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Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report
G Model JOMSMP-589; No. of Pages 5
ARTICLE IN PRESS Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology journal homepage: www.elsevier.com/locate/jomsmp
Case report
Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report Atsumu Kouketsu a,∗ , Aritsune Matsui a , Shiro Mori a , Haruka Saito a , Hikari Suzuki a , Yukiko Shibahara b , Hiroyuki Kumamoto c , Tetsu Takahashi a a Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry (Chief: Prof. Tetsu Takahashi), Japan b Department of Pathology, Tohoku University Graduate School of Medicine, Japan c Division of Oral Pathology, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, Japan
a r t i c l e
i n f o
Article history: Received 26 May 2016 Received in revised form 27 November 2016 Accepted 26 December 2016 Available online xxx Keywords: Actinomycosis Buccal mucosa Scraping cytology
a b s t r a c t Actinomycosis, a rare chronic granulomatous bacterial infection induced by Actinomyces species, colonizes the mouth, colon, and vagina. Although Actinomyces spp. are well-known oral commensals, actinomycosis is a rare oral infection. It is difficult to detect Actinomyces in biopsies, using histopathologic methods, or through examination of bacterial cultures; therefore, providing an accurate diagnosis is problematic. Recently, oral brush scraping cytology has been performed for the diagnosis of premalignant and malignant lesions, but it is difficult to determine the efficacy of this method based on the published reports, and whether it is a suitable tool for detecting Actinomyces infections in the general public. Here, we report a rare case of actinomycosis of the buccal mucosa in an 8-year-old boy that was successfully diagnosed by scraping cytology. He exhibited pain and swelling in the left buccal, and was admitted to our hospital for emergency care. Clinical examination revealed pyrexia, tachycardia, trismus, ingestion disorder, lethargy, and ulcer as well as having an indurated mass in the left buccal mucosa accompanied by strong pain. Following a clinical diagnosis of acute phlegmon of the left buccal mucosa, antibiotic and fluid therapy was performed. Because of detection of Actinomyces colonies at the ulcer surface using scraping cytology, we continued to administer long-term antibiotic therapy with penicillin for 2 months. The patient’s general condition was improved, and this was confirmed by laboratory results, and the trismus and painful nodular mass were successfully cured. The patient has shown no subsequent evidence of recurrence for 7 months of following treatment. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction Actinomycosis is a chronic, suppurative, and granulomatous infectious disease. In humans, the disease is caused mainly by Actynomyces israelii that is a species of Gram-positive, rod-shaped bacteria within the genus Actinomyces [1,2]. Known to live commensally within the human oral cavity, A. israelii is an opportunistic pathogen and a cause of cervicofacial actinomycosis as well as
夽 AsianAOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author at: Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan. E-mail address: kouketsu [email protected] (A. Kouketsu).
chest or abdominal infections. The main clinical symptoms of oral actinomycosis are painless or painful masses with board-like induration, the formation of multiple small abscesses, and trismus [1–3]. Moreover, positive results on bacterial culture examination, or histopathological detection of Actinomyces colonization in lesions or pus, is a necessary diagnostic criterion for this disease. Although common in the past, the presentation of these typical symptoms has become increasingly rare with the development and wider use of antibiotics; therefore, it is often difficult to accurately diagnose this disease. Scraping cytology is a type of exfoliative cytology, in which a brush is used to remove cells from the surface of lesions that can be observed in a smear preparation. This examination is superior to previous diagnostic methods, both in terms of the relative convenience for clinicians in obtaining samples, and in the reduction of stress on patients as it is a comparatively non-invasive procedure. Similar tests have been applied to gynecological examinations to screen for various conditions, and to diagnose many
http://dx.doi.org/10.1016/j.ajoms.2016.12.006 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
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ARTICLE IN PRESS A. Kouketsu et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2017) xxx–xxx
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Fig. 1. Image taken during the patient’s first visit to our department, showing an ulcer, painful indurated mass, redness, and swelling of the left buccal mucosa.
kinds of diseases early and easily. Although these results demonstrate the efficacy of this technique when applied to mucosa in other organs, at present there are relatively few medical facilities that employ scraping cytology for oral cavity examinations, therefore resulting a few clinical reports of the use of this method for diagnosing premalignant and malignant oral lesions [4–6]. Here, we report the successful diagnosis of a rare case of actinomycosis of the buccal mucosa in an 8-year-old boy, through the application of scraping cytology. 2. Case report An 8-year-old male patient was admitted to Department of Oral and Maxillofacial, Surgery Division of Dentistry, Tohoku University Hospital in September 2015 for emergency treatment, on complaint of pain in the left buccal mucosa and experiencing the opening difficulty of his mouth. The patient had no other recent history of infection related to injury, of related conditions, or of having taken prescribed medication. Physical examination revealed signs of an infection disorder, including cervical lymph node swelling, ulcer, a painful indurated mass, and redness and swelling of the left buccal mucosa, but revealed no fever (body temperature at time of examination, 37.3 ◦ C), drainage of pus from the buccal mucosa, or any abnormal blood test results, including inflammatory markers, at that time (Fig. 1). Only normal flora was detected in bacterial culture taken from a swab of the ulcer surface. A panoramic radiograph showed no abnormal findings in the teeth or jaw. He reported an incident in which he had accidentally bitten his left buccal mucosa. The clinical diagnosis was a buccal ulcer, related to the bite. The patient was treated with cefditoren pivoxil (3 × 0.1 g/day), and was then required to irrigate the affected area with normal saline until discharge. Ten days after the first oral administration of antibiotic, most of these symptoms had improved. In October 2015, 14 days after the first visit, the patient presented again with pain and swelling in the left buccal mucosa, and was readmitted to our hospital for emergency treatment. Clinical examination revealed pyrexia (38.5 ◦ C), tachycardia (heart rate, 106 beats/min), trismus (maximum 5 mm), an ingestion disorder, lethargy, and an increase in the size of the ulcer and indurated mass in the left buccal mucosa, with severe associated pain (Figs. 2 and 3). Laboratory findings indicated the presence of acute systemic inflammation (WBC 18,500/mm3 , C-reactive protein 1.0 mg/dL). The patient was admitted to a pediatric ward in our hospital, following the diagnosis of acute phlegmon of the left buccal mucosa, resulting from recurrence of infection of the original lesion. The infection of the buccal mucosa was treated with irrigation, followed by intravenous administration of the antibiotic cefmetazole (3 × 0.5 g/day). During the acute phase, bacterial culture exami-
nation and scraping cytology of the ulcer were performed. The scraping cytology method was performed according to the guidelines of the Japanese Association of Clinical Cytology in 2016. The patient’s mouth was washed before the procedure, and smears were taken from buccal mucosa under adequate illumination, by scraping with a sterilized commercially available nylon toothbrush. Using moderate pressure, the brush was repeatedly brushed in one direction over the entire lesion until pinpoint bleeding was obtained, and cells were extracted from the lamina propria or fat tissue layer. The material from the brush was spread onto the middle third of two clean, dry glass slides. The smears were fixed immediately with 95% isopropyl alcohol for staining using the Papanicolaou method. Significant bacterial colonization was not detected at the ulcer surface in bacterial culture examination. However, on cytological examination of the brush cytology oral smears, multiple colonies of Actinomyces were seen, in conjunction with other rod-shaped bacteria and epithelial tissue, and an inflammatory background. Actinomyces strangles with abundant mycelia radiating outwards are visible, accompanying neutrophilic inflammation (Fig. 3). Based on the guidelines of the Japanese Association of Clinical Cytology in 2016 with a cytotechnologist and two cytopathologists, the cytological results in accordance with the Bethesda System were negative for an intraepithelial lesion or malignancy. MR image acquired on day 3 showed an oval lesion of the left buccal mucosa, and indicated local granulomatous inflammation and the expanse of the abscess (Fig. 4). Considering these findings, we diagnosed the patient with actinomycosis of the buccal mucosa, and treated this infection by irrigation with the long-term antibiotic amoxicillin (3 × 0.5 g/day). The patient showed an improvement in general condition, with an increase in appetite and recovery from swelling and trismus. For this reason, the patient was discharged on day 5 (Fig. 5). Long term antibiotic therapy with amoxicillin was continued for 2 months, with continued monitoring of the patient’s condition after discharge. The ulcer and indurated mass were eliminated within 1 month after discharge, and the patient showed no evidence of recurrence within the 7-month follow-up period following the end of treatment with amoxicillin (Fig. 6).
3. Discussion Actinomycosis of the cervicofacial area is mainly attributed to infection with A. israelii. Actinomyces are normal commensal bacteria of the oral cavity, and colonize the mucosa, dental plaque, tartar, and tonsil fossa. These bacteria are considered to have low pathogenicity, and actinomycosis is generally developed as a result of concomitant or opportunistic infection [1–3]. This disease frequently develops in the maxilla and mandible bones [3]. Conversely, this infection is rarely confined only to soft tissue, as we presented in this case. It is generally believed that the contributing factors to the development of actinomycosis on this occasion were remaining suture threads from the initial treatment for buccal ulcer and a secondary infection resulting from oral surgery and bites [7–10]. For a definitive diagnosis of this disease, the existence of an Actinomyces colony, or detection of Actinomyces by bacterial culture, is required in addition to clinical symptoms, including board-like induration, formation of multiple small abscesses, and trismus [1,2]. However, the detection of Actinomyces in bacterial cultures is difficult, because of contamination by the normal bacterial flora from the oral cavity and the added complication of producing a suitable anaerobic culture [3,11]. In addition, it is thought that the growth of these bacteria is effected by many antibiotics, and that colonies can become latent as result of initial antibiotic therapy, therefore making their detection more difficult [3,12]. Many cases
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
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Fig. 2. A and B: Images taken at the time of the second emergency admission, showing trismus, and growth of the ulcer and indurated mass in left buccal mucosa, with associated strong pain.
Fig. 3. A and B: On cytological examination of brush cytology of the oral ulcer, multiple colonies of Actinomyces are seen, in conjunction with other rod-shaped bacteria and epithelial tissue, and an inflammatory background. Actinomyces strangles with abundant mycelia radiating outwards are visible accompanying neutrophilic inflammation (Papanicolaou stain, A × 100, B × 400).
Fig. 4. Axial T1-weighted MR imaging of the left buccal mucosa (Fig. 4A) showed an oval lesion with high signal intensity. Axial T2-weighted MR imaging (Fig. 4B) produced intermediate signal intensity in this mass (arrow).
of histopathological diagnoses of actinomycosis using resected specimens have been reported [7–10,12–14]. Detection for this bacteria with histopathological examinations, such as hematoxylin and eosin (H&E) staining and Grocott’s stain, using specimens
obtained from biopsies or excisions, has been required as an alternative to these inefficient bacterial culture examination methods [1,2]. However, the acquisition of samples via invasive surgical procedures places additional stress on patients and performing minor
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
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Fig. 5. Image taken at the time of discharge, showing the recovery from swelling and trismus, but a remaining slight ulcer and indurated mass.
surgery, such as biopsy or excision, is complicated by trismus. Previously, scraping cytology of the oral cavity has not been popular among oral clinicians. There are some reports in which this method has been applied to detect oral malignant tumors [4–6]; until now, however, cytology for detecting oral Actinomyces infections had not been reported. Some reports suggest that cytological examinations are useful in diagnosing pelvic or lung actinomycosis [11,15]. Cytology might also be useful in the preoperative diagnosis of pelvic or breast actinomycosis [11,15]; particularly, Matsuda et al. suggested that careful cytological examination might be provide a higher detection rate for Actinomyces, compared to pathology or bacteriology of pelvic actinomycosis [11]. The cytological presentation of actinomycosis of the oral cavity, breast, lung, and pelvis, includes basophilic granules of Actinomyces with an inflammatory background, and thin filamentous mycelia spreading outwards and to form Actinomyces colonies. Papanicolaou staining was used effectively in this case; however, Gram staining or Grocott-Gomori’s (or Gömöri) methenamine silver staining have also been useful for detecting Actinomyces colonization by cytological examination. For actinomycosis of the breast and hepatobiliary system, culture is difficult and positive only in a minority of cases, and a cytological diagnosis of actinomycosis is, in comparison, minimally invasive and quick [16,17]. It is generally more difficult to detect actinomycosis in the oral cavity by culture, because of the high microbial diversity and subsequent necessity for many suitable cell culture mediums. We believe this examination was suitable in this case, in which the patient was a child with trismus, and believe that this example provides an important evidence to support the application of cytology for examining pathologies of the oral cavity, without the requirement for additional examinations and their associated burden on patients. For the treatment for actinomycosis, with indurated mass in soft tissue, related to chronic fibrosis, as we presented in this case, prolonged high doses of antibiotics are required [3]. If an abscess or tubercle is formed in a deep region of the soft tissue, drainage, debridement, and excision of these lesions are recommended to convert the affected area to an aerobic environment. The mainstay antibiotic treatment is penicillin, which should be administered for 4–6 weeks, or occasionally longer. Other antibiotics, including erythromycin, streptomycin, lincomycin, vancomycin, cephalosporins, chloramphenicol, clindamycin, and tetracyclines have all been used with success [18–20]. More reliable treatment and the prevention of recurrent infections has been achieved using topical application of antibiotics, such as clindamycin or hyperbaric oxygen therapy, in addition to treatment with other antibiotics and surgical therapy [21]. In this case, although we recognized an ulcer and indurated mass in the deep area of soft tissue, we only prescribed long-term antibi-
Fig. 6. Clinical examination 7 months after the antibiotic treatment. The image shows a small segment of exposed bone in the patient’s right posterior mandible, but no evidence of acute inflammation.
otic therapy with amoxicillin without surgical treatments, such as debridement and excision, because of the quick cytology diagnosis and the patient’s age. After 8 weeks of treatment, the lesion had cleared and did not reappear within the 7-month follow-up period. Future reports of the successful application of scraping cytology for the diagnosis of actinomycosis and other oral cavity pathologies will establish the effectiveness of this method in wider clinical settings. Conflict of interest statement No sources of funding were used for this study. The authors declare no conflicts of interest or financial disclosures. All authors were participated in the preparation of the manuscript. Informed consent has been obtained for the use of patient details and images of the patient in this manuscript. References [1] Cawson RA, Odell EW. Cawson’s essentials of oral pathology and oral medicine. 8th ed. London: Churchill Livingstone; 2008. [2] Neville BW, Damm DD, Allen CM, Chi AC. Oral and maxillofacial pathology. 4th ed. Missouri: Saunders; 2015. [3] Hupp JR, Ellis III E, Tucker MR. Contemporary oral and maxillofacial surgery. 6th ed. Missouri: Mosby; 2013. [4] Trakroo A, Sunil MK, Trivedi A, Garg R, Kulkarni A, Arora S. Efficacy of oral brush biopsy without computer-assisted analysis in oral premalignant and malignant lesions: a study. J Int Oral Health 2015;7:33–8. [5] Gupta S, Shah JS, Parikh S, Limbdiwala P, Goel S. Clinical correlative study on early detection of oral cancer and precancerous lesions by modified oral brush biopsy and cytology followed by histopathology. J Cancer Res Ther 2014;2:232–8. [6] Babshet M, Nandimath K, Pervatikar SK, Naikmasur VG. Effcacy of oral brush cytology in the evaluation of the oral premalignant and malignant lesions. J Cytol 2011;28:165–72. [7] Vldakovié B, Macan D, Peric´ B, Manojlovic´ S. Actinomycosis of the cheek. Srp Arh Celok Lek 2014;142:472–5. [8] AbdullGaffar B, Ghandoor K, Ahli Q. Actinomycotic sinus of the buccal mucosa: a rare complication of cheek dimple creation. Aesthet Surg J 2014;34:80–2. [9] Bartell HL, Sonabend ML, Hsu S. Actinomycosis presenting as a large facial mass. Dermatol Online J [Internet] 2006 [cited 2016 April 20];12:[about 1 p.]. Available from: http://escholarship.org/uc/item/5493b2d7. [10] Park JK, Lee HK, Ha HK, Choi HY, Choi CG. Cervicofacial actinomycosis: CT and imaging findings in seven patients. Am J Neuroradiol 2003;24:331–5. [11] Matsuda K, Nakajima H, Khan KN, Tanigawa T, Hamaguchi D, Kitajima M, et al. Preoperative diagnosis of pelvic actinomycosis by clinical cytology. Int J Womens Health 2012;4:527–33. [12] Chatterjee RP, Shah N, Kundu S, Mahmud SA, Bhandari S. Cervicofacial actinomycosis mimicking osseous neoplasm: a rare case. J Clin Diagn Res 2015;9:29–31. [13] Gannepalli A, Ayinampudi BK, Baghirath PV, Reddy GV. Actinomycotic osteomyelitis of maxilla presenting as oroantral fistula: a rare case report. Case Rep Dent [Internet] 2015;2015:5, http://dx.doi.org/10.1155/2015/689240 [cited 2016 Apr 26]:2015:[5 p.].
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
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[14] Sun Y, Kuyama K, Fifita SF, Nogami T, Fukui K, Kondoh T, et al. Actinomycosis in radicular cyst: a case report and literature survey. Oral Med Pathol 2009;14:113–6. [15] Gupta C, Singh P, Bedi S, Kapur K. Primary actinomycosis of the breast masquerading as malignancy: diagnosis by fine needle aspiration cytology. Breast Care 2012;7:153–4. [16] Gosavi AV, Anvikar AR, Sulhyan KR, Manek DD. Primary actinomycosis of breast-A diagnosis on cytology. Diagn Cytopathol 2016;44:693–5. [17] Xing J, Rodriguez EF, Monaco SE, Pantanowitz L. Cytopathology of hepatobiliary-related actinomycosis. Acta Cytol 2016;60:179–84.
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[18] Topazian RG, Goldberg MH. Oral and maxillofacial infections. 2nd ed. Philadelphia: Saunders; 1988. [19] Emmanuelli JL. Infectious granulomatous diseases of the head and neck. Am J Otolaryngol 1993;14:155–67. [20] Martin MV. Antibiotic treatment of cervicofacial actinomycosis for patients allergic to penicillin: a clinical and in vitro study. Br J Oral Maxillofac Surg 1985;23:428–34. [21] Suzuki H, Takagi R, Imai N, Nagashima K. A case of actinomycosis in a child with allergies to many kinds of medicines. Pediatr Oral Maxillofac Surg 2002;12:15–20.
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
ARTICLE IN PRESS Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2017) xxx–xxx
Contents lists available at ScienceDirect
Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology journal homepage: www.elsevier.com/locate/jomsmp
Case report
Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report Atsumu Kouketsu a,∗ , Aritsune Matsui a , Shiro Mori a , Haruka Saito a , Hikari Suzuki a , Yukiko Shibahara b , Hiroyuki Kumamoto c , Tetsu Takahashi a a Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry (Chief: Prof. Tetsu Takahashi), Japan b Department of Pathology, Tohoku University Graduate School of Medicine, Japan c Division of Oral Pathology, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, Japan
a r t i c l e
i n f o
Article history: Received 26 May 2016 Received in revised form 27 November 2016 Accepted 26 December 2016 Available online xxx Keywords: Actinomycosis Buccal mucosa Scraping cytology
a b s t r a c t Actinomycosis, a rare chronic granulomatous bacterial infection induced by Actinomyces species, colonizes the mouth, colon, and vagina. Although Actinomyces spp. are well-known oral commensals, actinomycosis is a rare oral infection. It is difficult to detect Actinomyces in biopsies, using histopathologic methods, or through examination of bacterial cultures; therefore, providing an accurate diagnosis is problematic. Recently, oral brush scraping cytology has been performed for the diagnosis of premalignant and malignant lesions, but it is difficult to determine the efficacy of this method based on the published reports, and whether it is a suitable tool for detecting Actinomyces infections in the general public. Here, we report a rare case of actinomycosis of the buccal mucosa in an 8-year-old boy that was successfully diagnosed by scraping cytology. He exhibited pain and swelling in the left buccal, and was admitted to our hospital for emergency care. Clinical examination revealed pyrexia, tachycardia, trismus, ingestion disorder, lethargy, and ulcer as well as having an indurated mass in the left buccal mucosa accompanied by strong pain. Following a clinical diagnosis of acute phlegmon of the left buccal mucosa, antibiotic and fluid therapy was performed. Because of detection of Actinomyces colonies at the ulcer surface using scraping cytology, we continued to administer long-term antibiotic therapy with penicillin for 2 months. The patient’s general condition was improved, and this was confirmed by laboratory results, and the trismus and painful nodular mass were successfully cured. The patient has shown no subsequent evidence of recurrence for 7 months of following treatment. © 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
1. Introduction Actinomycosis is a chronic, suppurative, and granulomatous infectious disease. In humans, the disease is caused mainly by Actynomyces israelii that is a species of Gram-positive, rod-shaped bacteria within the genus Actinomyces [1,2]. Known to live commensally within the human oral cavity, A. israelii is an opportunistic pathogen and a cause of cervicofacial actinomycosis as well as
夽 AsianAOMS: Asian Association of Oral and Maxillofacial Surgeons; ASOMP: Asian Society of Oral and Maxillofacial Pathology; JSOP: Japanese Society of Oral Pathology; JSOMS: Japanese Society of Oral and Maxillofacial Surgeons; JSOM: Japanese Society of Oral Medicine; JAMI: Japanese Academy of Maxillofacial Implants. ∗ Corresponding author at: Division of Oral and Maxillofacial Surgery, Department of Oral Medicine and Surgery, Tohoku University Graduate School of Dentistry, 4-1 Seiryo-machi, Aoba-ku, Sendai, Miyagi, 980-8575, Japan. E-mail address: kouketsu [email protected] (A. Kouketsu).
chest or abdominal infections. The main clinical symptoms of oral actinomycosis are painless or painful masses with board-like induration, the formation of multiple small abscesses, and trismus [1–3]. Moreover, positive results on bacterial culture examination, or histopathological detection of Actinomyces colonization in lesions or pus, is a necessary diagnostic criterion for this disease. Although common in the past, the presentation of these typical symptoms has become increasingly rare with the development and wider use of antibiotics; therefore, it is often difficult to accurately diagnose this disease. Scraping cytology is a type of exfoliative cytology, in which a brush is used to remove cells from the surface of lesions that can be observed in a smear preparation. This examination is superior to previous diagnostic methods, both in terms of the relative convenience for clinicians in obtaining samples, and in the reduction of stress on patients as it is a comparatively non-invasive procedure. Similar tests have been applied to gynecological examinations to screen for various conditions, and to diagnose many
http://dx.doi.org/10.1016/j.ajoms.2016.12.006 2212-5558/© 2016 Published by Elsevier Ltd on behalf of Asian AOMS, ASOMP, JSOP, JSOMS, JSOM, and JAMI. 夽
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
G Model JOMSMP-589; No. of Pages 5
ARTICLE IN PRESS A. Kouketsu et al. / Journal of Oral and Maxillofacial Surgery, Medicine, and Pathology xxx (2017) xxx–xxx
2
Fig. 1. Image taken during the patient’s first visit to our department, showing an ulcer, painful indurated mass, redness, and swelling of the left buccal mucosa.
kinds of diseases early and easily. Although these results demonstrate the efficacy of this technique when applied to mucosa in other organs, at present there are relatively few medical facilities that employ scraping cytology for oral cavity examinations, therefore resulting a few clinical reports of the use of this method for diagnosing premalignant and malignant oral lesions [4–6]. Here, we report the successful diagnosis of a rare case of actinomycosis of the buccal mucosa in an 8-year-old boy, through the application of scraping cytology. 2. Case report An 8-year-old male patient was admitted to Department of Oral and Maxillofacial, Surgery Division of Dentistry, Tohoku University Hospital in September 2015 for emergency treatment, on complaint of pain in the left buccal mucosa and experiencing the opening difficulty of his mouth. The patient had no other recent history of infection related to injury, of related conditions, or of having taken prescribed medication. Physical examination revealed signs of an infection disorder, including cervical lymph node swelling, ulcer, a painful indurated mass, and redness and swelling of the left buccal mucosa, but revealed no fever (body temperature at time of examination, 37.3 ◦ C), drainage of pus from the buccal mucosa, or any abnormal blood test results, including inflammatory markers, at that time (Fig. 1). Only normal flora was detected in bacterial culture taken from a swab of the ulcer surface. A panoramic radiograph showed no abnormal findings in the teeth or jaw. He reported an incident in which he had accidentally bitten his left buccal mucosa. The clinical diagnosis was a buccal ulcer, related to the bite. The patient was treated with cefditoren pivoxil (3 × 0.1 g/day), and was then required to irrigate the affected area with normal saline until discharge. Ten days after the first oral administration of antibiotic, most of these symptoms had improved. In October 2015, 14 days after the first visit, the patient presented again with pain and swelling in the left buccal mucosa, and was readmitted to our hospital for emergency treatment. Clinical examination revealed pyrexia (38.5 ◦ C), tachycardia (heart rate, 106 beats/min), trismus (maximum 5 mm), an ingestion disorder, lethargy, and an increase in the size of the ulcer and indurated mass in the left buccal mucosa, with severe associated pain (Figs. 2 and 3). Laboratory findings indicated the presence of acute systemic inflammation (WBC 18,500/mm3 , C-reactive protein 1.0 mg/dL). The patient was admitted to a pediatric ward in our hospital, following the diagnosis of acute phlegmon of the left buccal mucosa, resulting from recurrence of infection of the original lesion. The infection of the buccal mucosa was treated with irrigation, followed by intravenous administration of the antibiotic cefmetazole (3 × 0.5 g/day). During the acute phase, bacterial culture exami-
nation and scraping cytology of the ulcer were performed. The scraping cytology method was performed according to the guidelines of the Japanese Association of Clinical Cytology in 2016. The patient’s mouth was washed before the procedure, and smears were taken from buccal mucosa under adequate illumination, by scraping with a sterilized commercially available nylon toothbrush. Using moderate pressure, the brush was repeatedly brushed in one direction over the entire lesion until pinpoint bleeding was obtained, and cells were extracted from the lamina propria or fat tissue layer. The material from the brush was spread onto the middle third of two clean, dry glass slides. The smears were fixed immediately with 95% isopropyl alcohol for staining using the Papanicolaou method. Significant bacterial colonization was not detected at the ulcer surface in bacterial culture examination. However, on cytological examination of the brush cytology oral smears, multiple colonies of Actinomyces were seen, in conjunction with other rod-shaped bacteria and epithelial tissue, and an inflammatory background. Actinomyces strangles with abundant mycelia radiating outwards are visible, accompanying neutrophilic inflammation (Fig. 3). Based on the guidelines of the Japanese Association of Clinical Cytology in 2016 with a cytotechnologist and two cytopathologists, the cytological results in accordance with the Bethesda System were negative for an intraepithelial lesion or malignancy. MR image acquired on day 3 showed an oval lesion of the left buccal mucosa, and indicated local granulomatous inflammation and the expanse of the abscess (Fig. 4). Considering these findings, we diagnosed the patient with actinomycosis of the buccal mucosa, and treated this infection by irrigation with the long-term antibiotic amoxicillin (3 × 0.5 g/day). The patient showed an improvement in general condition, with an increase in appetite and recovery from swelling and trismus. For this reason, the patient was discharged on day 5 (Fig. 5). Long term antibiotic therapy with amoxicillin was continued for 2 months, with continued monitoring of the patient’s condition after discharge. The ulcer and indurated mass were eliminated within 1 month after discharge, and the patient showed no evidence of recurrence within the 7-month follow-up period following the end of treatment with amoxicillin (Fig. 6).
3. Discussion Actinomycosis of the cervicofacial area is mainly attributed to infection with A. israelii. Actinomyces are normal commensal bacteria of the oral cavity, and colonize the mucosa, dental plaque, tartar, and tonsil fossa. These bacteria are considered to have low pathogenicity, and actinomycosis is generally developed as a result of concomitant or opportunistic infection [1–3]. This disease frequently develops in the maxilla and mandible bones [3]. Conversely, this infection is rarely confined only to soft tissue, as we presented in this case. It is generally believed that the contributing factors to the development of actinomycosis on this occasion were remaining suture threads from the initial treatment for buccal ulcer and a secondary infection resulting from oral surgery and bites [7–10]. For a definitive diagnosis of this disease, the existence of an Actinomyces colony, or detection of Actinomyces by bacterial culture, is required in addition to clinical symptoms, including board-like induration, formation of multiple small abscesses, and trismus [1,2]. However, the detection of Actinomyces in bacterial cultures is difficult, because of contamination by the normal bacterial flora from the oral cavity and the added complication of producing a suitable anaerobic culture [3,11]. In addition, it is thought that the growth of these bacteria is effected by many antibiotics, and that colonies can become latent as result of initial antibiotic therapy, therefore making their detection more difficult [3,12]. Many cases
Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006
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Fig. 2. A and B: Images taken at the time of the second emergency admission, showing trismus, and growth of the ulcer and indurated mass in left buccal mucosa, with associated strong pain.
Fig. 3. A and B: On cytological examination of brush cytology of the oral ulcer, multiple colonies of Actinomyces are seen, in conjunction with other rod-shaped bacteria and epithelial tissue, and an inflammatory background. Actinomyces strangles with abundant mycelia radiating outwards are visible accompanying neutrophilic inflammation (Papanicolaou stain, A × 100, B × 400).
Fig. 4. Axial T1-weighted MR imaging of the left buccal mucosa (Fig. 4A) showed an oval lesion with high signal intensity. Axial T2-weighted MR imaging (Fig. 4B) produced intermediate signal intensity in this mass (arrow).
of histopathological diagnoses of actinomycosis using resected specimens have been reported [7–10,12–14]. Detection for this bacteria with histopathological examinations, such as hematoxylin and eosin (H&E) staining and Grocott’s stain, using specimens
obtained from biopsies or excisions, has been required as an alternative to these inefficient bacterial culture examination methods [1,2]. However, the acquisition of samples via invasive surgical procedures places additional stress on patients and performing minor
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Fig. 5. Image taken at the time of discharge, showing the recovery from swelling and trismus, but a remaining slight ulcer and indurated mass.
surgery, such as biopsy or excision, is complicated by trismus. Previously, scraping cytology of the oral cavity has not been popular among oral clinicians. There are some reports in which this method has been applied to detect oral malignant tumors [4–6]; until now, however, cytology for detecting oral Actinomyces infections had not been reported. Some reports suggest that cytological examinations are useful in diagnosing pelvic or lung actinomycosis [11,15]. Cytology might also be useful in the preoperative diagnosis of pelvic or breast actinomycosis [11,15]; particularly, Matsuda et al. suggested that careful cytological examination might be provide a higher detection rate for Actinomyces, compared to pathology or bacteriology of pelvic actinomycosis [11]. The cytological presentation of actinomycosis of the oral cavity, breast, lung, and pelvis, includes basophilic granules of Actinomyces with an inflammatory background, and thin filamentous mycelia spreading outwards and to form Actinomyces colonies. Papanicolaou staining was used effectively in this case; however, Gram staining or Grocott-Gomori’s (or Gömöri) methenamine silver staining have also been useful for detecting Actinomyces colonization by cytological examination. For actinomycosis of the breast and hepatobiliary system, culture is difficult and positive only in a minority of cases, and a cytological diagnosis of actinomycosis is, in comparison, minimally invasive and quick [16,17]. It is generally more difficult to detect actinomycosis in the oral cavity by culture, because of the high microbial diversity and subsequent necessity for many suitable cell culture mediums. We believe this examination was suitable in this case, in which the patient was a child with trismus, and believe that this example provides an important evidence to support the application of cytology for examining pathologies of the oral cavity, without the requirement for additional examinations and their associated burden on patients. For the treatment for actinomycosis, with indurated mass in soft tissue, related to chronic fibrosis, as we presented in this case, prolonged high doses of antibiotics are required [3]. If an abscess or tubercle is formed in a deep region of the soft tissue, drainage, debridement, and excision of these lesions are recommended to convert the affected area to an aerobic environment. The mainstay antibiotic treatment is penicillin, which should be administered for 4–6 weeks, or occasionally longer. Other antibiotics, including erythromycin, streptomycin, lincomycin, vancomycin, cephalosporins, chloramphenicol, clindamycin, and tetracyclines have all been used with success [18–20]. More reliable treatment and the prevention of recurrent infections has been achieved using topical application of antibiotics, such as clindamycin or hyperbaric oxygen therapy, in addition to treatment with other antibiotics and surgical therapy [21]. In this case, although we recognized an ulcer and indurated mass in the deep area of soft tissue, we only prescribed long-term antibi-
Fig. 6. Clinical examination 7 months after the antibiotic treatment. The image shows a small segment of exposed bone in the patient’s right posterior mandible, but no evidence of acute inflammation.
otic therapy with amoxicillin without surgical treatments, such as debridement and excision, because of the quick cytology diagnosis and the patient’s age. After 8 weeks of treatment, the lesion had cleared and did not reappear within the 7-month follow-up period. Future reports of the successful application of scraping cytology for the diagnosis of actinomycosis and other oral cavity pathologies will establish the effectiveness of this method in wider clinical settings. Conflict of interest statement No sources of funding were used for this study. The authors declare no conflicts of interest or financial disclosures. All authors were participated in the preparation of the manuscript. Informed consent has been obtained for the use of patient details and images of the patient in this manuscript. References [1] Cawson RA, Odell EW. Cawson’s essentials of oral pathology and oral medicine. 8th ed. London: Churchill Livingstone; 2008. [2] Neville BW, Damm DD, Allen CM, Chi AC. Oral and maxillofacial pathology. 4th ed. Missouri: Saunders; 2015. [3] Hupp JR, Ellis III E, Tucker MR. Contemporary oral and maxillofacial surgery. 6th ed. Missouri: Mosby; 2013. [4] Trakroo A, Sunil MK, Trivedi A, Garg R, Kulkarni A, Arora S. Efficacy of oral brush biopsy without computer-assisted analysis in oral premalignant and malignant lesions: a study. J Int Oral Health 2015;7:33–8. [5] Gupta S, Shah JS, Parikh S, Limbdiwala P, Goel S. Clinical correlative study on early detection of oral cancer and precancerous lesions by modified oral brush biopsy and cytology followed by histopathology. J Cancer Res Ther 2014;2:232–8. [6] Babshet M, Nandimath K, Pervatikar SK, Naikmasur VG. Effcacy of oral brush cytology in the evaluation of the oral premalignant and malignant lesions. J Cytol 2011;28:165–72. [7] Vldakovié B, Macan D, Peric´ B, Manojlovic´ S. Actinomycosis of the cheek. Srp Arh Celok Lek 2014;142:472–5. [8] AbdullGaffar B, Ghandoor K, Ahli Q. Actinomycotic sinus of the buccal mucosa: a rare complication of cheek dimple creation. Aesthet Surg J 2014;34:80–2. [9] Bartell HL, Sonabend ML, Hsu S. Actinomycosis presenting as a large facial mass. Dermatol Online J [Internet] 2006 [cited 2016 April 20];12:[about 1 p.]. Available from: http://escholarship.org/uc/item/5493b2d7. [10] Park JK, Lee HK, Ha HK, Choi HY, Choi CG. Cervicofacial actinomycosis: CT and imaging findings in seven patients. Am J Neuroradiol 2003;24:331–5. [11] Matsuda K, Nakajima H, Khan KN, Tanigawa T, Hamaguchi D, Kitajima M, et al. Preoperative diagnosis of pelvic actinomycosis by clinical cytology. Int J Womens Health 2012;4:527–33. [12] Chatterjee RP, Shah N, Kundu S, Mahmud SA, Bhandari S. Cervicofacial actinomycosis mimicking osseous neoplasm: a rare case. J Clin Diagn Res 2015;9:29–31. [13] Gannepalli A, Ayinampudi BK, Baghirath PV, Reddy GV. Actinomycotic osteomyelitis of maxilla presenting as oroantral fistula: a rare case report. Case Rep Dent [Internet] 2015;2015:5, http://dx.doi.org/10.1155/2015/689240 [cited 2016 Apr 26]:2015:[5 p.].
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Please cite this article in press as: Kouketsu A, et al. Actinomycosis manifested in the buccal mucosa estimated with scraping cytology: A case report. J Oral Maxillofac Surg Med Pathol (2017), http://dx.doi.org/10.1016/j.ajoms.2016.12.006