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Varicella Zoster Virus and Internal Root Resorption: A Case Report Bita Talebzadeh, DDS,* Saeed Rahimi, DDS, MSc,† Amir Ardalan Abdollahi, DDS* Ahmad Nouroloyuni, DDS,* and Vahide Asghari, DDS* Abstract Introduction: Herpes zoster is a viral infection caused by the reactivation of the varicella zoster virus. One of the less well-recognized maxillofacial complications is tooth root resorption. To our knowledge, this is the first case report about internal resorption associated with varicella zoster virus involving different dental quadrants. Methods: A 38-year-old woman presented with internal resorption of maxillary canine and first premolar tooth roots on the right quadrant and generalized internal resorption of second molars of both mandibular quadrants. The patient’s medical history showed mild oral lichen planus and infection with varicella zoster virus (chickenpox) with severe clinical manifestations 5 years previously. The patient developed diabetes mellitus type I and hypothyroidism a short time after varicella zoster virus infection, and by the time of infection with this virus, oral lichen planus had progressed from the reticular pattern to the generalized severe erosive form. Viral etiology could also be considered in these diseases. The root canals of the affected teeth were debrided, irrigated, and dried, and calcium hydroxide paste was placed in the root canals for a week during the first treatment session. The root canals were obturated during the second session. Results: Six-month follow-up showed improvement of oral lichen planus and resolution of widening of periodontal ligament of the affected teeth, with follow-up radiographs revealing no periapical problems. Conclusions: It appears some cases of internal root resorption classified as idiopathic might have viral etiology. Therefore, it is recommended that patients be questioned about a history of chickenpox and herpes zoster. (J Endod 2015;-:1–7)
Key Words Diabetes mellitus type I, hypothyroidism, internal resorption, oral lichen planus, periapical lesions, varicella zoster virus
T
he varicella zoster virus (VZV) is the etiologic agent for 2 clinical entities, varicella or chickenpox and herpes zoster infection (HZI) (1). Varicella caused by the primary infection of VZV is a benign childhood disease producing eruptive vesicles. As a result of primary infection of varicella, a skin virus moves to a sensory nerve and remains in a latent state in a ganglion (1, 2). When VZV in the latent state is reactivated, it develops into HZI, which causes severe pain and painful vesicles in the skin and mucosa around the affected sensory nerve distribution (3, 4). Thoracolumbar dermatomes (T3-L3) are most commonly affected by HZI (1, 4). HZI may also affect the cranial nerves, with the trigeminal nerve most frequently affected (18.5%–22%) (1). Herpes zoster affecting the trigeminal nerve is generally unilateral; it generally affects a single branch among the 3 branches, mainly the first branch or the optic nerve. Oral manifestations can be observed when the maxillary and mandibular branches are affected (4). Oral vesicles appear mainly after a skin manifestation (3, 5). Sometimes, however, there may be mucosal involvement without skin lesions (5). The vesicles erupt and leave mucosal erosions, but no scar is left in most cases (3). The most significant complication of HZI is postherpetic neuralgia (5); other complications may include facial scarring, motor nerve palsy, optic neuropathy, blindness, encephalitis, and calcinosis cutis (6). All the members of the herpesvirus family have the ability of remaining latent in the cells of the host body and reactivation. There are some reports of herpes zoster virus’s role in the development of oral lichen planus (zosteriform lichen planus) (7). In addition, studies have reported the role of human herpesviruses in the involvement of endocrine glands with autoimmune diseases such as the role of cytomegalovirus (HHV-5) and herpes simplex virus types 1 and 2 (HHV 1, 2) in the development of diabetes mellitus type I and thyroiditis, respectively (8, 9). On the other hand, osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, skin scars, odontogenic pain, short irregular roots, missing teeth, calcification and necrosis of dental pulp, internal resorption, and periapical lesions have been previously described in association with oral manifestations of maxillary and mandibular branches involvement with VZV (10–15). However, this is the first case report in relation to the concurrency of herpes zoster virus (HHV-3) with diabetes mellitus type I and thyroiditis and internal resorption of teeth in different dental quadrants.
Case Report A 38-year-old woman presented with severe dental pain in the region of the first premolar of maxillary right side with deep mesial caries. The patient had a history of varicella zoster (chickenpox) 5 years previously, for which she had been admitted
From the *Department of Endodontics and †Dental and Periodontal Research Center, Department of Endodontics, Faculty of Dentistry, Tabriz University of Medical Sciences, Tabriz, Iran. Address requests for reprints to Dr Saeed Rahimi, Dental and Periodontal Research Center, Department of Endodontics, Faculty of Dentistry, Tabriz University of Medical Sciences, Tabriz 5166615713, Iran. E-mail address: [email protected] 0099-2399/$ - see front matter Copyright ª 2015 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2015.02.014
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Case Report/Clinical Technique to the intensive care unit in a hospital for 13 days. The patient reported that before affliction with chickenpox, she had mild oral lichen planus bilaterally in the buccal regions of the oral cavity; however, after infection with this virus, during the disease, and after that, she had experienced serious erosive lichen planus in all the areas of the oral cavity such as lips and gums (in the form of linear gingival erythema and in some areas as leukoplakia) (Fig. 1). The medical history of the patient showed affliction with diabetes mellitus type I and hypothyroidism after infection with VZV (chickenpox). The patient had taken levothyroxine for the treatment of hypothyroidism, had received insulin injections for diabetes mellitus type I, had used betamethasone mouthwash for reducing the inflammation due to generalized oral lichen planus, and had received estrogen and progesterone for the treatment of infertility. Usual blood tests, including full blood count, erythrocyte sedimentation rate, alkaline phosphatase, serum calcium, liver function tests, urea, and electrolytes, were in normal ranges. In oral examinations, severe generalized erosive lichen planus and severe generalized periodontitis were observed (Fig. 1). Radiographic examinations showed deep mesial caries in teeth #1, #5, #17, #18, #20, #31, and #32 and loss of teeth #4, #19, and #30. The patient had had tooth #4 removed because of crowding, as recommended by her dentist, and had lost teeth #19 and #30 because of deep dental caries, severe pain, and the hopeless prognosis of the teeth. Periapical radiographic examinations showed internal resorption of the coronal thirds of teeth #5 and #6 and generalized internal resorption of the root canals of teeth #18 and #31 (Fig. 2). In other teeth with caries or without caries no evidence of resorption was seen.
Clinical evaluation of the patient revealed continuous severe pain and exacerbation of pain with heat, cold, and percussion and increased response to electric pulp tester in teeth #5, #18, and #31, whereas in tooth #6, responses to heat, cold, and percussion and response to electric pulp tester were in normal ranges, and despite the internal resorption, no caries was detected in this tooth. The patient did not have any history of trauma, orthodontic treatment, bleaching, pulpotomy, and restorative treatments, resulting in excessive production of heat during tooth preparation, which has a role in the etiology of internal resorption through trauma to and loss of the odontoblastic layer and predentin (16). Radiographic views, vitality tests, and sensitivity to percussion were normal in other intact teeth.
Treatment Plan Because a tooth with internal resorption is prone to irreversible pulpitis and if the inflamed pulp remains untreated, perforation might occur, resulting in the loss of the tooth (17), the patient was given adequate information about other treatment options, including extraction of the teeth and replacement with prosthetic treatments or implants and also no treatment at all. The patient opted for a proper treatment plan with root canal treatment. Endodontic Treatment Steps Local anesthesia was administered with injection of 1.8 mL lidocaine with 1:80,000 epinephrine in the region of inferior alveolar nerve for mandibular teeth and infiltration for maxillary teeth. Because the
Figure 1. Photographs (A–D) show severe generalized erosive lichen planus and severe periodontitis.
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Figure 2. Primary periapical radiographs of teeth #5, #6, #18, and #31. (A and B) Internal resorption of cervical third of roots of teeth #5 and #6. (C) Generalized widening of root canals and periodontal ligament of tooth #18. (D) Internal resorption in cervical third of mesial root and generalized canal widening in distal root of tooth #31.
patient’s diabetes was controlled, we were able to use up to 2 cartridges of lidocaine with epinephrine for anesthesia (18, 19). Subsequently, long buccal nerve was also anesthetized, and after lip numbness for confirmation of anesthesia, cold test and electric pulp test (Element Diagnostic Unit; Sybron Endo, Glendora, CA) were used. If the tooth anesthesia was not complete, supplementary injections were used. Access cavities in these teeth were prepared, and the root canal orifices were determined. Isolation was completed with rubber dam. The initial working length was determined with a Root ZX apex locator (Morita Corp, Osaka, Japan) with the use of #15 hand K-file and confirmed by a digital radiographic technique (Kodak RVG 5100 Digital Radiography System; Kodak, Toronto, Ontario, Canada). During the endodontic steps the Root ZX apex locator was once again used to ensure working length accuracy. The root canals were prepared with RaCe rotary files (FKG Dentaire, La Choux-de-Fonds, Switzerland) according to manufacturer’s instructions; 5.25% sodium hypochlorite solution was used to irrigate the root canals because of its capacity to dissolve tissues and its antibacterial JOE — Volume -, Number -, - 2015
effects in areas inaccessible to endodontic instruments (20). Calcium hydroxide paste was placed in the root canals for better disinfection of resorbed areas, and eugenol temporary dressing (Zonalin; Associated Dental Products, Wiltshire, United Kingdom) was placed. One week later in the second session after removing the Ca(OH)2 paste with K-files and irrigation, 17% EDTA solution was used in the root canals for 1 minute to remove the smear layer, and 5.25% sodium hypochlorite solution was used as the final rinse. The root canals were dried with paper points, and the largest gutta-percha point that exhibited tugback at the working length in each canal was selected as the master apical file. Teeth #5 and #6 were obturated with gutta-percha with lateral condensation technique up to the first part of the resorbed area, and internal resorption areas were obturated with gutta-percha by using warm vertical compaction technique. Lateral condensation technique with gutta-percha was used for obturation of teeth #18 and #31, and temporary Zonaline dressing was placed. After the treatment, widening of the canals became more evident (Fig. 3). The patient was referred to
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Figure 3. Radiographs of teeth #5 (A), #6 (B), #18 (C), and #31 (D) immediately after completion of root canal treatment.
the Restorative Department for restoration of endodontically treated teeth. The patient was placed on clinical and radiographic follow-ups every 6 months to observe the improvement of oral lichen planus. Six-month and yearly radiographic evaluations were carried out for the development of new lesions, progression of previous lesions, and possible internal resorption in other teeth and root canals (Figs. 4 and 5) (15).
Discussion A review of the literature portrays the severity of destruction that VZV can create in teeth and the supporting structures. Osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, skin scars, odontogenic pain, short irregular roots, missing teeth, calcification and necrosis of the dental pulp, internal resorption, and periapical lesions have been previously described in association with VZV (10–15). This report presented the association between VZV and internal root resorption of teeth in different dental quadrants and in conjunction with diabetes mellitus type I and thyroiditis. No study has reported the association and possible relation of VZV and these complications. 4
Talebzadeh et al.
Internal root resorption is characterized by resorption of the internal aspect of the root by multinucleated giant cells at close proximity to granulation tissue within the pulp. Chronic inflammatory tissues are commonly found in the pulp, but they seldom lead to root resorption. Different hypotheses have been proposed to explain the origin of intrapulpal granulation tissues responsible for internal root resorption. On the basis of a widely accepted hypothesis, the infected coronal pulp tissue forms apical granulation tissue. According to another hypothesis, the granulation tissue involved has a non-pulpal origin, and it has been suggested that it originates from the vascular compartment cells or from cells in the periodontium. Dentinal tubules provide a route for communication to occur between the coronal necrotic tissue and the vital pulp. There are speculations that the tissue responsible for resorption does not originate from the pulp and is in fact a ’’metaplastic’’ tissue produced by the macrophage-like cells in the vascular compartment that invade the pulp. There are other speculations that a periodontium-like connective tissue replaces the pulpal tissue in the presence of internal resorption. These hypotheses do not contradict each other, and each might play a role in the formation of granulation tissue within the pulp under different clinical conditions. Apart from the presence of granulation tissue within the pulp, internal root JOE — Volume -, Number -, - 2015
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Figure 4. Improvement in oral lichen planus was observed after treatment with betamethasone mouthwash at 6-month follow-up.
resorption occurs when the odontoblastic layer and predentin are lost or undergo changes. It is not clear why predentin is lost at close proximity to granulation tissue; however, trauma has been implicated as an etiologic agent (2, 16) or as a factor triggering internal root resorption. Another plausible reason might be the excessive heat that is
generated when dentin is cut without adequate cooling. It is believed that the heat compromises and destroys the predentin layer, creating conditions suitable for internal resorption to occur in cases in which the coronal pulp becomes infected thereafter. In such situations, bacterial toxins might initiate an inflammatory reaction, and the
Figure 5. Periapical radiographs of teeth #5, #6, #18, and #31 at 6-month follow-up. (A–C) Permanent restorations of teeth with composite resin; widening of periodontal ligament of tooth #18 has been resolved. (D) Tooth #31 has been permanently restored with amalgam. No periapical problem is seen in these teeth.
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Case Report/Clinical Technique multinucleated giant cells in the vital pulp might be activated at close proximity to the denuded root surface. These plausible events have been confirmed by attempts to induce internal root resorption by diathermy technique (16). In relation to the relationship between VZV and internal root resorption discussed in the present report, various studies have suggested injuries to odontoblasts and tissue degeneration because of the viral infection (16, 21). It appears that loss of the odontoblastic layer and tissue degeneration because of contamination with this virus and the immunologic reactions to contamination of odontoblasts and its activation at pulpal nerve endings result in traumas to the predentin layer in addition to the loss of the odontoblastic layer, finally giving rise to the internal root resorption. Internal resorption of tooth root that is due to VZV infection was first reported by Solomon et al (10) in 1986. This case report included a 31-year-old woman with internal root resorption in teeth #21 and #23 who had a history of herpes zoster involving the maxillary branch of the left trigeminal nerve 4 years previously. The reason for the occurrence of internal resorption in teeth because of affliction with herpes zoster has been reported by Solomon et al; the dental pulp could be adversely affected by herpes zoster because the pulp contains terminal nerve endings as do the mucosa and skin (10). Earlier, Gregory et al (11) had reported a patient in whom all the left maxillary teeth except for central incisors, with little evidence of caries or filling, had become non-vital because of infection with this virus. Nonvitalization of the entire teeth of 1 quadrant has been attributed by Gregory et al to an episode of herpes zoster that the patient had suffered 8 years earlier that involved the maxillary division of the trigeminal nerve on that side, and this can indicate the central origin of damage versus the local factor (13, 14). Similar to this case report in which the teeth exhibited clinical signs just a short time before diagnosis, remaining asymptomatic for 5 years after the primary infection, in studies by Solomon et al (10) and Gregory et al (11), the teeth in question were asymptomatic and without clinical signs despite the pulpal disease for 4 and 8 years, respectively. This indicates the necessity of periodic clinical and radiographic evaluations in patients with a history of VZV for the diagnosis of pulpal and periapical diseases before the teeth develop questionable prognosis. Subsequent to that report, Schwartz and Kvorning (12) reported 10 cases of herpes zoster virus with postherpetic complications such as osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, and skin scars with unexplained condition of the pulp. Smith et al (13) also described a 15-year-old girl who had had chickenpox at 7 years of age, and because of the involvement of the lower right quadrant, severely scarred lip and chin could be seen on photographs, and the radiographs showed missing third molar bud and shortened roots with partially calcified pulp chamber and root canals of other 4 posterior right quadrant teeth. In this study, none of the anomalies seen in the quadrant afflicted with varicella zoster were observed on the left side or teeth that developed before 7 years of age (age of affliction with chickenpox), suggesting a direct correlation of these dental changes and penetration of the disease to mandibular neurovascular source during infection with VZV (13). In 1991 Wadden (14) reported a 70-year-old woman with a history of herpes zoster 3 years previously, and devitalization could be seen in 4 of 5 teeth in the left maxillary quadrant. On the other hand, Seltzer and Bender cited studies that showed injury to odontoblasts and degeneration as a result of systemic viral infection (22). The last case report about tooth resorption as a result of herpes zoster virus infection is related to Ramchandani and Mellor (15) in 2007, in which they reported a 72-year-old woman presenting with multiple periapical lesions and resorption of teeth in a single quadrant 17 6
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years after an attack of herpes zoster (shingles) of the maxillary division of the trigeminal nerve. This was the first report of simultaneous presence of multiple periapical lesions and resorption of teeth in association with this virus in a patient. Kakehashi et al (23) reported that apical periodontitis occurs only in the presence of bacterial infection of the exposed pulp. Therefore, it appears the periapical lesions in the study carried out by Ramchandani and Mellor (15) were associated with secondary bacterial contamination; loss of predentin and dentinal tubules in areas affected by internal resorption might have facilitated penetration of bacteria into the root canal, resulting in bacterial infection caused by viral infection to give rise to multiple periapical lesions. A delay in the appearance of clinical symptoms and signs after the patient was first contaminated with the virus (17 years in the study by Ramchandani and Mellor) was adequate for bacterial contamination and development of periapical periodontitis. An important consideration about the differential diagnosis of oral pain is the possibility of affliction with secondary herpes zoster infection that is always seen in patients older than 50 years of age, with their medical history showing dysfunction of the immune system. Thus, Eisenberg (24) and Verbin et al (25) described dental pain as the first prodromal sign of herpes zoster involving the second and third branches of the trigeminal nerve that occurs before other clinical signs. The role of VZV in the progression of internal resorption in different dental quadrants was very interesting in this case. It appears that some cases of internal resorption, especially multiple internal resorptions, which we consider as idiopathic, are not idiopathic in fact and might have viral etiology. Depending on the host’s resistance, the patient may experience mild subclinical herpes zoster, in which the only complication is pulp necrosis or internal resorption of the teeth. A technique used to diagnose this is pulp biopsy, which can be carried out through the pulp chamber or an excisional biopsy during apical surgery, followed by an attempt to identify viral elements by using new histopathologic methods or polymerase chain reaction technique (15). All the body and oral cavity areas were affected when the patient in this case report developed chickenpox. The generalized oral involvement was in the form of severe mucous and labial ulcers, and no improvements were observed in the oral and labial status after recovery from the disease, which might be explained by the capacity of the VZV to remain dormant, indicating a viral etiology for the oral manifestations. Mizukawa et al (26) carried out a study to evaluate the presence of VZV antigens in zosteriform lichen planus compared with those in linear lichen planus and reported the presence of these antigens only in the epithelial sweat glands in the zosteriform lichen planus, with no signs of these antigens in the linear lichen planus, which might indicate differences in the etiology between these 2 lichen planus forms and superimposition of oral lesions resulting from this virus in the acute phase of the linear lichen planus and exacerbation of oral lesions, resulting in erosive lichen planus. The presence of VZV antigens in skin lesions of the former might indicate the role of this virus in the pathogenesis of this variant. The involvement of all the body areas, the presence of labial and oral ulcers in the entire oral cavity, and conversion of the linear lichen planus to bilateral erosive lichen planus during the acute phase of the disease might indicate the bilateral involvement of the nerve in the orofacial area and latency of the virus in the trigeminal nerve ganglia on both sides. Activation of the virus in the sensory nerve endings of the second and third (maxillary and mandibular) branches of the nerve and in the right and left ganglia of the nerve might explain the loss of the odontoblastic layer and internal root resorption in different quadrants. In this context, in addition to internal root resorption of teeth #5 and #6 in the upper right quadrant, there was evidence of JOE — Volume -, Number -, - 2015
Case Report/Clinical Technique generalized internal resorption in teeth #18 and #31 of the lower right and left quadrants. Severe skin and oral lesions after affliction with chickenpox had resulted in admission into the intensive care unit because of severe oral pain, inability to eat, and the extent of the disease. After a short time, the patient had developed hypothyroidism and diabetes mellitus type I. According to studies, there is evidence of the role of some Herpesviridae family in the etiology of both these diseases through contamination of endocrine secreting cells and stimulation of host immune system to attack these cells and destroy them (8, 9). Therefore, affliction with VZV in this patient can also be described in the etiology of these diseases; however, more extensive molecular research is required to identify VZV in follicular thyroid cells that secrete thyroid hormones and beta Langerhans cells that secrete insulin.
Acknowledgments The authors thank Dr Majid Abdolrahimi for English editing of the article. The authors deny any conflicts of interest related to this study.
References 1. Gershon AA, Gershon MD, Breuer J, et al. Advances in the understanding of the pathogenesis and epidemiology of herpes zoster. J ClinVirol 2010;48:S2–7. 2. Mendieta C, Miranda J, Brunet LI, et al. Alveolar bone necrosis and tooth exfoliation following herpes zoster infection: a review of the literature and case report. J Periodontol 2005;76:148–53. 3. Mintz SM, Anavi Y. Maxillary osteomyelitis and spontaneous tooth exfoliation after herpes zoster. Oral Surg Oral Med Oral Pathol 1992;73:664–6. 4. Jain MK, Manjunath KS, Jagadish SN. Unusual oral complications of herpes zoster infection: report of a case and review of literature. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2010;110:e37–41. 5. Muto T, Tsuchiya H, Sato K, et al. Tooth exfoliation and necrosis of the mandible: a rare complication following trigeminal herpes zoster—report of a case. J Oral Maxillofac Surg 1990;48:1000–3. 6. Owotade FJ, Ugboko VI, Kolude B. Herpes zoster infection of the maxilla: case report. J Oral Maxillofac Surg 1999;57:1249–51. €zt€urkcan S, Sahın MT, et al. Wolf’s isotopic response: a case of zosteriform 7. T€urel A, O lichen planus. J Dermatol 2002;29:339–42. 8. Thomas D, Liakos V, Michou V, et al. Detection of herpes virus DNA in postoperative thyroid tissue specimens of patients with autoimmune thyroid disease. Exp Clin Endocrinol Diabetes 2008;116:35–9.
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9. Drew WL. Herpesviruses. In: Ryan KJ, Ray CG, eds. Sherris Medical Microbiology: An Introduction to Infectious Diseases, 4th ed. New York: McGraw Hill; 2004: 555–76. 10. Solomon CS, Coffiner MO, Chalfin HE. Herpes zoster revisited: implicated in root resorption. J Endod 1986;12:210–3. 11. Gregory WB, Brooks LE, Penick EC. Herpes zoster associated with pulp-less teeth. J Endod 1975;1:32–5. 12. Schwartz O, Kvorning SA. Tooth exfoliation, osteonecrosis of the jaw and neuralgia following herpes zoster of the trigeminal nerve. Int J Oral Surg 1982;1: 364–71. 13. Smith S, Ross JW, Scully C. An unusual oral complication of herpeszoster infection. Oral Surg Oral Med Oral Pathol 1984;57:388–9. 14. Wadden JV. Extensive endodontic involvement following herpes zoster attack to facial area: report of a case. Northwest Dent 1991;70:31. 15. Ramchandani PL, Mellor TK. Herpes zoster associated with tooth resorption and periapical lesions. Br J Oral Maxillofac Surg 2007;45:71–3. 16. Levin GL. Root resorption. In: Hargreaves KM, Goodis HE, Tay FR, eds. Seltzer and Bender’s Dental Pulp, 2nd ed. Hanover Park, IL: Quintessence Publishing; 2012: 410–6. 17. Handysides RA, Jaramillo DE, Ingle JI. Examination, evaluation, diagnosis and treatment planning. In: Ingle JI, Bakland LK, Baumgartner JC, eds. Ingle’s Endodontics. 6th ed. Hamilton, ON, Canada: BC Decker; 2008:528. 18. Khawaja NA, Khalil H, Parvin K, et al. An influence of adrenaline (1:80,000) containing local anesthesia (2% Xylocaine) on glycemic level of patients undergoing tooth extraction in Riyadh. Saudi Pharm J 2014;22:545–9. 19. Lalla RV, D’Ambrosio JA. Dental management considerations for the patient with diabetes mellitus. J Am Dent Assoc 2001;132:1425–32. 20. Haapasalo M, Qian W. Irrigants and intracanal medicaments. In: Ingle JI, Bakland LK, Baumgartner JC, eds. Ingle’s Endodontics, 6th ed. Hamilton, ON, Canada: BC Decker; 2008:997–9. 21. Kim NK, Kim BC, Nam JW, Kim HJ. Alveolar bone necrosis and spontaneous tooth exfoliation associated with trigeminal herpes zoster: a report of three cases. J Korean Assoc Oral Maxillofac Surg 2012;38:177–83. 22. Huber MA. Interrelationship of pulp and systemic disease. In: Hargreaves KM, Goodis HE, Tay FR, eds. Seltzer and Bender’s Dental Pulp, 2nd ed. Hanover Park, IL: Quintessence Publishing; 2012:471–3. 23. Kakehashi S, Stanley HR, Fitzgerald RJ. The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol 1965;20:340–9. 24. Eisenberg E. Intraoral isolated herpes zoster. Oral Surg Oral Med Oral Pathol 1978; 45:214. 25. Verbin RS,, Heineman HS,, Stiff RH. Localized odontalgia occurring during herpes zoster of the maxillary division of the fifth cranial nerve. Oral Surg Oral Med Oral Pathol 1968;26:441. 26. Mizukawa Y, Horie C, Yamazaki Y, Shiohara T. Detection of varicella-zoster virus antigens in lesional skin of zosteriform lichen planus but not in that of linear lichen planus. Dermatology 2012;225:22–6.
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Varicella Zoster Virus and Internal Root Resorption: A Case Report Bita Talebzadeh, DDS,* Saeed Rahimi, DDS, MSc,† Amir Ardalan Abdollahi, DDS* Ahmad Nouroloyuni, DDS,* and Vahide Asghari, DDS* Abstract Introduction: Herpes zoster is a viral infection caused by the reactivation of the varicella zoster virus. One of the less well-recognized maxillofacial complications is tooth root resorption. To our knowledge, this is the first case report about internal resorption associated with varicella zoster virus involving different dental quadrants. Methods: A 38-year-old woman presented with internal resorption of maxillary canine and first premolar tooth roots on the right quadrant and generalized internal resorption of second molars of both mandibular quadrants. The patient’s medical history showed mild oral lichen planus and infection with varicella zoster virus (chickenpox) with severe clinical manifestations 5 years previously. The patient developed diabetes mellitus type I and hypothyroidism a short time after varicella zoster virus infection, and by the time of infection with this virus, oral lichen planus had progressed from the reticular pattern to the generalized severe erosive form. Viral etiology could also be considered in these diseases. The root canals of the affected teeth were debrided, irrigated, and dried, and calcium hydroxide paste was placed in the root canals for a week during the first treatment session. The root canals were obturated during the second session. Results: Six-month follow-up showed improvement of oral lichen planus and resolution of widening of periodontal ligament of the affected teeth, with follow-up radiographs revealing no periapical problems. Conclusions: It appears some cases of internal root resorption classified as idiopathic might have viral etiology. Therefore, it is recommended that patients be questioned about a history of chickenpox and herpes zoster. (J Endod 2015;-:1–7)
Key Words Diabetes mellitus type I, hypothyroidism, internal resorption, oral lichen planus, periapical lesions, varicella zoster virus
T
he varicella zoster virus (VZV) is the etiologic agent for 2 clinical entities, varicella or chickenpox and herpes zoster infection (HZI) (1). Varicella caused by the primary infection of VZV is a benign childhood disease producing eruptive vesicles. As a result of primary infection of varicella, a skin virus moves to a sensory nerve and remains in a latent state in a ganglion (1, 2). When VZV in the latent state is reactivated, it develops into HZI, which causes severe pain and painful vesicles in the skin and mucosa around the affected sensory nerve distribution (3, 4). Thoracolumbar dermatomes (T3-L3) are most commonly affected by HZI (1, 4). HZI may also affect the cranial nerves, with the trigeminal nerve most frequently affected (18.5%–22%) (1). Herpes zoster affecting the trigeminal nerve is generally unilateral; it generally affects a single branch among the 3 branches, mainly the first branch or the optic nerve. Oral manifestations can be observed when the maxillary and mandibular branches are affected (4). Oral vesicles appear mainly after a skin manifestation (3, 5). Sometimes, however, there may be mucosal involvement without skin lesions (5). The vesicles erupt and leave mucosal erosions, but no scar is left in most cases (3). The most significant complication of HZI is postherpetic neuralgia (5); other complications may include facial scarring, motor nerve palsy, optic neuropathy, blindness, encephalitis, and calcinosis cutis (6). All the members of the herpesvirus family have the ability of remaining latent in the cells of the host body and reactivation. There are some reports of herpes zoster virus’s role in the development of oral lichen planus (zosteriform lichen planus) (7). In addition, studies have reported the role of human herpesviruses in the involvement of endocrine glands with autoimmune diseases such as the role of cytomegalovirus (HHV-5) and herpes simplex virus types 1 and 2 (HHV 1, 2) in the development of diabetes mellitus type I and thyroiditis, respectively (8, 9). On the other hand, osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, skin scars, odontogenic pain, short irregular roots, missing teeth, calcification and necrosis of dental pulp, internal resorption, and periapical lesions have been previously described in association with oral manifestations of maxillary and mandibular branches involvement with VZV (10–15). However, this is the first case report in relation to the concurrency of herpes zoster virus (HHV-3) with diabetes mellitus type I and thyroiditis and internal resorption of teeth in different dental quadrants.
Case Report A 38-year-old woman presented with severe dental pain in the region of the first premolar of maxillary right side with deep mesial caries. The patient had a history of varicella zoster (chickenpox) 5 years previously, for which she had been admitted
From the *Department of Endodontics and †Dental and Periodontal Research Center, Department of Endodontics, Faculty of Dentistry, Tabriz University of Medical Sciences, Tabriz, Iran. Address requests for reprints to Dr Saeed Rahimi, Dental and Periodontal Research Center, Department of Endodontics, Faculty of Dentistry, Tabriz University of Medical Sciences, Tabriz 5166615713, Iran. E-mail address: [email protected] 0099-2399/$ - see front matter Copyright ª 2015 American Association of Endodontists. http://dx.doi.org/10.1016/j.joen.2015.02.014
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Case Report/Clinical Technique to the intensive care unit in a hospital for 13 days. The patient reported that before affliction with chickenpox, she had mild oral lichen planus bilaterally in the buccal regions of the oral cavity; however, after infection with this virus, during the disease, and after that, she had experienced serious erosive lichen planus in all the areas of the oral cavity such as lips and gums (in the form of linear gingival erythema and in some areas as leukoplakia) (Fig. 1). The medical history of the patient showed affliction with diabetes mellitus type I and hypothyroidism after infection with VZV (chickenpox). The patient had taken levothyroxine for the treatment of hypothyroidism, had received insulin injections for diabetes mellitus type I, had used betamethasone mouthwash for reducing the inflammation due to generalized oral lichen planus, and had received estrogen and progesterone for the treatment of infertility. Usual blood tests, including full blood count, erythrocyte sedimentation rate, alkaline phosphatase, serum calcium, liver function tests, urea, and electrolytes, were in normal ranges. In oral examinations, severe generalized erosive lichen planus and severe generalized periodontitis were observed (Fig. 1). Radiographic examinations showed deep mesial caries in teeth #1, #5, #17, #18, #20, #31, and #32 and loss of teeth #4, #19, and #30. The patient had had tooth #4 removed because of crowding, as recommended by her dentist, and had lost teeth #19 and #30 because of deep dental caries, severe pain, and the hopeless prognosis of the teeth. Periapical radiographic examinations showed internal resorption of the coronal thirds of teeth #5 and #6 and generalized internal resorption of the root canals of teeth #18 and #31 (Fig. 2). In other teeth with caries or without caries no evidence of resorption was seen.
Clinical evaluation of the patient revealed continuous severe pain and exacerbation of pain with heat, cold, and percussion and increased response to electric pulp tester in teeth #5, #18, and #31, whereas in tooth #6, responses to heat, cold, and percussion and response to electric pulp tester were in normal ranges, and despite the internal resorption, no caries was detected in this tooth. The patient did not have any history of trauma, orthodontic treatment, bleaching, pulpotomy, and restorative treatments, resulting in excessive production of heat during tooth preparation, which has a role in the etiology of internal resorption through trauma to and loss of the odontoblastic layer and predentin (16). Radiographic views, vitality tests, and sensitivity to percussion were normal in other intact teeth.
Treatment Plan Because a tooth with internal resorption is prone to irreversible pulpitis and if the inflamed pulp remains untreated, perforation might occur, resulting in the loss of the tooth (17), the patient was given adequate information about other treatment options, including extraction of the teeth and replacement with prosthetic treatments or implants and also no treatment at all. The patient opted for a proper treatment plan with root canal treatment. Endodontic Treatment Steps Local anesthesia was administered with injection of 1.8 mL lidocaine with 1:80,000 epinephrine in the region of inferior alveolar nerve for mandibular teeth and infiltration for maxillary teeth. Because the
Figure 1. Photographs (A–D) show severe generalized erosive lichen planus and severe periodontitis.
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Figure 2. Primary periapical radiographs of teeth #5, #6, #18, and #31. (A and B) Internal resorption of cervical third of roots of teeth #5 and #6. (C) Generalized widening of root canals and periodontal ligament of tooth #18. (D) Internal resorption in cervical third of mesial root and generalized canal widening in distal root of tooth #31.
patient’s diabetes was controlled, we were able to use up to 2 cartridges of lidocaine with epinephrine for anesthesia (18, 19). Subsequently, long buccal nerve was also anesthetized, and after lip numbness for confirmation of anesthesia, cold test and electric pulp test (Element Diagnostic Unit; Sybron Endo, Glendora, CA) were used. If the tooth anesthesia was not complete, supplementary injections were used. Access cavities in these teeth were prepared, and the root canal orifices were determined. Isolation was completed with rubber dam. The initial working length was determined with a Root ZX apex locator (Morita Corp, Osaka, Japan) with the use of #15 hand K-file and confirmed by a digital radiographic technique (Kodak RVG 5100 Digital Radiography System; Kodak, Toronto, Ontario, Canada). During the endodontic steps the Root ZX apex locator was once again used to ensure working length accuracy. The root canals were prepared with RaCe rotary files (FKG Dentaire, La Choux-de-Fonds, Switzerland) according to manufacturer’s instructions; 5.25% sodium hypochlorite solution was used to irrigate the root canals because of its capacity to dissolve tissues and its antibacterial JOE — Volume -, Number -, - 2015
effects in areas inaccessible to endodontic instruments (20). Calcium hydroxide paste was placed in the root canals for better disinfection of resorbed areas, and eugenol temporary dressing (Zonalin; Associated Dental Products, Wiltshire, United Kingdom) was placed. One week later in the second session after removing the Ca(OH)2 paste with K-files and irrigation, 17% EDTA solution was used in the root canals for 1 minute to remove the smear layer, and 5.25% sodium hypochlorite solution was used as the final rinse. The root canals were dried with paper points, and the largest gutta-percha point that exhibited tugback at the working length in each canal was selected as the master apical file. Teeth #5 and #6 were obturated with gutta-percha with lateral condensation technique up to the first part of the resorbed area, and internal resorption areas were obturated with gutta-percha by using warm vertical compaction technique. Lateral condensation technique with gutta-percha was used for obturation of teeth #18 and #31, and temporary Zonaline dressing was placed. After the treatment, widening of the canals became more evident (Fig. 3). The patient was referred to
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Figure 3. Radiographs of teeth #5 (A), #6 (B), #18 (C), and #31 (D) immediately after completion of root canal treatment.
the Restorative Department for restoration of endodontically treated teeth. The patient was placed on clinical and radiographic follow-ups every 6 months to observe the improvement of oral lichen planus. Six-month and yearly radiographic evaluations were carried out for the development of new lesions, progression of previous lesions, and possible internal resorption in other teeth and root canals (Figs. 4 and 5) (15).
Discussion A review of the literature portrays the severity of destruction that VZV can create in teeth and the supporting structures. Osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, skin scars, odontogenic pain, short irregular roots, missing teeth, calcification and necrosis of the dental pulp, internal resorption, and periapical lesions have been previously described in association with VZV (10–15). This report presented the association between VZV and internal root resorption of teeth in different dental quadrants and in conjunction with diabetes mellitus type I and thyroiditis. No study has reported the association and possible relation of VZV and these complications. 4
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Internal root resorption is characterized by resorption of the internal aspect of the root by multinucleated giant cells at close proximity to granulation tissue within the pulp. Chronic inflammatory tissues are commonly found in the pulp, but they seldom lead to root resorption. Different hypotheses have been proposed to explain the origin of intrapulpal granulation tissues responsible for internal root resorption. On the basis of a widely accepted hypothesis, the infected coronal pulp tissue forms apical granulation tissue. According to another hypothesis, the granulation tissue involved has a non-pulpal origin, and it has been suggested that it originates from the vascular compartment cells or from cells in the periodontium. Dentinal tubules provide a route for communication to occur between the coronal necrotic tissue and the vital pulp. There are speculations that the tissue responsible for resorption does not originate from the pulp and is in fact a ’’metaplastic’’ tissue produced by the macrophage-like cells in the vascular compartment that invade the pulp. There are other speculations that a periodontium-like connective tissue replaces the pulpal tissue in the presence of internal resorption. These hypotheses do not contradict each other, and each might play a role in the formation of granulation tissue within the pulp under different clinical conditions. Apart from the presence of granulation tissue within the pulp, internal root JOE — Volume -, Number -, - 2015
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Figure 4. Improvement in oral lichen planus was observed after treatment with betamethasone mouthwash at 6-month follow-up.
resorption occurs when the odontoblastic layer and predentin are lost or undergo changes. It is not clear why predentin is lost at close proximity to granulation tissue; however, trauma has been implicated as an etiologic agent (2, 16) or as a factor triggering internal root resorption. Another plausible reason might be the excessive heat that is
generated when dentin is cut without adequate cooling. It is believed that the heat compromises and destroys the predentin layer, creating conditions suitable for internal resorption to occur in cases in which the coronal pulp becomes infected thereafter. In such situations, bacterial toxins might initiate an inflammatory reaction, and the
Figure 5. Periapical radiographs of teeth #5, #6, #18, and #31 at 6-month follow-up. (A–C) Permanent restorations of teeth with composite resin; widening of periodontal ligament of tooth #18 has been resolved. (D) Tooth #31 has been permanently restored with amalgam. No periapical problem is seen in these teeth.
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Case Report/Clinical Technique multinucleated giant cells in the vital pulp might be activated at close proximity to the denuded root surface. These plausible events have been confirmed by attempts to induce internal root resorption by diathermy technique (16). In relation to the relationship between VZV and internal root resorption discussed in the present report, various studies have suggested injuries to odontoblasts and tissue degeneration because of the viral infection (16, 21). It appears that loss of the odontoblastic layer and tissue degeneration because of contamination with this virus and the immunologic reactions to contamination of odontoblasts and its activation at pulpal nerve endings result in traumas to the predentin layer in addition to the loss of the odontoblastic layer, finally giving rise to the internal root resorption. Internal resorption of tooth root that is due to VZV infection was first reported by Solomon et al (10) in 1986. This case report included a 31-year-old woman with internal root resorption in teeth #21 and #23 who had a history of herpes zoster involving the maxillary branch of the left trigeminal nerve 4 years previously. The reason for the occurrence of internal resorption in teeth because of affliction with herpes zoster has been reported by Solomon et al; the dental pulp could be adversely affected by herpes zoster because the pulp contains terminal nerve endings as do the mucosa and skin (10). Earlier, Gregory et al (11) had reported a patient in whom all the left maxillary teeth except for central incisors, with little evidence of caries or filling, had become non-vital because of infection with this virus. Nonvitalization of the entire teeth of 1 quadrant has been attributed by Gregory et al to an episode of herpes zoster that the patient had suffered 8 years earlier that involved the maxillary division of the trigeminal nerve on that side, and this can indicate the central origin of damage versus the local factor (13, 14). Similar to this case report in which the teeth exhibited clinical signs just a short time before diagnosis, remaining asymptomatic for 5 years after the primary infection, in studies by Solomon et al (10) and Gregory et al (11), the teeth in question were asymptomatic and without clinical signs despite the pulpal disease for 4 and 8 years, respectively. This indicates the necessity of periodic clinical and radiographic evaluations in patients with a history of VZV for the diagnosis of pulpal and periapical diseases before the teeth develop questionable prognosis. Subsequent to that report, Schwartz and Kvorning (12) reported 10 cases of herpes zoster virus with postherpetic complications such as osteonecrosis of the jaw, exfoliation of teeth, severe periodontitis, and skin scars with unexplained condition of the pulp. Smith et al (13) also described a 15-year-old girl who had had chickenpox at 7 years of age, and because of the involvement of the lower right quadrant, severely scarred lip and chin could be seen on photographs, and the radiographs showed missing third molar bud and shortened roots with partially calcified pulp chamber and root canals of other 4 posterior right quadrant teeth. In this study, none of the anomalies seen in the quadrant afflicted with varicella zoster were observed on the left side or teeth that developed before 7 years of age (age of affliction with chickenpox), suggesting a direct correlation of these dental changes and penetration of the disease to mandibular neurovascular source during infection with VZV (13). In 1991 Wadden (14) reported a 70-year-old woman with a history of herpes zoster 3 years previously, and devitalization could be seen in 4 of 5 teeth in the left maxillary quadrant. On the other hand, Seltzer and Bender cited studies that showed injury to odontoblasts and degeneration as a result of systemic viral infection (22). The last case report about tooth resorption as a result of herpes zoster virus infection is related to Ramchandani and Mellor (15) in 2007, in which they reported a 72-year-old woman presenting with multiple periapical lesions and resorption of teeth in a single quadrant 17 6
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years after an attack of herpes zoster (shingles) of the maxillary division of the trigeminal nerve. This was the first report of simultaneous presence of multiple periapical lesions and resorption of teeth in association with this virus in a patient. Kakehashi et al (23) reported that apical periodontitis occurs only in the presence of bacterial infection of the exposed pulp. Therefore, it appears the periapical lesions in the study carried out by Ramchandani and Mellor (15) were associated with secondary bacterial contamination; loss of predentin and dentinal tubules in areas affected by internal resorption might have facilitated penetration of bacteria into the root canal, resulting in bacterial infection caused by viral infection to give rise to multiple periapical lesions. A delay in the appearance of clinical symptoms and signs after the patient was first contaminated with the virus (17 years in the study by Ramchandani and Mellor) was adequate for bacterial contamination and development of periapical periodontitis. An important consideration about the differential diagnosis of oral pain is the possibility of affliction with secondary herpes zoster infection that is always seen in patients older than 50 years of age, with their medical history showing dysfunction of the immune system. Thus, Eisenberg (24) and Verbin et al (25) described dental pain as the first prodromal sign of herpes zoster involving the second and third branches of the trigeminal nerve that occurs before other clinical signs. The role of VZV in the progression of internal resorption in different dental quadrants was very interesting in this case. It appears that some cases of internal resorption, especially multiple internal resorptions, which we consider as idiopathic, are not idiopathic in fact and might have viral etiology. Depending on the host’s resistance, the patient may experience mild subclinical herpes zoster, in which the only complication is pulp necrosis or internal resorption of the teeth. A technique used to diagnose this is pulp biopsy, which can be carried out through the pulp chamber or an excisional biopsy during apical surgery, followed by an attempt to identify viral elements by using new histopathologic methods or polymerase chain reaction technique (15). All the body and oral cavity areas were affected when the patient in this case report developed chickenpox. The generalized oral involvement was in the form of severe mucous and labial ulcers, and no improvements were observed in the oral and labial status after recovery from the disease, which might be explained by the capacity of the VZV to remain dormant, indicating a viral etiology for the oral manifestations. Mizukawa et al (26) carried out a study to evaluate the presence of VZV antigens in zosteriform lichen planus compared with those in linear lichen planus and reported the presence of these antigens only in the epithelial sweat glands in the zosteriform lichen planus, with no signs of these antigens in the linear lichen planus, which might indicate differences in the etiology between these 2 lichen planus forms and superimposition of oral lesions resulting from this virus in the acute phase of the linear lichen planus and exacerbation of oral lesions, resulting in erosive lichen planus. The presence of VZV antigens in skin lesions of the former might indicate the role of this virus in the pathogenesis of this variant. The involvement of all the body areas, the presence of labial and oral ulcers in the entire oral cavity, and conversion of the linear lichen planus to bilateral erosive lichen planus during the acute phase of the disease might indicate the bilateral involvement of the nerve in the orofacial area and latency of the virus in the trigeminal nerve ganglia on both sides. Activation of the virus in the sensory nerve endings of the second and third (maxillary and mandibular) branches of the nerve and in the right and left ganglia of the nerve might explain the loss of the odontoblastic layer and internal root resorption in different quadrants. In this context, in addition to internal root resorption of teeth #5 and #6 in the upper right quadrant, there was evidence of JOE — Volume -, Number -, - 2015
Case Report/Clinical Technique generalized internal resorption in teeth #18 and #31 of the lower right and left quadrants. Severe skin and oral lesions after affliction with chickenpox had resulted in admission into the intensive care unit because of severe oral pain, inability to eat, and the extent of the disease. After a short time, the patient had developed hypothyroidism and diabetes mellitus type I. According to studies, there is evidence of the role of some Herpesviridae family in the etiology of both these diseases through contamination of endocrine secreting cells and stimulation of host immune system to attack these cells and destroy them (8, 9). Therefore, affliction with VZV in this patient can also be described in the etiology of these diseases; however, more extensive molecular research is required to identify VZV in follicular thyroid cells that secrete thyroid hormones and beta Langerhans cells that secrete insulin.
Acknowledgments The authors thank Dr Majid Abdolrahimi for English editing of the article. The authors deny any conflicts of interest related to this study.
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9. Drew WL. Herpesviruses. In: Ryan KJ, Ray CG, eds. Sherris Medical Microbiology: An Introduction to Infectious Diseases, 4th ed. New York: McGraw Hill; 2004: 555–76. 10. Solomon CS, Coffiner MO, Chalfin HE. Herpes zoster revisited: implicated in root resorption. J Endod 1986;12:210–3. 11. Gregory WB, Brooks LE, Penick EC. Herpes zoster associated with pulp-less teeth. J Endod 1975;1:32–5. 12. Schwartz O, Kvorning SA. Tooth exfoliation, osteonecrosis of the jaw and neuralgia following herpes zoster of the trigeminal nerve. Int J Oral Surg 1982;1: 364–71. 13. Smith S, Ross JW, Scully C. An unusual oral complication of herpeszoster infection. Oral Surg Oral Med Oral Pathol 1984;57:388–9. 14. Wadden JV. Extensive endodontic involvement following herpes zoster attack to facial area: report of a case. Northwest Dent 1991;70:31. 15. Ramchandani PL, Mellor TK. Herpes zoster associated with tooth resorption and periapical lesions. Br J Oral Maxillofac Surg 2007;45:71–3. 16. Levin GL. Root resorption. In: Hargreaves KM, Goodis HE, Tay FR, eds. Seltzer and Bender’s Dental Pulp, 2nd ed. Hanover Park, IL: Quintessence Publishing; 2012: 410–6. 17. Handysides RA, Jaramillo DE, Ingle JI. Examination, evaluation, diagnosis and treatment planning. In: Ingle JI, Bakland LK, Baumgartner JC, eds. Ingle’s Endodontics. 6th ed. Hamilton, ON, Canada: BC Decker; 2008:528. 18. Khawaja NA, Khalil H, Parvin K, et al. An influence of adrenaline (1:80,000) containing local anesthesia (2% Xylocaine) on glycemic level of patients undergoing tooth extraction in Riyadh. Saudi Pharm J 2014;22:545–9. 19. Lalla RV, D’Ambrosio JA. Dental management considerations for the patient with diabetes mellitus. J Am Dent Assoc 2001;132:1425–32. 20. Haapasalo M, Qian W. Irrigants and intracanal medicaments. In: Ingle JI, Bakland LK, Baumgartner JC, eds. Ingle’s Endodontics, 6th ed. Hamilton, ON, Canada: BC Decker; 2008:997–9. 21. Kim NK, Kim BC, Nam JW, Kim HJ. Alveolar bone necrosis and spontaneous tooth exfoliation associated with trigeminal herpes zoster: a report of three cases. J Korean Assoc Oral Maxillofac Surg 2012;38:177–83. 22. Huber MA. Interrelationship of pulp and systemic disease. In: Hargreaves KM, Goodis HE, Tay FR, eds. Seltzer and Bender’s Dental Pulp, 2nd ed. Hanover Park, IL: Quintessence Publishing; 2012:471–3. 23. Kakehashi S, Stanley HR, Fitzgerald RJ. The effects of surgical exposures of dental pulps in germ-free and conventional laboratory rats. Oral Surg Oral Med Oral Pathol 1965;20:340–9. 24. Eisenberg E. Intraoral isolated herpes zoster. Oral Surg Oral Med Oral Pathol 1978; 45:214. 25. Verbin RS,, Heineman HS,, Stiff RH. Localized odontalgia occurring during herpes zoster of the maxillary division of the fifth cranial nerve. Oral Surg Oral Med Oral Pathol 1968;26:441. 26. Mizukawa Y, Horie C, Yamazaki Y, Shiohara T. Detection of varicella-zoster virus antigens in lesional skin of zosteriform lichen planus but not in that of linear lichen planus. Dermatology 2012;225:22–6.
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