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Pseudomonas aeruginosa Causing a Right Carotid Artery Mycotic Aneurysm After a Dental Extraction Procedure
Mayo Clin Proc, October 2002, Vol 77
Pseudomonas Carotid Mycotic Aneurysm
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Case Report
Pseudomonas aeruginosa Causing a Right Carotid Artery Mycotic Aneurysm After a Dental Extraction Procedure MARK C. KNOUSE, MD; ROBERT G. MADEIRA, MD; AND VICTOR J. CELANI, MD confirming the suspicion of any aneurysm, but angiography is the gold standard. Primary resection of the aneurysm with native vein interposition, in conjunction with prolonged antibiotic therapy, is the preferred strategy. A total of 6 cases thus far, including ours, have been clearly associated with dental surgical procedures. These cases are characterized by rapidly enlarging neck masses in the presence of fever. Microorganisms, particularly gramnegative rods, in contrast to normal oral flora, eg, streptococci and anaerobes, are often isolated. With prompt diagnosis and treatment, outcome is often satisfactory. Mayo Clin Proc. 2002;77:1125-1130
Mycotic aneurysms of the carotid arteries are rare. We describe a right carotid artery mycotic aneurysm in a 70year-old man. His symptoms began immediately after a complicated molar extraction and persisted until the diagnosis was made and surgical resection and repair were undertaken. Pseudomonas aeruginosa was isolated from multiple blood cultures and excised tissues. We review another 73 cases uncovered by an extensive literature search. Bacteremia, recent surgery, head and neck infections, dental infections, and endocarditis are the most common predisposing conditions. Computed tomography and magnetic resonance imaging are techniques for accurately
M
ycotic aneurysms of the carotid arteries are unusual. The earliest case reports emphasized syphilis, tuberculosis, and untreated endocarditis as the most common causes.1 Since the introduction of antibiotics, mycotic aneurysms are most often caused by hematogenous seeding of abnormal vascular endothelium.2 Other common mechanisms include direct spread of infection from a contiguous focus and trauma. Few mycotic aneurysms have been reported as a complication of dental surgery and infection. A review by Jebara et al3 in 1991 of 27 cases of carotid mycotic aneurysms showed that fully 44% were secondary to Staphylococcus aureus, 30% were caused by enteric gram-negative bacteria, streptococci were noted in 15%, and Salmonella species were seen in 11%. These percentages mirror those described for mycotic aneurysms of the abdominal aorta: 40% to 60% are caused by gram-positive bacteria, particularly staphylococci and streptococci, and 30% to 44% are caused by gram-negative bacteria including Salmonella.4 We describe a right carotid mycotic aneurysm caused by Pseudomonas aeruginosa. In addition, we review another 73 cases uncovered by an extensive review of the literature. Particular attention was paid to those cases associated with dental infection and dental surgery.
Four different literature searches were done in the MEDLINE database covering journal articles published from 1966 through June 2001. The searches included (1) “aneurysm,” “infected,” (2) “mycotic aneurysm” with “Pseudomonas” as a text word, (3) “mycotic aneurysm” with “carotid” as a text word, and (4) “tooth extraction”/ “adverse events” with “infection” as a text word. The review by Jebara et al3 was used extensively as a primary source for cases reported between 1966 and 1987. All citations were carefully cross-referenced for other reported cases. Cases were included for review if the reference provided proof of infection by either a positive Gram stain or culture for microorganisms from the aneurysm itself or from the inflammatory mass immediately surrounding the aneurysm. Cases were also included if the patient had positive blood cultures in conjunction with a clinical presentation indicative of a new carotid mycotic aneurysm. We excluded cases of carotid artery infection without aneurysm formation, cases with multiple arterial aneurysms, and foreign language references that were not translated into English. Radiographic criteria were not used to exclude any cases. Table 1 is the compilation of all accepted cases. 2,3,5-69 REPORT OF A CASE A 70-year-old man presented with severe mandibular pain approximately 2 months after a difficult dental procedure in which the right second molar had been sectioned and extracted in a sequential manner. Several hours after the procedure he began to have pain and increasing swelling in the right side of his neck. The pain and swelling increased
From the Division of Infectious Diseases (M.C.K.), Department of Internal Medicine (R.G.M.), and Division of Vascular Surgery (V.J.C.), Lehigh Valley Hospital, Allentown, Pa. Individual reprints of this article are not available. Address correspondence to Mark C. Knouse, MD, 1210 S Cedar Crest Blvd, Suite 2700, Allentown, PA 18103 (e-mail: [email protected]). Mayo Clin Proc. 2002;77:1125-1130
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© 2002 Mayo Foundation for Medical Education and Research
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1126 Pseudomonas Carotid Mycotic Aneurysm
Mayo Clin Proc, October 2002, Vol 77
Table 1. Etiology, Pathogens, and Outcomes of Carotid Mycotic Aneurysms* Etiology and pathogen
No. of cases (% of total)
Bacteremia Staphylococcus aureus Other staphylococci Salmonella Escherichia coli Streptococcus pneumoniae Klebsiella Yersinia Surgery S aureus Other staphylococci Beta streptococci Enterobacter species Proteus vulgaris Head/neck infections S aureus Streptococcus pyogenes Klebsiella/E coli Salmonella Endocarditis S aureus Other staphylococci Streptococcus viridans Other streptococci Dental surgery S aureus Enterococcus Salmonella Klebsiella/Bacteroides Pseudomonas
15 (20)
Penicillium Drug abuse S aureus Pseudomonas species Sinusitis Phycomycetes Aspergillus Mixed bacterial Meningitis Staphylococcus Aspergillus Trauma S aureus S pyogenes Leukemia Aspergillus Miscellaneous S aureus Salmonella group D Candida albicans Not stated Klebsiella species E coli/Proteus mirabilis S aureus Salmonella enteritidis Aspergillus
Outcomes (total/ survived)
Reference
4/3 1/1 4/4 3/2 1/1 1/1 1/1
2, 5-7 8 9-12 13-15 16 17 18
7/4 4/3 1/0 2/2 1/1
19-24 25-28 5 24, 29 30
4/3 1/1 1/1 1/1
31-34 35 36 37
2/2 1/NS 2/2 1/1
38, 39 40 41,42 3
1/1 1/1 1/1 1/1 1/1
43 44 45 46 Current case 47
15 (20)
7 (9)
6 (8)
6 (8)
1/0 4 (5) 3/1, NS 1/1
48-50 49
2/0 1/0 1/1
51, 52 53 54
2/2 1/0
36, 55 56
2/1 1/1
57, 58 59
3/2, NS
60-62
4 (5)
3 (4) 3 (4) 3 (4) 3 (4) 1/1 1/1 1/1
57 63 64
1/1 1/1 1/NS 1/1 1/0
65 66 67 68 69
5 (7)
*NS = not stated.
in intensity over the next several weeks. During this time he was treated with several oral antibiotics, most often entailing intermittent courses of amoxicillin.
The patient’s medical history was remarkable only for mild hypertension and a period of atrial fibrillation for which he had undergone cardioversion. He had no history of diabetes, transient ischemic attacks, strokes, known carotid disease, congestive heart failure, angina, or myocardial infarction. His medications at presentation were diltiazem and 1 aspirin daily. He had quit smoking 23 years previously and had no history of illicit drug use. His family history was notable for multiple cancers and heart disease. At admission, his vital signs were a temperature of 38.4°C, blood pressure of 172/98 mm Hg, heart rate of 105 beats/min, and unlabored respiratory rate of 16/min. The physical examination was remarkable only for an 8-cm pulsatile mass without overlying erythema or edema in the right neck. No masses were evident within the oropharynx. The heartbeat was regular with no murmurs noted. Findings on the rest of the examination were unremarkable. Laboratory data showed leukocytosis (leukocyte count, 12.0 × 109/L) with 83% neutrophils, 8% lymphocytes, and 9% monocytes by automated differential. Electrolyte levels and liver function test results were within normal limits. Computed tomography suggested an aneurysm or pseudoaneurysm at the right carotid bifurcation. An arteriogram revealed mild to moderate atherosclerotic disease of the aortic arch and carotid arteries. The view shown in Figure 1 confirmed the presence and filling of the aneurysm, which appeared to protrude from either the right carotid bifurcation or the origin of the right external carotid artery and was compressing the right internal jugular venous return. Multiple blood cultures were positive for P aeruginosa. The patient underwent an extensive surgical procedure that revealed a large posterior pseudoaneurysm, 4.5 × 5.0 cm, at the level of the carotid bifurcation, with a 2.5-cm hole in the posterior wall of the carotid bulb. With use of a small shunt to maintain intraoperative blood flow, a saphenous vein graft was anastomosed between the common carotid and the internal carotid arteries. Cultures of all excised tissue, including the pseudoaneurysm and adjacent lymph nodes, grew moderate amounts of P aeruginosa. Levofloxacin, gentamicin, and clindamycin were instituted empirically. The therapeutic regimen was changed to ceftazidime, tobramycin, and clindamycin once the culture results were known. The patient recovered quickly postoperatively, with rapid resolution of fever and excellent wound healing. No subsequent blood cultures were positive. He was discharged on the third postoperative day and received a 6-week course of home antibiotics consisting of intravenous cefepime and 2 weeks of concomitant tobramycin. During an 18-month follow-up, the patient has had no fevers, chills, pain, or soft tissue swelling. The surgical site remains well healed with only mild residual
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Mayo Clin Proc, October 2002, Vol 77
Figure 1. Carotid arteriogram showing large pseudoaneurysm (PA) at the right carotid artery bifurcation. CC = common carotid; IC = internal carotid.
numbness. Several negative blood cultures have been documented after antibiotic therapy was discontinued. DISCUSSION AND LITERATURE REVIEW Our MEDLINE searches with cross-referencing yielded 73 case reports of carotid mycotic aneurysms that met our criteria for inclusion (Table 1).2,3,5-69 By decade, there were 5 reports from 1966 through 1969, 20 reports in the 1970s, 24 reports in the 1980s, 22 reports in the 1990s, and 2 reports from 2000 through June 2001. Bacteremia with hematogenous seeding, postoperative infections, endocarditis, and cervical adenopathy or neck abscess were the most common causes. Staphylococcus aureus was the most common organism, being isolated in 25 of the 73 reports. Enterobacteriaceae were the next most common, with 8 reports associated with Salmonella species, 5 cases of Escherichia coli, and 4 of Klebsiella. Streptococci were reported in 9 cases. Aspergillus, phycomycetes, Penicillium, and other fungi were reported in 10 cases. Table 2 describes, by organism, the causes of carotid mycotic aneurysms from our review and contrasts the results with 2 other previously published
Pseudomonas Carotid Mycotic Aneurysm
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series.2,3 The series by Brown et al2 reviewed 194 mycotic aneurysms from all anatomical sites. Other than our case, 5 case reports of carotid mycotic aneurysm as a complication of underlying dental infection or extractions were found.43-47 The mortality rate was 17% for these cases with a mean follow-up of 51/2 months. The first report was that of an 11-year-old boy with an extensive Penicillium infection and associated rupture of his aneurysm, which developed after a maxillary tooth extraction.47 This patient died. The second case was that of a 68-year-old man with a mycotic aneurysm after tooth extraction for a dental abscess caused by Klebsiella and Bacteroides species.46 He was treated successfully with resection and vein reconstruction. The third case was that of an internal carotid mycotic aneurysm developing in a 17-year-old boy after a wisdom tooth extraction.44 “Enterococci” were isolated at surgery. This patient was treated with balloon thrombosis and aneurysm clipping. Both the second and third patients did well during follow-up of at least 6 months, without further sequelae. The fourth case was that of a 78-year-old woman with a chronic molar abscess.45 Salmonella typhi was isolated from surgical specimens, but her clinical course was not described. The fifth case, probably caused by S aureus, was that of a 10-year-boy who developed staphylococcal bacteremia several days after drainage of a tooth abscess.43 The authors reported a mycotic aneurysm of the intracavernous portion of the internal carotid artery, although the aneurysm was never excised or sampled for culture. He was the only patient described who was treated nonoperatively. He survived over a 3-month follow-up period. Our case has several unique clinical characteristics. The first is that the patient’s presentation was benign, considering his persistent Pseudomonas bacteremia. Although serious postdental extraction infections are common, they typically are limited to soft tissues of the neck, occasionally with tissue plane extension into the more dangerous neck spaces. Mycotic aneurysms are a rarely described complication. Finally, such infections usually involve oral flora including streptococci or anaerobes and occasionally S aureus or gram-negative bacilli. Pseudomonas aeruginosa generally accounts for only 3% of mycotic aneurysms, and those are usually associated with intravenous drug abuse.3 To our knowledge, this is the sixth reported case of a carotid mycotic aneurysm complicating a dental infection and the first such case reported with P aeruginosa as the causative organism. At the time of our patient’s molar extraction, infection of the root was evident. His pseudoaneurysm likely originated by direct extension from the adjacent infected focus, although we could not exclude hematogenous seeding of a preexisting atherosclerotic plaque. One theory is that the
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1128 Pseudomonas Carotid Mycotic Aneurysm
Mayo Clin Proc, October 2002, Vol 77
Table 2. Microbiology of Mycotic Aneurysms* 3
Organism Gram-positive Staphylococcus aureus Coagulase-negative staphylococci Staphylococcus species Streptococci Enterococci Gram-negative Klebsiella Escherichia coli Salmonella species Pseudomonas species Other gram-negative bacteria Anaerobic bacteria Fungi Aspergillus Phycomycetes Penicillium/Candida Unknown
Brown2 (all sites), %
Jebara (carotid arteries), %
Knouse (carotid arteries), % (No.)
42 28
60 44
62 (46) 34 (25)
10 1 30 1 2 15 4
12 4 44 11 11 11 4
8 (6) 7 (5) 12 (9) 1 (1) 31 (23) 5 (4) 7 (5) 11 (8) 3 (2)
8 3 1
7 NS NS
24
0
3
5 (4) 4 (3) 14 (10) 8 (6) 3 (2) 3 (2) 0
*Percentages do not total 100% because of rounding and cultures with multiple organisms. NS = not stated.
Pseudomonas infection was introduced at the time of surgery by contaminated irrigation water. A review of the oral surgeon’s practices revealed no changes in his surgical technique, and no complications such as excessive bleeding, nerve injury, or soft tissue emphysema were reported during or after the extraction. No new equipment or topical disinfectants had been used during the procedure. Follow-up discussions with the oral surgeon 1 year later revealed no new cases of Pseudomonas infections. Of the 5 previous reports describing carotid mycotic aneurysms associated with dental infections, only 4 provided sufficient detail to allow comparison to our case. The clinical syndrome seems fairly uniform: a rapidly enlarging neck mass beginning shortly after a dental procedure, usually a tooth extraction. In the 4 cases reviewed it appears that each mycotic aneurysm arose from direct extension from an infected focus. The mass was pulsatile in only 1 case. Of the 6 cases, 1 responded to antibiotic therapy alone.43 Carotid arteriograms were used in all cases to confirm the diagnosis and allow for surgical planning. Including our case, 2 of the 6 aneurysms involved the carotid bifurcation. All the surgically treated cases revealed an apparent dense inflammatory mass that required tedious dissections to free the aneurysm for resection. Of those cases with sufficient detail, 3 of 4 surgically treated patients did well postoperatively with follow-up times averaging 6 months. In 1 case treated nonoperatively, the patient survived but
experienced an early parietal lobe infarction with residual left hemiparesis.43 His mycotic aneurysm involved the intracavernous portion of the internal carotid artery. The term mycotic aneurysm, first used by Sir William Osler,70 today refers to any aneurysm caused by infection. Mycotic aneurysms in general remain a relatively uncommon clinical occurrence. Prior series have shown that mycotic aneurysms account for only 3% to 4% of all aneurysms inspected closely.71,72 Mycotic aneurysms of the carotid arteries are even rarer. The earliest case series emphasized the importance of tuberculosis and syphilis as underlying causes.1 Earlier reviews reported only 27 cases.3 Our search uncovered 73 case reports. Earlier case reports stressed the importance of injection drug use, trauma, and postoperative infections as underlying risk factors for the development of a mycotic aneurysm at this location.5,49 Our review reveals that overall bacteremia (20% of all cases), surgery (20%), soft tissue infections of the head and neck (9%), endocarditis (8%), and dental procedures or infections (8%) are the most common underlying factors, accounting for 49 of 74 cases. However, injection drug use, sinusitis, meningitis, trauma, and lymphoid disorders are also common causes. Dental-associated cases make up 8% of carotid mycotic aneurysms and are an entity worth considering in patients with fever or persistent neck swelling after dental procedures. Nine of the 15 postsurgical reports highlight the importance of carotid endarterectomy as an underlying cause.19,24-30 Graver and Mulcare27 performed a comprehensive review of postendarterectomy pseudoaneurysms, but only 6 of 50 cases involved infection. Dougherty et al28 found that 1% to 3% of endarterectomy grafts were complicated by infection. The remaining cases included a diverse array of underlying diseases and sources of infection (Table 1). Our review highlights the fact that the causative organisms in carotid mycotic aneurysms mirror the spectrum of mycotic aneurysms as a whole (Table 2).4,47,54,59,72 Gram-positive infections are more common than gram-negative rod infections. Aspergillus and other fungi make up a substantial number of cases (14%) and are usually seen in diabetic patients and other immunocompromised hosts. Common complications of aneurysms include rupture, hemorrhage, and thromboembolic complications with neurologic sequelae.73 The definitive treatment of carotid mycotic aneurysms is surgical resection of the aneurysm with reestablishment of arterial flow, if possible. Prolonged intravenous antibiotic therapy with bactericidal activity seems warranted, by analogy to other endovascular infections. The earliest reviews of carotid aneurysms revealed high mortality rates, approaching 70% to 90% with nonoperative treatment.1,48,74 The review of carotid mycotic aneurysms by Jebara et al3 revealed a mortality rate of 19%
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Mayo Clin Proc, October 2002, Vol 77
in 27 cases treated with multiple surgical modalities. The overall mortality in our review was similar at 20% (14 of 70 cases with known outcomes) for the entire series since 1966. However, since 1975 mortality was only 10% with the introduction of vein graft interpositioning, and 3 (60%) of the 5 deaths were due to Aspergillus. Ligation of the involved artery has been performed for about 200 years and was first performed by Sir Astley Cooper in 1805.75,76 Earliest case reports of mycotic carotid aneurysms emphasized this as the standard treatment modality.5,46,49,65 However, this procedure is associated with a high incidence of postoperative stroke, ranging from 50% to 60%,13,65 and also high postoperative mortality rates, ranging from 17% to 40%.3,46,65 The technique of vein graft interposition, in combination with excision of the aneurysm, was reported by Neugebauer and Hoyt77 in 1975 who used a reversed saphenous vein segment for a granulomatous carotid aneurysm. Monson and Alexander46 reintroduced this technique in 1980 as the preferred surgical approach for carotid mycotic aneurysms. The advantages of this procedure include maintenance of carotid artery blood flow, which minimizes the rate of postoperative strokes. Also, persistent infection can be minimized by avoidance of prosthetic materials.27,28 This technique has been reviewed by others and appears to be the preferred technique, if feasible.3,45 Cryopreserved arterial allografts can be used in situations in which suitable vein segments cannot be harvested.78 We thank Marcelo Gareca, MD, for his thoughtful review of the submitted manuscript.
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Suwanwela C, Suwanwela N, Charuchinda S, Hongsaprabhas C. Intracranial mycotic aneurysm of extravascular origin. J Neurosurg. 1972;36:552-559. Constantinides H, Passant C, Waddell AN. Mycotic pseudoaneurysm of common carotid artery mimicking parapharyngeal abscess. J Laryngol Otol. 2000;114:796-797. Ameli FM, Provan JL, Keuchler PM. Unusual aneurysms of the extracranial carotid artery. J Cardiovasc Surg (Torino). 1983;24: 69-73. Mahaley MS Jr, Spock A. An unusual case of intracranial aneurysm. In: Smith JL, ed. Neuro-ophthalmology. Vol 4. St Louis, Mo: CV Mosby Co; 1968:158-166. Desimplelaere J, Seynaeve P, Kockx M, Appel B, Gyselinck J, Mortelmans L. Mycotic pseudo-aneurysm of the extracranial carotid artery. J Belge Radiol. 1997;80:170-171. Willemsen P, De Roover D, Kockx M, Gerard Y. Mycotic common carotid artery aneurysm in an immunosuppressed pediatric patient: case report. J Vasc Surg. 1997;25:784-785. Rice HE, Arbabi S, Kremer R, Needle D, Johansen K. Ruptured Salmonella mycotic aneurysm of the extracranial carotid artery. Ann Vasc Surg. 1997;11:416-419. Loeys BL, Van Coster RN, Defreyne LR, Leroy JG. Fungal intracranial aneurysm in a child with familial chronic mucocutaneous candidiasis. Eur J Pediatr. 1999;158:650-652. Howell HS, Baburao T, Graziano J. Mycotic cervical carotid aneurysm. Surgery. 1977;81:357-359. Lambert MJ III, Johns ME, Mentzer R, Fitz-Hugh GS. Mycotic carotid artery aneurysm. Otolaryngol Head Neck Surg. 1979;87: 624-627. Welling RE, Taha A, Goel T, et al. Extracranial carotid artery aneurysms. Surgery. 1983;93:319-323. Grossi RJ, Onofrey D, Tvetenstrand C, Blumenthal J. Mycotic carotid aneurysm. J Vasc Surg. 1987;6:81-83. Iihara K, Makita Y, Nabeshima S, Tei T, Keyaki A. Aspergillosis of the central nervous system causing subarachnoid hemorrhage from mycotic aneurysm of the basilar artery—case report. Neurol Med Chir (Tokyo). 1990;30:618-623. Osler W. The Gulstonian lectures, on malignant endocarditis. BMJ. 1885;1:467-470. Parkhurst GF, Decker JP. Bacterial aortitis and mycotic aneurysms of the aorta: a report of 12 cases. Am J Pathol. 1955;31:821-836. Sommerville RL, Allen EV, Edwards JE. Bland and infected arteriosclerotic abdominal aortic aneurysms: a clinicopathologic study. Medicine (Baltimore). 1959;38:207-221. McCollum CH, Wheeler WG, Noon GP, DeBakey ME. Aneurysms of the extracranial carotid artery: twenty-one years’ experience. Am J Surg. 1979;137:196-200. Winslow N. Extracranial aneurysm of the internal carotid artery: history and analysis of the cases registered up to Aug. 1, 1925. Arch Surg. 1926;13:689-729. Webb RC Jr, Barker WF. Aneurysms of the extracranial internal carotid artery. Arch Surg. 1969;99:501-505. Cooper A. Account of the first successful operation performed on the carotid artery for aneurysm in the year of 1808 with postmortem examination in the year 1821. Guys Hosp Rep. 1836;1:53-59. Neugebauer MK, Hoyt TW. Carotid artery aneurysm of granulomatous origin. Am J Surg. 1975;130:362-365. Vogt PR, Brunner-La Rocca HP, Carrel T, et al. Cryopreserved arterial allografts in the treatment of major vascular infection: a comparison with conventional surgical techniques. J Thorac Cardiovasc Surg. 1998;116:965-972.
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Case Report
Pseudomonas aeruginosa Causing a Right Carotid Artery Mycotic Aneurysm After a Dental Extraction Procedure MARK C. KNOUSE, MD; ROBERT G. MADEIRA, MD; AND VICTOR J. CELANI, MD confirming the suspicion of any aneurysm, but angiography is the gold standard. Primary resection of the aneurysm with native vein interposition, in conjunction with prolonged antibiotic therapy, is the preferred strategy. A total of 6 cases thus far, including ours, have been clearly associated with dental surgical procedures. These cases are characterized by rapidly enlarging neck masses in the presence of fever. Microorganisms, particularly gramnegative rods, in contrast to normal oral flora, eg, streptococci and anaerobes, are often isolated. With prompt diagnosis and treatment, outcome is often satisfactory. Mayo Clin Proc. 2002;77:1125-1130
Mycotic aneurysms of the carotid arteries are rare. We describe a right carotid artery mycotic aneurysm in a 70year-old man. His symptoms began immediately after a complicated molar extraction and persisted until the diagnosis was made and surgical resection and repair were undertaken. Pseudomonas aeruginosa was isolated from multiple blood cultures and excised tissues. We review another 73 cases uncovered by an extensive literature search. Bacteremia, recent surgery, head and neck infections, dental infections, and endocarditis are the most common predisposing conditions. Computed tomography and magnetic resonance imaging are techniques for accurately
M
ycotic aneurysms of the carotid arteries are unusual. The earliest case reports emphasized syphilis, tuberculosis, and untreated endocarditis as the most common causes.1 Since the introduction of antibiotics, mycotic aneurysms are most often caused by hematogenous seeding of abnormal vascular endothelium.2 Other common mechanisms include direct spread of infection from a contiguous focus and trauma. Few mycotic aneurysms have been reported as a complication of dental surgery and infection. A review by Jebara et al3 in 1991 of 27 cases of carotid mycotic aneurysms showed that fully 44% were secondary to Staphylococcus aureus, 30% were caused by enteric gram-negative bacteria, streptococci were noted in 15%, and Salmonella species were seen in 11%. These percentages mirror those described for mycotic aneurysms of the abdominal aorta: 40% to 60% are caused by gram-positive bacteria, particularly staphylococci and streptococci, and 30% to 44% are caused by gram-negative bacteria including Salmonella.4 We describe a right carotid mycotic aneurysm caused by Pseudomonas aeruginosa. In addition, we review another 73 cases uncovered by an extensive review of the literature. Particular attention was paid to those cases associated with dental infection and dental surgery.
Four different literature searches were done in the MEDLINE database covering journal articles published from 1966 through June 2001. The searches included (1) “aneurysm,” “infected,” (2) “mycotic aneurysm” with “Pseudomonas” as a text word, (3) “mycotic aneurysm” with “carotid” as a text word, and (4) “tooth extraction”/ “adverse events” with “infection” as a text word. The review by Jebara et al3 was used extensively as a primary source for cases reported between 1966 and 1987. All citations were carefully cross-referenced for other reported cases. Cases were included for review if the reference provided proof of infection by either a positive Gram stain or culture for microorganisms from the aneurysm itself or from the inflammatory mass immediately surrounding the aneurysm. Cases were also included if the patient had positive blood cultures in conjunction with a clinical presentation indicative of a new carotid mycotic aneurysm. We excluded cases of carotid artery infection without aneurysm formation, cases with multiple arterial aneurysms, and foreign language references that were not translated into English. Radiographic criteria were not used to exclude any cases. Table 1 is the compilation of all accepted cases. 2,3,5-69 REPORT OF A CASE A 70-year-old man presented with severe mandibular pain approximately 2 months after a difficult dental procedure in which the right second molar had been sectioned and extracted in a sequential manner. Several hours after the procedure he began to have pain and increasing swelling in the right side of his neck. The pain and swelling increased
From the Division of Infectious Diseases (M.C.K.), Department of Internal Medicine (R.G.M.), and Division of Vascular Surgery (V.J.C.), Lehigh Valley Hospital, Allentown, Pa. Individual reprints of this article are not available. Address correspondence to Mark C. Knouse, MD, 1210 S Cedar Crest Blvd, Suite 2700, Allentown, PA 18103 (e-mail: [email protected]). Mayo Clin Proc. 2002;77:1125-1130
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© 2002 Mayo Foundation for Medical Education and Research
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Table 1. Etiology, Pathogens, and Outcomes of Carotid Mycotic Aneurysms* Etiology and pathogen
No. of cases (% of total)
Bacteremia Staphylococcus aureus Other staphylococci Salmonella Escherichia coli Streptococcus pneumoniae Klebsiella Yersinia Surgery S aureus Other staphylococci Beta streptococci Enterobacter species Proteus vulgaris Head/neck infections S aureus Streptococcus pyogenes Klebsiella/E coli Salmonella Endocarditis S aureus Other staphylococci Streptococcus viridans Other streptococci Dental surgery S aureus Enterococcus Salmonella Klebsiella/Bacteroides Pseudomonas
15 (20)
Penicillium Drug abuse S aureus Pseudomonas species Sinusitis Phycomycetes Aspergillus Mixed bacterial Meningitis Staphylococcus Aspergillus Trauma S aureus S pyogenes Leukemia Aspergillus Miscellaneous S aureus Salmonella group D Candida albicans Not stated Klebsiella species E coli/Proteus mirabilis S aureus Salmonella enteritidis Aspergillus
Outcomes (total/ survived)
Reference
4/3 1/1 4/4 3/2 1/1 1/1 1/1
2, 5-7 8 9-12 13-15 16 17 18
7/4 4/3 1/0 2/2 1/1
19-24 25-28 5 24, 29 30
4/3 1/1 1/1 1/1
31-34 35 36 37
2/2 1/NS 2/2 1/1
38, 39 40 41,42 3
1/1 1/1 1/1 1/1 1/1
43 44 45 46 Current case 47
15 (20)
7 (9)
6 (8)
6 (8)
1/0 4 (5) 3/1, NS 1/1
48-50 49
2/0 1/0 1/1
51, 52 53 54
2/2 1/0
36, 55 56
2/1 1/1
57, 58 59
3/2, NS
60-62
4 (5)
3 (4) 3 (4) 3 (4) 3 (4) 1/1 1/1 1/1
57 63 64
1/1 1/1 1/NS 1/1 1/0
65 66 67 68 69
5 (7)
*NS = not stated.
in intensity over the next several weeks. During this time he was treated with several oral antibiotics, most often entailing intermittent courses of amoxicillin.
The patient’s medical history was remarkable only for mild hypertension and a period of atrial fibrillation for which he had undergone cardioversion. He had no history of diabetes, transient ischemic attacks, strokes, known carotid disease, congestive heart failure, angina, or myocardial infarction. His medications at presentation were diltiazem and 1 aspirin daily. He had quit smoking 23 years previously and had no history of illicit drug use. His family history was notable for multiple cancers and heart disease. At admission, his vital signs were a temperature of 38.4°C, blood pressure of 172/98 mm Hg, heart rate of 105 beats/min, and unlabored respiratory rate of 16/min. The physical examination was remarkable only for an 8-cm pulsatile mass without overlying erythema or edema in the right neck. No masses were evident within the oropharynx. The heartbeat was regular with no murmurs noted. Findings on the rest of the examination were unremarkable. Laboratory data showed leukocytosis (leukocyte count, 12.0 × 109/L) with 83% neutrophils, 8% lymphocytes, and 9% monocytes by automated differential. Electrolyte levels and liver function test results were within normal limits. Computed tomography suggested an aneurysm or pseudoaneurysm at the right carotid bifurcation. An arteriogram revealed mild to moderate atherosclerotic disease of the aortic arch and carotid arteries. The view shown in Figure 1 confirmed the presence and filling of the aneurysm, which appeared to protrude from either the right carotid bifurcation or the origin of the right external carotid artery and was compressing the right internal jugular venous return. Multiple blood cultures were positive for P aeruginosa. The patient underwent an extensive surgical procedure that revealed a large posterior pseudoaneurysm, 4.5 × 5.0 cm, at the level of the carotid bifurcation, with a 2.5-cm hole in the posterior wall of the carotid bulb. With use of a small shunt to maintain intraoperative blood flow, a saphenous vein graft was anastomosed between the common carotid and the internal carotid arteries. Cultures of all excised tissue, including the pseudoaneurysm and adjacent lymph nodes, grew moderate amounts of P aeruginosa. Levofloxacin, gentamicin, and clindamycin were instituted empirically. The therapeutic regimen was changed to ceftazidime, tobramycin, and clindamycin once the culture results were known. The patient recovered quickly postoperatively, with rapid resolution of fever and excellent wound healing. No subsequent blood cultures were positive. He was discharged on the third postoperative day and received a 6-week course of home antibiotics consisting of intravenous cefepime and 2 weeks of concomitant tobramycin. During an 18-month follow-up, the patient has had no fevers, chills, pain, or soft tissue swelling. The surgical site remains well healed with only mild residual
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Mayo Clin Proc, October 2002, Vol 77
Figure 1. Carotid arteriogram showing large pseudoaneurysm (PA) at the right carotid artery bifurcation. CC = common carotid; IC = internal carotid.
numbness. Several negative blood cultures have been documented after antibiotic therapy was discontinued. DISCUSSION AND LITERATURE REVIEW Our MEDLINE searches with cross-referencing yielded 73 case reports of carotid mycotic aneurysms that met our criteria for inclusion (Table 1).2,3,5-69 By decade, there were 5 reports from 1966 through 1969, 20 reports in the 1970s, 24 reports in the 1980s, 22 reports in the 1990s, and 2 reports from 2000 through June 2001. Bacteremia with hematogenous seeding, postoperative infections, endocarditis, and cervical adenopathy or neck abscess were the most common causes. Staphylococcus aureus was the most common organism, being isolated in 25 of the 73 reports. Enterobacteriaceae were the next most common, with 8 reports associated with Salmonella species, 5 cases of Escherichia coli, and 4 of Klebsiella. Streptococci were reported in 9 cases. Aspergillus, phycomycetes, Penicillium, and other fungi were reported in 10 cases. Table 2 describes, by organism, the causes of carotid mycotic aneurysms from our review and contrasts the results with 2 other previously published
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series.2,3 The series by Brown et al2 reviewed 194 mycotic aneurysms from all anatomical sites. Other than our case, 5 case reports of carotid mycotic aneurysm as a complication of underlying dental infection or extractions were found.43-47 The mortality rate was 17% for these cases with a mean follow-up of 51/2 months. The first report was that of an 11-year-old boy with an extensive Penicillium infection and associated rupture of his aneurysm, which developed after a maxillary tooth extraction.47 This patient died. The second case was that of a 68-year-old man with a mycotic aneurysm after tooth extraction for a dental abscess caused by Klebsiella and Bacteroides species.46 He was treated successfully with resection and vein reconstruction. The third case was that of an internal carotid mycotic aneurysm developing in a 17-year-old boy after a wisdom tooth extraction.44 “Enterococci” were isolated at surgery. This patient was treated with balloon thrombosis and aneurysm clipping. Both the second and third patients did well during follow-up of at least 6 months, without further sequelae. The fourth case was that of a 78-year-old woman with a chronic molar abscess.45 Salmonella typhi was isolated from surgical specimens, but her clinical course was not described. The fifth case, probably caused by S aureus, was that of a 10-year-boy who developed staphylococcal bacteremia several days after drainage of a tooth abscess.43 The authors reported a mycotic aneurysm of the intracavernous portion of the internal carotid artery, although the aneurysm was never excised or sampled for culture. He was the only patient described who was treated nonoperatively. He survived over a 3-month follow-up period. Our case has several unique clinical characteristics. The first is that the patient’s presentation was benign, considering his persistent Pseudomonas bacteremia. Although serious postdental extraction infections are common, they typically are limited to soft tissues of the neck, occasionally with tissue plane extension into the more dangerous neck spaces. Mycotic aneurysms are a rarely described complication. Finally, such infections usually involve oral flora including streptococci or anaerobes and occasionally S aureus or gram-negative bacilli. Pseudomonas aeruginosa generally accounts for only 3% of mycotic aneurysms, and those are usually associated with intravenous drug abuse.3 To our knowledge, this is the sixth reported case of a carotid mycotic aneurysm complicating a dental infection and the first such case reported with P aeruginosa as the causative organism. At the time of our patient’s molar extraction, infection of the root was evident. His pseudoaneurysm likely originated by direct extension from the adjacent infected focus, although we could not exclude hematogenous seeding of a preexisting atherosclerotic plaque. One theory is that the
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Table 2. Microbiology of Mycotic Aneurysms* 3
Organism Gram-positive Staphylococcus aureus Coagulase-negative staphylococci Staphylococcus species Streptococci Enterococci Gram-negative Klebsiella Escherichia coli Salmonella species Pseudomonas species Other gram-negative bacteria Anaerobic bacteria Fungi Aspergillus Phycomycetes Penicillium/Candida Unknown
Brown2 (all sites), %
Jebara (carotid arteries), %
Knouse (carotid arteries), % (No.)
42 28
60 44
62 (46) 34 (25)
10 1 30 1 2 15 4
12 4 44 11 11 11 4
8 (6) 7 (5) 12 (9) 1 (1) 31 (23) 5 (4) 7 (5) 11 (8) 3 (2)
8 3 1
7 NS NS
24
0
3
5 (4) 4 (3) 14 (10) 8 (6) 3 (2) 3 (2) 0
*Percentages do not total 100% because of rounding and cultures with multiple organisms. NS = not stated.
Pseudomonas infection was introduced at the time of surgery by contaminated irrigation water. A review of the oral surgeon’s practices revealed no changes in his surgical technique, and no complications such as excessive bleeding, nerve injury, or soft tissue emphysema were reported during or after the extraction. No new equipment or topical disinfectants had been used during the procedure. Follow-up discussions with the oral surgeon 1 year later revealed no new cases of Pseudomonas infections. Of the 5 previous reports describing carotid mycotic aneurysms associated with dental infections, only 4 provided sufficient detail to allow comparison to our case. The clinical syndrome seems fairly uniform: a rapidly enlarging neck mass beginning shortly after a dental procedure, usually a tooth extraction. In the 4 cases reviewed it appears that each mycotic aneurysm arose from direct extension from an infected focus. The mass was pulsatile in only 1 case. Of the 6 cases, 1 responded to antibiotic therapy alone.43 Carotid arteriograms were used in all cases to confirm the diagnosis and allow for surgical planning. Including our case, 2 of the 6 aneurysms involved the carotid bifurcation. All the surgically treated cases revealed an apparent dense inflammatory mass that required tedious dissections to free the aneurysm for resection. Of those cases with sufficient detail, 3 of 4 surgically treated patients did well postoperatively with follow-up times averaging 6 months. In 1 case treated nonoperatively, the patient survived but
experienced an early parietal lobe infarction with residual left hemiparesis.43 His mycotic aneurysm involved the intracavernous portion of the internal carotid artery. The term mycotic aneurysm, first used by Sir William Osler,70 today refers to any aneurysm caused by infection. Mycotic aneurysms in general remain a relatively uncommon clinical occurrence. Prior series have shown that mycotic aneurysms account for only 3% to 4% of all aneurysms inspected closely.71,72 Mycotic aneurysms of the carotid arteries are even rarer. The earliest case series emphasized the importance of tuberculosis and syphilis as underlying causes.1 Earlier reviews reported only 27 cases.3 Our search uncovered 73 case reports. Earlier case reports stressed the importance of injection drug use, trauma, and postoperative infections as underlying risk factors for the development of a mycotic aneurysm at this location.5,49 Our review reveals that overall bacteremia (20% of all cases), surgery (20%), soft tissue infections of the head and neck (9%), endocarditis (8%), and dental procedures or infections (8%) are the most common underlying factors, accounting for 49 of 74 cases. However, injection drug use, sinusitis, meningitis, trauma, and lymphoid disorders are also common causes. Dental-associated cases make up 8% of carotid mycotic aneurysms and are an entity worth considering in patients with fever or persistent neck swelling after dental procedures. Nine of the 15 postsurgical reports highlight the importance of carotid endarterectomy as an underlying cause.19,24-30 Graver and Mulcare27 performed a comprehensive review of postendarterectomy pseudoaneurysms, but only 6 of 50 cases involved infection. Dougherty et al28 found that 1% to 3% of endarterectomy grafts were complicated by infection. The remaining cases included a diverse array of underlying diseases and sources of infection (Table 1). Our review highlights the fact that the causative organisms in carotid mycotic aneurysms mirror the spectrum of mycotic aneurysms as a whole (Table 2).4,47,54,59,72 Gram-positive infections are more common than gram-negative rod infections. Aspergillus and other fungi make up a substantial number of cases (14%) and are usually seen in diabetic patients and other immunocompromised hosts. Common complications of aneurysms include rupture, hemorrhage, and thromboembolic complications with neurologic sequelae.73 The definitive treatment of carotid mycotic aneurysms is surgical resection of the aneurysm with reestablishment of arterial flow, if possible. Prolonged intravenous antibiotic therapy with bactericidal activity seems warranted, by analogy to other endovascular infections. The earliest reviews of carotid aneurysms revealed high mortality rates, approaching 70% to 90% with nonoperative treatment.1,48,74 The review of carotid mycotic aneurysms by Jebara et al3 revealed a mortality rate of 19%
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Mayo Clin Proc, October 2002, Vol 77
in 27 cases treated with multiple surgical modalities. The overall mortality in our review was similar at 20% (14 of 70 cases with known outcomes) for the entire series since 1966. However, since 1975 mortality was only 10% with the introduction of vein graft interpositioning, and 3 (60%) of the 5 deaths were due to Aspergillus. Ligation of the involved artery has been performed for about 200 years and was first performed by Sir Astley Cooper in 1805.75,76 Earliest case reports of mycotic carotid aneurysms emphasized this as the standard treatment modality.5,46,49,65 However, this procedure is associated with a high incidence of postoperative stroke, ranging from 50% to 60%,13,65 and also high postoperative mortality rates, ranging from 17% to 40%.3,46,65 The technique of vein graft interposition, in combination with excision of the aneurysm, was reported by Neugebauer and Hoyt77 in 1975 who used a reversed saphenous vein segment for a granulomatous carotid aneurysm. Monson and Alexander46 reintroduced this technique in 1980 as the preferred surgical approach for carotid mycotic aneurysms. The advantages of this procedure include maintenance of carotid artery blood flow, which minimizes the rate of postoperative strokes. Also, persistent infection can be minimized by avoidance of prosthetic materials.27,28 This technique has been reviewed by others and appears to be the preferred technique, if feasible.3,45 Cryopreserved arterial allografts can be used in situations in which suitable vein segments cannot be harvested.78 We thank Marcelo Gareca, MD, for his thoughtful review of the submitted manuscript.
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