Clinical Cases Dent. Med. Probl. 2014, 51, 3, 402–409 ISSN 1644-387X
© Copyright by Wroclaw Medical University and Polish Dental Society
Katarzyna Banaszek1, A, B, D–F, Monika Łysakowska2, B–E, Jerzy Sokołowski1, E
PerioFilm Preparation in the Complicated Endodontic Retreatment of a Tooth with Apical Resorption During Orthodontic Therapy Ocena zastosowania preparatu PerioFilm w powikłanym leczeniu endodontycznym w trakcie leczenia ortodontycznego zęba z zaawansowaną resorpcją wierzchołkową 1 2
Department of General Dentistry, Chair of Restorative Dentistry, Medical University of Lodz, Lodz, Poland Department of Medical and Sanitary Microbiology, Medical University of Lodz, Lodz, Poland
A – research concept and design; B – collection and/or assembly of data; C – data analysis and interpretation; D – writing the article; E – critical revision of the article; F – final approval of article
Abstract The article presents the use of the PerioFilm adhesive dressing containing antibiotic piperacillin in the complicated endodontic retreatment of tooth 11 with severe apical resorption and alveolar bone loss in a young patient. Ongoing orthodontic therapy could lead to the loss of the tooth. Due to a suspicion of Enterococcus faecalis infection of the root canal system of tooth 11, additional microbiological examinations of Enterococcus faecalis strains sensitivity to piperacillin were performed. The piperacillin contained in the preparation was compared in vitro to other antibiotics and chemotherapeutics used in the treatment of Enterococcus faecalis infections. The results of the piperacillin action suggest that this antibiotic inhibits the growth of Enterococcus faecalis strains including those which are resistant to the other antibiotics and chemotherapeutics studied. The treatment caused inhibition of the inflammatory process and partial regeneration of the periapical bone tissues. Thus, it seems to be a valuable alternative and effective agent in the treatment of post-endodontic complications caused by Enterococcus faecalis infections (Dent. Med. Probl. 2014, 51, 3, 402–409). Key words: endo-perio syndrome, antibiotic, PerioFilm, endodontic retreatment, Enterococcus faecalis.
Streszczenie W pracy przedstawiono przypadek zastosowania preparatu PerioFilm w powikłanym powtarzanym wcześniej leczeniu endodontycznym w trakcie leczenia ortodontycznego zęba 11 z zaawansowaną resorpcją wierzchołkową. Substancją czynną w tym preparacie jest piperacylina, a nośnikiem mieszanka biodegradowalnych żywic. Uzyskano wstępnie dobre wyniki powtórnego leczenia endodontycznego tym preparatem. Ze względu na podejrzenie zakażenia o etiologii Enterococcus faecalis dotyczącego systemu kanałowego zęba 11 zdecydowano się przeprowadzić dodatkowe badania mikrobiologiczne wrażliwości szczepów ziarenkowca Enterococcus faecalis na pieperacylinę i inne chemioterapeutyki. Porównano in vitro działanie piperacyliny wchodzącej w skład preparatu do innych antybiotyków i chemioterapeutyków stosowanych w terapii zakażeń Enterococcus faecalis. Wyniki działania piperacyliny sugerują, że ma działanie hamujące wzrost szczepów Enterococcus faecalis, w tym tych, które są oporne na wiele badanych antybiotyków i chemioterapeutyków, zatem stanowi cenną alternatywę w leczeniu zakażeń w obrębie jamy ustnej powodowanych przez te drobnoustroje. Preparat PerioFilm wydaje się skuteczny w leczeniu powikłań powstałych w leczeniu zespołu endo-perio (Dent. Med. Probl. 2014, 51, 3, 402–409). Słowa kluczowe: zespół endo-perio, PerioFilm, antybiotyk, leczenie endodontyczne, Enterococcus faecalis.
PerioFilm Preparation in the Complicated Endodontic Retreatment of a Tooth
Root resorption is a frequent complication caused by mechanical trauma during orthodontic treatment. It often progresses from the root apex and involves the entire apex with periapical tissues [1]. Root resorption is more frequently detected in maxillary than mandibular teeth and is associated with impairment of the tooth supporting apparatus. Advanced periapical and marginal periodontitis result in alveolar bone loss and weaker support of the tooth root [1, 2]. Orthodontic treatment may be accompanied by the development of chronic gingivitis and periodontitis, frequently induced by lack of hygiene while wearing braces, which leads to destruction of the gingival connective tissue, periodontal ligament and alveolar bone, creating the pathway for bacteria between the oral cavity and the periapical region [3]. Chemomechanical preparation, attempts of eradication and root canal filling do not always completely eliminate bacterial flora. When voids and gaps are left in the filled canals and bacteria are additionally nourished by the inflammatory exudates from pathological pockets, secondary infection of the root canal system can occur [4, 5]. Examinations of the bacterial flora in the unsuccessfully treated canals have frequently shown the presence of Enterococcus faecalis [6–9]. A higher prevalence of infections caused by Enterococcus spp. strains is often associated with diagnostic and treatment procedures, improper application of antibiotics and increase in the number of immunocompromised patients. These microorganisms are naturally resistant to antibiotics and chemotherapeutics [10], thus the appearance of resistance to penicillin, aminoglycosides and fluoroquinolones poses a therapeutic challenge for clinicians. The aim of the study was to evaluate the Perio Film® preparation containing piperacillin in the complicated endodontic retreatment of a tooth with apical resorption during orthodontic therapy and to determine piperacillin efficiency against probable E. faecalis infection in vivo. PerioFilm, according to the manufacturer’s information, has not been so far used in endodontic treatment. Moreover, piperacillin activity was compared in vitro to other antibiotics and chemotherapeutics applied in the treatment of E. faecalis infections.
Case Report The product called PerioFilm is an adhesive dressing in the form of film used in dentistry (Italmed, Italy, Firenze; and Laboratorios Inibisa, S.A. Spain, Barcelona). The powder (100 mg) contains piperacillin sodium salt (100%) which is
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an active substance. The fluid (1 mL) is a solvent containing copolymers of aminoalkylmethacrylate, ammonium methacrylate, and 95% ethanol and water. An 18-year old female patient with braces on the maxilla reported a problem with tooth 11. During the eight-year orthodontic treatment (first with a removable orthodontic appliance and later with braces), she had developed some treatmentrelated complications such as periapical abscesses around tooth 11. Due to them, tooth 11 had been endodontically treated a few times. On the first clinical examination, the following symptoms were detected: grade 3 tooth mobility, pathological pockets 9 mm deep on the mesial and 7 mm deep on the distal surface with pus, purulent exudate from the pockets, chronic purulent apical periodontitis and an active fistula at the bottom of the pathological pocket (Fig. 1). Tooth 11 remained in the maxilla owing to the braces. Oral hygiene was poor. The braces were left on the upper teeth during the endodontic and periodontal treatment described in this article. Radiographs (Fig. 2a and b) showed transparency around the root apex of tooth 11, indicating a 2.5 mm wide bone destruction; inflammatory lesions involved bilaterally the entire root reaching the tooth crown. Shortening of 1/3 of the original root length (grade 4 root resorption according to Levander et al. [2, 11, 12]) with the loss of alveolar lamina dura up to 2/3 of the root length on the mesial side of tooth 11 and 21 and semicircularly rounded root apices of these teeth were identified. Due to the generalized inflammation of the marginal periodontium, periodontal treatment was performed as follows: supra- and subgingi-
Fig. 1. The lingual view of tooth 11. The arrow indicates the fistula orifice with purulent exudate on the mesial side of the tooth Ryc. 1. Widok zęba 11 od strony językowej. Strzałka wskazuje ujście przetoki z ropnym wysiękiem od strony mezjalnej zęba
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Fig. 2a–b. The radiographs of maxillary teeth (11 and 21). Transparency at the root apex of tooth 21, indicating inflammatory lesion of 2.5 mm wide, which involve bilaterally the entire root reaching the tooth crown. Mesial side of tooth 21 with the vertical bone loss. Shortening of 1/3 of the original root length of tooth 11 and 21 as compared to roots of tooth 12 and 22; root apices of tooth 11 and 21 rounded semicircularly. Partial loss of the alveolar process in the maxillary bone. The patient is wearing braces on these teeth: a) before retreatment; b) after removal of the root canal filling Ryc. 2a–b. Radiogramy zębów szczęki (11 i 21). Przy wierzchołku korzenia jest widoczne przejaśnienie odpowiadające odczynowi zapalnemu o szerokości do 2,5 mm, zmiany zapalne obejmują obustronnie cały korzeń, sięgając do korony zęba. Od strony mezjalnej zęba 21 pionowy zanik kostny. Skrócenie długości korzeni zębów 11 i 21 o ponad 1/3 długości w odniesieniu do korzeni zębów 12, 22; wierzchołki korzeni zębów 11, 21 półkoliście zaokrąglone. Widoczny jest częściowy zanik wyrostka zębodołowego kości szczękowej. Na zęby jest założony stały aparat ortodontyczny: a) przed ponownym leczeniem, b) po usunięciu wypełnienia z kanału korzeniowego
val scaling of all maxillary and mandibular teeth, curettage with hand instruments followed by the ultrasonic procedure, and pocket irrigation with 0.2% chlorhexidine solution. Although the canal of tooth 11 on the radiograph seemed (Fig. 2a) to be properly filled, it was decided to retreat it. The presented case should be regarded as an endo-perio lesion because the infection around tooth 11 involved deep pathological pockets reaching the root apex. The management of an endoperio lesion includes endodontic and periodontal treatment. During the endodontic retreatment, the patient was treated in aseptic conditions with the rubber dam isolation. The gutta-percha cone was removed with hand and rotary instruments ProTaper (Dentsply Maillefer). The color of the cone tip (1–2 mm) was changed from orange-pink to gray and green. A profuse purulent yellowish and green discharge was found in the canal. The initial working length was established electronically (apex locator IPEX, NSK, Japan). The canal instrumentation was performed with the “step-back” technique using Kerr files (Dentsply Maillefer); size # 40 initial IAF, size # 55 MAF and size # 80 FF. For irrigation, the following agents were
applied: 5.25% NaOCl solution (10 mL) with passive ultrasonic irrigation (a size 20 file), 15% EDTA (5 mL to remove smear layer), and 0.9% NaCl solution. Considering the therapeutic difficulties, endo-perio character of a lesion around tooth 11 and possibility of long-lasting infection induced by anaerobic Enterococcus species [3, 9], the authors decided to use PerioFilm containing piperacillin antibiotic as a local pharmacotherapy. The patient gave informed consent to the proposed treatment and the study was approved by the Bioethics Commission of the Medical University of Lodz, Poland: # RNN/92/13/KE. PerioFilm was prepared according to the manufacturer’s recommendations and applied to the paper-point dried canal with a 2.5 mL syringe and a blunt-ended thin needle from the kit. PerioFilm was inserted into the root canal up to the region of the resorbed apex. One or two PerioFilm drops were applied to the canal surface and gently blown with air-spray. The product hardened on contact with air. One minute after material hardening, access to the canal was tightly obturated with glassionomer cement. PerioFilm was applied 4 times in 7–10-day intervals.
PerioFilm Preparation in the Complicated Endodontic Retreatment of a Tooth
At the same time, PerioFilm (1–2 drops) was also applied to the bottom of the dried pathological pockets at the mesial, distal and lingual surfaces of tooth 11. After one minute, the material hardened. Following the last PerioFilm application (40 days from the beginning of the treatment), the canal was filled with a non-setting calcium hydroxide paste (Biopulp, Chema-Elektromet, Rzeszow, Poland) using a Lentulo spiral and the material was condensed in the canal orifice with a sterile cotton pellet. The access to the pulp cavity was obturated with a glass-ionomer cement. Considering the previous reoccurrence of the difficulties in the treatment of tooth 11, it was decided to check whether PerioFilm with piperacillin would also be efficient in eradicating E. faecalis strains, often very resistant to antibiotics. Until the completion of orthodontic treatment, the root canal of tooth 11 was filled with calcium hydroxide material and tightly obturated. Calcium hydroxide was used after the 4th application of PerioFilm to efficiently inhibit the process of resorption. High calcium hydroxide pH neutralizes lactic acid induced by osteoclasts, which in turn prevents dissolution of the bony structure. Moreover, an alkaline environment inhibits collagenase and acid phosphatase activity and activates alkaline phosphatase, which plays an important role in tissue repair. After the completion of the orthodontic treatment and stabilization of the treated tooth, the apical part of the root canal was filled with MTA material and lateral condensation of gutta-percha with sealer was used in the remaining portion of the canal; the crown was restored with a composite material.
Laboratory Examinations of Enterococcus faecalis Strains The strains used in this in vitro study derived from different materials: urine (n = 4), wound smears (n = 2), throat smears (n = 1), environmental smears (n = 2), and central venous catheter smear (n = 1). Clinical and reference strains (E. faecalis ATCC 29212, E. faecalis ATCC 51299) were stored at –70°C for further study. The affiliation of microorganisms to a particular species was determined with API 20 Strep tests (bioMerieux) according to the manufacturer’s instructions and confirmed by the PCR reaction for D-alanine-D-alanile ligase (ddl) genes [13]. Bacterial DNA was isolated by a Bacteria AX kit (A&A
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Biotechnology, Poland). PCR reactions were conducted in a volume of 50 μ in a Biometra thermocycler. The reaction mixture contained 0.7 U Supertherm polymerase (JMR), 60nM of primers [13] (IBB), 4.5mM MgCl2 (Qiagen), 5 μL of PCR buffer and 400μM dNTP (Qiagen). The obtained products were separated on 1.5% agarose gel (Prona) in TAE buffer and stained with ethidium bromide (Sigma). Examination of E. faecalis strain susceptibility to PerioFilm was performed on 10 clinical and 2 reference strains with the dilution method on liquid medium Mueller-Hinton (bioMerieux) according to the Clinical and Laboratory Standards Institute (CLSI) recommendations [14]. The dilutions of antibiotics were examined in the range from 1024 mg/L to 2 mg/L. Evaluation of bacterial sensitivity to antibiotics was performed with the diffusion disk method. The following antibiotics and chemotherapeutics (Becton Dickinson) were analyzed: ampicillin (10 µg), penicillin (10 U), chloramphenicol (30 µg), ciprofloxacin (10 µg), erythromycin (15 µg), gentamicin (120 µg), streptomycin (300 µg), linezolid (30 µg), tetracycline (30 µg), teicoplanin (30 µg), and vancomycin (30 µg). Examination of the sensitivity to drugs was conducted on medium Mueller-Hinton II (bioMerieux). The media were incubated in 37°C for 16–18 h, and 24 h for vancomycin. The obtained results were interpreted according to the recommendations of the National Reference Centre for Drug Sensitivity of Microorganisms [15] and CLSI [14].
Clinical Management Forty days after the commencement of the study, the clinical examination revealed tooth stabilization, a decrease in grade 3 mobility to grade 2, lack of marginal periodontitis, reduction in pathological pocket depth from 9 mm to 5 mm on the mesial side of the tooth and from 7 mm to 2 mm on the distal side. The fistula closed after the first application of PerioFilm. A radiograph showed the healing of the periapical tissues (Fig. 3).
Drug Sensitivity of the Strains Studied A strain resistant to penicillin and ampicillin (59p) was the only strain moderately sensitive to piperacillin. This strain was also resistant to ciprofloxacin, erythromycin, and gentamicin, with a moderate level of resistance to chloramphenicol, streptomycin and tetracycline. The remain-
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K. Banaszek, M. Łysakowska, J. Sokołowski Table 1. Drug sensitivity of the studied E. faecalis strains to piperacillin (PerioFilm) Tabela 1. Lekowrażliwość badanych szczepów E. faecalis na piperacylinę (PerioFilm)
Fig. 3. The radiograph of teeth 11 and 21. Partial healing of periapical tissue of tooth 11. The state after the removal of the root canal material Ryc. 3. Radiogram zębów 11 i 21. Częściowe zmniejszenie odczynu zapalnego wokół korzenia zęba 11. Stan po usunięciu materiału wypełniającego kanał korzeniowy
Items
Strain no.
Minimal inhibitory concentration (MIC) value (μg/L)
1.
44p
8
2.
59p
32
3.
38p
2
4.
51p
2
5.
53p
2
6.
92p
2
7.
103p
2
8.
1p
16
9.
61p
16
10.
70p
16
11.
ATCC 29212 Sensitive to vancomycin
16
12.
ATCC 51299 Resistant to vancomycin
4
MIC range for strains resistant to piperacillin: ≥ 128. MIC range for strains moderately resistant to piperacillin: ≥ 32 g/L ≤ 64 g/L. MIC range for strains sensitive to piperacillin: ≤ 16 ug/L.
ing strains, despite the resistance to different antibiotics (mainly tetracycline (n = 9), ciprofloxacin (n = 7), erythromycin (n = 5), penicillin (n = 4), ampicillin (n = 4), and streptomycin (n = 3), appeared to be sensitive to piperacillin. The detailed results are presented in Table 1 and Table 2.
Discussion Due to the acute course of the disease, the composition of the bacterial flora in the root canal system and in the pathological pockets was not tested at the time of the patient’s first visit.
Table 2. Drug sensitivity of the examined E. faecalis strains Tabela 2. Lekowrażliwość badanych szczepów E. faecalis Items
Strain no.
AMP
C
CIP
E
GM
IMP
LNZ
P
S
TE
TEC
VA
1.
44p
S
S
R
S
R
S
S
R
S
R
S
S
2.
59p
R
I
R
R
R
S
S
R
I
I
S
S
3.
38p
S
R
R
R
R
S
S
S
R
R
S
S
4.
51p
S
S
I
S
S
S
S
S
S
R
S
S
5.
53p
S
S
I
I
S
S
S
S
S
R
S
S
6.
92p
R
S
R
R
R
S
S
S
R
R
S
S
7.
103p
S
I
I
R
R
S
S
S
R
R
S
S
8.
1p
S
S
R
S
R
S
S
S
S
R
S
S
9.
61p
R
S
R
I
S
S
S
R
S
R
S
S
10.
70p
R
I
R
R
R
S
S
R
S
R
S
S
Description of abbreviations used: AMP – ampicillin (10 µg), CIP – ciprofloxacin (5 µg), C – chloramphenicol (30 µg), E – erythromycin (15 µg), GM – gentamicin (120 µg), LNZ – linezolid (30 µg), P – penicillin 10U, S – streptomycin (300 µg), TE – tetracycline (30 µg), TEC – teicoplanin (30 µg), VA – vancomycin (30 µg); S – sensitive strain; I – moderately sensitive strain; R – resistant strain.
PerioFilm Preparation in the Complicated Endodontic Retreatment of a Tooth
PerioFilm was used due to its wide spectrum of activity. The concentration of piperacillin released from the preparation maintained at the dose of 8.5 mg/L for 8–10 days and inhibited 90% of anaerobic bacteria in the in vitro study [16]. In our previous in vitro study on extracted human teeth, PerioFilm quickly hardened on contact with air as a result of evaporation of an organic component, i.e. ethanol, leaving a thin film that remained on the root surface in high humidity conditions, and gradually underwent biodegradation, releasing the antibiotic [17]. Enterococcus faecalis species have frequently been isolated and associated with persistent periapical periodontitis [6, 7]. The pathogenicity of E. faecalis may be related to their capability to survive in difficult conditions for a longer time, even with lack of nutritional substances [18]. The virulence of E. faecalis strains can result from its ability to invade dentinal tubules and to adhere to collagen fibers in the presence of serous exudate [6]. Due to the suspicion of Enterococcus faecalis infection concerning the root canal of tooth 11, additional microbiological examinations of strain sensitivity to piperacillin were performed. Multidrug resistant strains were chosen to compare their sensitivity to that of piperacillin. The study showed that strains of 9 clinical isolates of E. faecalis and 2 reference strains, E. faecalis ATCC 51299 resistant to vancomycin and E. faecalis ATCC 29212 sensitive to vancomycin, did not indicate resistance to PerioFilm piperacillin. Only one strain revealed a moderate level of sensitivity to piperacillin. At the same time it was also resistant to ampicillin, ciprofloxacin, erythromycin, gentamicin, penicillin, and moderately sensitive to chloramphenicol, streptomycin, and tetracycline. Antibiotic therapy favors selection and spreading of resistant strains, an example of which is the frequent occurrence of resistance to tetracycline [19], which is in compliance with the results of this study. Lack of sensitivity to gentamicin (HLAR, High Level Aminoglycoside Resistance) was noticed in 7 strains of E. faecalis, whereas to streptomycin in three. The occurrence of resistance to gentamicin differs among countries, e.g. in Sweden it was only 1.9% [19] and in the USA 50% of the strains examined showed resistance [20]. In our study, seven E. faecalis strains were resistant to ciprofloxacin. This confirms a growing increase in resistance to this drug due to its frequent use [21]. The percentage of resistance to erythromycin was low among enterococci isolated in Sweden (8.5%) [19], but a much higher level of resistance (25%) was reported in the USA [20].
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As shown in the literature, enterococci isolated from root canals often do not react to antibiotic therapy [22]. Therefore, effective agents which might be applied in the treatment of oral cavity infections induced by these bacteria should be searched for. PerioFilm with piperacillin appears to be such a preparation. The occurrence of resistance to piperacillin was previously found among 71.8% of E. faecalis strains isolated from bile tracts. Those strains were also highly resistant to ampicillin (76.7%) [23]. According to the literature, the percentage of strains resistant to piperacillin isolated from different clinical materials amounted to 53.4% [24], but the Swedish data showed a much lower percentage [25, 26]. However, up to 98% of E. faecalis strains which were sensitive to ampicillin remained sensitive to piperacillin with the inhibitor, and 96% of strains to imipenem [27]. In our study, only one of four E. faecalis strains resistant to ampicillin was moderately resistant to piperacillin (PerioFilm). Moreover, all of the investigated strains were sensitive to linezolid, which is in accordance with literature reports [28, 29]. The results of this study confirm that Perio Film is a valuable agent with high activity against E. faecalis strains that often cause infections within root canals [6–8]. Thus, it seems that this agent can be successfully used to eradicate microorganisms in infections induced after root canal treatment. However, sometimes despite adequate root canal treatment, some microorganisms can survive in the parts of the root canal system which are unavailable to instruments and irrigants [30, 31]. The pathogenic factor from the infected canal contributes to resorption of the alveolar bone and the apical cementum without the presence a mechanical injury. In the presented case, the mechanical injury of the tooth induced by wearing braces additionally resulted in formation of the advanced resorption of the root apex and the alveolar bone, favoring the development of endo-perio lesion.
Conclusions The clinical study revealed efficiency of the piperacillin contained in the PerioFilm preparation which was used in the complicated endodontic retreatment of a tooth with apical resorption during orthodontic therapy. Piperacillin inhibited the growth of Enterococcus faecalis strains, including those which were resistant to the other antibiotics and chemotherapeutics studied, thus making it a valuable option in the treatment of oral cavity infections induced by these microorganisms.
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Address for correspondence: Katarzyna Banaszek Department of General Dentistry Chair of Restorative Dentistry Medical University of Lodz Pomorska 251 92-231 Lodz Poland E-mail:
[email protected] Conflict of interest: None declared Received: 22.03.2014 Revised: 19.04.2014 Accepted: 22.05.2014 Praca wpłynęła do Redakcji: 22.03.2014 r. Po recenzji: 19.04.2014 r. Zaakceptowano do druku: 22.05.2014 r.
