[Downloaded free from http://www.jcpconline.org on Monday, October 30, 2017, IP: 36.230.120.

81]

Original Article
Incidence and Clinical Profile of Patients with Frozen Shoulder after
Cardiac Surgery
M Chokkalingam1, MBBS, MD, DNB Cardiology; S Saradha2, MBBS, MD, DLO; A Navitha1, BSc, Cardiac Technology;
Pradeep G Nayar1, MBBS, MD, DNB Cardiology

Departments of 1Cardiology Background: Frozen shoulder is a condition characterized by pain and global restriction of

Abstract
and 2Pharmacology, Chettinad movement with loss of external rotation. Cardiac surgery may predispose frozen shoulder as
Hospital and Research patients tend to immobilize their upper limbs after surgery. Objectives: The aim of this study is
Institute, Chennai, to analyze the clinical profile of patients presenting with symptoms of periarthritis shoulder and
Tamil Nadu, India to determine the incidence of frozen shoulder among patients undergoing cardiac surgery as well
as to find the factors associated with its development. Methods: It is a clinical observational
study done in the Cardiology Department of Chettinad Hospital and Research Institute, Chennai,
between August 2015 and May 2016, on 100 patients who underwent cardiac surgery and
attended the follow‑up session as an outpatient. Data were collected by face‑to‑face interview
using a standardized questionnaire. Respondents presenting with pain and restricted movement of
shoulder joint with positive limitation in lateral rotation, abduction, and medial rotation (LAM)
test were considered to have frozen shoulder. Each participant was followed up for 3 months
postcardiac surgery. Results: The mean age of the study participants was 53.63 ± 13.03 years, and
65% were males. Of the 100 participants, 20 (20%) developed frozen shoulder. Age (P < 0.01),
diabetes mellitus (<0.01), hypertension (P < 0.001), type of surgery (P < 0.02), and regularity
of physiotherapy follow‑up (P < 0.01) had significant association with positive LAM test on
univariate analysis. However, on multivariate logistic regression analysis, only hypertension and
physiotherapy regularity were found to have a trend toward a significant independent association
with the occurrence of frozen shoulder (P = 0.090 and 0.097, respectively). Conclusion: The
present study shows that cardiac surgery increases the risk of developing frozen shoulder during
the early postoperative period. Statistically significant correlation existed between positive LAM
test and age of the patients, presence of diabetes mellitus and hypertension, type of cardiac
surgery, and the regularity of physiotherapy follow‑up.

Received: April, 2017.

Keywords: Adhesive capsulitis, cardiac surgery, frozen shoulder, limitation in lateral rotation,
Accepted: June 2017. abduction, and medial rotation test

Introduction Stage II: Both active and passive movements of shoulder were
restricted.
T he frozen shoulder otherwise known as adhesive
capsulitis was identified as a separate clinical entity
by Duplay in 1872.[1] It is one of the most common causes
Stage III: Shoulder pain was negligible, and patients could
move their shoulder to certain extent.
of shoulder pain and disability. The prevalence of frozen
shoulder is 2%–3% worldwide.[2] It occurs usually between Frozen shoulder can be divided into primary and secondary forms.
40 and 70 years of age.[3] It is a common problem in our In the primary form, there is no associated disease or a history
country in the 5th and 6th decades of life. There is a female of trauma or surgery of the shoulder. Secondary form may be
preponderance, but there is no predilection for race. due to traumatic injury, surgery (including but not limited to the
shoulder), or other causes for which shoulder was immobilized.
Frozen shoulder is a condition characterized by pain and
global restriction of movement with loss of external rotation. Address for correspondence: Dr. S Saradha,
It clinically categorized into three stages. Department of Pharmacology, Chettinad Hospital and Research
Institute, Chennai, Tamil Nadu, India.
Stage I: Patients could not actively move their shoulder due to E‑mail: [email protected]
acute pain, but full range of passive movements was possible.

This is an open access article distributed under the terms of the Creative Commons
Access this article online Attribution-NonCommercial-ShareAlike 3.0 License, which allows others to remix, tweak,
Quick Response Code: and build upon the work non-commercially, as long as the author is credited and the new
Website: www.jcpconline.org creations are licensed under the identical terms.

For reprints contact: [email protected]

How to cite this article: Chokkalingam M, Saradha S, Navitha A, Nayar PG.

DOI: 10.4103/JCPC.JCPC_17_17 Incidence and clinical profile of patients with frozen shoulder after cardiac
surgery. J Clin Prev Cardiol 2017;6:142-6.

142 © 2017 Journal of Clinical and Preventive Cardiology | Published by Wolters Kluwer - Medknow
[Downloaded free from http://www.jcpconline.org on Monday, October 30, 2017, IP: 36.230.120.81]

Chokkalingam, et al.: Frozen shoulder after cardiac surgery

In our experience, there was a correlation between postcardiac Correlation between age and LAM test
surgery patients and frozen shoulder. This study was designed Among 20 patients with positive LAM test, 5% were
to check the hypothesis if cardiac surgery can predispose in ≤30 years of age category, 5% were in 31–45 years
frozen shoulder. category, 30% were in 46–60 years category, and 60% were
in >60 years category [Table 1]. The mean age of LAM
Objectives test positive participants was 61.35 years whereas that of
1. To assess the incidence of frozen shoulder in patients LAM‑negative participants was 51.70 years [Table 2]. Thus,
undergoing cardiac surgery advancing age was a statistically significant risk factor for the
incidence of frozen shoulder.
2. To determine the clinical profile of patients who develop
frozen shoulder after cardiac surgery. Correlation between cardiovascular risk
factors and LAM test
Methods The occurrence of frozen shoulder was significantly associated
It is a cross‑sectional, clinical observational study. This study with the presence of hypertension and diabetes. Of the 37
was done in the Cardiology Department of Chettinad Hospital hypertensive participants, 14 (37.8%) developed frozen shoulder
and Research Institute, Chennai, between August 2015 and whereas only 6 (9.5%) of those without hypertension developed
May 2016. Institutional Human Ethics Committee approval this complication (P < 0.001) [Table 1]. Similarly, diabetics
was obtained before the study was started. also had significantly higher incidence of frozen shoulder as
compared to nondiabetics (32.5% vs. 11.7%, P < 0.001).
All patients above 18 years of age with no history of previous
shoulder problems and who presented for follow‑up till Type of surgery and LAM test
3 months after cardiac surgery were included. Informed Out of 62 patients who underwent coronary bypass
consent was taken from all the participants. One hundred surgery (CABG) with or without valve surgery, 18 (29.0%)
patients fulfilling the above criteria were included in the developed frozen shoulder. This was significantly higher than
study. The data were collected on key variables of interest in patients who underwent isolated valve surgery (2 of 35,
from the respondents by face‑to‑face interview using a 5.7%, P = 0.006) [Table 1].
standardized questionnaire by a trained physician assistant. Correlation between physiotherapy follow-up
The questionnaire included the demographic data of the
and LAM test
patient, symptoms of frozen shoulder, details of comorbid
In patients who had undergone regular physiotherapy, only
diseases such as diabetes, hypertension and dyslipidemia,
14% developed frozen shoulder and 86% did not develop
type of cardiac surgery, number of postoperative visits, and
the frozen shoulder. In contrast, 33% of those who did not
regularity of physiotherapy follow‑up. have regular physiotherapy follow‑up developed frozen
Respondents presenting with pain and restricted movement shoulder (P = 0.013) [Table 1].
of shoulder joint with positive limitation in lateral rotation,
Independent predictors for postoperative
abduction, and medial rotation (LAM) test were considered as
frozen shoulder
having frozen shoulder.
A multivariate analysis was performed to identify the independent
Follow‑up to physiotherapy was categorized into regular, predictors for the risk of developing postoperative frozen shoulder
irregular, and no follow‑up. The study participants were [Table 3]. Age, diabetes, hypertension, type of surgery (i.e.,
followed up for 3 months post operatively. CABG or not), and regularity of the physiotherapy follow‑up
were included as independent variables. Of these risk factors,
Statistical analysis only hypertension and physiotherapy regularity were found to
Data collected was expressed as actual numbers and have a trend toward a significant independent association with the
percentages. The statistical significance was calculated using occurrence of frozen shoulder (P = 0.090 and 0.097, respectively).
Mann–Whitney U‑test and Pearson’s Chi‑square test to check
the significance between the incidence of frozen shoulder
Discussion
after cardiac surgery in comparison with the regularity Idiopathic frozen shoulder is a self‑limiting regional skeletal
of physiotherapy follow‑up and associated comorbidities. problem of unknown etiology. Clinically, patients first
Multivariate logistic regression analysis was performed to experience a phase of pain, progressing to a freezing stage
when glenohumeral motion is lost, followed by a thawing
study the independent predictors of the development of frozen
phase when pain gradually subsides and most of the lost
shoulder after a cardiac surgery.
motion returns.
Results The common risk factors include diabetes, old age,
The mean age of the study participants was 53.63 ± 13.03 years postoperative period, especially after cardiac surgery and
and 65% were males; 40% had diabetes and 37% had postpacemaker implantation.
hypertension. Of the 100 participants , 20 (20%) developed Frozen shoulder begins with an early phase of pain which
frozen shoulder [Table 1]. eventually leads to stiffness. This suggests that there is an

Journal of Clinical and Preventive Cardiology ¦ Volume 6 ¦ Issue 4 ¦ October-December 2017 143
[Downloaded free from http://www.jcpconline.org on Monday, October 30, 2017, IP: 36.230.120.81]

Chokkalingam, et al.: Frozen shoulder after cardiac surgery

Table 1: Association between various parameters and LAM test

Parameters LAM test Mann–Whitney
Negative (80) Positive (20) U‑test
Count Percentage Count Percentage Z P
Sex
Male 52 65.00 13 65.00 0.000 1.000
Female 28 35.00 7 35.00
Age (years)
≤30 6 7.50 1 5.00 −2.557 0.011
31-45 17 21.25 1 5.00
46-60 34 42.50 6 30.00
>60 23 28.75 12 60.00
Diabetes
Absent 53 66.25 7 35.00 −2.539 0.011
Present 27 33.75 13 65.00
Hypertension
Absent 57 71.25 6 30.00 −3.400 0.001
Present 23 28.75 14 70.00
Dyslipidemia
Absent 73 91.25 18 90.00 −0.499 0.618
Present 7 8.75 2 10.00
Type of surgery
CABG 40 50.00 16 80.00 −2.198 0.028
MVR 20 25.00 2 10.00
AVR 9 11.25 0 0
DVR 4 5.00 0 0
CABG + AVR 2 2.50 1 5.00
CABG + MVR 2 2.50 1 5.00
Others 3 3.75 0 0
Number of visits −0.960 0.337
≤5 41 51.25 13 65.00
6-10 25 31.25 4 20.00
>10 14 17.50 3 15.00
Physiotherapy follow‑up −2.498 0.013
Regular follow‑up 61 77.22 10 50.00
Irregular follow‑up 18 22.78 9 45.00
No follow‑up 0 0 1 5.00
LAM=Limitation in Lateral rotation, abduction and medial rotation, CABG=Coronary artery bypass graft, MVR=Mitral valve replacement,
AVR=Aortic valve replacement, DVR=Double valve replacement

Table 2: Correlation between age and LAM test Codman in 1934, described a diagnostic criterion comprising
LAM test (mean±SD) Independent samples t‑test of idiopathic onset, painful restriction of all glenohumeral
Negative Positive t P movements with limitation of flexion, and external rotation
Age 51.70±12.66 61.35±11.85 −3.086 0.003* with a normal radiograph.[6]
*P<0.05 is considered as statistically significant. SD=Standard In our study, 20% of the study population developed frozen
deviation, LAM=Lateral rotation, abduction, and medial rotation shoulder. In a previous study from the United States, Tuten
et al. demonstrated a higher incidence (33%) of adhesive
inflammatory response which later evolves into a fibrotic capsulitis of the shoulder in male postcardiac surgery
reaction.[4] Currently accepted theory is that there is an initial patients.[7]
active fibroblastic proliferation with subsequent transformation
Age appeared to be an important risk factor for frozen shoulder
of fibroblasts to myofibroblasts.[4,5] This causes an inflammatory
in our study as the incidence of frozen shoulder increased with
contracture of the shoulder, decrease in the capsular volume,
increasing age. However, there was no gender predilection.
and restriction of the glenohumeral movements.[3] The role
of matrix metalloproteinases in the construction of the Adhesive capsulitis or frozen shoulder is considered to be one of
extracellular matrix and in the various cytokines that control the long‑term complications of diabetes. While the prevalence
collagen deposition has also been described. of frozen shoulder is only 2% in the general population, it is

144 Journal of Clinical and Preventive Cardiology ¦ Volume 6 ¦ Issue 4 ¦ October-December 2017
[Downloaded free from http://www.jcpconline.org on Monday, October 30, 2017, IP: 36.230.120.81]

Chokkalingam, et al.: Frozen shoulder after cardiac surgery

Table 3: Independent predictors of frozen shoulder incidence in this study

Predictor variable B SE Wald df P Exp (B) 95% CI for Exp (B)
Lower Upper
Age 0.036 0.034 1.136 1 0.287 1.037 0.970 1.107
Diabetes 0.214 0.709 0.091 1 0.762 0.807 0.201 3.238
Hypertension 1.073 0.633 2.871 1 0.090 2.925 0.845 10.122
CABG 1.168 0.933 1.568 1 0.210 3.216 0.517 20.021
Regular physiotherapy 0.980 0.591 2.748 1 0.097 2.664 0.836 8.484
Constant −3.027 2.208 1.879 1 0.170 0.006
SE=Standard error, CI=Confidence interval, CABG=Coronary artery bypass graft

reported to occur in 10%–29% of those with diabetes. Studies • Long‑term outcomes were not evaluated as the patients
have shown that adhesive capsulitis is caused by glycosylation were followed up only for 3 months postcardiac surgery.
of the collagen within the shoulder joint triggered by the
presence of high blood sugars.[8] Adipose tissue may also have Conclusion
a role to play in these patients. Adipocytes secrete proteins and It can be concluded that cardiac surgery increases the
cytokines such as tumor necrosis factor alpha and interleukin‑6 chances of development of frozen shoulder during the early
resulting in overproduction of other proinflammatory cytokines, postoperative period. Older age, presence of diabetes and
which in turn exacerbate inflammation. Chronic inflammation, hypertension, type of cardiac surgery, and the regularity of
production of free fatty acids from adipocytes, increased physiotherapy follow‑up are important risk factors for the
expression of synovial vascular endothelial growth factor result development of frozen shoulder postcardiac surgery. Regular
in persistence of inflammation and limited disease resolution.[9‑12] follow‑up with continuous physiotherapy after cardiac surgery
Consistent with these results, we also found a significantly may be helpful in reducing the incidence of frozen shoulder in
higher incidence of frozen shoulder among diabetics. the early postoperative period.
Among the different types of cardiac surgeries, CABG was
Acknowledgment
associated with significantly greater risk of causing frozen
All the authors are thankful to Chettinad Hospital and
shoulder as compared to other forms of cardiac surgeries.
Research Institute and Professor S Govindaraju for his
The underlying mechanism for this association is difficult to
statistical assistance.
explain but may be related to the differences in age and the
prevalence of other risk factors such as diabetes. Financial support and sponsorship
Patients in the postoperative period tend to restrict the Nil.
movement of upper limbs due to fear of pain, which tends
to precipitate the development of frozen shoulder. Therefore, Conflicts of interest
physiotherapy plays a vital role during this period. In our There are no conflicts of interest.
study, the regularity with which the patient attends the
follow‑up sessions for physiotherapy was categorized as References
regular, irregular, and no follow‑up. Regular physiotherapy 1. Duplay E. De la periarthritescapulo‑humérale et des raideurs
was associated with significantly lower risk of developing de l`épaule qui ensont la conséquence. Arch Gen Med
frozen shoulder with 76% of LAM score negative participants 1872;20:513‑42.
being in the regular follow‑up group. 2. Manske RC, Prohaska D. Diagnosis and management of adhesive
capsulitis. Curr Rev Musculoskelet Med 2008;1:180‑9.
Thus, it may be suggested that regular postoperative 3. Robinson CM, Seah KT, Chee YH, Hindle P, Murray IR. Frozen
physiotherapy to the upper limbs should be insisted to the shoulder. J Bone Joint Surg Br 2012;94:1‑9.
patients by the medical and paramedical personnel as it can 4. Hand GC, Athanasou NA, Matthews T, Carr AJ. The pathology
prevent the development of frozen shoulder in the immediate of frozen shoulder. J Bone Joint Surg Br 2007;89:928‑32.
postoperative period. 5. Bunker TD, Anthony PP. The pathology of frozen shoulder.
A dupuytren‑like disease. J Bone Joint Surg Br 1995;77:677‑83.
Early diagnosis with prompt referral and treatment may
6. Codman EA. The Shoulder: Rupture of the Supraspinatus Tendon
prevent progression to chronic, treatment‑resistant adhesive
and Other Lesions in or about the Subacromial Bursa. Thomas
capsulitis. When diagnosed early, it can be treated by Todd; 1934..
application of heat to the affected area, giving nonsteroidal 7. Tuten HR, Young DC, Douoguih WA, Lenhardt KM,
anti‑inflammatory drugs and intra‑articular corticosteroid Wilkerson JP, Adelaar RS. Adhesive capsulitis of the
injections. Physiotherapy and stretching exercises can widen shoulder in male cardiac surgery patients. Orthopedics
the range of the shoulder movement. 2000;23:693‑6.
8. Tighe CB, Oakley WS Jr. The prevalence of a diabetic
Limitations condition and adhesive capsulitis of the shoulder. South Med J
• Small sample size limits our study; due to time 2008;101:591‑5.
constraint, we had to stop enrollment. 9. Sugimoto R, Enjoji M, Nakamuta M, Ohta S, Kohjima M,

Journal of Clinical and Preventive Cardiology ¦ Volume 6 ¦ Issue 4 ¦ October-December 2017 145
[Downloaded free from http://www.jcpconline.org on Monday, October 30, 2017, IP: 36.230.120.81]

Chokkalingam, et al.: Frozen shoulder after cardiac surgery

Fukushima M, et al. Effect of IL‑4 and IL‑13 on collagen 11. Glass CK, Olefsky JM. Inflammation and lipid signaling in the
production in cultured LI90 human hepatic stellate cells. Liver etiology of insulin resistance. Cell Metab 2012;15:635‑45.
Int 2005;25:420‑8. 12. Kanter JE, Kramer F, Barnhart S, Averill MM,
10. Kaviratne M, Hesse M, Leusink M, Cheever AW, Davies SJ, Vivekanandan‑Giri A, Vickery T, et al. Diabetes promotes
McKerrow JH, et al. IL‑13 activates a mechanism of tissue an inflammatory macrophage phenotype and atherosclerosis
fibrosis that is completely TGF‑beta independent. J Immunol through acyl‑CoA synthetase 1. Proc Natl Acad Sci U S A
2004;173:4020‑9. 2012;109:E715‑24.

146 Journal of Clinical and Preventive Cardiology ¦ Volume 6 ¦ Issue 4 ¦ October-December 2017