Effects of shock wave therapy on inflammatory markers in diabetic and non-diabetic frozen shoulder - jpr solutions

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Research Article

Effects of shock wave therapy on inflammatory markers in
diabetic and non-diabetic frozen shoulder
Magdy Mostafa Ahmed1*, Shahesta Ahmed Osama2, Mohammed Naeem Mohamed3,
Samar HassabAllah Kassem4, Ahmed Tamer Farag Ahmed5

                                                          ABSTRACT

    Aim: The aim of the study was to investigate the effect of shock wave therapy on inflammatory markers in diabetic and
    non-diabetic frozen shoulder. Materials and Methods: This study was conducted on 50 subjects with frozen shoulder. They
    were classified according to the fasting blood sugar (FBS) level into two groups. The diabetic group had FBS level of more
    than or equal to 126 mg/dl, while the non-diabetics group had FBS level of  0.05). However, there was a greater percentage of improvement in non-diabetic group than in the diabetic group.
    Conclusion: Shock wave is effective in reducing pain, disability, and inflammatory markers, as well as improving shoulder
    ROM in both diabetic and non-diabetic patients with frozen shoulder, with a greater improvement in non-diabetics.

    KEY WORDS: Diabetes, Frozen shoulder, Inflammatory markers, Non-diabetes, Shock wave

INTRODUCTION                                                         inflammatory cells, including T and B cells,
                                                                     macrophages, and mast cells, as well as elevated
Frozen shoulder is a clinical debilitating painful                   levels of inflammatory markers (interleukins and
condition characterized by inflammatory adhesions                    cytokines) in shoulder capsule biopsies from frozen
and stiffness of the glenohumeral capsule, as well                   shoulder patients.[6] The occurrence of a high
as the painful restriction in both active and passive                level of chronic inflammatory cytokines cells is
movements of the shoulder, especially external                       related to angiogenesis, neurogenesis, and capsular
rotation.[1] Pain and functional impairment could limit              inflammation and may lead to increased frozen
activities of daily living and disturb sleep at night on             shoulder pain.[7]
the affected side.[2] The prevalence of frozen shoulder
among diabetics and non-diabetics is about 11–30%                    Physiotherapy is widely adopted as an initial and first
and 2–10%, respectively.[3,4] The higher prevalence in               line of treatment in a frozen shoulder and can improve
diabetic patients may be attributed to microvascular                 outcome scores. There are many methods of physical
abnormalities that delay collagen repair and cause                   therapy treatment for idiopathic or secondary frozen
degenerative alterations.[5]                                         shoulder as passive exercises and gentle pendulum
                                                                     exercises.[8]
The pathogenesis of frozen shoulder is not fully
understood in spite of its high prevalence. Recent                   Extracorporeal shock wave therapy is a new
research has identified increased expression of                      conservative therapeutic modality that deals with
                                                                     musculoskeletal pain caused by different conditions.[9]
                      Access this article online                     It helps regeneration of new blood capillary in the
     Website: jprsolutions.info    ISSN: 0975-7619
                                                                     affected lesion, accelerates the healing process of
                                                                     connective tissue, decreases pain, and finally facilitates
1
 Department of Physical Therapy for Internal Diseases, Faculty of Physical Therapy, October 6 University, Giza, Egypt,
2
 Department of Physical Therapy for Orthopedics, Faculty of Physical Therapy, October 6 University, Giza, Egypt,
3
 Department of Physical Therapy for Basic Sciences, Faculty of Physical Therapy, Beni Suef University, Beni Suef, Egypt,
4
 Department of Biochemistry, Faculty of Medical Applied Science, October 6 University, Giza, Egypt, 5Department of
Orthopedic Medicine, Faculty of Medicine, October 6 University, Giza, Egypt

*Corresponding author: Magdy Mostafa Ahmed, Department of Physical Therapy for Internal Diseases, Faculty of Physical
Therapy, October 6 University, Giza, Egypt. E-mail: dr.mgdy.mostafa91@gmail.com

Received on: 21-09-2019; Revised on: 16-10-2019; Accepted on: 27-11-2019

    296                                                                          Drug Invention Today | Vol 14 • Issue 2 • 2020
Magdy Mostafa Ahmed, et al.

the function of the shoulder joint.[10] In addition, it             Shock wave therapy
activates the rate of fibroblasts proliferation, synthesis          All patients in both groups received shock wave
of collagen, and gene expression for cytokines and/or               therapy once per week, for 4 weeks. The treatment
growth factors. Both effects of extracorporeal shock                position was sitting with the full support of the back;
wave therapy on enhancing blood flow and activating                 the affected shoulder was exposed, and a coupling
fibroblasts collaborate to accelerate the repairing                 gel was applied on it to limit the loss of energy at the
process.[11]                                                        interface between skin and applicator head. Then,
                                                                    the shock wave was applied close to the insertion
To the best of our knowledge, there was no study                    of rotator cuff muscle on the most trigger point. The
compared the efficacy of shock wave therapy on                      shock wave applied 2000 impulses in one session. The
systemic inflammation in diabetic versus non-diabetic               density of energy was 0.22 mJ/mm², the pulse rate was
frozen shoulder. Therefore, this study aimed to assess              10/s, and the frequency was 1–15 Hz.[13]
the effect of shock wave intervention on major
inflammatory cytokines (C-reactive protein [CRP]                    Therapeutic exercise program
and interleukin-6 [IL-6]) in diabetic and non-diabetic
                                                                    Each patient in both groups received a therapeutic
frozen shoulder.
                                                                    exercise program in the form of passive stretching
                                                                    exercise, strengthening exercise, and mobilization
MATERIALS AND METHODS                                               for the shoulder joint, 3 times per week, for 4 weeks.
Design                                                              The passive stretching exercise was applied for
                                                                    the shoulder capsule and its musculature and was
The work was designed as a prospective comparative
                                                                    repeated for 3 times, with 30 s of hold and 10 s of a
study, a pre- and post-test. It was conducted between
                                                                    rest period in between.[14] The strengthening exercises
March 2018 and April 2019 and followed the
                                                                    were performed for the stabilization of shoulder
guidelines of Declaration of Helsinki on the conduct
                                                                    muscles. First, the repetition maximum was identified,
of human research.
                                                                    depending on the pattern of movement of patient and
Participants                                                        patient’s reactions; pain and fatigue were considered.
                                                                    The strength training exercise was performed in the
A sample of 50 patients (27 females and 23 males) was
                                                                    form of three sets, every one duplicated 10 times, with
recruited from the out-patient clinic of physical therapy
                                                                    brief rest between each one.[15] The mobilization of the
at October 6 University Hospitals, Giza, Egypt. To be
                                                                    shoulder was used to decrease pain and increase ROM
included in the study, the participants were chosen
                                                                    of the shoulder joint. Sustained traction mobilization
adult patients suffering from frozen shoulder for 2 to
                                                                    technique with grades (I, II, III, and IV) and Maitland
9 months (stage 1; the painful phase). They should
                                                                    oscillatory technique in the form of anterior, inferior,
have three hallmarks for the diagnosis of frozen
                                                                    and posterior glide were applied.[16]
shoulder, including severe limitation of joint motion,
exaggerated pain (particularly in evening time), and                Outcome Measures
significant loss of external rotation range of motion
(ROM) during passive and active movement.[12] The                   Visual analog scale (VAS)
patients’ ages ranged from 40 to 60 years old. The                  It was used to assess the severity of pain before and
diabetic patients were diagnosed as type 2 diabetes                 after treatment for both groups. It consists of a 10 cm
for at least 5 years (fasting blood sugar [FBS] ≥                   line with varying degrees of pain intensity from 0 (no
126 mg/dl), while the non-diabetics patients had FBS                pain) to 10 (killing pain). Patients were instructed
of
Magdy Mostafa Ahmed, et al.

was calculated by averaging the scores of pain and                            statistically non-significant difference (P > 0.05).
disability subscales.[18]                                                     However, there was a greater percentage of
                                                                              improvement with regard to VAS in non-diabetic group
Shoulder ROM                                                                  (75%) than in the diabetic group (64.55%) [Table 2].
The shoulder ROM was evaluated, by electro
goniometer device, for all patients in both groups                            The SPADI showed a statistically significant reduction
pre- and post-treatment. The assessment was done                              (P < 0.05) within both groups. The post-treatment
for shoulder flexion, abduction, and internal rotation                        comparison of both groups revealed a statistically
for every patient. Three continuous measures were                             non-significant difference (P > 0.05). However, there
recorded in each direction and the average of them                            was a greater percentage of improvement with regard
was taken.[19]                                                                to SPADI in the non-diabetic group (78.3%) than in
                                                                              the diabetic group (74.3%) [Table 2].
Inflammatory markers levels
                                                                              The shoulder ROM in all directions (flexion,
Blood samples were collected from each patient in                             abduction, and internal rotation) showed a statistically
both groups pre- and post-treatment to measure the                            significant increase (P < 0.05) within both groups.
levels of inflammatory markers, including CRP and                             The post-treatment comparison of both groups
IL-6. The serum CRP was controlled by utilizing                               revealed a statistically non-significant difference
the CRP latex agglutination test. The occurrence                              (P > 0.05). However, there were greater percentages of
of agglutination demonstrated a level of CRP in                               improvement with regard to shoulder ROM in flexion,
the sample >8 mg/L. The absence of agglutination                              abduction, and internal rotation in the non-diabetic
demonstrated a CRP level of ≤ 8 mg/L. The level                               group (50.01%, 56.3%, and 72.07%) than in diabetic
of plasma IL-6 was determined, using ELISA unit,                              group (46.86%, 49.32%, and 63.3%) [Table 2].
according to the technique of Feldmann et al.[20]
                                                                              The inflammatory markers (CRP and IL-6) showed a
Statistical Analysis                                                          statistically significant reduction (P < 0.05) within both
The mean and standard deviation (SD) were used for the                        groups. The post-treatment comparison of both groups
expression of results for data analysis. Unpaired t-test                      revealed a statistically non-significant difference
was used to compare various variables between groups.                         (P > 0.05). However, there were greater percentages
Paired t-test was performed within the same group for                         of improvement with regard to CRP and IL-6 in the
various variables as compare pre- and post-assessment                         non-diabetic group (67.28.6% and 43.4%) than in the
in normal data. The analysis of data was done using                           diabetic group (57.89% and 34.6%) [Table 2].
Statistical Package for the Social Sciences computer
program (version 23 windows). The significance of                             DISCUSSION
research was determined at P ≤ 0.05.
                                                                              To the best of our knowledge, no previous work
                                                                              has studied the effects of shock wave therapy on
RESULTS                                                                       inflammatory markers in the diabetic and non-diabetic
Both groups were similar at baseline (P > 0.05)                               patients with frozen shoulder. Therefore, this research
regarding age, duration of illness, weight, BMI, and                          is considered the first study on this point. Accordingly,
all outcome measures [Tables 1 and 2]. However,                               the results cannot be compared or discussed directly
there was a significant difference between both groups                        with other research outcomes.
regarding FBS (P < 0.05) [Table 1].
                                                                              The mean age of frozen shoulder patients in this
The VAS showed a statistically significant                                    investigation was 52.7 ± 7.5 years. This is consistent
reduction (P < 0.05) within both groups. The post-                            with Harris et al.[21] who found that frozen shoulder
treatment comparison of both groups revealed a                                was very rarely noticed early below the age of 40 years.
                                                                              A clinical study by Ulusoy et al.[22] in Turkey showed
Table 1: Basic characteristics of patients in both groups                     that the average age of frozen shoulder is somewhere
                                                                              in the range of 40–60 years. One study conducted
Characteristics          Diabetic   Non-diabetic P value                      by Watson[23] suggested that the higher prevalence
                       group (n=25) group (n=25)
                                                                              of frozen shoulder in older individuals may be due
Age (years)               52.7±7.8            52.4±7.1          0.62NS
                                                                              to aging as there are inflammatory reactions in the
Duration of               6.3±2.58            6.1±2.32          0.84NS
                                                                              shoulder joint and its ligament.
illness (month)
Weight (kg)              76.4±6.2              78.1±9.1         0.42NS
                                                                              The results of the current study showed a significant
BMI (kg/m²)              27.8±2.8             28.3±2.97          0.1NS
FBS (mg/dl)             178.34±11.6           86.75±7.2         0.001S        reduction in VAS, SPADI, and levels of inflammatory
 P>0.05, SP
Magdy Mostafa Ahmed, et al.

Table 2: The VAS, SPADI, shoulder ROM, and inflammatory markers for both groups
Items                                            Diabetic group (n=25)                        Non-diabetic group (n=25)                           P value*
VAS
  Pre-treatment                                            7.9±1.2                                         7.6±1.34                                 0.22NS
  Post-treatment                                          2.8±0.92                                         1.9±0.73                                 0.08NS
  % of improvement                                          64.55                                            75.0
  P value**                                                0.000S                                           0.000S
SPADI
  Pre-treatment                                            7.4±1.2                                         6.92±1.3                                 0.36NS
  Post-treatment                                          1.9±0.85                                         1.5±0.68                                  0.1NS
  % of improvement                                           74.3                                            78.3
  P value**                                                0.001S                                           0.001S
Shoulder flexion
  Pre-treatment                                         94.35±6.38                                      96.79±6.87                                  0.47NS
  Post-treatment                                        138.52±12.3                                     145.2±11.15                                 0.16NS
  % of improvement                                         46.86                                           50.01
  P value**                                               0.001S                                          0.001S
Shoulder abduction
  Pre-treatment                                         103.53±7.98                                     102.1±7.63                                   0.1NS
  Post-treatment                                       154.66±20.32                                     159.5±10.97                                 0.54NS
  % of improvement                                         49.32                                            56.3
  P value**                                               0.001S                                          0.001S
Shoulder internal rotation
  Pre-treatment                                          23.33±4.57                                       24.6±4.26                                 0.28NS
  Post-treatment                                          38.2±6.21                                      42.33±2.44                                 0.35NS
  % of improvement                                           63.3                                           72.07
  P value**                                                0.001S                                          0.001S
CRP (mg/L)
  Pre-treatment                                           12.54±1.3                                      10.24±1.24                                  0.2NS
  Post-treatment                                          5.28±1.15                                       3.35±0.48                                 0.21NS
  % of improvement                                          57.89                                           67.28
  P value**                                                 0.001S                                          0.001S
IL-6 (ng/ml)
  Pre-treatment                                           13.3±3.8                                        11.33±1.6                                 0.52NS
  Post-treatment                                          8.7±2.56                                        6.41±0.95                                 0.08NS
  % of improvement                                          34.6                                             43.4
  P value**                                                0.001S                                           0.001S
*Intergroup comparison; **intragroup comparison of the results pre- and post-treatment. NSP>0.05, SP
Magdy Mostafa Ahmed, et al.

The favorable effect of passive stretching exercises           markers, as well as increasing shoulder ROM in both
on frozen shoulder patients could be related to the            diabetic and non-diabetic frozen shoulder, with a
tensile stresses on the non-contractile connective             greater improvement in non-diabetics.
tissue in and around the muscle. Furthermore, it
produces inhibition of the muscular contractile                ACKNOWLEDGMENTS
elements by the Golgi tendon organ that causes reflex
relaxation of the muscle thus enabling the muscle to           The authors would like to thank all individuals who
elongate against less muscle tension.[33] Application          contributed to the completion of this work.
of passive stretching at low intensity and velocity for
long period induces breakdown of the collagen fibers           AUTHORS’ CONTRIBUTIONS
bonds, resulting in flexibility improvement, ROM
                                                               MM, SA, and MN, conceived of the study, designed
increase, and functional recovery.[34] The positive
                                                               the study protocol, and drafted the manuscript.
effect of mobilization on the frozen shoulder could be
                                                               MM, SA, and MN wrote the manuscript. MM is the
attributed to its influence on breaking down adhesions,
                                                               corresponding author and supervisor of the research.
realigning collagen, increasing fiber gliding through
                                                               SH helped us in drafting the revised manuscript and
particular movements stressing the capsular tissues,
                                                               substantively helped us to revise the manuscript.
inducing rheological alterations in synovial fluid,
                                                               All authors have reviewed the final version of the
increasing fluid exchange between synovial tissue and
                                                               manuscript and approve it for publication.
the cartilage matrix, and enhancing the turnover of
synovial fluid.[35]
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                                                                            Source of support: Nil; Conflicts of interest: None Declared

      Drug Invention Today | Vol 14 • Issue 2 • 2020                                                                                      301
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