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Dalia Khalil

Margareta Hultin
Linda Andersson Fred
Nina Parkbring Olsson
Bodil Lund

Authors affiliations:
Dalia Khalil, Margareta Hultin, Department of
Dental Medicine, Division of Periodontology,
Karolinska Institutet, Huddinge, Sweden
Linda Andersson Fred, Nina Parkbring Olsson,
Swedish Public Dental Service, Stockholm, Sweden
Bodil Lund, Department of Dental Medicine,
Division of Orofacial Diagnostics and Surgery,
Karolinska Institutet, Huddinge, Sweden and
Department of Oral and Maxillofacial Surgery,
Karolinska University Hospital, Stockholm, Sweden

Antibiotic prescription patterns among


Swedish dentists working with dental
implant surgery: adherence to
recommendations

Key words: antibiotic prophylaxis, implant insertion, prescription behavior


Abstract
Objectives: To investigate antibiotic prophylaxis prescription behaviors among Swedish dentists
working with dental implant surgery and the influence of scientific reviews.
Material and methods: An observational questionnaire study was conducted in 2008 and 2012.
Dental clinic addresses were found through online search services of Swedish telephone directories.
The questionnaires were posted to eligible dentists (120 in 2008, 161 in 2012) in the Stockholm
region, Sweden. Absolute frequencies were used to describe the data. Chi-square tests were

Corresponding author:
Dalia Khalil, DDS
Department of Dental Medicine
Division of Periodontology
Karolinska Institutet
P.O. Box 4064, SE-141 04 Huddinge, Sweden
Tel.: +46 768256380
Fax: +46 87118343
e-mail: Dalia.Khalil@ki.se

applied to assess statistically significant differences.


Results: The response rate was 75% in 2008 and 88% in 2012. In 2008, 88% of the dentists
routinely prescribed antibiotic prophylaxis when performing implant surgery and 74% in 2012
(P = 0.01). There was a significant reduction in the dentists prescription patterns as 65% prescribed
a single dose in 2012, compared to 49% in 2008 (P = 0.04). Amoxicillin was the drug of choice for
47% of the respondents in 2012, and 21% in 2008 (P = 0.01). Dentists without postgraduate clinical
training were significantly more prone to extend antibiotic administration after surgery (P < 0.009).
Conclusions: There is a wide variation in the choice of compound and prescription patterns of
prophylactic antibiotic prior to implant insertion. A reduction in antibiotic prescription to a single
dose was observed comparing 2008 and 2012, probably influenced by scientific reviews. Dentists
with postgraduate education are more likely to limit antibiotic usage.

Date:
Accepted 18 March 2014
To cite this article:
Khalil D, Hultin M, Fred LA, Olsson NP, Lund B. Antibiotic
prescription patterns among Swedish dentists working with
dental implant surgery: adherence to recommendations.
Clin. Oral Impl. Res. 00, 2014, 16
doi: 10.1111/clr.12402

Dental implants insertion is a routine treatment modality for the rehabilitation of partially and completely edentulous jaws. Longterm follow-up has shown successful results
in a previous number of studies (Albrektsson
et al. 1988; Lekholm et al. 1999; Ekelund
et al. 2003; Jemt & Johansson 2006). Moreover, implant survival rates of 9095% have
been reported in longitudinal studies of up to
20 years (Pjetursson et al. 2004; Lekholm
et al. 2006; Roos-Jansaker et al. 2006;
Astrand et al. 2008). Despite the high success
rates, failures do occur and may be categorized as either early failures, occurring prior
to prosthetic restoration, or late failures, after
placement of the prosthesis. Causes for early
implant failures include lack of primary
implant stability, surgical trauma, and perioperative contamination (Sakka et al. 2012).
Late failures have been suggested to be associated with occlusal overload and peri-implantitis (Klinge et al. 2012; Naert et al.
2012; Sakka et al. 2012; Chang et al. 2013).

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Oral surgical procedures are often graded as


class II (clean-contaminated surgery), with a
rate of local infection of 1015%. The incidence of infections is reduced to 1% with
proper surgical technique and prophylactic
antibiotics (Olson et al. 1984; Peterson 1990).
Antibiotics have been used in the last decade
to prevent local and systemic bacterial infective complications. However, the harm to the
public health and the undesirable effects of
antibiotics when used as prophylaxis regimens cannot be neglected (Bidault et al.
2007). The potential benefit of antibiotic regiments during routine dental implant insertion is a controversial subject, and many
dentists remain convinced of the positive
influence of antibiotics during routine
implant surgery while others believe they
have no effect.
Health authorities have reported on the
importance of reducing the total use of antibiotics (Huovinen & Cars 1998), primarily because their overuse can lead to the emergence

Khalil et al  Antibiotics during dental implant insertion

and development of resistant bacterial


strains. Side effects such as interaction with
other drugs, gastro-intestinal tract distress,
secondary infection, toxicity, and allergic
reactions must also be considered (Lawler
et al. 2005; Resnik & Misch 2008). The risk
of inappropriate use of antibiotics and widespread antibiotic resistance appear to be far
more important than possible perceived benefit (Tong & Rothwell 2000). A scenario in
which all antibiotics become ineffective for
treating even common infections in the near
future has been suggested by the Global Economic Forum which ranked the development
of antibiotic resistance as one of the 31 global risks for 2014 (weforum 2014).
Sweden is a leading country in the field of
implant dentistry and the technique first
introduced by P.I. Br
anemark and collaborators during the 1970s (Branemark et al. 1977).
The surgical technique developed for placing
dental implants also included antibiotic regimens during surgery and a postoperative
healing period of 10 days (Adell et al. 1985).
Today, dental implant surgery is routinely
performed by general dentists as well as specialists, and the number of dental implants
placed has dramatically increased (Narby
et al. 2008). Antibiotic prescriptions among
dentists in Sweden slowly increased until
2007; however, since then, a small reduction
in antibiotic prescription has been noticed
(Blomgren et al. 2009). Penicillin V is the
most commonly prescribed drug, representing
75% of all antibiotics prescribed by dentists
in Sweden (Hellman et al. 2013).
The Swedish strategic program against
antibiotic resistance (Strama) recently published revised recommendations for antibiotic prescription in conjunction with implant
surgery (Blomgren et al. 2009). The Swedish
Council on Health Technology Assessment
(SBU), which is responsible for assessment of
several scientific topics in medical and dental
health care, published a literature review in
2010 regarding antibiotic prophylaxis in surgery, including dental implant procedures
(Ahlberg et al. 2010). As it is of out-most
importance to implement a national guideline on the use of antibiotics, the influence
of recommendations and reviews as means in
this strategic work needs to be assessed. It is,
therefore, of interest to compare the antibiotic prescription patterns before and after
these publications.
The aim of this study was to investigate
the antibiotic prescription patterns among
dentists in the Stockholm region who perform dental implant surgery and to assess
their adherence to recommendations and

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Clin. Oral Impl. Res. 0, 2014 / 16

scientific reviews on antibiotic routines during dental implant surgery.

Material and methods


Study design

This study is based on an observational questionnaire survey with two cohorts conducted
in 2008 and 2012 to investigate whether the
recommendations of Swedish strategic programme against antibiotic resistance (Strama)
(Blomgren et al. 2009) and the scientific
review from SBU (Ahlberg et al. 2010) influenced the antibiotic regimens prescribed by
Swedish dentists, who performed >20 dental
implant surgical procedures per year. An
anonymous questionnaire was sent to all eligible dentists in Stockholm region, Sweden.
Data collection

Dental clinics were identified through online


search services of the Swedish telephone
directory (www.hitta.se and www.eniro.se)
using key words implant, dental clinic,
and Stockholm region. Clinics were then
contacted via telephone, and the project was
explained to the dentists. In 2008, the questionnaires were sent to all eligible dentists
who agreed to participate (120 dentists in 76
clinics), and in 2012, they were sent to the
same clinics with the additions of new clinics established in the intervening period (161
dentists in 105 clinics). The questionnaire
included a prepaid envelope and a cover letter
explaining the purpose of the study ensuring
confidentiality would be maintained. In both
surveys, reminder letters were sent to all
included clinics.
Questionnaire

The questionnaire included two open and 10


closed questions. The first part included
demographic data on gender, age, undergraduate training, number of years of clinical experience, implant surgical experience, and
implant education. The second part asked
about the presence of local clinical guidelines,
routines used at the clinic, and policies regarding antibiotic prescription prior to implant
insertion as well as local or systematic factors
influencing prescription patterns. Two questions inquired about potential benefits from
the establishment of national guidelines and
interest in gaining information about antibiotic resistance. The 2012 survey included five
additional questions concerning respondents
knowledge of the recent recommendations
and scientific review from Strama and SBU, if
these had influenced their prescribing
behavior.

Data analysis

Statistical analysis was performed using SPSS


for Windows release 21.0 (SPSS Inc., Chicago,
IL, USA). Absolute frequencies were used to
describe the data and chi-square tests to
assess statistically significant differences, and
the level of significance was P < 0.05.

Results
The response rate in 2008 was 75% (n = 90)
and 88% (n = 142) in 2012. Due to missing
data, primarily regarding routines in prescribing prophylactic antibiotics prior to implant
placement, five and nine questionnaires were
excluded in 2008 and 2012, respectively.
Therefore, 85 responses from 2008 and 133
from 2012 were included in the analyses.
Table 1 shows the demographic data for
participating dentists. The majority of dentists were male (79%, 2008; 75%, 2012) and
in 55 years or older. With regard to their education in implant dentistry, 46% (n = 39) in
2008 had received clinical postgraduate training while the corresponding figure for 2012
was 40% (n = 53). In 2008, 54% (n = 46)
reported they had participated in a single
course in implant dentistry and 60% (n = 80)
in 2012. Moreover, 53% (n = 45) had over
10 years of experience in implant surgery in
2008 and 64% (n = 83) in 2012. Dentists
without postgraduate clinical training were
significantly more prone to extend antibiotic
prophylactic administration beyond the day
of surgery (P < 0.009).
There was a significant reduction in the
number of the dentists reporting the use of a
defined local rationale for antibiotic prescriptions during implant surgical procedures
between 2008 and 2012 (P = 0.04). There was
a significant reduction in the number of routinely prescribed antibiotics between the
cohorts (P = 0.01; Table 2).
Figure 1 illustrates the significant change
in the antibiotics prescribed (P = 0.006). In
2008, 67% (n = 50) of the dentists prescribed
phenoxymethylpenicillin (PcV), while 21%
(n = 16) prescribed amoxicillin. In 2012, 43%
(n = 42) of dentists prescribed PcV and 47%
(n = 46) prescribed amoxicillin. Other antibiotics, such as metronidazole and clindamycin, were less frequently used.
There was also a significant reduction in
the number of dentists prescribing antibiotic
beyond the day of surgery between 2008 and
2012 (P = 0.04). In 2012, 65% (n = 63) of the
respondents prescribed a single dose of antibiotics compared to 49% (n = 35) in 2008. In
2012, only 35% (n = 34) of the dentists
prescribed an antibiotic course for 3 days

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Khalil et al  Antibiotics during dental implant insertion

Table 1. Demographic data


2008
n = 85
n (%)

Characteristic

Gender
Male
66 (79)
Female
18 (21)
Age (years)
2534
6 (7)
3544
18 (21)
4554
28 (33)
>55
33 (39)
Undergraduate training
Swedish university
82 (98)
Abroad university
2 (2)
Implant education
Single Course
46 (54)
Not specified
46
Clinical postgraduate training
39 (46)
Oral and maxillofacial surgery
21
Periodontics
15
Pedodontics
1
Prosthodontics
1
Information about antibiotics in implant education
Yes
79 (93)
No
6 (7)
Clinical experience (years)
<10
5 (6)
1020
24 (29)
20
55 (65)
Implant experience (years)
<10
40 (47)
10
45 (53)

2012
n = 133
n (%)

P-value

99 (75)
33 (25)

0.547

11
33
29
60

(8)
(25)
(22)
(45)

0.343

128 (97)
4 (3)

0.777

80 (60)
80
53 (40)
33
14
1
0

0.379

Discussion

122 (92)
11 (8)

0.745

14 (11)
38 (29)
77 (60)

0.436

47 (36)
83 (64)

0.111

NS, non-significant differences; N, number of respondents.

Table 2. Number of dentists using local clinical


guidelines and the frequency of antibiotic prescriptions
2008
n (%)

2012
n (%)

Use clinic guidelines


Yes
73 (86)
97 (74)
No
12 (14)
34 (26)
Routinely prescribe antibiotics
Yes
75 (88)
98 (74)
No
10 (12)
35 (26)

P-value
0.038

0.010

compared to 51% (n = 36) in 2008. There


were a substantial number of different regimens reported. Although the collection of
reported regimens differed quantitatively and
qualitatively between the two time points,
no statistically significant difference could be
seen (Table 3).
In both surveys, more than 88% (n = 70,
2008; n = 115, 2012) of the dentists indicated
there was a need for national guidelines.

Fig. 1. Type of antibiotics used and prescription patterns in 2008 and 2012.

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Moreover, over 50% (n = 45, 2008; n = 80,


2012) were interested in gaining more information about antibiotic resistance.
In the 2012 questionnaire, 58% (n = 77) of
the respondents stated that they had read the
recent publications on antibiotic prescription
in implant dentistry, 82% (n = 62) of them
benefited from the information, and 33%
(n = 24) reported to have changed their antibiotic prescription pattern. A majority of dentists (96%) who had not read the recent
recommendations and review on antibiotic
prescription expressed an interest in reading
these publications. Accordingly, this suggests
that the dentists who read the publications
were more likely to prescribe a single dose
antibiotics (P = 0.004).

The high response rate to both questionnaires


lends strength to the results of this study and
allows for comparison between the two surveys. The present study showed a wide variation in the type and duration of prophylactic
antibiotic in connection with implant insertion among Swedish dentists. As the Stockholm region represents 20% of the Swedish
population, these surveys may be considered
as a representative sample of the antibiotic
prescription patterns of all Swedish dentists
who perform implant surgery. The data were
interpreted for those who prescribed antibiotics merely under special circumstances, such
as medical or local surgical factors, as not
prescribing routinely. However, the results
showed that the majority of Swedish dentists
surveyed routinely prescribe prophylactic
antibiotics prior to dental implant surgery, a
finding in agreement with a recent European
study from United Kingdom where 72% of
those surveyed routinely prescribed prophylactic antibiotics in conjunction with implant
insertion (Ireland et al. 2012). The similarity
is most likely due to the lack of clearly conclusive consensus regarding antibiotic prophylaxis in implant dentistry in Europe
(Ireland et al. 2012). However, as the scientific evidence regarding appropriate use of
antibiotics for implant surgery is not conclusive, the currently available information does
not provide the clinician with clear guidelines. It may be difficult for practicing clinicians to interpret the scientific evidence in
these recommendations and, subsequently, to
decide whether or not antibiotic prophylaxis
is appropriate. In addition, to protect the
patient from treatment complications, which
also may result in financial consequences
for both therapist and patient, prescription of

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Clin. Oral Impl. Res. 0, 2014 / 16

Khalil et al  Antibiotics during dental implant insertion

Table 3. Prescription regimens for phenoxymethylpenicillin, amoxicillin, metronidazole, and clindamycin in 2008 and 2012
n
PcV

2008

2012

2 g 1 h pre-op + 2 g 6 h postop
2 g 1 h pre-op + 1 g 6 h postop
1 g 1 h pre-op + 1 g evening
1 g pre-op
2 g pre-op
3 g pre-op
1 g b.i.d 9 710 days
2 g b.i.d 9 710 days
1 g t.i.d 9 35 days
1 g t.i.d 9 56 days
1 g t.i.d 9 710 days
2 g t.i.d 9 10 days
1 g t.i.d 9 30 days
Amoxicillin
1,5 g pre-op
2 g pre-op
750 mg 9 3 pre-op
3 g pre-op
750 mg 9 2 1 h pre-op + 750 mg 9 2 6 h postop
2 g 1 h pre-op + 2 g 6 h postop
750 mg 9 3 1 h pre-op + 750 mg 9 3 6 h postop
300 mg b.i.d 9 10 days
750 mg b.i.d 9 5 days
750 mg b.i.d 9 710 days
500 mg t.i.d 9 57 days
1 g b.i.d 9 710 days
2 g pre-op + 500 mg t.i.d 9 7 days
23 g Amoxicillin pre-op + PcV 1 g t.i.d 9 7 days
Metronidazole
400 mg 9 5 days
Clindamycin
300 mg b.i.d 9 10 days
600 mg 1 h pre-op

17
2
1
0
4
0
3
7
2
0
12
0
1

11
1
0
1
5
1
2
4
0
2
9
2
0

0
7
2
2
0
0
0
1
0
3
1
0
0
0

1
27
1
1
1
4
1
0
1
1
0
3
3
1

2
0

0
1

b.i.d, twice per day.


t.i.d, three times per day.
N, number of dentists reporting regimen.

antibiotics might be a reasonable choice


(Wardh et al. 2009).
During the 4 years between the surveys,
there was a noticeable change in the antibiotic
prescribed, as amoxicillin became the preferred drug of choice. Amoxicillin is widely
prescribed in conjunction with implant surgery, and its effect on reducing implant failures has been investigated in several clinical
trials (Dent et al. 1997; Ireland et al. 2012; Esposito et al. 2013). There are pharmacokinetic
reasons for replacing other substances (i.e.,
PcV) with amoxicillin as the absorption rate of
PcV is less predictable. For example, PcV
needs a more frequent dosing to maintain and
adequate concentration in blood, while amoxicillin shows superior absorption and bioavailability (Resnik & Misch 2008). These
characteristics, in combination with good coverage of the oral microflora, render amoxicillin
a suitable choice for antibiotic prophylaxis in
oral surgery.
A change in antibiotic prescription patterns was observed, as more than half of the
(65%) respondents in 2012 prescribed a single

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Clin. Oral Impl. Res. 0, 2014 / 16

perioperative dose, rather than an extended


regimen. A meta-analysis showed fewer
patients who received a single pre-operative
dose of antibiotics experienced implant failures compared to placebo or no treatment
(Esposito et al. 2010, 2013). However, the
studies included contained scientific weaknesses, as none of them reported significant
differences in implant failures between intervention and control groups due to the small
number of patients involved and they were
probably under-powered. Others suggest that
the benefits of prophylactic antibiotic are
negligible (Mazzocchi et al. 2007; Ahmad &
Saad 2012; Tan et al. 2014). A recent national
recommendation from the Swedish Medical
Product Agency suggests that 2 g amoxicillin
may be considered 1 h before implant insertion (Blomgren et al. 2012).
The more restrictive approach to antibiotic
therapy observed among dentists with postgraduate clinical training could be related
to their training, which includes an emphasis on both the benefits and the undesirable effects of antibiotics. Furthermore, a

short-term antibiotic educational program


showed promising results in educating den
tists on antibiotic usage (Ocek
et al. 2008).
Another possible reason for the more restrictive approach among the experienced dentists
is that they may be more confident of their
surgical skills and aseptic conditions in their
clinics, thus reducing the need for antibiotic
prophylaxis. Most dentists in our surveys
were in the older age group. This may be
explained by the tradition in Sweden to provide implant treatment in specialist clinics
where dentists with postgraduate training are
responsible for implant insertions. In addition, undergraduate implant education in
Sweden focuses mainly on the theoretical
part, and dentists interested in specializing in
implant surgery continue their postgraduate
education and, therefore, are somewhat older
before they enter practice. This observation
was confirmed by a survey of undergraduate
dental schools in 18 European countries
which showed that, although all schools provided theoretical courses, almost half
reported that students assist with implant
surgery, but only 5% actually perform patient
surgeries (De Bruyn et al. 2009).
Dental implant placement could predispose
patients to bacteremia (Takai et al. 2005; Bolukbasi et al. 2012), another reported that
implant placement does not significantly
increase the risk of developing bacteremia
(Pineiro et al. 2010). Bacteremia is more frequently associated with daily oral activities
such as mastication and tooth brushing, and
is strongly influenced by oral health (Lockhart et al. 2009; Termine et al. 2009; Legout
et al. 2012). Antibiotic prophylaxis can be
used for prevention of bacteremia in patients
that for medical reasons are susceptible to
distant or local site infection (Glauser et al.
1983). Approximately half of the dentists we
surveyed in 2008 (40% in 2012) agreed with
this concept and recommended antibiotics
only due to medical or local surgical factors.
However, today, the medical risk of these
intermittent bacteremia episodes is debated
(Thornhill et al. 2011).
The majority of the dentists surveyed
reported a need for national guidelines
addressing use of antibiotics and implant surgery, and more than half were interested in
information about antibiotic resistance. Our
study shows a noticeable shift from a defined
local rationale for antibiotic prescriptions to
national recommendation. The implementation of practice guidelines may result in
improved antimicrobial treatment behaviors
and reduce infection rates, excluding antimicrobial resistance control without further

2014 John Wiley & Sons A/S. Published by John Wiley & Sons Ltd

Khalil et al  Antibiotics during dental implant insertion

additional measures (Foucault & Brouqui


2007).
Considering the high response rate to both
surveys and the relatively large sample of
dentists in the Stockholm region, it may be
speculated that conclusions from this study
can be extrapolated for the entire country.
Although this study has some weaknesses
(i.e., questionnaire has not been formally validated), its merits override this issue by
showing that implementing guidelines and
postgraduate clinical training are important
in resolving conflicts over the appropriate use
of antibiotics in implant surgery.
As the responses to the questionnaire were
anonymous, it was not possible to analyze
changes in individual dentist behaviors

between the two surveys. However, as this


was not the aim of the study, the study
design can be regarded as relevant to our
defined objectives.
In conclusion, the results of the study
show that between 2008 and 2012, there was
a wide variation in the choice of compound
and prescription patterns of prophylactic antibiotic prior to implant insertion. Although
approximately one-third of the respondents
prescribed multiple doses in 2012, there was
a reduction in the antibiotic prescription to a
single dose between 2008 and 2012. This suggests that the recommendations and the scientific review may have influenced dentists
to reduce the antibiotic usage. Also, it seems
that postgraduate education results in a more

cautious approach to antibiotic prescription.


Further studies are required to investigate the
effect of prophylactic antibiotics in lowering
the risk of implant failure.

Acknowledgements: The authors


would like to thank Staffan Nilsson who
aided the statistical analysis and Magnus
Gustafsson for language guidance during the
writing process. The study financially
supported by Scandinavian Society for
Antimicrobial Chemotherapy (SSAC) and
Stockholm County Council. The authors
acknowledge that there is no conflict of
interest.

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