Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:

A Case Control Series Study among Iraqi People at Mosul City

Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis

(A Case Control Series Study among Iraqi People at Mosul City)
*Dr. Ali Salah Fadhil, MBChB-CABM, Lecturer in Internal Medicine
Department of medicine, Nineveh College of Medicine, University of Mosul
**Dr. Fakhir Yousif Hussain , MBChB-FIBMS
Assist. Prof. in Internal Medicine, Department of Medicine, College of Medicine,
University of Mosul
***Dr. Sulieman Ahmad Salow , MBChB, Nineveh health directorate
Abstract
Objective: The aim of this study was to evaluate type 2 diabetes mellitus as a risk
predictor of Knee Osteoarthritis (OA). Design: A case control series study. Setting:
The present study had the approval from regional research committee of Nineveh
Health Directorate, and the scientific research committee of Collage of Medicine,
University of Mosul, Mosul, Iraq. The current study was performed during the period
between Nov.1st, 2011 and Jun.1st, 2012 at Al-waffaa health center for diabetes
researches and management, and at the rheumatology outpatient clinic at Ibn Sina
teaching hospital. Patients and methods: The study was conducted on 65 patients;
known cases of type 2 diabetes mellitus, whose ages range between 40 - 50 years old
were randomly enrolled in the study. Another group consists of 65 patients non
diabetics, matched for age with the patients group, and was kept as control group.
Both studied groups were subjected to measurement of fasting blood sugar (FBS) and
HbA1c was done for patients group to evaluate glycemic control. X-ray examination
of both knees were obtained for both groups and taken in standing position (stress
position), the findings were recorded according to the severity of osteoarthritis found
on examination. Results: The data obtained from the study revealed that there is a
significant difference, regarding knee joint space narrowing grading: grade 1 JSN (Joint
Space Narrowing) was higher in diabetic group than non diabetic one, while grade 2 and
grade 3 JSN were noted to occur only in diabetic group. Diabetic group patients have high
numbers of osteophytes in grades 1, 2, 3 and 4. Diabetic patients have high numbers of
subchondral sclerosis than non-diabetic ones. Conclusion: There was a positive correlation
between diabetes mellitus type 2 and osteoarthritis of the knee joint, in other ward Type 2
diabetes predicts the development of severe OA of the knee independent of age and other
known risks for OA. Our findings strengthen the concept of a strong metabolic component in
the pathogenesis of OA.

Tikrit Medical Journal 2013;19(2): 325-338 523

Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City
Introduction
Diabetes mellitus (DM) affects
connective tissues in many ways and
causes different alterations in
periarticular and skeletal system
(Arkkila and Gautier, 2003).
Several musculoskeletal
disorders have been described in
diabetic patients those can be divided
into three categories:
A. disorders which represent
intrinsic complications of diabetes,
such as limited joint mobility or
diabetic cheiroarthropathy, stiff hand
syndrome, and diabetic muscular
infarction.
B. disorders with an increased
incidence among diabetics, such as
Dupuytrens disease, shoulder
capsulitis, neuropathic arthropathy,
osteopenia (in type 1 DM), flexor
tenosynovitis, septic arthritis, acute
proximal neuropathy, proximal motor
neuropathy, pyomyositis and the
diffuse idiopathic skeletal hyperostosis
(DISH) syndrome.
C. The disorders those possibly
associated with diabetes have been
proposed but not proven yet, such as
osteoarthritis and the carpal tunnel
syndrome (Arkkila and Gautier, 2003).
Arthritis is among the leading
causes of disability, and osteoarthritis
(OA) is the most common type of
arthritis (Kremers H& Gabriel S,
2005).
Osteoarthritis is the most
common cause of musculoskeletal
disability and it is one of the most
common joint disorders in the elderly
(Flatharta et al., 2006).
It is now understood that OA is
a disorder of the whole joint organ and
not just the cartilage. At the
macroscopic level, the key
characteristics of an OA joint are
swelling, fibrillation, erosion and
eventual loss of articular cartilage,
523 Tikrit Medical Journal 2013;19(2): 325-338
together with the remodeling of
underlying bone resulting in
subchondral sclerosis, bone cysts, an
increase in metaphyseal bone and the
development of osteophytes (Felson et
al., 2000).
The end point of OA is
eburnation, in which the focal loss of
cartilage at the articulating surface of a
bone reaches the stage where the
underlying bone exposed and subjected
to increasingly localized overloading
soft- tissue structures in and around the
joint are also affected (Dawson et al.,
2004) these structures include
synovium, which undergo modest
inflammatory infiltrates; ligaments,
which are often lax; and bridging
muscle, which become week (Brandit,
2010).
Knee OA, the most frequent
form of lower extremity OA, was the
primary diagnosis for 430,000 hospital
discharges and 14 billion dollars of
hospital charges in the 2004 US
(Dillon et al., 2006), and 12.1%
(annualized prevalence) of Americans
age 60 years had symptomatic
radiographic knee OA in the 1991–
1994 (Jordan et al., 2007).
One statistic that has been used
extensively to describe person-level
risk is lifetime risk, which is the
probability of developing a condition
over the course of a lifetime. Lifetime
risk has been reported for various
chronic conditions and risk factors,
including coronary heart disease,
hypertension, diabetes, and breast
cancer (Lloyd-Jones et al., 2004).
This measure conveys the risk
of these conditions in terms that are
understandable to both clinical and lay
audiences. The knee is the most
frequently involved joints site
associated with disability in OA
(Andriacchi et al., 2000).
Risk factors such as age ,sex ,
trauma , overuse , genetic , and obesity
can each make contributions to the
Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City

process of injury in different pain , increasing age , decreasing

compartments of the joint ,such risk educational status, obesity , female
factors can serve as initiators that gender , comorbidity , and quadriceps
promote abnormal biochemical muscle weakness ; the role of
processes involving the cartilage , psychosocial factors , notably
bone, and synovium( Abramson and depression and anxiety, is less clear
Attur , 2009) . (Creamer et al ., 2000) .
Disability in knee OA is
influenced by many factors including

Patients, Materials and 5. Gout and pseudo gout crystals.

6. Mal alignment.
Methods 7. Neoplastic conditions.
8. History of operation for
The present study had approval
meniscectomy.
from regional research committee of
Mosul health administration, and the 9. Endocrine disorders (acromegaly,
scientific research committee of thyroid diseases, cushing
Collage of Medicine, University of syndrome).
Mosul, Mosul, Iraq. The study was 10. Age ˃50 years.
performed during the period between Control group
Nov.1st, 2011 and Jun.1s, 2012 at Al- Sixty five females and males,
waffaa health center diabetic research non diabetics, matched for age with the
and management, and in the patients group, were enrolled as control
rheumatology outpatient department at group.
Ibn Sina teaching hospital.
Data collection
Study design; Controlled case series
collection The data were collected directly
from the studied patients by the
Subjects investigator himself during interview
Diabetic patients after obtaining consent.
Sixty five female and male
patients, known to have type 2 diabetes Methods
mellitus (according to American After an overnight fasting both of
diabetes association criteria) registered the patients and control groups, were
in Al-waffaa center, whose ages range subjected to the following biochemical
between 40 - 50 years were randomly and radiological assessment:
enrolled in the study.
Biochemical profile measurements
Inclusion criteria Fasting blood sugar (FBS) was
done for control group to exclude
Diabetic patients whose ages range diabetes, while in patients group FBS
between 40 - 50 years old. and HbA1c were done to evaluate
glycemic control. The World Health
Exclusion criteria
Organization definition of diabetes is
1. History of trauma. for a single raised glucose reading with
2. Inflammation: Local and Systemic symptoms, otherwise raised values on
inflammatory condition. two occasions, of either (Valdez,
3. History of previous local injection. 2009).
4. Blood diseases.
Tikrit Medical Journal 2013;19(2): 325-338 523
Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City
 fasting plasma glucose ≥ 7.0
mmol/l (126 mg/dl) or
 with a glucose tolerance test,
two hours after the oral dose a
plasma glucose ≥ 11.1 mmol/l
(200 mg/dl)
A glycated hemoglobin (HbA1c) of
greater than 6.5% is another method of
diagnosing diabetes as is a random
blood sugar of greater than 11.1
mmol/l (200 mg/dL) in association
with typical symptoms (Knowler et al.,
2002).
The biochemical profiles were
performed at the laboratory of Ibn
Sina Teaching Hospital.
Standard kits were used to
measure biochemical profiles
suggested in this study; tests performed
and interpreted following instructions
outlined in each kit.
Clinical and Radiological
examination
Both groups were subjected to X-
ray examination of both knees in
standing position, and the findings
were recorded according to the severity
of osteoarthritis found in the
examination.
Results
Table (1) shows the ages, FBS
and HbA1c of all studied groups.
There was no statistically significant
difference between the age groups.
523 Tikrit Medical Journal 2013;19(2): 325-338
The criteria for OA (ACR) of
the knee include the presence of knee
pain plus at least three of the following
characteristics:
• Age greater than 50 years
• Morning stiffness lasting less than 30
minutes
• Crackling or grating sensation
(crepitus)
• Bony tenderness of the knee
• Bony enlargement of the knee
• No detectable warmth of the joint to
the touch (Hiadari, 2011).
Statistical Analysis
Standard statistical methods
used to determine the mean and
standard deviation. Paired t-test and
two sample t-test were used to compare
the results of various parameters
among the studied groups. Linear
regression analysis (Person Correlation
Coefficients) (r) was performed for
finding the degree of association
between different parameters.
Some values expressed as
Mean ± SD and P value of <0.05 was
considered to be statistically
significant.
FBS of the control subjects is within
normal range, while those of diabetic
patients is high when compared with
the control group (P= 0.001).
Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City

Table (1): The Ages, FBS of the studied groups, and HbA1c of diabetic patients.
Data expressed as Mean±SD.

Parameters Control (N=65) Diabetics (N=65) P. value

Age (in years) 44.5±3.42 45.4±3.13 0.214

FBS(mmol/l) 5.61±0.77 10.0±4.18 0.001

HbAIc --- 8.3±1.70 ---

Table (2) shows the results of the grading of right knee joint space narrowing
(JSN) in both groups. Grade 1 JSN was higher in diabetic group, while grade 2 and
grade 3 JSN was only observed in diabetic group.

Table (2): The X-Ray finding of the right knee joint of both studied groups.
Data expressed as number and percentage

Control ( N=65) Diabetic (N=65)

Grade of JSN P. value
No. % No. %

Grade 0 38 58.5 10 15.4 0.001

Grade 1 27 42.5 39 60.0 0.001

Grade 2 0 0.0 13 20 0.032

Grade 3 0 0.0 3 4.6 0.244

Table (3) shows the results of the grading of left knee joint narrowing space in
both groups .There is a significant differences, grade 1 JSN was higher in diabetic
group, while grade 2 and grade 3 JNS were only in diabetic group.

Tikrit Medical Journal 2013;19(2): 325-338 523

Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City

Table (3): The X-Ray finding (JSN) of the left knee joint of both studied
groups .Data expressed as number and percentage.

Control (N =65) Diabetic (N=65)

Grade of JSN P. value
No. % No. %

Grade 0 39 60.0 7 10.8 0.001

Grade 1 26 40.0 42 64.6 0.001

Grade 2 0 0.0 13 20.0 0.032

Grade 3 0 0.0 3 4.6 0.244

Table (4) shows the presence of the osteophyte of right knee joint in both
groups. Diabetic group patients have high numbers of osteophytes in grades 1, 2, 3
and4.

Table (4): The X-Ray finding (osteophytes) of the right knee joint
Of both studied groups .Data expressed as number and percentage

Control (N=65) Diabetic (N=65)

Grade of
P. value
osteophytes
No. % No. %

Grade 0 54 83.1 40 61.5 0.005

Grade 1 11 16.9 16 24.6 0.278

Grade 2 0 0.0 5 7.7 0.020

Grade 3 0 0.0 2 3.1 0.496

Grade 4 0 0.0 2 3.1 0.496

Table (5) shows the presence of the osteophyte of left knee joint in both
groups. Diabetic group patients have high numbers of osteophytes in grades 1, 2, 3
and4.

553 Tikrit Medical Journal 2013;19(2): 325-338

Type 2 Diabetes Mellitus As a Risk Predictor for Knee Osteoarthritis:
A Case Control Series Study among Iraqi People at Mosul City

Table (5): The X-Ray finding (osteophytes) of the left knee joint of both studied
groups .Data expressed as number and percentage.

Control (N=65) Diabetic (N=65)

Grade of
P. value
osteophytes
No. % No. %

Grade 0 57 87.7 38 58.5 0.001

Grade 1 8 12.3 19 29.2 0.278

Grade 2 0 0.0 4 6.2 0.020

Grade 3 0 0.0 2 3.1 0.496

Grade 4 0 0.0 2 3.1 0.496

Table (6) shows the correlation between FBS and joint narrowing space of left
side (JSNL) in the studied groups, there are a statistically significant positive
correlation (p = 0.001, and 0.003) respectively.

Tikrit Medical Journal 2013;19(2): 325-338 553

 Tikrit Medical Journal 2013;19(2): 325-338
Table (6): The correlation between FBS and JSN in the studied groups. Data expressed as
Mean±SD.
The side FBS
(in millimeter)
Left knee 7.86±3.71
Right knee 7.86±3.71
Discussion
Several studies have reported an
association of early OA and diabetes. Both
large and small joint OA have been reported
to be increased in type 2 diabetes. However,
OA of the weight-bearing joints in type 2
diabetic patients may be related to their
obesity and not to the diabetes itself. It is not
yet known whether diabetes is a risk factor
for OA independent of obesity (Kim et al.,
2001).
The current study involved 130
individuals divided into two groups of 65
individuals. The study was designed to
investigate the prevalence of knee
osteoarthitis in patients with type 2 diabetes
mellitus in comparison with non diabetic
patients. Sixty five patients type 2 diabetics,
regularly followed up at the Al- Waffa
Center for Diabetes management and
research in Mosul, were enrolled in the
study. The mean age of the patients was
45.4±3.13 years and the mean duration of
the diabetes disease was 10.1 years.
Sixty five apparently healthy, non
diabetic subjects their mean age 44.5±3.42
years were enrolled as control group.
The groups were matched concerning
the number and their ages as confirmed
statistically by the absence of significant
552
JSN P. value
r
0.79±0.71 0.252 0.001
0.77±0.71 0.259 0.003
differences between the studied groups. This
matching of individual groups number, and
age may exclude any effect of these
parameters on the results of the study.
The diabetic patients in our study were
uncontrolled chronic patients, and the FBS
reported among such patients were high as
compared with the controls 10.0±4.18;
5.61±0.77 mmol/l respectivlly (Table 1).
Higher levels of FBS in patients with
diabetes are thought that they have poor
glycemic control, and will lead to cellular
damage and are ultimately responsible for
the complications of diabetes (Guerci et al.,
2001) , including nephropathy, retinopathy,
neuropathy and macro and microvascular
damage (Salman ,2004).
The data obtained in the present study
which demonstrated high uncontrolled level
of FBS was in agreement with the data
reported in the majority of the previous
studies ( Cagliero ,2003).
Higher level of glucose was observed
among IDDM and NIDDM patients (13.4,
11.1 mmol/l, respectively) compared to
control group (4.8 mmol/l)( Cagliero
,2003),measured FBS in 2 types of diabetic
patients, newly diagnosed type 2 patients
and patients on oral hypoglycemic agents.
Both types of diabetic patients showed
higher FBS (198 mg/dl for newly diagnosed
and 185 mg/dl for the oral hypoglycemic
 Tikrit Medical Journal 2013;19(2): 325-338
group) compared to control group (90
mg/dl).
High FBS, was also reported by (Mark
et al., 2008) who demonstrated FBS of
205.47 mg/dl for the diabetic patients and
96.95 mg/dl for controls. In other study
which evaluated glycemic state of the
diabetic patients by measuring FBS and
HbA1C. Both parameters were identified
higher than those identified in the control
group (Orozco et al., 2008).
The elevated FBS in the diabetic
patients demonstrated in the present study
may add some light on the fact that the
majority of prolonged duration of diabetic
with uncontrolled FBS may contribute to the
appearance of diabetic complications. The
existence of a significant positive correlation
between FBS and osteoarthritis (JSN and
osteophyte) in both knee joints of diabetic
group is an indicator of the probable effect
of diabetes in the occurrence of
osteoarthritis.
Diabetes is widely known to induce
metabolic derangement leading to oxidant-
antioxidant imbalance (Davis et al., 2009).
The increase in oxidative stress may
probably be related to the abnormal
metabolic milieu such as hyperglycemia,
dyslipidemia, and elevated free fatty acids,
which commonly occur in patients who have
diabetes and less than perfect glycemic
control (Gorman & Krook 2011).
Hyper-glycemia may lead to an
increased generation of free radicals via
multiple mechanisms such as glucose auto
oxidation, non-enzymatic glycation, the
polyol pathway and reduced antioxidant
defense system (Davis et al., 2009).
The pathophysiology of these
disorders in diabetic patients is not obvious.
It could be associated with connective tissue
disorders, such as the formation of
abnormally glycosylated end products or the
impaired degradation of byproducts, it could
be indirectly related to the vasculopathy and
neuropathy commonly complicating the
primary disease, or finally, it could be
attributed to a combination of factors
(Douloumpakas et al.,2012) .
A study done by (Andrianakos et al.,
2006), the prevalence of osteoarthritis in
type 2 diabetic patients was found to be
significantly higher than the estimated
prevalence in the general population. In a
large study on osteoarthritis including 1026
patients, the mean fasting glucose
concentration was higher in subjects with
osteoarthritis (OA) than in subjects without
OA (Cimmino and Cutolo ,1990).
Diabetes was observed to be
accompanied by an increased production of
free radicals and/or impaired antioxidant
defense capabilities, indicating a central
contribution for reactive oxygen species in
the onset, progression and pathological
consequences of disease (Anabela and
Carlos, 2006).
The results of our study may be
explained by motor and sensory dysfunction
of muscle may be important factors in the
pathogenesis of articular damage.
It is well accepted fact that patients
with OA have muscle weaknesses and a
vibratory sense loss in the regional OA joint.
Interestingly, this neurological dysfunction
is present locally and throughout the body,
suggesting a generalised alteration of the
peripheral nervous system. Two main
neurological syndromes have been described
in diabetes.
The first is the Charcot
neuroarthropathy, a rare but devastating
complication leading to joint deformity and
eventually amputation or secondary OA.
The second is a symmetric, mainly sensory
polyneuropathy often accompanied by
autonomic neuropathy. This latter diabetic
neuropathy could be one of the suggested
alterations of the peripheral nervous system
seen in patients with OA leading to muscle
555
 Tikrit Medical Journal 2013;19(2): 325-338

weaknesses and joint laxity (Berenbaum, Scientific Understanding

2011).
of Osteoarthritis, Arthritis
This speculates that such peripheral
nerve impairment induced by diabetes could Research &Therapy.
be an added risk factor for OA in patients
Vol.11:227
with diabetes.
 American Academy of
Conclusion; Knee joint space narrowing
grade 1 was higher in diabetic group than Orthopedic Surgeons
non diabetics, while grade 2 and grade 3 (2004) Osteoarthritis of
JSN were noted to occur only in diabetic
patients also diabetic patients have high the knee: State of the
numbers of osteophytes in grades 1, 2, 3and condition.
4, these findings strengthen the concept of a
strong metabolic component in the  American Diabetes Association,
pathogenesis of OA hence, we can consider (2000). Type 2 diabetes in
Type 2 DM as a predictor for the
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independent of age and other known risks Pediatrics; 105 (3):671-
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680.
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 Andriacchi TP, Lang PL,
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‫الخالصة‬

‫إٌ انٓذف يٍ ْذِ انذراسخ ْٕ يعزفخ اَزشبر انزٓبة يفظم انزكجخ انسٕفبَ‪ ٙ‬نذٖ انًزضٗ انًظبث‪ ٍٛ‬ثذاء انسكز يٍ‬
‫انًُط انثبَ‪ٔ ٙ‬ثبنزبن‪ ٙ‬رحز٘ طالح‪ٛ‬خ كٌٕ داء انسكز يٍ انًُط انثبَ‪ ٙ‬كعبيم خطٕرح اسزقظبئ‪ ٙ‬النزٓبة انزكجخ انسٕفبَ‪.ٙ‬‬
‫أجز‪ٚ‬ذ ْذِ انذراسخ عهٗ ع‪ ُّٛ‬عشٕائ‪ٛ‬خ رزكٌٕ يٍ ‪ 33‬يز‪ٚ‬ض يظبث‪ ٍٛ‬ثذاء انسكز يٍ انًُط انثبَ‪ٔ ٙ‬انذ‪ ٍٚ‬رززأح‬
‫أعًبرْى ث‪ 33-33 ٍٛ‬سُّ‪.‬‬
‫انًجًٕعخ انثبَ‪ٛ‬خ ْٔ‪ ٙ‬انع‪ُٛ‬خ انضبثطخ رزكٌٕ يٍ ‪ 33‬شخض غ‪ٛ‬ز يظبث‪ ٍٛ‬ثذاء انسكز يٍ َفس انفئخ انعًز‪ٚ‬خ ‪.‬‬
‫رى إرسبل جً‪ٛ‬ع األشخبص ٔانًزضٗ انًشبرك‪ ٍٛ‬ف‪ ٙ‬انذراسخ يٍ انًجًٕعز‪ ٍٛ‬ال جزاء فحض َسجخ انسكز ف‪ ٙ‬انذو‬
‫قجم رُبٔنٓى اإلفطبر (‪ٔ )FBS‬فحض (‪ )HbA1c‬نهًجًٕعخ االٔنٗ فقط‪ٔ .‬كذنك رى إرسبنٓى ال جزاء انفحٕص انشعبع‪ٛ‬خ نًفظم‬
‫انزكجز‪ ٍٛ‬ف‪ ٙ‬كال انًجًٕعز‪ٔ ٍٛ‬رى رسج‪ٛ‬م انُزبئج حست ٔجٕد انًؤشزاد انذانخ عهٗ ٔجٕد سٕفبٌ انزكجخ‪.‬‬
‫اسزخهظذ انذراسخ ٔجٕد عالقخ ا‪ٚ‬جبث‪ ّٛ‬ث‪ ٍٛ‬داء انسكز يٍ انًُط انثبَ‪ٔ ٙ‬انزٓبة يفظم انزكجخ انسٕفبَ‪ ٙ‬يًب ‪ٚ‬ؤ‪ٚ‬ذ‬
‫ٔجٕد عالقخ ا‪ٚ‬ض‪ٛ‬خ جذن‪ٛ‬خ قٕ‪ٚ‬خ ٔراء انزغ‪ٛ‬زاد انًزقذيخ النزٓبة يفظم انزكجخ انسٕفبَ‪ٔ ٙ‬يٍ ْذا ‪ًٚ‬كٍ اقزاح داء انسكز يٍ‬
‫انًُط انثبَ‪ ٙ‬كعبيم خطٕرح ‪ًٚ‬كٍ يٍ خالنّ رٕقع احزًبن‪ٛ‬خ حظٕل انزٓبة يفظم انزكجخ انسٕفبَ‪ ٙ‬ثعذ عزل كم يٍ عبيم رقبدو‬
‫انعًز ٔعٕايم انخطٕرح االخزٖ انز‪ ٙ‬اسزثُزٓب انذراسخ نزظٕ‪ٚ‬ت انُزبئج‪.‬‬

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