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14]

Original Article

Effect of citric acid, tetracycline,

and doxycycline on instrumented
periodontally involved root surfaces:
A SEM study
Gurparkash Singh Chahal, Kamalpreet Chhina,1 Vipin Chhabra,1 Rakhi Bhatnagar,1
Amna Chahal

Departments of Abstract:
Periodontology Background: A surface smear layer consisting of organic and inorganic material is formed on the root surface
and Implantology, following mechanical instrumentation and may inhibit the formation of new connective tissue attachment to the
Genesis Institute of root surface. Modification of the tooth surface by root conditioning has resulted in improved connective tissue
Dental Sciences and attachment and has advanced the goal of reconstructive periodontal treatment. Aim: The aim of this study was
Research, Ferozepur, to compare the effects of citric acid, tetracycline, and doxycycline on the instrumented periodontally involved root
surfaces in vitro using a scanning electron microscope. Settings and Design: A total of 45 dentin samples obtained
Punjab, 1B. R. S.
from 15 extracted, scaled, and root planed teeth were divided into three groups. Materials and Methods: The root
Dental College and conditioning agents were applied with cotton pellets using the “Passive burnishing technique” for 5 minutes. The
Hospital, Panchkula, samples were then examined by the scanning electron microscope. Statistical Analysis Used: The statistical
Haryana, India analysis was carried out using Statistical Package for Social Sciences (SPSS Inc., Chicago, IL, version 15.0 for
Windows). For all quantitative variables means and standard deviations were calculated and compared. For more
than two groups ANOVA was applied. For multiple comparisons post hoc tests with Bonferroni correction was
used. Results: Upon statistical analysis the root conditioning agents used in this study were found to be effective
in removing the smear layer, uncovering and widening the dentin tubules and unmasking the dentin collagen
matrix. Conclusion: Tetracycline HCl was found to be the best root conditioner among the three agents used.
Key words:
Access this article online Citric acid, scanning electron microscope, tetracycline hydrochloride
Website:
www.jisponline.com
DOI:
10.4103/0972-124X.128196
INTRODUCTION For over 90 years, agents of various types have
been placed on root surfaces in attempts to

P
Quick Response Code:
eriodontal diseases lead to loss of
attachment and exposure of root surface
of the teeth to the oral environment. Exposed
cementum shows number of changes including
accumulation of plaque and calculus on the
surface, hypermineralized or demineralized
surface areas, loss of collagen cross banding, and
contamination with cytotoxin and endotoxins
which cause depression in cell growth and
viability of fibroblasts thus interfering with the
new attachment.[1]
modify the diseased tooth structure and for
the regeneration of periodontal tissues. Such
treatment not only removes the smear layer but
also enlarges dentinal tubules into which healing
connective tissue can enter. Citric acid, tetracycline
hydrochloride, doxycycline hydrochloride,
phosphoric acid, sodium hypochlorite, ethylene
diamine tetra acetic acid (EDTA), fibronectin,
laminin, Cohn’s factor, stannous fluoride, etc.,
are some of the chemical agents that have been
used for root conditioning.[4]

Address for Complete decontamination of the affected root Citric acid has been shown to change the
correspondence: surface is not possible with mechanical methods surface characteristics of treated root surfaces
Dr. Gurparkash Singh alone.[2] After hand or ultrasonic scaling of the by removing the smear layer, exposing the
Chahal, root surface, a surface smear layer (2-15 μm in dentinal tubules and making the tubules appear
43-H, Bhai Randhir thickness) consisting of organic and inorganic wider and with funnel-shaped orifices. [5,6]
Singh Nagar, Ludhiana, material, with particles varying in size from less It partially exposes collagen from radicular
Punjab - 141 012, India.
than 1 μm to more than 15 μm is formed on the dentin which has been shown to improve fibrin
E-mail: gpchahal29@
gmail.com
root surface[2] which serves as a barrier between linkage and consequently inhibit epithelial
the periodontal tissues and the root surface and downgrowth to stimulate fibrous attachment
Submission: 09-04-2013 may inhibit the formation of new connective and migration.[7] It may also act as a potent
Accepted: 17-08-2013 tissue attachment to the root surface.[3] antibacterial agent.[6]

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Chahal, et al.: Effect of citric acid, tetracycline, and doxycycline on instrumented periodontally involved root surfaces: A SEM study
Tetracyclines are a group of bacteriostatic antimicrobials
effective against a wide range of organisms and successfully
tested in both animal models and clinical studies. Tetracycline
studies demonstrate multiple beneficial properties toward
regeneration; enhanced attachment and growth of gingival
fibroblasts; good anti-collagenase activity; high substantivity;
inhibition of parathyroid hormone-induced bone resorption and
anti-inflammatory action. Dentin root surface demineralization
by low pH tetracycline increases fibronectin, an extracellular
matrix glycoprotein, binding. The adsorbed or bound
fibronectin enhances fibroblast attachment and growth
while suppressing epithelial cell attachment and growth.
Furthermore, the slow release of biologically active tetracycline
from the tooth surface occurs for at least 48 hours and up to
14 days.[8]
Doxycycline is effective against suspected causative microflora
of periodontitis and has antienzymatic properties. Topical
application of doxycycline has shown a long-lasting
substantivity on periodontally diseased root surfaces.
Antibacterial effect of doxycycline on root conditioned
specimens persisted for 14 days.[9]
This study was undertaken to compare the effects of citric
acid, tetracycline, and doxycycline on the instrumented
periodontally involved root surfaces in vitro using a scanning
electron microscope.
MATERIALS AND METHODS
For the present study, 15 single rooted anterior teeth indicated
for extraction due to advanced chronic periodontitis were
selected from the outpatient department, Department of
Periodontology and Oral Implantology.
Freshly extracted single rooted human teeth with proximal
attachment loss of 5 mm or more, no history of root planing
or prophylaxis in the past 6 months, no history of acute
pain or swelling, absence of any restoration or caries were
selected.
Preparation of the specimen
• A total of 45 dentin samples were obtained from the
periodontally affected mid root region of 15 extracted
teeth Following extraction, the teeth were washed
and cleaned using a soft bristle brush and stored in
distilled water
Figure 1: Surface morphology of root specimen treated with citric acid (pH 1)
at a magnification of ×2000
Journal of Indian Society of Periodontology - Vol 18, Issue 1, Jan-Feb 2014
• Scaling and root planing of root surfaces was done to obtain
smooth, shiny hard surface
• Samples were obtained from the cervical two thirds of the
root by making two parallel grooves 0.5 mm depth with
circular disc under copious water irrigation
• The first groove was positioned horizontally at the CEJ and
the second groove was made parallel to the first and apical
to it. The portion of tooth above and below these grooves
was sectioned off
• Three longitudinal root sections were then prepared from
each tooth by cutting the cervical two thirds of the root into
two halves first and then splitting one of the halves into two
more halves by cutting perpendicular to the first cut
• The three samples from each tooth were stored in individual
containers containing distilled water.
Root conditioning agents
The experimental groups were divided into A, B, and C based
on the type of conditioning done
• A – Application of saturated citric acid (pH 1) for 5 minutes.
Saturated citric acid solution was prepared by slowly adding
anhydrous citric acid powder to 50 ml of distilled water using a
magnetic stirrer until no more crystals dissolved in the solution
• B – Application of tetracycline HCl (pH 1.6). Tetracycline
HCl (250 mg/ml) was made by mixing 500 mg in 2 ml of
sterile water
• C – Application of doxycycline (pH 2.2). Doxycycline HCl
solution (100 mg/ml) was made by mixing doxycycline
HCl powder (100 mg) in sterile water (1 ml).
Application of the solutions
• Application of the respective agents on the sample was done
passively with cotton pellets saturated with the agent that
were changed every 30 seconds for a total period of 5 minutes
• Following treatment, samples were rinsed with distilled
water for 20 seconds and air dried.
Scanning photomicrographs of the root surfaces were taken
at ×2000 and ×6000 magnification [Figures 1-6]. The specimens
were examined for total number of tubules, number of patent
tubules, percentage of patent tubules, and diameter of tubules and
the results were statistically analyzed [Table 1 and Graphs 1-4].
OBSERVATION AND RESULTS
Scaled and root planed tooth surfaces after treatment with
root conditioning agents for 5 minutes appeared smooth to
Figure 2: Surface morphology of root specimen treated with citric acid (pH 1)
at a magnification of ×6000
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Chahal, et al.: Effect of citric acid, tetracycline, and doxycycline on instrumented periodontally involved root surfaces: A SEM study

Figure 3: Surface morphology of root specimens treated with tetracycline (pH 1.6) Figure 4: Surface morphology of root specimens treated with tetracycline (pH 1.6)
at a magnification of ×2000 at a magnification of ×6000

Figure 5: Surface morphology of root specimens treated with doxycycline (pH 2.2) Figure 6: Surface morphology of root specimens treated with doxycycline (pH 2.2)
at a magnification of ×2000 at a magnification of ×6000

undulating with numerous well-defined round to oval dentinal Table 1: Total number of tubules, number of patent
tubule orifices. Tubule orifices were irregular in shape, several tubules, percentage of patent tubules, and diameter of
being flared or funnel shaped. Some of the tubular orifices tubules in root sections in the three experimental groups
were occluded. Citric acid Tetracycline Doxycycline
Total number of tubules 25.00 26.00 22.33
The multiple comparisons Bonferroni test was applied to Number of patent tubules 11.47 15.07 8.73
compare the three groups. The mean number of total tubules per % of patent tubules 45.69 57.97 39.16
unit area in the tetracycline HCl-treated group was higher than Diameter of tubules (um) 2.20 2.45 1.76
in the doxycycline group and the citric acid group. The mean
difference in total number of tubules in specimens treated with Table 2: Mean comparison of total number of tubules
tetracycline and doxycycline was highly significant (P = 0.001). between all the three study groups
Similarly, the mean difference in total number of tubules
(I) Group (J) Group Mean difference (I-J) Std. error Sig.
in specimens treated with citric acid and doxycycline was
significant (P < 0.05), but the mean difference in total number Post hoc tests
Citric acid Tetracycline −1.000 0.955 0.903
of tubules in specimens treated with citric acid and tetracycline Citric acid Doxycycline 2.667(*) 0.955 0.024*
was not significant (P > 0.05) [Table 2 and Graph 5]. Doxycycline Tetracycline −3.667(*) 0.955 0.001**

The multiple comparisons Bonferroni test for the comparison of

number of patent tubules per unit area between the three study Table 3: Mean comparison of number of patent tubules
groups showed high significance (P < .001) results [Table 3 per unit area between all the three study groups
and Graph 6]. (I) Group (J) Group Mean difference (I-J) Std. error Sig.
Post hoc tests
The multiple comparisons Bonferroni test for the comparison Citric acid Tetracycline −3.600 (*) 0.606 <.001**
of percentage of patent tubules between the three study groups Citric acid Doxycycline 2.733 (*) 0.606 <.001**
Tetracycline Doxycycline 6.333 (*) 0.606 <.001**
showed high significance (P < .001) results [Table 4 and Graph 7].

The mean diameter of tetracycline HCl-treated specimens was
higher than the citric acid group and the doxycycline group.
The mean difference of tubule diameter in citric acid-treated
specimens and tetracycline-treated specimens was not
significant (P > .05).
Similarly, the mean difference of tubule diameter in citric
acid-treated specimens and doxycycline-treated specimens
was not statistically significant (P >.05) but the mean difference
between tetracycline and doxycycline was statistically
significant (P < 0.05) [Table 5 and Graph 8].

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Chahal, et al.: Effect of citric acid, tetracycline, and doxycycline on instrumented periodontally involved root surfaces: A SEM study

27 16 15.07
Mean number of tubules per
26
26 14

No. of patent tubules per

25 11.47
25 12
unit area

10 8.73

unit area
24
8
23 22.33
6
22
4
21
2
20 0
Citric acid Tetracycline HCl Doxycycline Citric acid Tetracycline HCl Doxycycline
Agent used Agent used

Graph 1: Graphic representation of mean number of tubules per unit area in the Graph 2: Graphic representation of mean number of patent tubules per unit area in
three study groups the three study groups

70 3

Diameter of patent tubules

57.97 2.45
Percentage of patent tubules

60 2.5
2.2
50 45.69 2 1.76
39.16

(in μm)
40
1.5
30
1
20
0.5
10
0
0 Citric Acid Tetracycline HCl Doxycycline
Citric Acid Tetracycline HCl Doxycycline
Agent used
Agent used
Graph 4: Graphic representation of mean diameter of tubules (μm) in the
Graph 3: Graphic representation of percentage of patent tubules in each group three study groups

4 7
Mean difference in number of tubules

3.66 6.33
Mean no. of patent tubules per

3.5 6
3 2.66 5
2.5
3.6
unit area

4
per unit area

2
3 2.73
1.5
1 2
1
0.5 1
0 0
Tetracycline HCl Citric acid Tetrracycline HCl Tetracycline HCl Citric acid Tetracycline HCl
and and and and and and
citric acid doxycycline doxycycline citric acid doxycycline doxycycline
Agent compared Agents compared

Graph 5: Graphic representation of group-wise mean difference of total number of Graph 6: Graphic representation of group-wise mean difference of patent number of
tubules per unit area tubules per unit area

20 18.8 0.8
Mean difference in percentage of

Mean difference in diameter

18 0.68
0.7
16 0.6
14 12.27
patent tubules

12 0.5 0.44
10 0.4
8 6.52 0.3 0.24
6 0.2
4
0.1
2
0 0
Tetracycline HCl Citric acid Tetracycline HCl Tetracycline HCl Citric acid Tetracycline HCl
and and and and and and
citric acid doxycycline doxycycline citric acid doxycycline doxycycline
Agents compared Agents compared

Graph 7: Graphic representation of group-wise mean difference of percentage of Graph 8: Graphic representation of group-wise mean difference of diameter of
patent tubules patent tubules (μm)

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Chahal, et al.: Effect of citric acid, tetracycline, and doxycycline on instrumented periodontally involved root surfaces: A SEM study
Table 4: Mean comparison of percentage of patent tubules
between all the three study groups
(I) Group (J) Group Mean difference (I-J) Std. error Sig.
Post hoc tests
Citric acid Tetracycline −12.27867 (*) 1.34486 <.001**
Citric acid Doxycycline 6.52733 (*) 1.34486 <.001**
Tetracycline Doxycycline 18.80600 (*) 1.34486 <.001**
Table 5: Mean comparison of diameter of tubules between
all the three study
(I) Group (J) Group Mean difference (I-J) Std. error Sig.
Post hoc tests
Citric acid Tetracycline −0.24867 0.24938 0.583
Citric acid Doxycycline 0.44067 0.24938 0.193
Tetracycline Doxycycline 0.68933 (*) 0.24938 0.023*
DISCUSSION
The single, most common primary etiological factor in
periodontal disease is bacterial plaque. Periodontitis-affected
root surfaces undergo histologic, physical, chemical, and
immunochemical changes that may make them poor
base for attachment and proliferation of fibroblasts. Root
biomodification has been advocated as an effective way to
remove the smear layer and condition the roots for better
regeneration. Root biomodification uses acid substances
or chelating agents to remove the smear layer and expose
root collagen fibers. Independent of being conditioned, the
collagen from the root surface attaches to fibrin present in a
clot, preventing epithelial downgrowth, and forms a scaffold
for cell development and mature collagen fiber attachment.[10]
Citric acid, tetracycline, and tetracycline derivatives such as
minocycline HCl, doxycycline HCl, are frequently used as
root conditioners, since their acid pH partially demineralizes
the planed root surfaces, eliminating the smear layer, opening
and widening the dentin tubules, and exposing various
components (i.e. type I collagen, proteoglycans, fibronectin,
growth factors) of cementum extracellular matrix or dentin
extracellular matrix.[11] Several in vitro studies have suggested
that root surface modifications by tetracycline HCl or by citric
acid could influence the behavior of periodontal fibroblasts,
improving their attachment and spreading.[12] Some of the
mechanisms by which this can occur include (i) induced
cementogenesis, (ii) collagen splicing, (iii) fibronectin
fibrin-collagen binding thereby inhibiting epithelial apical
migration, and (iv) enhanced fibroblast chemotaxis, migration,
and attachment. [12-15] Other investigations have reported
similar findings even though treatment variation existed
in their experimental technique. [1] Contrastingly, Polson
and Hanes (1987) were not able to demonstrate any fiber
attachment to periodontitis-affected cementum following
citric acid treatment. Differences between studies likely relate
to basic biomechanical factors of periodontal wound healing
overriding the experimental condition in the study by Polson
and Hanes.[6]
Mechanical instrumentation of the root surfaces was done in
order to remove the hypermineralized surface layer present on
the periodontitis-affected roots and obtain a smooth glass-like
surface.[16]
36
Application of the respective root conditioners on the sample
was done passively with cotton pellets saturated with
the agent that were changed every 30 seconds for a total
period of 5 minutes. The “Passive Burnishing Technique”
for application of root conditioner has been preferred over
burnishing technique as the latter may itself form smear layer
which partially or completely obliterate the dentinal tubule
openings.[10] Changing pellets every 30-seconds helped to
apply a constant concentration of the drug over the application
interval. It has been suggested that this procedure enhances
a chemical/mechanical action which chemically loosens
inorganic material and surface debris, thereby exposing
underlying dentin to demineralizing action of fresh acid.[16]
SEM analysis of the conditioned root surfaces revealed that
removal of smear layer by tetracycline HCl (250 mg/ml) and
citric acid was better than doxycycline (100 mg/ml). This could
be attributed to the lower pH of tetracycline HCl (pH 1.6) and
citric acid (pH 1) as compared to doxycycline HCl (pH 2.2).
Removal of the smear layer was near total following a 5 minute
application of citric acid, tetracycline, and doxycycline group
except for few areas which were covered by debris. This
debris may be (i) fragments of enamel, cementum, or dentin
chipped off during instrumentation; (ii) foreign material that
contaminated the surface during preparation of the specimen
for SEM; (iii) precipitation artifacts resulting from interactions
between buffer and fixative materials or between the specimen
and these materials; or (iv) a combination of the above (Lasho,
O’Leary and Kafrawy).[1]
A maximum mean total number of tubules were found
in tetracycline HCl-treated specimens followed by citric
acid-treated specimens followed by doxycycline. Lafferty
TA, Gher ME and Gray JL also reported that conditioning
with tetracycline HCl and citric acid produced comparable
surface characteristics when used on periodontally diseased
human root surfaces.[17] This is probably because pH of citric
acid (pH 1) and tetracycline HCl (pH 1.6) was acidic enough
to expose similar and considerable number of dentinal
tubules whereas pH of doxycycline (pH 2.2) was less acidic
as compared to the other two agents. These results are in
accordance with studies done by Madison and Hokett and
Shetty, Dinesh and Seshan.[8,4]
Tetracycline-treated specimens had the highest number of
patent tubules when compared to citric acid and doxycycline.
Doxycycline-treated specimens had the least number of
patent tubules among the three agents used. These results
are in agreement with earlier studies.[8,18,19] On the contrary,
Sterrett JD, Simmons J, Whitford G, and Russell CM found
that citric acid solution (pH 1.6) was more effective than
tetracycline (150 mg/ml) in demineralizing dentin which
could be attributed to the lesser concentration (150 mg/ml) of
tetracycline used.[15]
The diameter of tetracycline HCl conditioned specimens was
significantly more than doxycycline. The diameter of citric
acid-treated specimens was more than doxycycline-treated
specimens but less than tetracycline-treated specimens.
Garberoglio and Braimstrom (1976), Tronstad (1973),
Hanes, O’Brien, and Garnick (1987) have also shown that
in addition to removing the smear layer these agents also
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Chahal, et al.: Effect of citric acid, tetracycline, and doxycycline on instrumented periodontally involved root surfaces: A SEM study
enlarge the openings of the dentinal tubules as demonstrated
by the increase in tubule diameter following treatment with
them.[3] This enlargement or widening of the tubule orifice
can be attributed to the preferential demineralization of the
peritubular dentin by these agents.
In the present study, it was found that root conditioning in
all the three experimental groups helped in the removal of
smear layer, exposure of dentinal tubules, and also widening
of dentinal tubule orifices in vitro. The type and degree of
instrumentation of the specimens before acid treatment and
the angulation of the electron beam may have affected the
appearance of the root surface and dentinal tubular orifices
slightly.
CONCLUSION
The root conditioning agents used in this study were found
to be effective in removing the smear layer, uncovering and
widening the dentin tubules, and unmasking the dentin
collagen matrix. However, among the three groups, the results
were best in tetracycline HCl conditioned group showing
that the 250 mg/ml concentration of tetracycline HCl is best
suited to be used as root conditioning agent. Hence, the
application of tetracycline HCl as a root conditioner might have
a significant role in periodontal wound healing and futuristic
new attachment in vivo.
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How to cite this article: Chahal GS, Chhina K, Chhabra V,
Bhatnagar R, Chahal A. Effect of citric acid, tetracycline, and
doxycycline on instrumented periodontally involved root surfaces:
A SEM study. J Indian Soc Periodontol 2014;18:32-7.
Source of Support: Nil, Conflict of Interest: None declared.
37