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Dirofilaria repens presenting as a premasseteric nodule
Dirofilaria repens presenting as a premasseteric nodule ¨ zmen, MD,b Cem Sezer, MD,c Reha Yavuzer, MD,d Osman Latifogˇlu, MD,a Selahattin O e ¨ mer Uluogˇlu, MD,f Ankara, Turkey Ku¨rs¸at Altintas¸, MD, and O GAZI UNIVERSITY AND ANKARA UNIVERSITY
Dirofilariasis is a rare zoonosis that is mainly seen with subcutaneous or pulmonary involvement. Natural hosts are dogs, cats, jackals, and raccoons; however, humans can rarely become an accidental host for the parasite. In the reported case, infection manifested as a subcutaneous nodule, representing a significant diagnostic challenge for both the surgeon and the pathologist. A case of a 62-year-old man with a premasseteric soft tissue mass caused by Dirofilaria repens is presented with histopathologic confirmation. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:217-20)
Dirofilariasis is a rare zoonosis that is mainly seen with subcutaneous or pulmonary involvement. The natural hosts of the parasite are dogs, cats, foxes, jackals, and raccoons.1-4 Man is an accidental host for the filaria. The most common presentation is a subcutaneous or submucosal nodule, usually in areas not covered by clothes, such as the head and limbs, and the thoracic wall. Filaria dies in human tissue and provokes a local inflammatory response, manifesting clinically as a subcutaneous nodule. Most subcutaneous and conjunctival infections are caused by Dirofilaria repens, and Dirofilaria immitis is responsible for pulmonary dirofilariasis. The Aedes, Culex, and Anopheles mosquitoes are considered responsible for transmission of the parasite.5 In Europe, subcutaneous dirofilariasis is most often seen in the countries around the Mediterranean Sea. To our knowledge, this is the fourth case reported in Turkey.5-7 CASE REPORT A 62-year-old man was seen with a deep mass of the right cheek, lateral to the masseter. The patient had been aware of the lesion for 2 months. The mass was about 1 cm in diameter, semirigid on palpation, and loosely fixed to the masseter.
a
Associate Professor, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. b Resident, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. c Assistant Professor, Department of Pathology, Gazi University, Ankara, Turkey. d Assistant Professor, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. e Professor, Department of Microbiology, Ankara University, Ankara, Turkey. f Professor, Department of Pathology, Gazi University, Ankara, Turkey. Received for publication Dec 4, 2001; returned for revision Jan 18, 2002; accepted for publication Mar 7, 2002. © 2002 by Mosby, Inc. 1079-2104/2002/$35.00 ⫹ 0 7/14/125275 doi:10.1067/moe.2002.125275
Because moderate pain and hyperemia were associated with the mass, a 10-day course of antibiotics was administered, producing resolution of the signs of inflammation. To elucidate the nature of the mass and to define its relation with the parotid gland, radiologic investigations were performed. Ultrasound scan study and computed tomographic scan examination revealed a cystic mass approximately 1 cm in diameter containing solid areas, localized in the subcutaneous fat with minimal extension into underlying masseteric fascia (Fig 1, A, B). No connection was found with the parotid gland. The lesion was excised with local anesthesia with 2% lidocaine and 1:200.000 adrenaline infiltration. After an extra oral incision, the mass was reached and dissected out from the surrounding tissues. Because the mass extended into the masseteric fascia, sharp dissection was necessary in this region. The excised specimen measured 1.5 ⫻ 0.9 ⫻ 0.7 cm and showed a yellowish color (Fig 1, C). The capsule was hard, encompassing a yellowish jelly-like material. Histopathologic examination revealed a granulomatous inflammatory reaction containing epithelioid histiocytes, foreign body giant cells, and eosinophiles. Within this inflammatory reaction, the nematode was clearly identified (Fig 2, A, B). After surgical excision of the nematode, the swelling completely resolved, and the patient has shown full recovery. No additional nodules were detected in any other body area.
DISCUSSION Although dirofilariasis exhibits a global distribution, the zoonosis is rare. Areas endemic for the parasite include the southeastern United States, Europe, and Australia.8 In Europe, especially in the areas around the Mediterranean sea (Italy, Spain, and Greece), and in the tropical, subtropical, and warm temperate regions of the world, zoonotic filarial infection in humans is caused by D repens, D immitis and Dirofilaria tenuis.9,10 Important species of the genus Dirofilaria are D repens, D immitis, Dirofilaria ursi, and D tenuis. The natural hosts of D immitis and D repens are dogs, cats, and foxes.11-13 The host of D tenuis is the raccoon, and 217
218 Latifogˇ lu et al
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY August 2002
Fig 1. A, Ultrasound scan revealed well-defined cystic mass with solid parts. B, Computed tomographic scan: axial section of computerized tomographic scan clarified location of mass, which was lying just over masseter muscle. C, Gross specimen: entire mass, which was covered by hard capsule tissue, was surgically removed.
the host of D ursi is the bear. Dogs are the most frequent reservoir host. Man is considered an accidental host, infected by a bite of an infected mosquito of the genera Aedes, Anopheles, or Culex. In humans, Dirofilaria species develop into unmated worms that neither reproduce nor release microfilariae. Human-to-human and human-to-arthropod transmission does not occur. Subcutaneous nodules in D repens infection occur most commonly in uncovered areas, such as the arms, legs, and head. In this case, we did not suspect D tenuis as the responsible organism because raccoons are not found in Turkey. Wild dogs, cats, and foxes are quite common in this region, making D repens a more likely causative agent. In contrast, a case occurring in Florida would be expected to be the result of D tenuis. Thus, knowledge of natural inhabitants of the region where the case occurs guides infections agent identification. The nematode is thought to grow gradually, with the time elapsed between onset of the infection and detection of the nodule typically at least 6 months. The parasite is constrained inside an inflammatory nodule, generally located in subcutaneous tissue or rarely in other tissues or organs, where it can survive for several months or even years.14 Although most of the cases are
asymptomatic, some may have pruritus, edema, arthritis, and subcutaneous swellings.15 Eosinophilia also has been described. This case was associated with moderate pain and hyperemia, leading to antibiotic therapy before surgical removal. Diagnosis generally depends on histologic examination. The clinician is most unlikely to suspect the parasitic nature of the nodule before biopsy, apart from situations where the parasite becomes visible, as when located under the conjunctiva. It is not uncommon for the filaria to die inside the inflammatory nodule. Subsequent invasion of inflammatory cells destroys parasite morphologic characteristics. Sometimes the entire body of the nematode may disappear, leaving in its place an empty circular imprint.14 In such cases, the definitive diagnosis becomes difficult to establish. Although serology and skin testing have not proven particularly helpful in confirmation of dirofilariasis because of inadequacies in test specificity and sensitivity, use of polymerase chain reaction technology has been suggested.16 Transmission of infection from the human host does not occur because these worms rarely grow to be sexually mature, and in no case, has microfilariemia been
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Fig 2. A, Histopathologic examination of lesion showed long nematode within lesion (hematoxylen eosin stain; magnification, ⫻100). B, Closer view of transverse section of nematode (hematoxylen eosin stain; magnification, ⫻400).
observed in human infections with these parasites.15,17 Microfilaremia has been reported in prednisolonetreated macaques.18-20 Excisional biopsy is both diagnostic and therapeutic.21 Symptoms quickly resolve after the removal of the worm. Because only a single worm is present in most cases, there is no need for further treatment.22 This pattern was confirmed in our case, as removal of the nodule led to symptom resolution and cure. REFERENCES 1. McLean JD, Beaver PC, Michalek H. Subcutaneous dirofilariasis in Okinawa, Japan. Am J Trop Med Hyg 1979;28:45. 2. Arvanitis PG, Vakalis NC, Damanakis AG, Theodossiadis GP. Ophthalmic dirofilariasis. Am J Ophthalmol 1997;123:689-91. 3. Harrus S, Harmelin A, Rodrig S, Favia G. Dirofilaria repens infection in a dog in Israel. Am J Trop Med Hyg 1999;61:639-41.
4. Jariya P, Sucharit S. Dirofilaria repens from the eyelid of a woman in Thailand. Am J Trop Med Hyg 1983;32:1456-7. 5. Logar J, Novsak S, Rakovec S, Stanisa O. Subcutaneous infection caused by Dirofilaria repens imported to Slovenia. J Infect 2001;42:72-4. 6. Kucukaydin M, Sahin I. The third case of dirofilariasis conjunctivae in Turkey. Mikrobiyol Bull 1986;20:25-8. 7. Cancrini G, Allende E, Favia G, Burnay F, Anton F, Simon F. Canine dirofilariasis in two cities of southeastern Spain. Vet Parasitol 2000;92:81-6. 8. Collins BM, Jones AC, Jimenez F. Dirofilaria tenuis infection of the oral mucosa and cheek. J Oral Maxillofac Surg 1993;51: 1037-40. 9. van den Ende J, Kumar V, Van Gompel A, van den Ende E, Puttemans A, Geerts M, et al. Subcutaneous dirofilariasis caused by Dirofilaria (nochitella) repens in a Belgian patient. Int J Dermatol 1995;34:274-7. 10. Herzberg AJ, Boyd PR, Gutierrez Y. Subcutaneous dirofilariasis in Collier County, Florida, USA. Am J Surg Pathol 1995;19: 934-9.
220 Latifogˇ lu et al
11. Stayerman C, Szvalb S, Sazbon A. Dirofilaria repens presenting as a subcutaneous nodule in the penis. BJU Int 1999;84:746-7. 12. Bradham RR, Locklair PR, Grimball A. Bilateral pulmonary nodules caused by Dirofilaria immitis. Ann Thorac Surg 1990; 50:312-3. 13. Eberhard ML, Daly JJ, Weinstein S, Farris HE. Dirofilaria immitis from the eye of a dog in Arkansas. J Parasitol 1977;63:978. 14. Pampiglione S, Rivasi F, Canestri-Trotti D. Pittfalls and difficulties in histological diagnosis of human dirofilariasis due to Dirofilaria (Nochitella) repens. Diagn Microbiol Infect Dis 1999; 34:57-64. 15. Fuentes I, Cascales A, Ros JM, Sansano C, Gonzalos-Arribas JL, Alvar J. Human subcutaneous dirofilariasis caused by Dirofilaria repens in Ibiza, Spain. Am J Trop Med Hyg 1994;51:401-4. 16. Favia G. Molecular diagnosis of Dirofilaria repens is not a dream. Diagn Microbiol Infect Dis 2000;37:81-2. 17. Font RL, Neafile RC, Perry HD. Subcutaneous dirofilariasis of the eyelid and ocular adnexa. Report of Six cases. Arch Ophthalmol 1980;98:1079-82. 18. MacDougall LT, Magoon CC, Fritsche TR. Dirofilaria repens manifesting as a breast nodule. Diagnostic problems and epidemiologic considerations. Am J Clin Pathol 1992;97:625-30.
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY August 2002 19. Wong MM. Experimental dirofilariasis in macaques. II. Susceptibility and host responses to Dirofilaria repens of dogs and cats. Am J Trop Med Hyg 1976;25:88-93. 20. Wong MM, Lim KC. Experimental dirofilariasis in macaques III. Susceptibility and host response to Dirofilaria tenuis of racoons. Am J Trop Med Hyg 1976;25:94-8. 21. Hira PR, Madda JP, al-Shamali MA, Eberhard ML. Dirofilariasis in Kuwait: first report of human infection due to Dirofilaria repens in the Arabian Gulf. Am J Trop Med Hyg 1994;51:590-2. 22. Ruiz-Moreno JM, Bornay-Llinares FJ, Proetp Maza G, Medrans M, Simon F, Eberhard ML. Subconjunctival infection with Dirofilaria repens: serological confirmation of cure following surgery. Arch Ophthalmol 1998;116:1370-2. Reprint requests: Reha Yavuzer, MD Baris¸ Sitesi 87. Sokak N0: 24 06530 Mustafa Kemal Mahallesi Ankara, Turkey [email protected]
Dirofilariasis is a rare zoonosis that is mainly seen with subcutaneous or pulmonary involvement. Natural hosts are dogs, cats, jackals, and raccoons; however, humans can rarely become an accidental host for the parasite. In the reported case, infection manifested as a subcutaneous nodule, representing a significant diagnostic challenge for both the surgeon and the pathologist. A case of a 62-year-old man with a premasseteric soft tissue mass caused by Dirofilaria repens is presented with histopathologic confirmation. (Oral Surg Oral Med Oral Pathol Oral Radiol Endod 2002;94:217-20)
Dirofilariasis is a rare zoonosis that is mainly seen with subcutaneous or pulmonary involvement. The natural hosts of the parasite are dogs, cats, foxes, jackals, and raccoons.1-4 Man is an accidental host for the filaria. The most common presentation is a subcutaneous or submucosal nodule, usually in areas not covered by clothes, such as the head and limbs, and the thoracic wall. Filaria dies in human tissue and provokes a local inflammatory response, manifesting clinically as a subcutaneous nodule. Most subcutaneous and conjunctival infections are caused by Dirofilaria repens, and Dirofilaria immitis is responsible for pulmonary dirofilariasis. The Aedes, Culex, and Anopheles mosquitoes are considered responsible for transmission of the parasite.5 In Europe, subcutaneous dirofilariasis is most often seen in the countries around the Mediterranean Sea. To our knowledge, this is the fourth case reported in Turkey.5-7 CASE REPORT A 62-year-old man was seen with a deep mass of the right cheek, lateral to the masseter. The patient had been aware of the lesion for 2 months. The mass was about 1 cm in diameter, semirigid on palpation, and loosely fixed to the masseter.
a
Associate Professor, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. b Resident, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. c Assistant Professor, Department of Pathology, Gazi University, Ankara, Turkey. d Assistant Professor, Department of Plastic and Reconstructive Surgery, Gazi University, Ankara, Turkey. e Professor, Department of Microbiology, Ankara University, Ankara, Turkey. f Professor, Department of Pathology, Gazi University, Ankara, Turkey. Received for publication Dec 4, 2001; returned for revision Jan 18, 2002; accepted for publication Mar 7, 2002. © 2002 by Mosby, Inc. 1079-2104/2002/$35.00 ⫹ 0 7/14/125275 doi:10.1067/moe.2002.125275
Because moderate pain and hyperemia were associated with the mass, a 10-day course of antibiotics was administered, producing resolution of the signs of inflammation. To elucidate the nature of the mass and to define its relation with the parotid gland, radiologic investigations were performed. Ultrasound scan study and computed tomographic scan examination revealed a cystic mass approximately 1 cm in diameter containing solid areas, localized in the subcutaneous fat with minimal extension into underlying masseteric fascia (Fig 1, A, B). No connection was found with the parotid gland. The lesion was excised with local anesthesia with 2% lidocaine and 1:200.000 adrenaline infiltration. After an extra oral incision, the mass was reached and dissected out from the surrounding tissues. Because the mass extended into the masseteric fascia, sharp dissection was necessary in this region. The excised specimen measured 1.5 ⫻ 0.9 ⫻ 0.7 cm and showed a yellowish color (Fig 1, C). The capsule was hard, encompassing a yellowish jelly-like material. Histopathologic examination revealed a granulomatous inflammatory reaction containing epithelioid histiocytes, foreign body giant cells, and eosinophiles. Within this inflammatory reaction, the nematode was clearly identified (Fig 2, A, B). After surgical excision of the nematode, the swelling completely resolved, and the patient has shown full recovery. No additional nodules were detected in any other body area.
DISCUSSION Although dirofilariasis exhibits a global distribution, the zoonosis is rare. Areas endemic for the parasite include the southeastern United States, Europe, and Australia.8 In Europe, especially in the areas around the Mediterranean sea (Italy, Spain, and Greece), and in the tropical, subtropical, and warm temperate regions of the world, zoonotic filarial infection in humans is caused by D repens, D immitis and Dirofilaria tenuis.9,10 Important species of the genus Dirofilaria are D repens, D immitis, Dirofilaria ursi, and D tenuis. The natural hosts of D immitis and D repens are dogs, cats, and foxes.11-13 The host of D tenuis is the raccoon, and 217
218 Latifogˇ lu et al
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY August 2002
Fig 1. A, Ultrasound scan revealed well-defined cystic mass with solid parts. B, Computed tomographic scan: axial section of computerized tomographic scan clarified location of mass, which was lying just over masseter muscle. C, Gross specimen: entire mass, which was covered by hard capsule tissue, was surgically removed.
the host of D ursi is the bear. Dogs are the most frequent reservoir host. Man is considered an accidental host, infected by a bite of an infected mosquito of the genera Aedes, Anopheles, or Culex. In humans, Dirofilaria species develop into unmated worms that neither reproduce nor release microfilariae. Human-to-human and human-to-arthropod transmission does not occur. Subcutaneous nodules in D repens infection occur most commonly in uncovered areas, such as the arms, legs, and head. In this case, we did not suspect D tenuis as the responsible organism because raccoons are not found in Turkey. Wild dogs, cats, and foxes are quite common in this region, making D repens a more likely causative agent. In contrast, a case occurring in Florida would be expected to be the result of D tenuis. Thus, knowledge of natural inhabitants of the region where the case occurs guides infections agent identification. The nematode is thought to grow gradually, with the time elapsed between onset of the infection and detection of the nodule typically at least 6 months. The parasite is constrained inside an inflammatory nodule, generally located in subcutaneous tissue or rarely in other tissues or organs, where it can survive for several months or even years.14 Although most of the cases are
asymptomatic, some may have pruritus, edema, arthritis, and subcutaneous swellings.15 Eosinophilia also has been described. This case was associated with moderate pain and hyperemia, leading to antibiotic therapy before surgical removal. Diagnosis generally depends on histologic examination. The clinician is most unlikely to suspect the parasitic nature of the nodule before biopsy, apart from situations where the parasite becomes visible, as when located under the conjunctiva. It is not uncommon for the filaria to die inside the inflammatory nodule. Subsequent invasion of inflammatory cells destroys parasite morphologic characteristics. Sometimes the entire body of the nematode may disappear, leaving in its place an empty circular imprint.14 In such cases, the definitive diagnosis becomes difficult to establish. Although serology and skin testing have not proven particularly helpful in confirmation of dirofilariasis because of inadequacies in test specificity and sensitivity, use of polymerase chain reaction technology has been suggested.16 Transmission of infection from the human host does not occur because these worms rarely grow to be sexually mature, and in no case, has microfilariemia been
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Latifogˇ lu et al 219
Fig 2. A, Histopathologic examination of lesion showed long nematode within lesion (hematoxylen eosin stain; magnification, ⫻100). B, Closer view of transverse section of nematode (hematoxylen eosin stain; magnification, ⫻400).
observed in human infections with these parasites.15,17 Microfilaremia has been reported in prednisolonetreated macaques.18-20 Excisional biopsy is both diagnostic and therapeutic.21 Symptoms quickly resolve after the removal of the worm. Because only a single worm is present in most cases, there is no need for further treatment.22 This pattern was confirmed in our case, as removal of the nodule led to symptom resolution and cure. REFERENCES 1. McLean JD, Beaver PC, Michalek H. Subcutaneous dirofilariasis in Okinawa, Japan. Am J Trop Med Hyg 1979;28:45. 2. Arvanitis PG, Vakalis NC, Damanakis AG, Theodossiadis GP. Ophthalmic dirofilariasis. Am J Ophthalmol 1997;123:689-91. 3. Harrus S, Harmelin A, Rodrig S, Favia G. Dirofilaria repens infection in a dog in Israel. Am J Trop Med Hyg 1999;61:639-41.
4. Jariya P, Sucharit S. Dirofilaria repens from the eyelid of a woman in Thailand. Am J Trop Med Hyg 1983;32:1456-7. 5. Logar J, Novsak S, Rakovec S, Stanisa O. Subcutaneous infection caused by Dirofilaria repens imported to Slovenia. J Infect 2001;42:72-4. 6. Kucukaydin M, Sahin I. The third case of dirofilariasis conjunctivae in Turkey. Mikrobiyol Bull 1986;20:25-8. 7. Cancrini G, Allende E, Favia G, Burnay F, Anton F, Simon F. Canine dirofilariasis in two cities of southeastern Spain. Vet Parasitol 2000;92:81-6. 8. Collins BM, Jones AC, Jimenez F. Dirofilaria tenuis infection of the oral mucosa and cheek. J Oral Maxillofac Surg 1993;51: 1037-40. 9. van den Ende J, Kumar V, Van Gompel A, van den Ende E, Puttemans A, Geerts M, et al. Subcutaneous dirofilariasis caused by Dirofilaria (nochitella) repens in a Belgian patient. Int J Dermatol 1995;34:274-7. 10. Herzberg AJ, Boyd PR, Gutierrez Y. Subcutaneous dirofilariasis in Collier County, Florida, USA. Am J Surg Pathol 1995;19: 934-9.
220 Latifogˇ lu et al
11. Stayerman C, Szvalb S, Sazbon A. Dirofilaria repens presenting as a subcutaneous nodule in the penis. BJU Int 1999;84:746-7. 12. Bradham RR, Locklair PR, Grimball A. Bilateral pulmonary nodules caused by Dirofilaria immitis. Ann Thorac Surg 1990; 50:312-3. 13. Eberhard ML, Daly JJ, Weinstein S, Farris HE. Dirofilaria immitis from the eye of a dog in Arkansas. J Parasitol 1977;63:978. 14. Pampiglione S, Rivasi F, Canestri-Trotti D. Pittfalls and difficulties in histological diagnosis of human dirofilariasis due to Dirofilaria (Nochitella) repens. Diagn Microbiol Infect Dis 1999; 34:57-64. 15. Fuentes I, Cascales A, Ros JM, Sansano C, Gonzalos-Arribas JL, Alvar J. Human subcutaneous dirofilariasis caused by Dirofilaria repens in Ibiza, Spain. Am J Trop Med Hyg 1994;51:401-4. 16. Favia G. Molecular diagnosis of Dirofilaria repens is not a dream. Diagn Microbiol Infect Dis 2000;37:81-2. 17. Font RL, Neafile RC, Perry HD. Subcutaneous dirofilariasis of the eyelid and ocular adnexa. Report of Six cases. Arch Ophthalmol 1980;98:1079-82. 18. MacDougall LT, Magoon CC, Fritsche TR. Dirofilaria repens manifesting as a breast nodule. Diagnostic problems and epidemiologic considerations. Am J Clin Pathol 1992;97:625-30.
ORAL SURGERY ORAL MEDICINE ORAL PATHOLOGY August 2002 19. Wong MM. Experimental dirofilariasis in macaques. II. Susceptibility and host responses to Dirofilaria repens of dogs and cats. Am J Trop Med Hyg 1976;25:88-93. 20. Wong MM, Lim KC. Experimental dirofilariasis in macaques III. Susceptibility and host response to Dirofilaria tenuis of racoons. Am J Trop Med Hyg 1976;25:94-8. 21. Hira PR, Madda JP, al-Shamali MA, Eberhard ML. Dirofilariasis in Kuwait: first report of human infection due to Dirofilaria repens in the Arabian Gulf. Am J Trop Med Hyg 1994;51:590-2. 22. Ruiz-Moreno JM, Bornay-Llinares FJ, Proetp Maza G, Medrans M, Simon F, Eberhard ML. Subconjunctival infection with Dirofilaria repens: serological confirmation of cure following surgery. Arch Ophthalmol 1998;116:1370-2. Reprint requests: Reha Yavuzer, MD Baris¸ Sitesi 87. Sokak N0: 24 06530 Mustafa Kemal Mahallesi Ankara, Turkey [email protected]