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(Radiology. 1999;213:369-374.)
© RSNA, 1999

Head and Neck Imaging

Lemierre Syndrome: Forgotten but Not Extinct-Report of Four Cases1

Nicholas J. Screaton, MRCP, FRCR, James G. Ravenel, MD, Paul J. Lehner, MRCP, PhD, E. Robert Heitzman, MD and Christopher D. R. Flower, FRCP, FRCR

1 From the Departments of Radiology (N.J.S., C.D.R.F.) and Clinical Medicine (P.J.L.), Addenbrooke's Hospital, Hills Road, Cambridge, UK CB2 2QQ; and the Department of Radiology, State University of New York, Syracuse (J.G.R., E.R.H.). Received November 24, 1998; revision requested December 22; revision received February 10, 1999; accepted March 26. Address reprint requests to N.J.S. (e-mail: njs28@radiol .cam.ac.uk).


   Abstract
TOP
 Abstract
Introduction
 Case 1
 Discussion
 References
 
Four cases of Lemierre syndrome are reported in which metastatic abscesses resulted from septic thrombosis of the internal jugular vein secondary to bacterial pharyngitis. While chest radiographic findings were nonspecific, results of computed tomography (CT) of the thorax in each case were highly suggestive of septic pulmonary emboli. Internal jugular venous thrombosis was demonstrated at ultrasonography and contrast material-enhanced CT.

Index terms: Lemierre syndrome (new), 60.2163, 60.722, 907.751 • Lung, cavitation, 60.12112, 60.1241, 60.1298, 60.2163, 60.2812, 60.282 • Pharyngitis, 262.12112, 262.1298, 262.20, 262.28 • Veins, jugular, 907.122, 907.1298, 907.751 • Veins, thrombosis, 907.751


   Introduction
TOP
 Abstract
 Introduction
Case 1
 Discussion
 References
 
Lemierre syndrome, also known as postanginal sepsis or necrobacillosis, is an uncommon but potentially life-threatening complication of acute pharyngotonsillitis. Anaerobic oropharyngeal infection may result in septic thrombophlebitis of the ipsilateral internal jugular vein with subsequent septicemia and septic embolization, which cause metastatic abscesses, commonly in the lungs and less commonly in the large joints. In 1936, Lemierre (1) gave a detailed description of the condition reported by Schottmuller in 1918 that came to bear Lemierre's name and indicated that the clinical findings were "so characteristic that mistake is almost impossible."

In the preantibiotic era, Lemierre syndrome was common and often followed a fulminant course, with a mortality rate of 90% (1). In recent years, the widespread use of antibiotics in the management of acute oropharyngeal infection has led to a rapid decline in the prevalence of Lemierre syndrome. Lack of familiarity with this condition, which patients may have when they present to the ear, nose, and throat surgeon, physician, or pediatrician, can lead to serious delay in diagnosis and may explain why it has been referred to as "a forgotten disease" (2).

Over the past 2 decades, occasional case reports and literature reviews pertaining to Lemierre syndrome have been published in the medicine, pediatrics, and otorhinolaryngology literature (2–11), but reports in the radiology literature have been scant (12,13). The purpose of this case report is to heighten radiologists' awareness of this syndrome to expedite diagnosis of a syndrome that often manifests as nonspecific clinical and chest radiographic findings. In the appropriate clinical setting, results of computed tomography (CT) of the chest suggestive of septic emboli or imaging evidence of internal jugular venous thrombosis should lead the radiologist to consider the diagnosis of Lemierre syndrome.

We describe cases in four patients with anaerobic pulmonary sepsis associated with internal jugular venous thrombosis secondary to pharyngotonsillitis; two of these patients presented to each of our institutions within 2 months of the other patient presenting to the same institution. Each had classic clinical presentations and radiologic findings characteristic of Lemierre syndrome. None of the patients had clinical evidence of endocarditis or extrapulmonary septic emboli. The clinical and radiologic findings in each case are summarized in Tables 1 and 2; case 1 is described in detail.


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  		TABLE 1. Clinical Features
 

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  		TABLE 2. Diagnostic Investigations
 

   Case 1
TOP
 Abstract
 Introduction
 Case 1
Discussion
 References
 
A 17-year-old female adolescent presented with a 10-day history of sore throat, fever, and neck pain, which had been treated by her family practitioner with oral administration of erythromycin without response. At admission to the hospital, she was febrile and tachycardic with tender bilateral cervical lymphadenopathy and erythematous, enlarged tonsils. Examination of the chest was performed, but findings were unremarkable. The patient had neutrophilia and elevated levels of inflammatory markers; the radiograph of the chest obtained at admission was unremarkable. Cefotaxime and erythromycin then were intravenously administered.

On postadmission day 2, the patient developed cough, bilateral pleuritic chest pain, and subcostal abdominal pain. A radiograph of the chest (Fig 1a) at this stage revealed airspace disease in the middle and lower zones of the lung. Cultures of blood drawn at admission grew F necrophorum, a provisional clinical diagnosis of Lemierre syndrome was made, and intravenously administered metronidazole was added to her therapy.



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  		Figure 1. Case 1. (a) Anteroposterior radiograph of the chest demonstrates nonspecific bibasal consolidation. (b) Conventional transverse CT scan shows multiple bilateral peripheral pulmonary nodules (arrowheads) and a larger wedge-shaped area of consolidation (arrow) in the lingula. (c) Conventional transverse CT scan demonstrates central cavitation of one of the nodules (arrowhead). (d) Contrast-enhanced transverse CT scan obtained 10 days after c, prior to surgical decortication, shows bilateral pleural collections with pleural enhancement (arrowheads), which is in keeping with empyema.

 


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  		Figure 1. Case 1. (a) Anteroposterior radiograph of the chest demonstrates nonspecific bibasal consolidation. (b) Conventional transverse CT scan shows multiple bilateral peripheral pulmonary nodules (arrowheads) and a larger wedge-shaped area of consolidation (arrow) in the lingula. (c) Conventional transverse CT scan demonstrates central cavitation of one of the nodules (arrowhead). (d) Contrast-enhanced transverse CT scan obtained 10 days after c, prior to surgical decortication, shows bilateral pleural collections with pleural enhancement (arrowheads), which is in keeping with empyema.

 


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  		Figure 1. Case 1. (a) Anteroposterior radiograph of the chest demonstrates nonspecific bibasal consolidation. (b) Conventional transverse CT scan shows multiple bilateral peripheral pulmonary nodules (arrowheads) and a larger wedge-shaped area of consolidation (arrow) in the lingula. (c) Conventional transverse CT scan demonstrates central cavitation of one of the nodules (arrowhead). (d) Contrast-enhanced transverse CT scan obtained 10 days after c, prior to surgical decortication, shows bilateral pleural collections with pleural enhancement (arrowheads), which is in keeping with empyema.

 


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  		Figure 1. Case 1. (a) Anteroposterior radiograph of the chest demonstrates nonspecific bibasal consolidation. (b) Conventional transverse CT scan shows multiple bilateral peripheral pulmonary nodules (arrowheads) and a larger wedge-shaped area of consolidation (arrow) in the lingula. (c) Conventional transverse CT scan demonstrates central cavitation of one of the nodules (arrowhead). (d) Contrast-enhanced transverse CT scan obtained 10 days after c, prior to surgical decortication, shows bilateral pleural collections with pleural enhancement (arrowheads), which is in keeping with empyema.

 
Transverse CT scans of the chest and upper abdomen (Fig 1b, 1c) were obtained 4 days later with a Somatom Plus 4 system (Siemens Medical Systems, Erlangen, Germany) after the intravenous administration of 100 mL of iopamidol 300 (Niopam; Merck, West Point, Pa) (300 mg of iodine per milliliter). This showed numerous pulmonary nodules with varying degrees of cavitation that were situated predominantly in the periphery of the lung. Some nodules showed evidence of feeding vessels. Larger peripheral wedge-shaped areas of consolidation demonstrated peripheral enhancement with central areas of reduced attenuation; their appearances were suggestive of septic infarction. Consolidation at both lung bases and large bilateral pleural effusions were also noted. No evidence of thrombus was seen in the pulmonary arteries at a subsegmental level at CT pulmonary arteriography. In the abdomen, there was no evidence of hepatic or splenic abscess.

Ultrasonography (US) of the neck veins demonstrated compressible internal jugular veins bilaterally, with no filling defect directly evident. However, partial or complete loss of cardiac pulsatility and respiratory phasicity in the right jugular venous system at spectral Doppler US assessment implied proximal obstruction. Anticoagulation was commenced, and an occlusive thrombus was confirmed on postadmission day 10 with results of venography.

Despite appropriate antimicrobial therapy, the patient remained unwell, with persistent fever and breathlessness. The enlarging pleural effusions were drained, but no organisms were cultured. A repeat CT scan (Fig 1d) obtained on postadmission day 16 showed overall improvement but also a persistent large right pleural effusion, with pleural enhancement in keeping with empyema, and multiple peripheral pulmonary cavities. A right-sided surgical decortication was performed on postadmission day 21 for a persistent loculated pleural fluid collection; surgical findings were in keeping with empyema associated with intrapulmonary abscess. The patient made rapid postsurgical improvement and was discharged on day 35.


   Discussion
TOP
 Abstract
 Introduction
 Case 1
 Discussion
References
 
While F necrophorum has remained the most common pathogen in Lemierre syndrome since Lemierre's original series (1) and accounts for 81% of the cases in the recent review by Sinave and colleagues (9), other Fusobacterium species were responsible for infection in 11% of Sinave and colleagues' patients, and other gram-negative organisms were responsible in 8%. F necrophorum forms part of the normal oropharyngeal flora and is peculiar in its ability to invade as a primary pathogen without the presence of serious underlying disease.

Infection of the parapharyngeal space, which may occur secondary to direct spread of oropharyngeal infection or by lymphatic or tonsillar venous dissemination, is central to the development of Lemierre syndrome. Infection at this site may affect not only the carotid sheath and its contents but also cranial nerves IX–XII, with consequent neurologic signs and symptoms. Internal jugular venous thrombosis that results from the adjacent inflammatory process or extension from the tonsillar veins acts as a nidus of infection that may spread hematogenously and result in septicemia and septic embolization, which occur most commonly in the lungs (9). In a recent literature review, 97% of 38 patients had evidence of pleuropulmonary septic emboli, and 15% developed septic arthritis (9). Hepatic and splenic abscesses (8), osteomyelitis (8), meningitis (9), epidural abscess (9), and diffuse encephalopathy are also described in association with this syndrome.

Patients with Lemierre syndrome typically present with acute pharyngitis followed 3–10 days later by the development of a fever (temperature > 38.5°C), rigors, and malaise with the onset of septicemia. Many patients present with an array of nonspecific symptoms and clinical findings. At the time of presentation to hospital, both the signs and symptoms of pharyngitis were prominent in three of our four patients, but in one patient (case 3) there were no pharyngitic features. As Hall (14) so eloquently warned, "Be not deceived by a comparatively innocent-appearing pharynx, as the veins of the pharynx may be carrying the death sentence for your patient." Internal jugular venous thrombosis typically causes pain, tenderness, swelling along the line of the vein, and trismus; involvement of the lower cranial nerves may result in hoarseness and dysphagia. However, these findings may be minor and readily overlooked.

Treatment of Lemierre syndrome, as with other causes of septic pulmonary emboli, requires a prolonged course of high-dose, intravenously administered antibiotics. However, when the diagnosis of Lemierre syndrome is suspected, antibiotics with good anaerobic activity should be included in the initial therapy. The definitive antibiotic regimen is dependent on the results of susceptibility testing. Anticoagulation, by enhancing resolution of the source of septic embolization, may expedite recovery (7).

The radiologic findings in Lemierre syndrome are integral to its diagnosis. Referral to the radiology department may be for the evaluation of symptoms caused directly by an internal jugular venous clot or for imaging of the septic embolic complications. Awareness of this syndrome by the radiologist should lead to the suggestion of Lemierre syndrome whether by demonstration of internal jugular venous thrombosis at CT or US or through chest CT findings suggestive of septic emboli.

Three of our patients (cases 1, 2, and 4) presented with symptoms in the neck that preceded the onset of pulmonary symptoms. Results from US or CT imaging of the neck corroborated the clinical diagnosis of Lemierre syndrome in two of these cases; these were the first studies to suggest this diagnosis in the other case. In case 3, pulmonary symptoms preceded symptoms in the neck by 5 days; CT results were instrumental in making the diagnosis in this case and supported the diagnosis in the other cases.

The critical feature of Lemierre syndrome is the presence of septic pulmonary emboli. Although at presentation clinical features of septic emboli were apparent in only one of our patients (case 3), in the remaining three patients classic features developed soon after admission.

While septic emboli may produce the characteristic chest radiographic appearance of multiple peripheral, round, and wedge-shaped opacities that progress rapidly to cavitation (15), the findings are frequently nonspecific (16), as in our patients. In only one of our patients (case 3) was cavitation evident on the initial chest radiograph; this was diagnosed as simple cavitating pneumonia. One patient (case 2) had patchy consolidation, and two patients (cases 1 and 4) had clear lungs on the initial radiographs; even at later examinations, the changes were nonspecific and more suggestive of bronchopneumonia.

On the other hand, CT revealed diagnostic information in all four patients, there being characteristic CT features of septic infarcts with multiple predominantly peripheral nodules, showing cavitation in three cases. In one patient (case 1), peripheral opacities showed peripheral enhancement with central areas of reduced attenuation following intravenous administration of contrast medium; this enhancement is a feature characteristic of septic infarction (17,18). A clearly identifiable feeding vessel leading into some of the nodules was present in three of our patients (cases 1, 2, and 3). This so-called feeding vessel sign is also characteristic of septic pulmonary embolism and is found in 67% of patients with this diagnosis (17,18).

Pleural effusions developed in cases 1 and 2, with progression to empyema in case 1. In both instances, these complications were best appreciated on CT scans.

In all of our patients, CT results provided additional information not apparent on chest radiographs and indicated the likelihood of septic pulmonary emboli. These findings are consistent with those of Huang et al (17) and Kuhlman et al (18), who found that in patients with septic pulmonary embolism, CT was the first diagnostic imaging modality to produce results suggestive of the diagnosis of septic pulmonary emboli in 46% and 33% of patients, respectively. The absence of proximal thrombus at CT pulmonary angiography suggests that microemboli, rather than the macroembolic clot burden more typical of acute pulmonary embolism, are responsible for the pulmonary findings in Lemierre syndrome.

Patients with Lemierre syndrome frequently present with nonspecific pain and swelling over the sternocleidomastoid muscle, which results from septic jugular venous thrombosis; in three of our patients (cases 1, 2, and 4), symptoms in the neck preceded the onset of pulmonary symptoms and were severe enough to warrant radiologic investigation.

Noninvasive cross-sectional imaging techniques have superseded contrast-enhanced venography for identification of both the presence and the cause of venous obstruction (19). US is readily available and inexpensive, avoids the use of ionizing radiation, and demonstrates most thrombi. US findings include the presence of noncompressible thrombus, frequently associated with venous distention, and the absence of flow (case 1) (20). The US finding of complete or partial loss of cardiac pulsatility and respiratory phasicity at pulse-wave Doppler US interrogation, as in case 2, may alert the operator to the presence of proximal thrombi in areas inaccessible to direct US examination (eg, behind the clavicle) (21). Another area relatively inaccessible to US is toward the skull base, where the mandible inhibits full visualization. In contrast, CT and magnetic resonance (MR) imaging enable visualization of the entire internal jugular vein, as well as assessment of the thorax for proximal extension of thrombus or a proximal compressive cause of venous obstruction.

Contrast-enhanced CT characteristically demonstrates jugular venous distention with a thickened enhancing wall and a hypoattenuating filling defect (cases 3 and 4). Edema of the surrounding soft tissues is often present (22,23). The optimal technique involves imaging before and during intravenous injection of contrast material to avoid difficulties posed by clots at varying stages of evolution. If the diagnosis of Lemierre syndrome is suspected clinically or on the basis of chest CT findings, CT of the neck vessels should be performed at the same time as CT of the chest.

MR imaging, with its flow sensitivity and excellent soft-tissue contrast, has been shown to be an effective modality for the identification and characterization of thrombi (24), although cost and availability currently limit its use.

In conclusion, Lemierre syndrome, although much less common than in the preantibiotic era, still occurs and is potentially life-threatening. While, in retrospect, the constellation of clinical features is often relatively specific, lack of awareness of this entity frequently leads to delay in its diagnosis. Correct diagnosis is important, since treatment requires inclusion of an antibiotic with good anaerobic coverage.

Radiologic investigation is frequently instrumental in reaching a specific diagnosis. Patients may present to the radiology department for investigation of symptoms resulting from septic jugular venous thrombosis or its embolic consequences, particularly septic pulmonary emboli. Contrast-enhanced CT and US of the internal jugular veins are both sensitive in the detection of internal jugular venous thrombosis; characteristic CT appearances of septic pulmonary emboli may be the main clue to the correct diagnosis. The radiologist should be aware of Lemierre syndrome, particularly in a young, previously well patient without a history of drug abuse, and should suggest this diagnosis when radiologic and clinical features are compatible with septic emboli.



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  		Figure 2. Case 2. Transverse US image of the left internal jugular vein (LT IJV)(calipers) shows occlusion by echogenic thrombus. A normal common carotid artery (arrowheads) is also shown.

 



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  		Figure 3. Case 3. (a) Posteroanterior radiograph of the chest shows a cavity (arrowhead) in the right midzone and an area of consolidation in the lingula. (b) Conventional transverse CT scan shows multiple peripheral lung nodules (arrowheads), with cavitation in two large wedge-shaped areas of consolidation (arrows).

 



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  		Figure 3. Case 3. (a) Posteroanterior radiograph of the chest shows a cavity (arrowhead) in the right midzone and an area of consolidation in the lingula. (b) Conventional transverse CT scan shows multiple peripheral lung nodules (arrowheads), with cavitation in two large wedge-shaped areas of consolidation (arrows).

 



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  		Figure 4. Case 4. Contrast-enhanced transverse CT scan of the neck demonstrates a hypoattenuating, nonocclusive intraluminal thrombus (arrowhead) within the left internal jugular vein.

 


   Footnotes
 
Author contributions: Guarantor of integrity of entire study, N.J.S.; study concepts and design, N.J.S., C.D.R.F., J.G.R., E.R.H.; definition of intellectual content, N.J.S., C.D.R.F., J.G.R., E.R.H.; literature research, N.J.S., P.J.L., J.G.R.; clinical studies, N.J.S., P.J.L., J.G.R.; data acquisition, N.J.S., P.J.L., J.G.R.; data analysis, N.J.S.; manuscript preparation, N.J.S.; manuscript editing, C.D.R.F., P.J.L., J.G.R., E.R.H.; manuscript review, all authors.


   References
TOP
 Abstract
 Introduction
 Case 1
 Discussion
 References
 

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