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Correspondence to: Daryll Baker, Consultant Surgeon, UCL Division of Medicine, Royal Free Campus, University College London, Pond Street, NW32QG London, UK
Infective native extracranial carotid artery aneurysms are rare, and their management is variable due to a lack of evidence assessing outcomes.
Methods
We performed a systematic literature review following PRISMA guidelines to identify all reported cases of infective native extracranial carotid artery aneurysms between January 1970 and March 2021.
Results
This study identified 193 infective native aneurysms of the extracranial carotid artery from 154 sources. Patients were predominantly male (71.4%), and age ranged from 6 months to 89 years old. The most common presenting features were a neck mass and fever, but also included hemorrhage, respiratory distress, and neurological symptoms. Most aneurysms were located in the internal carotid artery (47.4%). Staphylococcus (23.3%) was the most commonly identified causative pathogen, followed by Mycobacterium tuberculosis (20.9%). Most appeared to become infected by direct local spread. Treatment strategies involved open surgical methods in 101 cases and an endovascular approach in 41 cases. In 4 cases, a hybrid method involving concurrent endovascular and open surgical management was undertaken. In 5 cases, there was antibiotic treatment alone. In the open surgery–treated group, the complication rate was 20.8% compared to 13.2% in the endovascular group. Mortality rate was 5.6%.
Conclusions
Our review identified 193 cases of infective native extracranial carotid artery aneurysms. Direct local spread of a staphylococcus infection was the commonest cause. Endovascular management was associated with fewer early complications than open surgical management.
Introduction
Aneurysms of the extracranial carotid artery are uncommon, constituting less than 1% of all peripheral artery aneurysms.
These aneurysms can result from previous surgery or trauma, as well as infection. This review focuses on infective native (previously termed mycotic) extracranial carotid artery aneurysms caused by direct local invasion of an adjacent abscess through the vascular wall, or by hematogenous spread. Quick recognition and correct urgent treatment of infective native carotid artery aneurysms is important as mortality is at least 20%.
This study analyses presenting features reported, management strategies implemented, and their outcomes, with a view to gain insight into this rare pathology and its management.
Methods
A systematic review of the literature following PRISMA guidelines was undertaken (Fig. 1). MEDLINE and EMBASE databases were searched by 2 authors for all reported cases of extracranial carotid artery aneurysms between January 1970 and March 2021. The following search terms were used and combined with AND/OR search operators: “infect∗,” “abscess,” “mycotic,” “carotid,” “aneurysm,” “pseudoaneurysm”. “Aneurysm, infected” and “carotid artery diseases” subject headings were used. Titles and abstracts were screened before full-text papers were reviewed. Exclusion criteria included intracranial, post-traumatic, noninfective native and iatrogenic aneurysms (after carotid endarterectomy, neck surgery or other interventions such as a central line), and cancer or radiotherapy of the head and neck. Case reports, case series, and retrospective analyses were all included with duplicate cases removed. Conference abstracts or non-English language abstracts were included if they gave sufficient detail to ensure they fit the inclusion criteria. Reference lists of key papers were searched, and Web of Science was used to citation check these papers.
Fig. 1Flow chart for this systematic review, created according to Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.
For each case, country, gender, age, presentation, location and size of aneurysm, aetiology, management, outcome, and length of follow-up were recorded. Data were analysed where available and the number of cases included for each section of analysis is provided with the relevant figure.
Results
Database searching produced 647 papers, reduced to 554 after duplicates were removed. One hundred and fifty-four papers were included in the qualitative analysis: 126 full-text papers and 28 abstracts.
Mycotic extracranial internal carotid artery aneurysms: case report and review. 23rd National Congress of the Italian Society of Young Surgeon (SPIGC).
Extracranial internal carotid artery Salmonella infective native aneurysm complicated by occlusion of the internal carotid artery: depiction by color Doppler sonography CT and USA.
Ligation of the common carotid artery for the management of a infective native pseudoaneurysm of an extracranial internal carotid artery. A case report and review of the literature.
Thrombin injection failure with subsequent successful stent-graft placement for the treatment of an extracranial internal carotid pseudoaneurysm in a 5-year-old child.
Internal carotid artery pseudoaneurysm and ischemic stroke secondary to retropharyngeal and parapharyngeal abscess: a case report and review of the literature.
Giant pseudoaneurysm of the internal carotid artery causing upper airway obstruction in a 10-month-old infant treated by endovascular occlusion and surgical drainage.
Lemierre's syndrome associated infective native aneurysm of the external carotid artery with primary internal carotid artery occlusion in a previously healthy 18-year-old female.
Of the 133 cases that reported the patients’ gender, 95 (71%) of extracranial infective native carotid artery aneurysms occurred in males. The age of patients ranged from 6 months to 89 years and had a bimodal distribution with peaks in childhood and after 50 years old (Fig. 3).
Fig. 3Age distribution of patients with infective native aneurysms of the extracranial carotid artery (N = 136). Three children of unknown age were included as 15. For each age group, the upper-bound is included and the lower is not.
Presenting features were given in 131 cases, and are outlined in Table I, with the most common being a neck mass. Bleeding was a presenting feature in 23 patients (17.6%) which was from the mouth and/or nose in 18 patients; from the ear in 3; and from a neck mass in 2.
Table IPresenting features of infective native aneurysms of the extracranial carotid artery (N = 131)
Feature
Number
Percentage (%)
Neck mass/swelling
122
93%
Fever
76
58%
Dysphagia
27
21%
Hemorrhage
23
18%
Respiratory distress
16
12%
Ischemic stroke
13
10%
Dyspnea
10
8%
Headache
10
8%
Hemorrhagic shock
6
5%
The total number of presenting features is not equal to the number of patients used in the analysis because multiple features occurred in individual patients. Hemorrhage includes nasopharyngeal bleeding, oral bleeding and bleeding from the neck mass.
Thirteen patients (10%) presented with features of an ischemic stroke. These were anterior (carotid) circulation strokes, with features including partial or full hemiparesis and altered speech. Where mentioned, this was felt to be due to occlusion of the carotid artery or to septic emboli.
Before intervention, 43 patients presented with peripheral neurological deficits (Table II). A hoarse voice was a feature present in 23 patients and believed to be due to a vagus nerve palsy.
Table IIPreprocedural extra cranial nerve deficits associated with infective native aneurysms of the extracranial carotid artery (N = 124)
Neurological deficit
Number
Percentage (%)
Hoarseness
23
18.5
Horner's syndrome
19
15.3
Other cranial nerve deficits
8
6.5
Speech changes
3
2.4
Total
43
34.7
Percentages are of 124, the number of cases where the presence or absence of a preprocedural neurological deficit was described.
The location of the infective native extracranial carotid artery aneurysm was recorded in 133 cases, with the internal carotid artery being the commonest site (63 aneurysms, 47.4%) (Fig. 4).
Fig. 4The location of infective native extracranial carotid artery aneurysms with percentages given to the nearest whole number (N = 133). Two aneurysms involved multiple locations of the carotid artery.
The causative pathogen was reported in 129 cases, detected from a blood culture or culture of aneurysm vessel wall or surrounding tissues (Fig. 5). Occasionally the pathogen was detected by other means, but it was included in this analysis if the authors believed it to be the causative agent. Staphylococcus bacteria was the most frequently identified pathogen, in 30 patients (23.3%), followed by Mycobacterium tuberculosis which was identified in 27 patients (20.9%). Staphylococcus aureus was isolated in 28 of the 30 patients, with 9 of these specified to be methicillin-resistant staphylococcus aureus. Staphylococcus epidermis and a mixed growth of staphylococcus epidermidis and staphylococcus capitis were identified in the other 2 patients. A clear source was suspected in 103 cases. In 74 (76%) cases this was due to direct spread of a local infection. In 50 of these, the direct spread was from pharyngeal or tonsillar abscess or infections; in 15 from cervical adenitis. Six were the result of a dental infection or procedures; 2 cases from otitis media or externa and 1 case from osteomyelitis. Twenty (19.4%) cases where the source was identified were due to a bacteraemia and 9 (8.7%) due to septic emboli from infective endocarditis.
Fig. 5Causative pathogens of infective native aneurysms of the extracranial carotid artery (N = 135). Six aneurysms were polymicrobial and 123 were monomicrobial, therefore 135 pathogens were included in the analysis which is not equal to the number of aneurysms.
The management strategy was described in 152 cases. All received antibiotics. Duration of antibiotic therapy was inconsistent between studies, varying from 10 days to 6 months, with a mean duration of 7.6 weeks (median 6 weeks). Five patients had antibiotic treatment alone and all others underwent invasive intervention as well. Of these, 101 had open surgical procedures and 42 endovascular procedures. Four had hybrid procedures involving concurrent endovascular and surgical techniques. Of the 5 patients treated conservatively, with antibiotic therapy alone and no surgical intervention, 1 patient died 25 days after developing a neck swelling. The authors state a response was seen to antibiotic therapy with CRP falling from 203 to 23 mg/l and the patient died after developing aspiration pneumonia.
For these patients managed conservatively, causative agents were as follows: 2 salmonella, MRSA, E. Coli, unspecified.
We found patient age had a significant impact on selected treatment strategy: the majority of paediatric cases were treated endovascularly (64%) whereas most adults were managed with open surgery (75%). On a similar note, aneurysms affecting the common carotid artery or carotid bifurcation were preferentially treated with open surgery, 79% and 85% respectively, compared to aneurysms affecting the internal or external carotid arteries, where 50% in both groups were managed endovascularly.
Surgical techniques were described in 96 cases (Table III) with surgical resection and graft interposition being the most common. Various conduits were employed. The venous grafts used for interposition included saphenous vein grafts in 33 cases, 1 external jugular vein, 1 axillary vein and in 3 reports the origin of the vein grafts were not specified. Of the synthetic grafts, 2 were Dacron and 5 were polytetrafluoroethylene, 1 of which was soaked in rifampicin prior to insertion. Two of the biological grafts were bovine grafts and 1 was cadaveric. Two of the grafts used were unspecified. In the 8 cases where the patch was used to close the defect, the patch was venous in 5 cases, and autologous pericardium, bovine pericardium, and Gore-Tex in 1 case each.
Table IIISurgical techniques used in open surgical management of infective native aneurysms of the extracranial carotid artery (N = 96)
In the open surgery treatment group, 80 mentioned outcome and 19 of these had complications (23.8%). The complications for the open surgery treatment groups are outlined in Table IV, with graft occlusion or stenosis being the most common. Surgical resection and graft interposition surgery had a high complication rate of 20% with 10 out of 50 cases reporting complications. Complications were reported in 7 of the 29 cases (24.1%) that underwent surgical ligation alone.
Table IVComplications following open surgery treatment of infective native aneurysms of the extracranial carotid artery. Nineteen patients experienced 1 or more complications out of a total of 80 treated with open surgery (23.8%). The total number of complications is not 19 as some patients suffered multiple complications
Of the 42 endovascular procedures that were described (Table V), endovascular coil occlusion was the commonest technique employed. Coil occlusion was used in both the internal carotid artery and external carotid artery. The groups are too small to make judgments about complication rates for different techniques. Stent aneurysm exclusion was used in 13 patients, with 9 using covered stents and 4 using bare stents. In the endovascular treatment group, 38 cases mentioned outcome and of these, 5 had complications (13.2%). The complications following endovascular surgery treatment are outlined in Table VI, with failure being the most common, defined as recurrence of the aneurysm.
Table VEndovascular techniques used to manage infective native aneurysms of the extracranial carotid artery (N = 38)
Table VIComplications of endovascular treatment of infective native aneurysms of the extracranial carotid artery. Five patients had complications out of a total of 38 (13.2%)
Four patients underwent hybrid procedures. In 3 cases, the carotid artery was balloon occluded while the aneurysm was managed with open repair. In 1 case the vessel was stented, and the aneurysm then resected.
Of the 44 cases whose follow-up was at least 6 months, recurrence of aneurysm (1 specifies reinfection; one does not) occurred in 2 cases, 5 weeks and 2 years after initial management. One aneurysm was managed endovascularly and the other was managed surgically.
Overall mortality was 5.6%. Seven out of 126 patients where outcome was clearly stated died before treatment or within 30 days of an intervention. Of these 7 patients, 4 died before surgical management and 3 died after. Causes of death for these patients are outlined in Table VII, with the most common being septic shock due to an unresolved carotid infection and death before treatment with an unspecified cause. Ten deaths occurred more than 30 days after treatment, and only 1 was related to the infective native aneurysm. This patient died on day 81 following surgical management due to progression of their Pythiosis insidiosum infection.
The duration of follow-up was specified in 83 cases and the mean follow-up duration was 10 months.
Table VIICause of death in patients who died before treatment or within 30 days of treatment for an infective native aneurysm of the extracranial carotid artery (N = 7)
This systematic review aimed to identify all cases of extracranial carotid artery infective native aneurysms reported between January 1970 and March 2021. In total, 155 sources were identified which described 193 cases. Most patients presented with a neck mass. Neurological deficits occurred in a third of patients, with hoarseness occurring most commonly in a fifth of patients. Almost half of the extracranial carotid infective native aneurysms occurred in the internal carotid artery.
Almost 3-quarters of extracranial carotid artery aneurysms occurred in males which is similar to other less extensive studies.
Sex differences in abdominal aortic aneurysms have been identified in the literature and it has been suggested that oestrogen may contribute to differences in arterial wall structure compared to males (less collagen and more elastin in females) and play a protective role against growth of aneurysms.
Thus, men may be more susceptible to aneurysm formation generally, including those caused by infection. Another possibility is that increased prevalence of atherosclerosis in men
The bimodal age distribution observed may be due suboptimal immune responses in children and older patients, resulting in more frequent and more aggressive infections that can cause infective native extracranial carotid artery aneurysms. A weaker immune response is present in children due to innate and adaptive immune system immaturity, and present in older patients due to immunosenescence. Cases were reported from 36 different countries worldwide. Generally, many more cases were reported from developed countries. The North America and Europe reported the most cases. South Africa reported several cases of infective native extracranial carotid artery aneurysms caused by tuberculosis. Tuberculosis is equally prevalent in other African countries (world bank data), yet we did not identify any cases of infective native extracranial carotid artery aneurysms reported by any other African country. This is likely to represent under reporting rather than a lack of cases from other African countries.
Infective native aneurysms develop in 4 different ways: bacterial seeding from direct spread of infection from an extravascular source; bacteraemia; septic emboli from infective endocarditis and vascular trauma and inoculation. Where a bacterial source was suspected over 3-quarters were due to direct local spread. Infective native aneurysms caused by vascular injury were excluded from this review.
Twenty-three different causative pathogens were identified, with Staphylococcus spp. accounting for almost a quarter and Mycobacterium tuberculosis a fifth of cases. These pathogens commonly cause infections involving the parapharyngeal space or cervical lymph nodes, allowing for direct spread of infection. This is consistent with aortic infective native aneurysms where Staphylococcus is often a causative pathogen.
All patients undergoing open or endovascular surgical procedures were given antibiotics, usually for prolonged periods. Open surgery was the preferred management strategy for infective native aneurysms of the extracranial carotid artery. Although the most accessible, this may also reflect the period over which cases were reviewed, as early on endovascular approaches would have been in their infancy. In contrast, over half of the paediatric cases were treated endovascularly. The reports on paediatric aneurysm intervention are more recent generally than the bulk of the studies reviewed, and this could reflect a trend towards a preferential endovascular option. Complication rates were higher in the open surgery treated group (23.8%) compared to the endovascularly treated group (13.2%). The most used surgical technique was vessel resection and graft interposition (51%), followed by surgical ligation (30%). Unfortunately, most cases did not specify if these ligations were only performed in patients with occluded internal carotid arteries or completely patent circle of Willis. It should be noted that ligation of an internal carotid artery can have severe consequences.
Endovascular coil occlusion was the commonest endovascular technique; however, the group size was too small to comment on complication rates. Four patients underwent hybrid procedures with endovascular techniques used during open surgery.
This may be related to causative bacteria as Knouse et al. found a high mortality due to Aspergillus infections of the head and neck and our review identified only 1 infective native aneurysm due to Aspergillus infection. It is plausible that mortality due to infective native aneurysms of the extracranial carotid artery is lower now at 5.6% compared to 20% reported 50 years ago due to improved management strategies; however, publication bias is also likely to have contributed as well.
This review has several limitations. Firstly, despite attempting to identify as many relevant papers as possible, some may have been missed since they were primarily case reports, and only 2 databases were searched. Ideally Scopus would have been searched as well. This was mitigated by searching reference lists and citation checking reviews we used. Secondly, due to the rarity of infective native aneurysms of the extracranial carotid artery, the sample size was small. This was particularly true when data were divided by management type, for example the endovascular group contained only 38 patients. Therefore, values may not be representative of true values in a larger sample, and this made it not possible to compare complication rates for different management strategies. As discussed previously, the distribution of cases across the world lacked cases from several countries, particularly less developed countries, suggesting possible underrepresentation of cases from certain countries. Additionally, non-English language countries are likely to be underrepresented. This was attempted to be mitigated by including non-English language articles, but this could only be done where an English, French or Spanish abstract was available. Cases may also be overrepresented in some areas where large review papers have been included. For example, many cases from South Africa came from 2 large review papers.
Follow-up duration was very variable, within a mean of 10 months, therefore it is difficult to understand the long-term implications. Lastly, our final mortality rate was low compared to previous studies. This is likely due to publication bias, suggesting an underrepresentation of cases.
Comparing treatment modalities was challenging due to the rarity of the pathology and the evolution of surgical and endovascular techniques. Our impression is that endovascular techniques are becoming increasingly favoured, however, there is no firm evidence to base this on due to the small sample size. Risk factors for the development of these aneurysms, other than an abscess, were difficult to assess due to varied patient detail provided in case reports. Additionally, since our search started from 1970, it is not possible to comment on the completion of the circle of Willis as angiograms were not available or undertaken for most patients included in this study.
We recommend the continued reporting of infective native aneurysms of the extracranial carotid artery through a world database, with a view to develop our understanding of long-term outcomes as well as of which endovascular or surgical techniques have the best outcomes for patients. Awareness of this rare pathology and its presentation should be promoted due to its high mortality and the benefit of early recognition and intervention. This diagnosis should be considered in any patient presenting with a neck mass, especially since pulsations are not always felt. Endovascular methods have a lower complication rate; therefore, this is recommended as the preferred management strategy if clinically appropriate. Further research is required to assess the efficacy of endovascular techniques in a larger group of patients with infective native aneurysms of the extracranial carotid artery.
Conclusion
Infective native aneurysms of the extracranial carotid artery are rare. This pathology must be considered in any patient presenting with a neck mass, to enable early intervention. Our analysis identified that infective native extracranial carotid artery aneurysms are most commonly caused by Staphylococcus by direct spread of a local infection. Most aneurysms were managed with open surgery. Whilst a lower complication rate was observed in the endovascular group, recommendations cannot be made from this study alone. In all cases appropriate antibiotics are recommended. Continued reporting and analysis of infective native aneurysms of the extracranial carotid artery is recommended to understand whether endovascular coil occlusion or stent insertion has preferable outcomes.
References
Sörelius K.
Wanhainen A.
Furebring M.
et al.
The microbiology of infective native aortic aneurysms in a population-based setting.
Mycotic extracranial internal carotid artery aneurysms: case report and review. 23rd National Congress of the Italian Society of Young Surgeon (SPIGC).
Extracranial internal carotid artery Salmonella infective native aneurysm complicated by occlusion of the internal carotid artery: depiction by color Doppler sonography CT and USA.
Ligation of the common carotid artery for the management of a infective native pseudoaneurysm of an extracranial internal carotid artery. A case report and review of the literature.
Thrombin injection failure with subsequent successful stent-graft placement for the treatment of an extracranial internal carotid pseudoaneurysm in a 5-year-old child.
Internal carotid artery pseudoaneurysm and ischemic stroke secondary to retropharyngeal and parapharyngeal abscess: a case report and review of the literature.
Giant pseudoaneurysm of the internal carotid artery causing upper airway obstruction in a 10-month-old infant treated by endovascular occlusion and surgical drainage.
Lemierre's syndrome associated infective native aneurysm of the external carotid artery with primary internal carotid artery occlusion in a previously healthy 18-year-old female.
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