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Suryasnata Nayak, MDS.*, Shashirekha Govind, MDS.*, Amit Jena, MDS.**, Priyanka Samal, M.D.***, Naresh
Kumar Sahoo, M.D.****, Shakti Rath, Ph.D.*****
*Department of Conservative Dentistry and Endodontics, Institute of Dental Sciences, Siksha O Anusandhan Deemed to be University, Bhubaneswar,
Odisha, India, **Department of Conservative Dentistry and Endodontics, SCB Dental College, Cuttack, Odisha,***Department of Hematology, IMS
& SUM Hospital, Siksha O Anusandhan Deemed to be University, Bhubaneswar, Odisha, India, ****Department of Chemistry, Institute of Technical
Education and Research, Sikhsa O Anusandhan Deemed to be University, Bhubaneswar, Odisha, India, *****Central Research Laboratory, Institute
of Dental Sciences, Siksha O Anusandhan Deemed to be University, Bhubaneswar, Odisha, India.
Evaluation of Oral Hygiene Status, Salivary Fluoride
Concentration and Microbial Level in Thalassemic
and Hemophilic Patients
ABSTRACT
Objective:isstudy aimed to evaluateoral hygiene status,salivary uoride concentration, andStreptococcus
mutansandLactobacilluslevels in saliva of thalassemic, hemophilic and individuals without any other systemic disorders.
Materials and Methods: A total 162 individuals (44 healthy individuals, 86 thalassemic and 32 hemophilic patients)
were selected, and randomly (n=30 in each group), the patients were allocated to Group A: individuals without
any systemic condition, Group B: thalassemic patients, and Group C: hemophilic patients. Detailed case history,
DMFT/DMFS, and OHI-S index were recorded. An aliquot of 5 ml of saliva wascollected from each patient to
determine the salivary uoride concentration and predominant microbial colony in saliva. e data were analyzed
bychi-square testofindependence andnonparametric Kruskal-Wallis H test.
Results: e mean debris and calculus index among groups A, B, and C was0.55 ± 0.43, 0.61 ± 0.46, 0.46 ± 0.47 and
0.33 ± 0.48, 0.18± 0.34, and 0.15 ± 0.34, respectively. e DMFTscore for group Awas high (1.93 ± 1.86, 1.67 ±
1.92) compared to groups B (0.40 ± 0.77, 0.67 ± 1.37) and C (0.47 ± 0.68, 0.30 ± 0.54). e uoride concentrations
among three groups (A, B, and C) were0.06 ± 0.07, 0.12 ± 0.13,and0.12 ± 0.13 ppm respectively.e number of
colony-forming units was highest in the healthy individual>hemophilic>thalassemicand presence of predominant
microorganisms showedinsignicant association among the groups (p=0.323).
Conclusion:Compared to healthy individuals, thalassemic and hemophilic patients had better oral hygiene.
Keywords: Dental caries; uorides; hemophilia; thalassemia; saliva; lactobacillus; Streptococcus mutans (Siriraj Med
J 2022; 74: 314-322)
Corresponding author: Shashirekha Govind
E-mail: shashirekha123@yahoo.com
Received 29 July 2021 Revised 1 December 2021 Accepted 3 December 2021
ORCID ID: https://orcid.org/0000-0003-4992-3087
http://dx.doi.org/10.33192/Smj.2022.38
All material is licensed under terms of
the Creative Commons Attribution 4.0
International (CC-BY-NC-ND 4.0)
license unless otherwise stated.
INTRODUCTION
alassemia is a genetic blood disorder that can
result in the abnormal formation (partial or complete
synthesis of
α- globin or β- globin chains in hemoglobin,
a tetramer of
α
2
β
2
) of hemoglobin.
1
e two main types
are alpha and beta-thalassemia.
2
e patient becomes
thalassemia major if a gene defect is inherited from both
parents. If the defect is inherited only from one parent,
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SMJ
it is known as thalassemia minor. Such individuals are
carriers of the disease and most of the time remain
asymptomatic.
3
Hemophilia is a rare hereditary condition, resulting in
prolonged and uncontrolled bleeding either spontaneously
or subsequently aer trauma. It inherits an X- linked
recessive pattern, which occurs mostly in males. It occurs
due to the absence of one or more clotting factors that
lead to prolonged clotting time and excessive bleeding
that can cause risk to life. e two most common forms
are hemophilia A and hemophilia B which are caused
by factors VIII and IX deciency, respectively.
4
Dental caries is a disease of microbial origin.
5
In addition to Lactobacillus and Actinomyces species,
“Streptococcus mutans” (gram-positive facultative
anaerobic cocci commonly found in the oral cavity of a
human) is the most common pathogen associated with
caries.
6,7
According to literature Ora-facial abnormalities
(protrusion of maxillary incisors, wide spacing of teeth,
occlusion abnormalities, and nasal deformity) are common
in thalassemic patient and high caries prevalence in
thalasemic and hemophilic patients.
8,9
Authors have
observed that the prevalence of caries experienced was
low in hemophiliacs.
10
Dental practioners should be aware
of the risk associated with the procedures among the
aforementioned patients. Early detection and prevention
of dental caries is an eective caries-control strategy.
Fluoride in saliva promotes tooth remineralization by
producing less soluble uorapatite crystals.
11
As a result,
it is essential to determinewhether thalassemia and
hemophilia patients are more prone to tooth decay than
the general population. e purpose of this study was to
investigate: a) comparing the oral hygiene status of patients
with thalassemia, hemophilia, and healthy individuals,
b) determining their salivary uoride concentration,
and c) identifying the predominant microorganism (S.
mutans and Lactobacillus) levels in saliva. e hypothesis
for this study was that the categorical variables had no
association.
MATERIALS AND METHODS
e study was approved by the Ethics Committee
Institute of Medical Sciences (IMS) and Sum Hospital
Siksha ‘O’ Anusandhan Deemed to be University (Ref.
No. DMRI IMS. SH/SOA/180319). e research was
carried out between 2018 and 2020. G* power soware,
version 3.1.9 (available at http://www.gpower.hhu.de/
en.html) was used to calculate sample size based on the
results of previous studies.
12,13
Individual group sample
size was n=30, with the level of signicance and power
of test set at 5% and 80%, respectively (total 90). Sample
selection is described in Fig 1. e inclusion criteria
were thalassemic or hemophilic patients above the age
of 14 years (individuals visiting “Institute of Dental
Sciences” and “Institute of Medical Science and SUM
Hospital”), healthy individuals without any bleeding
disorder or systemic condition, visiting the Institute of
Dental Sciences for a dental check-up. e exclusion
criteria were: other bleeding or clotting disorders and
chronic systemic conditions, hormonal disorders, uoride
therapy patients, medications aecting the salivary ow
rate (β-blockers, antihistamines, antipsychotics, anti-
inammatory drugs, etc.), patients below the age of 14
years, and dental uorosis (according to modied Dean’s
uorosis index i.e.:questionable/0.5 to severe/4).
All patients provided written informed consent (in
the case of patients below the age of 18, written informed
consent was taken from their parents /gaurdian). A sample
size of 90 patients (n=30 in each group) was allocated
using randomization soware (www.radomization.com).
Group A [Control group]: Healthy individuals (who did
not have any bleeding or clotting disorder and satised
the exclusion criteria) Group B: alassemic patients,
Group C: Hemophilic patients. Each patient had a detailed
case record and oral hygiene status, which included the
DMFT (Decayed- Missed- Filled- Teeth) and (debris
& calculus) OHI-S (Oral Hygiene Index- Simplied)
indexes. A single dental practitioner performed the
patients’ dental examinations (Fig 2). Five milliliters of
unstimulated saliva was collected from each individual
minimum 30 minutes aer eating and stored separately in
sterile sample collection bottles. Each patient’s saliva was
collected between 10 a.m. to 3 p.m. (No specic instructions
regarding oral hygiene maintenance was advised). Saliva (5
mL) were divided into Part I (4 mL) to determine salivary
uoride concentration and Part II (1 mL) to determine
predominant microbiota and colony-forming units
(Fig 1).
Measurement of salivary uoride concentration
e 4 ml of saliva samples were centrifuged at 1500
rpm for 3 min, and the supernatant was stored in close
lid containers at 4
o
C for a maximum of 48 hours. Aer
the readings were standardized using uoride standard
solution, the saliva samples were diluted with TISAB III
(Total Ionic Strength Adjustment Buer- III) reagent
(Merck India) and used to quantify salivary uoride
concentration using an Orion Star A 214ASIC pH meter
with a uoride ion-selective electrode. For each sample,
the results were acquired three times, and the mean
values for each group were recorded individually.
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Fig 1. Flow chart of sampling of groups and methodology.
Determination of the salivary microbial level
One milliter of saliva sample was stored in close
lid containers at 37
o
C for a maximum of 48 hours and
used for microbiological culture on nutrient agar and
blood agar plates. e plates were incubated in a bacterial
incubator for 24 hours at 37
o
C. e predominant colony
was identied and subjected to Gram’s staining. e stained
slides were observed under a microscope (Olympus India)
at 40x and 100x magnications in oil immersion. e
predominant microora for each sample was determined
under the microscope. e number of colony-forming
units (CFU) was counted for the predominant microora
of each sample. e results were recorded and subjected
to statistical analysis.
Statistical analysis
Statistical analysis was performed using IBM SPSS
statistics 24.0, South Asia Private Ltd. www.spss.co.in. e
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Fig 2. Clinical pictures of the three groups; 2a-2c) Intraoral pictures of healthy individual, 2d-2f) Intraoral pictures of thalassemic patients,
2g- 2i) Intraoral pictures of hemophilic patients.
test of association of patient group was done following
cross tabulation procedure followed by Chi-square test of
independence. echi-Square testofindependencewas
used to determine if there was a signicant relationship
between two categoricalvariables. e null hypothesis
for thistestwas that there is no relationship between
the categorical variables.
Comparison of age, decayed teeth, filled teeth,
calculus, and uoride levels among the three groups
of patients was performed following nonparametric
Kruskal-Wallis test, as these variables failed to pass the
Shapiro Wilki normality test. e Kruskal-Wallis H test,
a is the nonparametric analog of one-way analysis of
variance and detects dierences in distribution location.
e mean, SD and quartiles were calculated following a
descriptive statistics procedure. Colony-forming units
(CFUs) is the estimate of the number of viable bacteria
or fungal cells in a sample and have been classied into
three groups: 10+ to 20+, 30+ to 50+, and 80+ to 150+.
e level of signicance was kept at p<0.05.
RESULTS
e demographic details are the mean age of patients
in healthy individuals, thalassemic and hemophilic were
18.73 ± 2.59, 20.20 ± 8.91, 18.27 ± 4.23 years respectively.
e dierence in the distribution of age among the three
groups was not signicant (p=0.374). In hemophilic group
all the patients were males. e male-female proportions
in the control group were 46.7% and 53.3% and in the
thalassemic group were 56.7% and 43.3%, respectively.
e mean debris index among groups A, B, and C
was 0.55 ± 0.43, 0.61 ± 0.46, and 0.46 ± 0.47, respectively.
e median debris among the three groups was in the
range of 0.915 with IQR (interquartile range): 0.000 to
1.000 to 0.330 with an IQR: 0.00 to 1.00. e mean calculus
index among groups A, B, and C was 0.33 ± 0.48, 0.18 ±
0.34, and 0.15 ± 0.34, respectively. e median calculus
among the three groups was in the range of 0.000 with
IQR: 0.000 with IQR: 0.00 to 0.000 to 0.000 with IQR
0.000 to 1.000. e OHI-S (debris and calculus) among
the groups was stastistically insignicant (Tables 1&2).
e DMFT (decayed and lled) score for group A
(control) was high (1.93 ± 1.86, 1.67 ± 1.92) compared
to groups B (0.40 ± 0.77, 0.67 ± 1.37) and C (0.47 ± 0.68,
0.30 ± 0.54). e DMFT scores among Groups B and
C were statistically insignicant compared to Group A
(p=0.000). However, clinically Group C showed lower
DMFT scores (Figs 3&4). e uoride concentrations
among the three groups were 0.06 ± 0.07, 0.12 ± 0.13,
and 0.12 ± 0.13 ppm. e mean dierence among the
three groups was statistically insignicant (p=0.566)
(Table 3).
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318
TABLE 1. Comparison of Debris among groups.
TABLE 2. Comparison of Calculus among groups.
Group N Mean ± SD Q1 Q2 (Median) Q3 Minimum Maximum
Control 30 0.55 ± 0.43 0.000 0.580 1.000 0 1
Thalassemic 30 0.61 ± 0.46 0.000 0.915 1.000 0 1
Hemophilic 30 0.46 ± 0.47 0.000 0.330 1.000 0 1
Kruskal Wallis
Test 'p' value 0.465
Group N Mean ± SD Q1 Q2 (Median) Q3 Minimum Maximum
Control 30 0.33 ± 0.48 0.000 0.000 1.000 0 1
Thalassemic 30 0.18 ± 0.34 0.000 0.000 0.330 0 1
Hemophilic 30 0.15 ± 0.32 0.000 0.000 0.000 0 1
Kruskal Wallis
Test 'p' value 0.288
1.93
0.4
0.47
-1
0
1
2
3
4
Mean
Error Bar ± SD
CONTROL THALASSEMIC HEMOPHILIC
1.67
0.67
0.30
-1
0
1
2
3
4
Mean
Error Bar ± SD
CONTROL THALASSEMIC HEMOPHILIC
Fig 3. Comparison of mean
Decayed tooth among groups.
Fig 4. Comparison of mean
Filled tooth among groups.
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TABLE 3. Comparison of Fluoride concentration (in ppm) among groups.
Group
Fluoride level in ppm
N Mean ± SD Q1 Q2 (Median) Q3 Minimum Maximum
Control 30 0.06 ± 0.07 0.019 0.027 0.054 0.002 0.254
Thalassemic 30 0.12 ± 0.13 0.018 0.036 0.230 0.001 0.453
Hemophilic 30 0.10 ± 0.11 0.014 0.025 0.201 0.001 0.321
Kruskal Wallis
Test 'p' value 0.566
e proportions of S. mutans and Lactobacillus in
group A were 86.7% and 10.0%, group B 93.3% and 6.7%,
and group C were 80.0% and 20.0%, respectively. e
predominant microorganisms did not have a signicant
association among the groups (p=0.323). e association
between decayed teeth and dierent colony forming
groups was 0.71± 0.95 in the 10+ - 20+ CFU group,
which increased to 3.36± 2.20 in the 80+ - 150+ CFU
group compared to the control group. In group B, 0.13
± 0.35 in 10+ - 20+ CFU group which increased to 2.00
± 1.00 in 80+ - 150+ CFU group and for group C was
0.00 ± 0.00 in 10+ -20+ CFU group which increased to
1.17 ± 0.75 in 80+ - 150+ CFU group. e number of
colony-forming units was highest in healthy individuals
and lowest in thalassemic patients. e increased CFU
level has a signicant association with a higher number
of decayed teeth (Tables 4&5).
e correlation of age, number of decayed teeth
and uoride showed that age did not have a signicant
correlation with the number of decayed teeth or uoride
in the healthy and hemophillic groups. However, age had
a signicant positive correlation of 0.40 with uoride in
the thalssemic group (p<0.05). e number of decayed
teeth showed no statistically signicant correlation with
uoride in any of the three groups (p>0.05).
DISCUSSION
Saliva is an important predictor of oral health status.
e preference for unstimulated saliva in this study is
attributable to the fact that “stimulated saliva has increased
ow rate, dilution, and change in pH”.
11,4,15
During the
collection of a saliva sample, it was observed that the
salivary ow rate was higher in young individuals than in
adults, which is in accordance with a meta-analysis that
revealed that the maturing process is directly associated
with a decreased salivary ow rate and is unaected by
medications.
16
The hemophilic group had only male patients
considering “hemophilia inherits in an x-linked recessive
pattern that occurs primarily in males”.
17
Females become
TABLE 4. Association of Predominant Microorganisms in groups.
PM
Group
Total
χ
2
, p
Control Thalassaemic Hemophilic
No. % No. % No. % No. %
S. Mutans 26 86.7 28 93.3 24 80 78 86.7
Candida 1 3.3 0 0 0 0 1 1.1
χ
2
= 4.671
Lactobacillus 3 10 2 6.7 6 20 11 12.2 p=0.323
Total 30 100 30 100 30 100 90 100
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carriers and are usually asymptomatic, although in rare
situations, they may develop hemophilia symptoms.
18,19
A case-control study found that children and adolescents
with hemophilia had similar caries experiences and
had no signicant dierences in oral hygiene or dietary
habits.
20,21
Group B’s age ranged from 15 to 54 years
old, whereas group C’s age ranged from 14 to 32 years
old. alassemic patients have low IgA levels in their
saliva and endocrine dysfunction, which increases their
risk of decay.
22,23
e results of the present study are in
accorandace with the aforementioned studies.
When compared to healthy persons, patients
with blood disorders had compromised oral health,
particularly poor periodontal conditions (gingival and
plaque index) in - thalassemia and sickle cell anemia
patients.
24,25
Individuals aected and their families’ physical
and psychological well-being was impacted (involves
regular visit, chelation therapy, and uncertainties about
the future), and studies have shown that thalassemia
patients have a higher rate of caries, which could be
attributed to aberrant tooth morphology, abnormal pits
and ssures, and changes in salivary components and
volume.
13,23
Despite the foregoing reasoning, the current
investigation found a minor rise in mean clinical debris
(0.61 ± 0.46), an improved calculus index (0.18 ± 0.34),
and a lower DFMT score (0.40 ± 0.77) when compared
to the control group. Among the groups (A; 0.06 ±
0.07, C; 0.10 ± 0.11), group B (0.12 ± 0.13) had a higher
clinical uoride level. e proportion of the predominant
microorganisms S.mutans and Lactobacillus was slightly
greater than that in the control group, but the dierence
was statistically insignicant (p=0.323). Only one patient
in the control group exhibited Candida, whereas groups
B and C had none.
In a study of hemopliliacs’ oral and general health-
related quality of life, researchers noted that psychological
behavior and mental health were lower, but that self-
assessing oral health state and regularly perceiving
dental treatment needs were higher than in healthy
people.
26
is is consistent with the ndings of the current
investigation, in which these patients were well-versed
in the consequences of poor dental hygiene and the
risk of caries. When compared to the thalassemia and
control groups, the debris index (0.46 ± 0.47), calculus
index (0.15 ± 0.32) and DMFT score (0.47 ± 0.68) were
lower. e control group’s DMFT scores were statistically
signicant (p=0.000).
Salivary uoride concentration was clinically evident
in groups C and D when compared to the control group.
is could be because these patients are more aware of the
importance of maintaining good dental hygiene. ere
was no test of gender association in the hemophilic group
because all of the cases were males. In comparison to
the thalassemic and control groups, the proportions of
S. mutans, Candida, and Lactobacillus were lower (80.0%,
0%, and 20.0%, respectively) in the hemophilic group.
Previous research has found that patients with blood
problems had a greater S. mutans and Lactobacillus count
in their saliva than healthy people.
27,28
e presence of a
certain microorganism was not revealed by an increase
TABLE 5. Comparison of mean number of decayed teeth by CFUs within groups.
Group
Decayed tooth
CFU Control Thalassaemic Hemophilic
N Mean ± SD Median N Mean± SD Median N Mean ± SD Median
(IQR) (IQR) (IQR)
10+ - 20+ 7 0.71±0.95 0(0,2) 15 0.13±0.35 0(0,0) 10 0.00±0.00 0(0,0)
30+ - 50+ 12 1.33±0.89 1(1,2) 12 0.33±0.65 0(0,0.75) 14 0.50±0.65 0(0,1)
80+ - 150+ 11 3.36±2.20 3(2,4) 3 2.00±1.00 2 6 1.17±0.75 1(0.75,2)
Total 30 1.93±1.86 2(0.75,3) 30 0.40±0.77 0(0,1) 30 0.47±0.68 0(0,1)
Kruskal Wallis
Test 'p' value
0.004 0.003 0.003
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in the number of colony-forming units in the groups
(p≥ 0.05).
e current study revealed that thalassemic and
hemophilic patients were well aware of the conditions
and potential problems associated with poor oral health.
e majority of patients visited the dentist every six
months for a routine dental examination, and the parents
/gaurdian of patients under the age of 18 yrs. were well
aware of the issue.
9
Any dental invasive surgery should
be performed aer factor replacement/ transfusion.
29,30
Hematologists should inform such patients about dental
problems and treatments, and encourage them to visit
the dentist on a frequent basis to avoid complications.
Further studies into the impacts of various uoride
therapy methods, specic microbiological load, and pain
perception during dental treatment can be considered for
a large thalassemic and hemophilic population (dierent
location, depending on socioeconomic status of the
individual and their families).
CONCLUSION
e current study concludes that the OHI-S (debris &
calculus) index and mean salivary uoride concentration
was statistically insignicant among the groups (p>0.05).
DMFT scores were less in thalassemic and hemophilic
patients compared to the healthy individuals. e number
of colony-forming units was higher in healthy individuals
and lowest in thalassemic patients. Dentists should be
aware of and knowledgeable about the risks involved
when treating thalassemic and hemophilic patients. Early
detection and recognition of oral health concerns will
help patients nancially and in terms of reducing the
risk. According to the current ndings, the incidence
of caries, gingivitis, and microorganism in thalassemic
and hemophilic patients is clinically significant. To
receive safe, comprehensive oral care, these patients’
families, guardians, physicians, and dental clinicians
must work collaboratively.
ACKNOWLEDGEMENT
None
Disclosure Statement
e authors have no conicts of interest to declare.
Funding Sources
Have no such funding sources involved.
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