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Braz J Oral Sci. January/March 2008 - Vol. 7 - Number 24
Oral signs and salivary parameters as
indicators of possible osteoporosis and
osteopenia in postmenopausal women -
A study of 45 subjects
Siva Reddy1
Ramalingam Karthikeyan2
Herald Justin Sherlin2
Natesan Anuja2
Ramani Pratibha3
Premkumar Priya3
Thiruvengadam Chandrasekar4
1Postgraduate Student
2Senior Lecturer
3Assistant Professor
4Professor and Head, Department of Oral
Pathology, College of Dental Surgery, Saveetha
University, Chennai, Tamil Nadu, India
Received for publication August 08, 2007
Accepted - April 07, 2008
Correspondence to:
Pratibha Ramani
Department of Oral Pathology,
College of Dental Surgery, Saveetha University,
162, PH Road, Velappanchavadi, Chennai –
600077.
Phone: + 91 9841414603
Fax: + 9144-26800892
Email: dr_pratibha@rediffmail.com
Abstract
Aim: To correlate the oral signs, salivary calcium, phosphorus, alkaline
phosphatase levels and dental radiographic findings in postmenopausal
osteoporotic, osteopenic and non-osteoporotic women. Materials and
Methods: Forty-five subjects were selected based on bone mineral
density (BMD) analyses and were assigned to 3 groups (n=15): Group
1 - established osteoporotic women; Group II - established osteopenic
women; Group III (control) - non-osteoporotic women. Complete oral
and radiographic examination, saliva collection and analysis of calcium,
phosphorus and alkaline phosphatase were performed. Results: The
results were tabulated and analyzed for statistical significance using
the Mann-Whitney U-test. There was statistically significant difference
(p<0.05) in salivary calcium, phosphorus and alkaline phosphatase
levels when osteoporotic and osteopenic women were compared to
the controls. Conclusion: Salivary parameters can be used as indicators
to aid in the diagnosis of osteoporosis and osteopenia in
postmenopausal women.
Key words:
osteoporosis, osteopenia, salivary alkaline phosphatase
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Braz J Oral Sci. 7(24):1508-1512 Oral Signs and Salivary Parameters as Indicators of Possible Osteoporosis and Osteopenia in Postmenopausal Women - A Study of 45 Subjects
Introduction
Osteoporosis is a chronic systemic skeletal disease
characterized by low bone mass and micro-architectural
deterioration, resulting in increased bone fragility and
susceptibility to fracture. The World Health Organization
(WHO) has defined osteoporosis and osteopenia based on
normal bone mineral density (BMD). In the United States,
osteoporosis affects more than 25 million people and
predisposes patients to more than 1.3 million fractures
annually1.
Women are at greater risk for osteoporosis after menopause.
Premenopausal estrogen levels are protective, as is hormone
replacement therapy2-4. Early menopause, either naturally
occurring, drug or surgically induced without hormone
replacement therapy predisposes to osteoporosis5.
Data suggest that panoramic radiograph findings, such as
progressive periodontal disease, alveolar bone resorption,
tooth loss and endosteal resorption of the mandibular inferior
cortex, may indicate general osteoporosis. If low BMD can
be related to certain oral signs, the possibility of latent
osteoporosis might prompt dentists to refer these patients
for medical evaluation6.
Chemicals in serum and urine can serve as markers for
monitoring bone loss, new bone formation and the
effectiveness of therapy in patients with osteoporosis. A
large number of markers have been discovered for both bone
formation and bone resorption7-9. Over the years, several
studies have been performed in order to establish methods
for diagnosis or prognosis of oral disease with saliva. The
value of saliva as an indicator of systemic disease has also
been explored10.
The aim of the study was to estimate the salivary calcium,
phosphorus and alkaline phosphatase levels and correlate
the salivary findings, radiographic changes and periodontal
status in osteopenic osteoporotic and healthy
postmenopausal women.
Materials and Methods
The study comprised postmenopausal women aged 45 to75
years recruited from the Outpatient Department of
Orthopedics at Saveetha Medical Hospital, Chennai, Tamil
Nadu, India. After being clinically examined by an orthopedic
surgeon, the patients were assessed for BMD using an
ultrasound densitometer (Furuno CM-100 Nishinomiya,
Japan). According to the WHO, spine BMD is categorized
as follows: Normal: T score is above -1.0; Osteopenic: T
score is between -1.0 to -2.5 and Osteoporotic: T score is
below -2.5. Based on these criteria and according to the BMD
results, 45 subjects were selected and assigned to three
groups. Group I (study group) comprised of 15 established
osteopenic postmenopausal women, aged 45 to75 years,
without any other preexisting systemic diseases, such as
primary or secondary hyperparathyroidism, osteomalacia,
rheumatoid arthritis and multiple myeloma; Group II (study
group) comprised of 15 established osteoporotic
postmenopausal women, aged 45 to 70 years, without any of
the aforementioned systemic diseases; and Group III (control
group) comprised of 15 postmenopausal women, aged 45 to
70 years, without osteopenia or osteoporosis or any of the
aforementioned systemic diseases. The study and control
groups were analyzed for the following parameters:
measurement of mandibular cortical width, Russel’s
periodontal index and salivary parameters, like calcium,
phosphorus and alkaline phosphatase levels.
Panoramic radiographs were obtained by using Kodak T-
mat G/RA, 5x12 inch panoramic dental film. The mandibular
cortical width was measured at the site of mental foramen on
the radiographs, in accordance to Taguchi et al.11-12. Standard
UCLA procedure was used for saliva collection13.
Approximately 5 mL of saliva were collected from each
subject and centrifuged at 2,500 rpm for 5 minutes. The
centrifugation resulted in a saliva sample free of large particle
debris and reduced viscosity, thereby allowing a more
accurate and reproducible analysis. All samples were
subjected to biochemical evaluation. Calcium was estimated
by using a commercially available kit, based on the O-
cresolphthalein complexone method (Crest bio-systems, Goa,
India). Phosphorus was estimated by using a commercially
available phosphorus kit, which functions on the basis of
Gomori’s method. (Crest bio-systems, India). Alkaline
phosphatase was estimated by using a commercially
available alkaline phosphatase kit, which functions on the
basis of Modified Kind & King’s method (Crest bio-systems,
India).
Statistical Analysis
Means and standard deviations of age, menopause,
periodontitis, number of missing teeth, salivary levels of
calcium, phosphorus and alkaline phosphatase, and inferior
mandibular cortical width were calculated for all groups.
Mann-Whitney U test was used for comparisons between
groups (α=0.05).
Results
Tables 1, 2 and 3 present the comparisons between Group I
and Group II, Group I and Group III and Group II and Group
III, respectively.
The parameters of age, postmenopausal time, number of
missing teeth, salivary levels of calcium, phosphorus and
alkaline phosphatase, and inferior mandibular cortical width
were statistically significant comparing the study groups to
the control group. Periodontitis was not statistically
significant in all comparisons.
Regarding age, the osteoporotic, osteopenic and control
groups had mean ages of 63.73, 60.33 and 51.26 years,
respectively. There was a significant increase of age in
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Variable Group I Group III p-value
Age (years) 63.73 51.26 0.000
Menopause (years) 13.86 4.86 0.000
Periodontitis (%) 73 53 0.264
Number of missing teeth 8.66 2.4 0.000
Calcium (mg/dL) 7.80 4.57 0.000
Phosphorus (mg/dL) 12.94 8.66 0.001
Alkaline phosphatase (K.A. Units) 3.8 1.47 0.000
Inferior mandibular
cortical width (mm) 4.33 5.03 0.007
Table 2 – Mean values and respective comparisons (Mann
Whitney U-test) between Group I (osteopenic
postmenopausal women) and Group III (control women)
Variable Group II Group III p-value
Age (years) 60.33 51.26 0.000
Menopause (years) 11.33 4.86 0.000
Periodontitis (%) 60 53 0.723
Number of missing teeth 6.6 2.4 0.002
Calcium (mg/dL) 7.36 4.57 0.000
phosphorus (mg/dL) 11.89 8.66 0.001
Alkaline phosphatase (K.A. Units) 3.81 1.47 0.000
Inferior mandibular
cortical width (mm) 4.7 5.03 0.298
Table 3 - Mean values and respective comparisons (Mann
Whitney U-test) between Group II (osteoporotic
postmenopausal women) and Group III (control women)
Variable Group I Group II p-value
Age (years) 63.73 60.33 0.087
Menopause (years) 13.86 11.33 0.446
Periodontitis (%) 73 60 0.113
Number of missing teeth 8.66 6.6 0.213
Calcium (mg/dL) 7.80 7.36 0.346
Phosphorus (mg/dL) 12.94 11.89 0.868
Alkaline phosphatase (K.A. Units) 3.8 3.81 0.105
Inferior mandibular
cortical width (mm) 4.33 4.7 0.164
Table 1 - Mean values and respective comparisons (Mann
Whitney U-test) between Group I (osteopenic
postmenopausal women) and Group II (osteoporotic
postmenopausal women)
osteoporotic and osteopenic group compared to the control
women.
The osteoporotic, osteopenic and control groups showed a
postmenopausal mean duration of 13.86, 11.33 and 4.86 years,
respectively.
Salivary parameters, such as calcium, phosphorus, alkaline
phosphatase levels and oral signs like the periodontal status,
number of missing teeth and inferior mandibular cortical width
were assessed. The normal/standard values mentioned as per
literature were 5.2 mg/dL (1.35 mMol/L) and 17.18 mg/dL (5.5
mMol/L) for salivary calcium and phosphorus, respectively.
No standard values were available for alkaline phosphatase
levels in saliva.
The mean number of missing teeth for the osteoporotic,
osteopenic and control groups was 8.66, 6.6 and 2.4,
respectively. The mean inferior mandibular cortical width in
osteoporotic, osteopenic and control women was of 4.33 mm,
4.7 mm and 5.03 mm, respectively. Salivary calcium levels in
the osteoporotic, osteopenic and control groups showed mean
values of 7.80 mg/dL, 7.36 mg/dL and 4.57 mg/dL. There was a
significant increase in calcium levels of the osteoporotic and
osteopenic patients when compared to the healthy controls.
Salivary phosphorus levels in osteoporotic, osteopenic and
control groups showed mean values of 12.94 mg/dL, 11.33
mg/dL and 8.66 mg/dL, respectively.
Alkaline phosphatase levels in the osteoporotic, osteopenic
and control groups showed mean levels of 3.8, 3.81 and 1.47
K.A.Units, respectively. There was a significant increase in
alkaline phosphatase levels in patients with osteoporosis and
osteopenia when compared to the controls.
Discussion
Osteoporosis and osteopenia are chronic systemic skeletal
diseases characterized by low bone mass and micro-
architectural deterioration with a consequent increase in the
bone fragility and susceptibility to fracture. According to the
WHO, osteoporosis is present when BMD is 2.5 standard
deviations (SD) below the normal value seen in young patients.
Osteopenia is defined as bone density levels are between 1
SD and 2.5 SD below normal BMD.
Density of the jaw bones differs according to the region,
ranging from D1 to D4 where. D1 represents high-density
regions like the anterior mandible and D4 represents low-
density regions like the posterior maxilla. In procedures such
as implant placement and prosthodontics, density of the jaw
bones plays a major role in determining the outcome. There is
evidence that osteoporosis and osteopenia have a direct effect
on jaw bones, resulting in resorption and reduction in density.
The osseointegration between bone and implants could also
be compromised in such cases. Studies have shown that the
generalized osteoporosis has a significant effect on the
periodontal health status, thus compromising tooth support14.
An early diagnosis and intervention strategy may lead to better
treatment outcomes.
Several oral signs, namely alveolar bone resorption15-21,
periodontal condition14,20,22, number of missing teeth 20,23-26,
mandibular BMD measured on oral radiographs14,16-19,27-32,
thickness of mandible on panoramic radiographs6,11-12,20 and
inferior cortex morphology30, have been evaluated in order to
distinguish between normal and osteoporotic population.
Over 50 years ago, Fuller Albright33 noted that postmenopausal
Braz J Oral Sci. 7(24):1508-1512 Oral Signs and Salivary Parameters as Indicators of Possible Osteoporosis and Osteopenia in Postmenopausal Women - A Study of 45 Subjects
1511
women lost excessive amounts of calcium in their urine and
thus introduced biochemical markers into the clinical arena.
Subsequently, a number of markers have been discovered for
both bone formation and bone resorption. Alkaline
phosphatase and osteocalcin serve as markers for bone
formation. Urinary calcium and type I collagen-related peptides
serve as markers for bone resorption7-9.
Common biochemical markers for osteoporosis include
calcium, phosphorus, type I collagen-related peptides, alkaline
phosphatase and osteocalcin, which are routinely assessed
in the blood. Innumerable studies have tried to establish
methods for diagnosis or prognosis of oral disease using
salivary analysis. The value of saliva as an indicator of systemic
diseases, such as autoimmune disorders, cardiovascular,
endocrine, renal and infectious diseases and cancer, has also
been explored10.
Calcium and phosphorus are present as inorganic components
of saliva, which quantitatively accounts as the main mineral
component of the human skeletal system. Some of the alkaline
phosphatase is also secreted into the saliva and may thus
serve as a biochemical marker for bone turnover. The currently
available techniques for in vivo bone mass measurement
techniques are expensive and may not be effective to screen
the general population. Hence, saliva, which is an ultra-filtrate
of plasma, could be used as a simple, efficient, non-invasive
and cost-effective diagnostic resource.
Many studies have attempted to show a causal relationship
between osteoporosis, osteopenia and periodontal disease.
In the present investigation, 73% of the osteoporotic group
and 60% of the osteopenic group were affected by
periodontitis. In a case-control study, Von Wowern et al.14
found significantly greater periodontal attachment loss in
osteoporotic women than in normal women. Elders et al.22
observed no significant correlation between periodontitis and
spinal BMD. Likewise, Kribbs20 did not find significant
difference between the osteoporotic and non-osteoporotic
groups in mean probing depth of pockets or recession from
the cementoenamel plus probing depth, which is a
measurement of periodontal attachment loss.
Studies have shown that age and menopause17,34-36 are the
two main risk factors for osteoporosis and osteopenia in
women. The results of the present study are supportive to
these findings.
In the present study, there was a significant increase in the
number of missing teeth in the study groups compared to the
control group, which suggests that tooth loss might be related
to osteoporosis and osteopenia in postmenopausal women.
Several authors20,23-26 have reported that tooth loss is related
osteoporosis and osteopenia. The relationship between the
cause of tooth loss and the general mineral status is not known.
Tooth loss is caused by multiple factors, such as caries,
periapical and periodontal disease and tooth fracture. Ward
and Mason37 suggested that although osteoporosis may have
no effect on the periodontal status, it may influence the rate of
bone loss in chronic periodontitis. The findings of the present
study are consistent with the current literature, which suggests
that the number of missing teeth is higher in patients affected
by osteoporosis and osteopenia.
There was significant decrease of mandibular cortical
width in osteoporotic women when compared to the control
group. Taguchi et al.11,12 have shown that the mandibular cortical
width was correlated to the mandibular cortical BMD, which
rapidly decreases after the 5th decade of life in women. Kribbs
et al.20 reported that osteoporotic women could not be
distinguished from normal women on the basis of thickness
of the cortex at the angle of the mandible. The mandibular
bone is thicker than other bones in the body, like spine, hip
and femur, which means that the mandible is significantly
affected only by severe bone resorptive conditions, such as
osteoporosis, when compared to less severe conditions, like
osteopenia, as reflected in the present study.
There was a significant increase in phosphorus levels in
osteoporotic and osteopenic women compared to the healthy
controls. Sewon et al.38 reported that there was significantly
increased salivary calcium in the women with low BMD and
no significant difference in phosphate levels. However, our
study showed significantly increased levels of calcium and
phosphorus between osteoporotic and osteopenic groups.
Sewon et al.39 observed that hormone replacement therapy in
postmenopausal women significantly decreases the salivary
calcium levels. Estrogen deficiency in postmenopausal women
is accompanied by increased bone resorption. This could be
attributed to the loss of direct effects on osteoclasts and their
precursors, but indirect actions on the immune system may
also be involved. The productions of cytokines like IL-1, TNF-
á and IL-6 can potentially enhance bone resorption and can
be suppressed by physiological doses of estrogen40.
Studies have proven that an increased level of calcium in the
urine is a marker for the resorption of bone7-9. Bone resorption
releases calcium into the serum, which is filtered into the urine
and excreted. The present study also showed an increased
level of calcium in saliva, which is an ultra filtrate of plasma.
To the best of knowledge, this is the first study to measure the
salivary alkaline phosphatase levels in postmenopausal
osteoporotic, osteopenic and non-osteoporotic/osteopenic
women. Our data showed a significant increase in alkaline
phosphatase levels in the osteoporotic and osteopenic
patients when compared to the controls. Since there is no
standard level published in the literature for salivary alkaline
phosphatase, the values were compared to those of the
control group. Alkaline phosphatase is a marker for bone
turnover. Ross et al.9 and Taguchi et al.41 reported that the
levels of serum total alkaline phosphatase and bone-specific
alkaline phosphatase are increased in subjects with low BMD.
Likewise, the present study showed significantly higher
levels of salivary alkaline phosphatase in osteoporotic and
osteopenic subjects than in the controls. However, before
salivary parameters and oral signs can be used as predictors
for these systemic diseases, further investigations are
needed to support any definite conclusions.
Braz J Oral Sci. 7(24):1508-1512 Oral Signs and Salivary Parameters as Indicators of Possible Osteoporosis and Osteopenia in Postmenopausal Women - A Study of 45 Subjects
1512
The results of the present study demonstrate that
assessment of salivary parameters, such as calcium,
phosphorus and alkaline phosphatase, along with some oral
signs like periodontitis and number of missing teeth may be
important indicators to aid in the diagnosis of osteoporosis
and osteopenia in postmenopausal women.
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