Axial posture disorders in Parkinson’s disease: Clinical correlates and future treatment directions 1

Abstract

BACKGROUND:

Postural disorders are frequently observed in Parkinson’s disease (PD). The underlying mechanisms that cause postural disorders are not fully understood and the majority of these disorders have no response to antiparkinsonian treatments. These disabling conditions require further investigation to better understand the underlying mechanisms in order to develop effective treatments.

OBJECTIVE:

The aim of this study was to investigate the frequency of axial postural disorders in PD and to determine the associated clinical risk factors.

METHODS:

In this single-center clinical trial, the data of PD patients were reviewed retrospectively. The frequencies of postural disorders were determined, and the demographic clinical characteristics of the patients were compared.

RESULTS:

The records of 127 patients with idiopathic PD were analyzed. Axial posture disorders were found in 42.6% of patients. Patients with axial posture disorders were older when the disease onset was detected, amongst these patients the condition was also longer lasting. The mean levodopa dose was higher in the patients with posture disorders. The initial symptom was bradykinesia and the Hoehn and Yahr’s score was $\geqslant$ 3 in the majority of the patients with posture disorder. Additionally, constipation, hallucinations, postural instability, and falls were significantly more common in patients with posture disorders.

CONCLUSION:

Posture disorders were observed in nearly half of PD patients and were more frequently observed in patients with an advanced condition. In addition, our investigation has found that it is crucial to follow up with patients who present with bradykinesia for the development of postural disorder.

Keywords

Axial Parkinson’s disease posture posture disorders treatment

1. Introduction

Parkinson’s disease (PD) is a chronic neurodegenerative disorder, which is characterized by three cardinal features: Resting tremor, rigidity, and bradykinesia. PD is also characterized by disabling nonmotor features and postural disorders [1, 2]. In fact, the definition of these postural deformities was reported with the definition of the disease. James Parkinson first described the stooped posture of patients with PD in 1817 in his “Essay on the Shaking Palsy” [3, 4]. Stooped posture, camptocormia, antecollis, and Pisa syndrome were discussed in these postural deformities [1, 4, 5, 6, 7, 8, 9, 10, 11, 12, 13].

The most commonly recognized type of postural deformity is the stooped posture which is characterized by flexion of the thoracal spine, hips, and knees, and rounding of the shoulders [1, 5, 6, 13, 14]. Another posture disorder camptocormia is an abnormal posture with marked involuntary flexion of the thoracolumbar spine more than 45 ${}^{\circ}$ . Camptocormia is mainly observed in patients while they stand or sit and usually disappears in the recumbent position or with some maneuvers like volitionally extending the trunk [1, 4, 5, 6, 7, 8, 14, 15]. Antecollis which is also known as ‘dropped head’ refers to a pronounced forward flexion of the head and neck [5, 9, 14, 16]. Lastly, Pisa syndrome is a condition that results from lateral flexion of the trunk and typically increases in the standing position and the severity is alleviated in the supine position. Pisa syndrome appears to not cause mechanical restriction to trunk movements [1, 5, 14, 17, 18].

Axial postural disorders are commonly observed in Parkinson plus syndromes and are also common in PD patients when compared to similar age groups [19]. A retrospective observational study showed that 1/3 of patients with PD had a deformity of their limbs, neck, or trunk [5, 14]. Also the frequencies of specific postural disorders in PD are reported between 3% and 17.6% for camptocormia, 8.5% and 60% for Pisa syndrome, and up to 6% for dropped head [5, 8, 9, 14, 16, 20, 21]. In addition to parkinsonian syndromes, camptocormia, Pisa syndrome, and dropped head have also been reported with some hereditary or idiopathic dystonias and conditions with muscle weakness such as amyotrophic lateral sclerosis, myasthenia gravis, and inflammatory myopathy. Pisa syndrome has been described also in some dementias including Alzheimer’s disease and Lewy body dementia [4, 6, 7, 22, 23].

The underlying pathophysiology of these deformities is largely unknown even though multiple factors have been discussed in the pathophysiology of postural deformities. Contributing factors include rigidity, dystonia, myopathy, proprioceptive disintegration, drugs, soft tissue changes, and degenerative spinal changes [5, 7, 8, 14].

Due to the ill-defined mechanisms which cause PD and associated postural deformities their clinical management remains difficult and the treatment options offered are limited and often non-effective. Most of the postural deformities are discussed as levodopa unresponsive situations. Anticholinergic drugs and botulinum toxin can be used in patients who have dystonic features. Deep brain stimulation has also been used and has variable effects depending on the stimulation area and the patient characteristics. Physiotherapy is the only auxiliary treatment method that has currently been used [1, 5, 6, 7, 24].

Although postural deformities were defined for the first time in the literature with the definition of the disease, interest in this subject has increased in more recent times. In addition to the well-known motor and nonmotor symptoms of PD, postural disorders may also contribute to disability and affect the quality of daily life by restricting mobility and inducing falls. Additionally, postural disorders may also be indirectly attributed to rheumatological or orthopedic conditions. But, their frequency should not be underestimated. Also, it is important to define the related factors in order to monitor patients in the risk group. Each new research on this subject will accumulate knowledge and enable a better understanding of risk factors and mechanisms which will collectively contribute to the development of a more effective approach.

The aim of this study is to reveal the frequencies and clinical correlates of axial postural disorders in idiopathic PD patients.

2. Material and methods

In this single-center cross-sectional study, the prevalence of axial posture disorders in PD and its relationship with the demographics and clinical features were investigated. The patients who were evaluated in the movement disorders clinic and diagnosed with PD according to the United Kingdom Parkinson’s Disease Society Brain Bank Diagnostic Criteria were included in the study [25]. All the patients who had Parkinson’s plus syndrome were excluded. Postural disorders were diagnosed by a physical medicine and rehabilitation specialist doctor and board-certified neurologists. Radiologic investigations were also performed on the patients with camptocormia and antecollis to exclude orthopedic conditions and electromyographic (EMG) tests were performed to identify the etiology of the postural disorder. The demographics and clinical features of patients with and without axial posture disorder were compared. The evaluated demographic and clinical features were age, gender, PD onset age, duration of PD, initial symptom, Hoehn and Yahr (H-Y) stage, daily dose of levodopa, dopa agonist, amantadine, and monoamine oxidase inhibitor (MAOI) usage, family history, postural instability, levodopa-induced dyskinesia and history of constipation, REM sleep behavior disorder, falls, swallowing difficulty, hallucination, depression and cognitive impairment.

Statistical analyses were performed using the statistical software program IBM SPSS Statistics version 22.0. Pearson Chi-Square test, Mann-Whitney U test, and one-sample $T$ -test were used for comparative analysis. The value of $p<$ 0.05 was considered statistically significant.

3. Results

A total of 127 records of idiopathic PD patients were screened for axial posture disorders. Axial posture disorder was found in 55 patients (42.6%). Most frequently, anteflexion was detected in 34.9% of PD patients and 81.8% of patients with axial posture disorder. Camptocormia was observed in 6.2%, antecollis in 2.3%, and Pisa syndrome in 1.6% of all the patients included in this study. Multiple posture disorder was observed in 4 patients (3.1%), while camptocormia and Pisa syndrome was detected in one patient, anteflexion and Pisa syndrome was also observed in one patient, and camptocormia and antecollis in 2 patients. Although 61.8% of the patients with axial posture disorders were male, there was no significant statistical relationship between gender and having posture disorders.

Patients with axial posture disorders were older in follow-up (mean 77.24 vs. 71.06 years) and at disease onset (mean 69.44 vs. 63.22 years; $P<$ 0.05) compared with patients without axial posture disorder and also axial posture disorder group had a longer disease duration (mean 7.94 vs. 7.03 years; $P<$ 0.05). Moreover, the mean levodopa dose was higher in the patients with posture disorder (522.55 vs. 367.36 mg/d; $P<$ 0.05). The initial symptom was bradykinesia in 78.2% of patients with posture disorder and 52.8% of patients without the disorder ( $P<$ 0.05). H-Y score was $\geqslant$ 3 in 51% of patients with axial posture disorder and $<$ 3 in 91.7 % of patients without posture disorder ( $P<$ 0.05).

There was no significant difference for the use of amantadine, dopa agonist, MAOI, and history of REM sleep behavior disorder, swallowing difficulty, cognitive impairment, depression, and levodopa-induced dyskinesia between the two groups. Whereas constipation, hallucinations, postural instability, and falls were significantly more common in the patients with axial posture disorders ( $P<$ 0.05).

Demographic, clinical characteristics and comparative statistics results of the patients are summarised in Table 1.

4. Discussion

A total of 127 records of idiopathic PD patients were screened in this present study. Axial posture disorders were observed in 42.6% of the study population. PD onset at an older age, presentation with bradykinesia, and having a severe disease were found to be associated with having axial posture disorder.

It has previously been reported that posture disorders are common in PD patients compared to similar age groups [31]. The studies which included posture disorders in both extremities and the axial structure, reported the frequency of postural deformities in up to 1/3 of the patients [5, 14]. The present study, which only includes axial posture disorders revealed that nearly half of the patients have posture disorders.

Anteflexion posture is the best documented and common posture disorder related to PD [26]. Subsequently, the frequency for camptocormia, has been reported between 3% and 17.6% in different studies [5, 8, 13, 14, 19, 20]. Dropped head frequency is reported to the highest 6% [5, 9, 13, 14, 16]. The frequency for Pisa syndrome has also been reported with a very wide range of 8.5 to 60% [13]. Anteflexion was observed in 34.9% of all patients and 81.8% of the study population with posture disorders. The frequency of 6.2% for camptocormia and 2.3% for the dropped head in the present study is consistent with the literature. Ethnic reasons have been suggested for the broad range of frequencies, especially for lateral flexion and camptocormia. Cyprus is the birthplace of 70% of all the patients, while in 27% of studied patients the birthplace was Turkey. It has been reported that camptocormia and antecollis are observed more frequently in Asian patients [13, 19]. In addition, the different clinical features of PD patients included in the studies, especially the stage, may explain this difference in frequency.

The frequencies found in the literature and the current study indicate that postural disorders are also an important feature of idiopathic PD [6, 14]. Unfortunately, in addition to the well-known motor symptoms necessary for definite diagnosis and premotor symptoms for early diagnosis of PD, less attention has been paid to these postural disorders. Postural disorders, however, especially more marked forms like dropped head syndrome and camptocormia may cause a significant increase in

Table 1
Demographic and clinical characteristics of patients

		PD with posture abnormalities						PD without posture abnormalities ${}^{{\dagger}}$ $n=$ 72 $n$ (%)	All PD patients $n=$ 127 $n$ (%)	$P$ value ${}^{{\dagger}*}$
		Anteflexion posture ( $n$ )	Camptocormia ( $n$ )	Pisa syndrome ( $n$ )	Antecollis ( $n$ )	Multiple posture abnormality ( $n$ )	Total ${}^{{\dagger}}$ $n=$ 55 $n$ (%)
Gender	Male Female	27 19	6 2	2 0	2 1	3 1	34 (61.8) 21 (38.2)	49 (68.1) 23 (31.9)	83 (65.4) 44 (34.6)	0.464
Mean age (year)		77.15	77.86	84	78	81.5	77.24	71.06	73.74
Mean age at disease onset (year)		69.88	67.38	71	69.67	70.75	69.44	63.22	65.88	0.004 ${}^{*}$
Mean disease duration (year)		7.44	10.5	13	8.33	10.75	7.94	7.03	7.42	0.0000 ${}^{*}$
Initial symptomes	Tremor Bradikinesia	11 35	1 7	1 1	0 3	1 3	12 (21.8) 43 (78.2)	34 (47.2) 38 (52.8)	46 (36.2) 81 (63.8)	0.003 ${}^{*}$
H-Y score	$<$ 3 $\geqslant$ 3	25 21	1 7	0 2	2 1	1 3	27 (49) 28 (51)	66 (91.7) 6 (8.3)	93 (73.2) 34 (26.8)	0.0000 ${}^{*}$
LevoDopa dose. mean (mg/d)		483.48	762.5	650	633.33	700	522.55	367.36	434.57	0.018 ${}^{*}$
Agonist use	Yes No	9 37	4 4	2 0	2 1	3 1	14 (25.5) 41 (74.5)	25 (34.7) 47 (65.3)	39 (30.7) 88 (69.3)	0.262
Amantadine use	Yes No	4 42	2 6	0 2	1 2	1 3	6 (10.9) 49 (89.1)	5 (6.9) 67 (93.1)	11 (8.7) 116 (91.3)	0.431
MAO inh. use	Yes No	14 32	3 5	1 1	1 2	1 3	18 (32.7) 37 (67.3)	26 (36.1) 46 (63.9)	44 (34.6) 83 (65.4)	0.655
Levodopa-induced dyskinesia	Yes No	8 38	0 8	0 2	0 3	0 4	8 (14.5) 47 (85.5)	6 (8.3) 66 (91.7)	14 (11) 113 (89)	0.005
Postural instability	Yes No	21 24	7 1	2 0	2 1	3 1	30 (54.5) 25 (45.5)	7 (9.7) 65 (90.3)	37 (29.1) 90 (70.9)	0.0000 ${}^{*}$
History of falls	Yes No	15 31	6 2	2 0	2 1	4 0	21 (38.2) 34 (61.8)	7 (9.7) 65 (90.3)	28 (22) 99 (78)	0.0000 ${}^{*}$
Cognitive imparement	Yes No	16 30	5 3	2 0	1 2	3 1	21 (38.2) 34 (61.8)	11 (15.3) 61 (84.7)	32 (25.2) 95 (74.8)	0.005
Swallowing difficulty	Yes No	7 39	3 5	2 0	1 2	3 1	10 (18.2) 45 (81.8)	4 (5.6) 68 (94.4)	14 (11) 113 (89)	0.053
Hallucination	Yes No	14 31	4 4	1 1	1 2	2 2	18 (33.3) 36 (66.7)	9 (12.9) 61 (87.1)	27 (21.8) 97 (78.2)	0.006 ${}^{*}$
Depression history	Yes No	11 34	4 4	1 1	0 3	1 3	15 (27.8) 39 (72.2)	19 (27.5) 50 (72.5)	34 (27.6) 89 (72.4)	0.976
REM sleep behavior disorder	Yes No	7 39	0 8	0 2	0 3	0 4	7 (12.7) 48 (87.3)	12 (16.7) 60 (83.3)	19 (15) 108 (85)	0.537
Constipation	Yes No	20 26	4 4	1 1	1 2	2 2	24 (43.6) 31 (56.4)	11 (15.3) 61 (84.7)	35 (27.6) 92 (72.4)	0.0003 ${}^{*}$
Family history	Yes No	2 44	1 7	0 2	1 2	0 4	4 (7.3) 51 (92.7)	6 (8.3) 66 (91.6)	10 (7.9) 117 (92.1)	0.55

${}^{{\dagger}}P$ value represent the comparement of total PD with posture abnormalities and PD without posture abnormalities. ${}^{*}P$ value $<$ 0.005 was accepted statistically significant.

disability in PD patients, independent from other motor symptoms [14, 21, 26, 27, 28].

It is a common finding that posture disorders occur in patients with more advanced disease states detected by UPDRS and/or H-Y, both in studies that include axial posture disorders and extremities together, and in studies that include specific axial posture disorders such as camptocormia, dropped head and Pisa syndrome [1, 5, 6, 8, 10, 14, 19, 20, 29, 30]. In addition to the severity of the disease, camptocormia, and other axial posture disorders have been observed more frequently in patients with long disease duration [1, 19, 20]. It has been well documented that the majority of patients with postural disorders used levodopa, with higher doses and longer periods [8, 14, 19]. Nevertheless, PD patients especially with camptocormia are less responsive to levodopa than those without this deformity, but also have fewer levodopa-induced limb dyskinesias and motor complications [1, 5, 10, 31]. The use of high doses of levodopa in these patients is discussed as a consequence related with the advanced disease level. Many studies indicate also that patients with anterior and/or lateral flexion are older [1, 5, 21, 24]. On the contrary, in a study with PD patients with joint and skeletal deformities together with another independent study that concentrated on camptocormia, it was stated that the patients with posture disorders were younger and had earlier onset of PD [7, 14].

In this study, a more advanced disease state detected by H-Y and a longer disease duration were found in patients with axial posture disorders. The mean age of the patients with posture disorders and the mean age at onset of PD was more advanced than the group without posture disorders. Also, these patients commonly used levodopa and were administered higher doses of levodopa compared to PD patients without posture disorders. The mean levodopa dose used by patients with postural disorders was quite high (522.55 mg/d). The average dose becomes even higher, especially when the milder anteflexion group was excluded (686.46 mg/d). Hallucinations were also common in the posture disorder group, most likely due to higher dosage use of levodopa.

In a study examining conditions that correlate not only with the presence of bending but also with its severity, a relationship was observed between the severity of bending and the history of vertebral surgery amongst female patients, no relationship however was found with age, disease duration, severity, duration of treatment and dose [19]. There are studies that state that camptocormia is more prevalent in males [1, 21]. A correlation between gender and the presence of postural disorders was not observed in the present study.

Considering the disease characteristics, it was reported that camptocormia was observed more frequently in patients with axial dominant disease, motor fluctuations, and dysautonomic symptoms [1, 21]. There are also studies that indicate a relationship between the presence of cognitive impairment and depression [8, 19, 32].

In the present study, axial postural disorders were detected more frequently in patients with constipation as a premotor symptom and bradykinesia as the initial symptom. It is known that the functional connectivity between cortical and subcortical motor areas is different in two subtypes of PD and diminished in the bradykinesia dominant subtype [33, 34]. Furthermore, no relation was found between cognitive impairment and the presence of postural disorder, possibly due to the fact that the information regarding the presence of cognitive impairment is based on the statements of the patients or their relatives, which can be an important limiting factor.

Some patients may present with a combination of postural deformities in both sagittal and coronal planes [5, 7, 8, 14, 26]. Multiple posture deformities were observed in 4 patients (3.1%). Pisa syndrome was always observed together with an additional postural disorder in the study population. Although it is discussed in the literature whether they are together as part of the same pathological process or coincidentally, we believe that there are common pathways that affect their coexistence [26]. For this reason in this study, axial deformities of the neck and trunk were examined together. There are not many studies evaluating posture disorders that also concern the axial structure. We suggest that their common clinical features, drug nonresponsiveness, being observed in patients with advanced age and disease stage, and their coexistence made it possible to evaluate them in the same study group.

The underlying pathophysiology of these deformities is largely unknown. Myopathy and dystonia have mostly been discussed in the mechanism of camptocormia and dropped head. In fact, there are also publications reporting neurophysiological and pathological findings regarding suspicions that myopathy is not the primary mechanism [5, 35]. The evidence comes from these studies suggested that the myopathy seen in camptocormia and dropped head actually occurs secondary to excessive forward bending. In addition, it is known that dystonia actually occurs through dopaminergic and cholinergic pathways that may also indicate central control of postural disorders. At least there is a large group of a patient whose posture problem pathogenesis cannot be explained by a specific cause such as dystonia or myopathy. The posture disorders are unresponsive to levodopa treatment and are seen in the advanced disease stage. However, the posture returns to normal with a small peripheral maneuver. All this suggests that while revealing the mechanism of axial posture disorders, we should actually focus on the organization of the posture centrally and what happens in PD.

Postural stability is related to a well-functioning sensory input system, vestibular system, vestibular, and somatosensory cortical structures. Complex networks exist among all these structures that contribute to postural stability. Additionally, the neurotransmitters, especially dopamine and choline, in these networks support postural control [33, 36, 37]. The ability to receive and process vestibular and somatosensory impulses and compensation mechanisms are also impaired in PD besides the main pathology. In addition, body position image, stability, and adaptation to changing conditions are affected by the function of basal ganglia and the cortical structures, especially the vestibular cortex [33, 36, 38]. In functional MRI studies showing striatocortical and cerebellocortical connections, the activity of striatocortical circuits decreases with dopamine denervation in PD, and the activities of cerebellocortical circuits increase as a possible compensation mechanism. While compensation can be achieved in the early stage, it remains insufficient with disease progression [39, 40]. As a result, the center of mass shifts, and postural stability is impaired in PD. PD patients may have both forward and lateral posture and balance problems [33].

Response to levodopa treatments, especially for forward postural disorders and postural stability, is low [1, 5, 6, 7, 24, 33, 41]. This supports the contribution of other neurotransmitters. Postmortem studies showed that decreased pedunculopontine nucleus (PPN) neurons are associated with the variant of PD with bradykinesia and rigidity, and also frequent falls.

Postural disorders were detected more frequently in the patients with bradykinesia dominant onset in the present study. PPN is the major cholinergic nucleus [33, 42, 43]. Besides, unlike other classical stimulation intervention areas, PPN-deep brain stimulation (DBS) has more satisfactory results in symptoms related to walking and posture in patients with PD [44]. Also, it has been reported that patients with postural instability and falls have lower thalamocortical AchE levels, and cholinergic treatments decrease falls in PD patients [45]. Moreover, their occurrence with dementia where cholinergic denervation is at the forefront emphasizes the importance of cholinergic pathways in the mechanism of postural disorders.

Levodopa unresponsiveness of postural disorders is frequently explained by the fact that the disease is seen in the later stages. It is however important to consider that with the progression of PD, failure of both dopaminergic and cholinergic pathways occur.

In the light of all the knowledge in the literature, and our findings, postural disorders are common in patients who have bradykinesia predominant onset and frequent falls. It may be beneficial to consider the cholinergic system for future treatment goals and to add methods for processing sensory inputs or supporting compensatory mechanisms.

Since this study is a cross-sectional study, the data is based on patient records and statements. Additionally, although the number of the general study population is sufficient, the limited number of some rare postural disorder subgroups leads to limitations in statistical analysis and conclusions. This study, which evaluated only axial posture disorders, provided the first data in PD patients. Future studies involving larger patient groups will provide more detailed information.

5. Conclusion

Posture disorders were observed in nearly half of the idiopathic PD patients and were more frequently observed in patients which presented longer disease duration, advanced levels of the condition, and patients with late-onset disease. In addition, this study revealed that it is important to monitor the condition of patients who present with bradykinesia, as these patients are in a higher risk category for developing postural disorders.

Ethics statement

This was a retrospective non-interventional observational study. Ethical approval was thus not required. The Declaration of Helsinki was followed throughout the study.

Funding

None to report.

Footnotes

Acknowledgments

The authors would like to thank Ferdiye Taner for her contribution to the English language review of the manuscript.

Conflict of interest

The researchers claim no conflicts of interest.

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Axial posture disorders in Parkinson’s disease: Clinical correlates and future treatment directions 1

Abstract

BACKGROUND:

OBJECTIVE:

METHODS:

RESULTS:

CONCLUSION:

Keywords

1. Introduction

2. Material and methods

3. Results

4. Discussion

Table 1 Demographic and clinical characteristics of patients

Ethics statement

Funding

Footnotes

Acknowledgments

Conflict of interest

References

Table 1
Demographic and clinical characteristics of patients