (Research Electronic Data Capture) web-based software platform hosted by Aarhus University, Denmark. 

The survey was structured into three sections. The first section contained information on the study design and rationale. The second section contained the final Danish version of the NFOGQ. A link to a video of a PD patient experiencing an episode of FoG was embedded in this section. Participants were asked to complete the questionnaire twice: at study entry and after two weeks to evaluate the test-retest reliability of the survey. The final section of the online survey was designed to assess the validity of the translation (Validation Questionnaire). For each of the questions contained in the NFOGQ, participants had to indicate 1) whether they understood the question 2) whether the available responses were appropriate and 3) they were invited to give a narrative description of the objective of the question.

The survey commenced on 1 August 2022 and terminated on 1 January 2023.

Trial registration: not relevant.

RESULTS

Issues encountered during the translation process

Initial forward translations were not entirely in agreement with each other. There was disagreement in the translation of “freezing of gait” as one translator opted to transfer the word “freezing” directly into the translation, whereas the other opted for the literal Danish translation. This discrepancy was resolved during harmonisation into a translation of “freezing of gait”: “fastfrysning af gang”. Questions 1 and 2 did not differ between the two forward translators. Question 3 differed in translation, as the term “turning” does not have a correlate in Danish in the context of gait. This was solved in one of the translations by translating “turning” into two words and using them both, joined by a “/”. The two chosen translations specifically indicate “when changing direction” (“Ved retningsskift”) and “when you are trying to turn” (“når du prøver at dreje”). The next difference between the forward translations was observed in Question 5, as “gait initiation” does not have a correlate in Danish. In the harmonisation, a workable translation (“når du skal tage det første skridt”) was chosen. For Question 9, the translations differed according to the word “score”. This was harmonised into the Danish word for the verb “score” (“vurdér”).

Regarding back-translation, the team agreed that it was comparable to the original English in substance.

The two patients who reviewed the harmonised Danish translation found that the questionnaire was easy to answer and had no concerns or suggestions to improve it. No further changes were made to the harmonised Danish version.

Results of self-reported survey

Overall, 101 responses to the survey were received in the course of the study period. Among the 101 respondents, 92 indicated a diagnosis of PD and were included in further analyses. The demographics are shown in Table 1.

Among the respondents, 36 people (35.7%) indicated experiencing freezing within the past month.

Results of Danish New Freezing of Gait Questionnaire

Among the 92 respondents indicating a diagnosis of PD, 36 indicated experiencing FoG in the previous month and 56 did not. Stratifying the prevalence of freezing by age disclosed no discernible relationship, see Figure 1 A.

Correlation between prevalence and disease duration, however, was more pronounced. Indeed, when performing a weighted linear regression on prevalence of FoG as a function of disease duration, we achieved a good linear fit (R² = 0.5682, p = 0.0308). The correlation indicated a 3.9 percentage point increase in prevalence per year of living with PD with a 50% prevalence at 7.87 years.

Among the 36 respondents indicating FoG, average severity according to the NFOGQ was 21.6 (95% confidence interval (CI): 19.3-23.9). The indicated severity, NFOGQ total score, showed no significant correlations with age or disease duration. Severity broken down by question is indicated in Figure 2.

Results of the validation questionnaire

In total, 33 patients (36.23%) completed the validation questionnaire. Participants indicated that they understood the objective of the questions. Two participants reported problems understanding one of the Danish NFOGQ questions. One participant reported that they did not understand Question 1, indicating presence of FoG during the preceding month. The reason given was they had never experienced FoG.

Another participant stated not understanding Question 2, concerning frequency of FoG. The reason given was that they did not understand why they needed to state their weekly FoG frequency when the overall questionnaire inquiries about the previous month.

Regarding suitability of response options, responses were deemed appropriate by most respondents (81.8-100%, depending on question). One person replied that they found the available responses unsuitable to their case as they had never experienced FoG. Another person found that the available responses did not accurately reflect the severity of their FoG and, finally, one participant responded that the available responses lacked discrimination between ON and OFF freezing.

The respondents were prompted to describe each of the questions in the questionnaire. Respondents gave accurate descriptions (79.2-100%), indicating suitable phrasing of the questions. However, some of the descriptions provided were ambiguous, making it unclear whether the participant had fully understood them. One participant offered the following description for Questions 3-6 “The question is impossible to misinterpret” (Danish: “Spørgsmålet er for mig entydigt), and another provided a similar description for Questions 4-8 (“Det er simple spørgsmål. De kan ikke misforstås”).

One respondent misinterpreted the intention of Questions 4 and 9 by describing it as referring to the state of their PD in general, not specifically to FoG. One participant interpreted Question 3 as being about their gait function in general, not specifically about FoG. Finally, one respondent offered a “?” as explanation for Question 7.

Retest results

In total, 19 respondents completed the retest. The range of discrepancy in the test-retest was 13 (–7-6) points. However, there were outliers as the mean change was 2.16 points (95% CI: 1.11-3.20 points) and the median 2 points.

DISCUSSION

Here, we have detailed the process of translating and adapting the NFOGQ into Danish for use among Danish-speaking PD patients. We assessed the applicability of the Danish NFOGQ and the prevalence of FoG in this cohort.

The adaptation of the NFOGQ into Danish produced an easy to read and understand questionnaire that may be used in the clinic to evaluate the presence, duration, complexity and severity of FoG. However, an important point, which was also raised by one of the respondents, is the questionnaire’s lack of discrimination between ON and OFF states. Given this, we have amended the Danish version. The Danish version now contains an additional item (Question 6.a): “Hvor stor en procentdel af dine fastfrysninger finder sted imens din parkinson medicin virker, som den skal? Det vil sige, når du har taget din medicin som du skal, og du føler den virker.” (Eng: What percentage of your episodes of freezing occur while your medication for Parkinson’s disease is working as intended? That is, when you have ingested your medication as prescribed and feel as though it is workin.”) The available answers to the question are 0%, less than 25%, 26-50%, 51-75% or 76-100% (Danish: 0% Jeg har ingen fastfrysninger, imens min medicin virker, mindre end 25%, mere end 25 men mindre en 50%, 51-75%, 75-100%, alle eller næsten alle mine fastfrysninger er imens, jeg har taget min medicin, og den virker). The final Danish NFOGQ, including this adjustment, is provided in Appendix 1.

The prevalence of FoG in our survey was 35.7%. Furthermore, we were able to confirm a significant correlation between disease duration and the prevalence of FoG.

However, other estimates of FoG prevalence vary between studies with ranges from 5% to 85.9% [4, 7, 8]. A large systematic review of 66 studies calculated a weighted mean prevalence of 50.6%. Our results seem to agree with this finding.

As in the original English questionnaire, the version of the Danish NFOGQ used for the online survey contained no specific question to differentiate between FoG occurring in the ON or OFF state. Therefore, we are unable to report whether the 35.7% of the patients who reported FoG in our study were experiencing ON-FoG, OFF-FoG or both. This distinction may have significant clinical implications. In fact, if the episodes of freezing occurred during the OFF states, this would suggest that a significant proportion of respondents were not optimally medicated. One reason for this may be that the patients themselves do not recognize FoG as a symptom of dopamine deficiency, poor compliance or related factors. Hopefully, the adjusted version of the Danish NFOGQ provided in Appendix 1 will allow clinicians and researchers to obtain this information. It will also allow researchers to better identify patients with episodes of FoG exclusively during the ON medication state. This will be crucial for future studies designed to achieve a better understanding of the pathophysiology of ON-FoG and novel treatments [9].

CONCLUSION

Our validation indicated that the questionnaire is readily understood by patients and is robust across time. Furthermore, our cohort-based survey indicated that FoG is a prominent symptom among Danish patients with PD.