Lemierre syndrome, also called postanginal septicemia, involves septic thrombophlebitis of the internal jugular vein (IJV), usually secondary to an acute oropharyngeal infection and frequently complicated by metastatic infections. It was first well characterized by Lemierre (49) in 1936, who reported 20 cases from his personal experience, 18 of whom died. It was a relatively common disease with a high mortality in the preantibiotic era. Since the introduction of antibiotics and their widespread use for the treatment of pharyngeal infections, there has been a substantial decrease in both the incidence and mortality of postanginal septicemia. Because of this, the syndrome is frequently overlooked when it appears today (41,57,73).
The usual etiologic agent in Lemierre syndrome is Fusobacterium necrophorum (41,57,73), a normal inhabitant of the oral cavity, the female genital tract, and the gastrointestinal tract (38). F. necrophorum is a strictly anaerobic, nonmotile, non-spore-forming, Gram-negative rod (38,41,50,57,73). It has a characteristic pleomorphic morphology on Gram-stained smears, with filaments, short rods, and coccoid elements (38).
We conducted the present review to increase the physician’s awareness of this disorder, as a high degree of clinical suspicion is essential to diagnose the syndrome. Accurate and timely diagnosis is critical because untreated disease is usually fatal, and highly effective treatments are available. The syndrome may not be as rare as believed, and is likely both overlooked and underreported.
To better characterize the important aspects of this syndrome, we searched the MEDLINE (National Library of Medicine, Bethesda, MD) database for case reports in the last 20 years using Lemierre’s syndrome and Fusobacterium necrophorum as keywords. We selected cases in which a head or neck infection (such as pharyngitis, otitis, odontogenic infection, mastoiditis) was associated with either 1) thrombophlebitis of the IJV (demonstrated by magnetic resonance imaging (MRI), computed tomography (CT), or ultrasound) or 2) positive cultures for F. necrophorum in the presence of metastatic infections. One hundred sixteen case reports were available for review (1–12,14–21,23–29,32–34,36,37,42–48a,51–56,58–71,74,75,77,78,80–92), and 1 additional case was found in a web-based search using the same keywords (61). We also included the 2 cases seen in our medical center (Jackson Memorial Hospital, Miami, FL) within the past year. Based on the criteria mentioned above, we selected a total of 109 cases for analysis.
A 17-year-old man presented with a sore throat and a right neck mass. The patient described a sore throat that started 7 days before admission, followed 3 days later by an enlarging mass on the right side of his neck, associated with dysphagia and subjective fever. The patient was allergic to penicillin. He reported no alcohol, tobacco, or illegal drug use. On physical examination, the patient appeared acutely ill but in no respiratory distress. He had mild erythema of the oropharynx, with mild right-sided oropharyngeal swelling. Examination of the neck revealed a large tender mass adjacent to the anterior border of the sternocleidomastoid muscle, measuring approximately 8 × 10 cm. The rest of the physical exam was unremarkable.
Laboratory studies on admission revealed a white blood cell count of 7.6 with 84% neutrophils, 10% lymphocytes, 5% monocytes, and 1% eosinophils. Hemoglobin was 14.1 g/dL and hematocrit, 42%. Electrolytes and renal function were normal. Erythrocyte sedimentation rate was 34 mm/h, and C-reactive protein level was 13 ng/mL. Plain neck films demonstrated a soft tissue density in the right paraspinal area consistent with soft tissue swelling. CT scan of the neck showed marked soft tissue swelling in the right posterior triangle of the neck, extending from the submandibular level to the lower cervical spine. There was tracking fluid throughout the fascial planes of the right side of the neck from the level of the right palatine tonsil to the hypopharynx, with effacement of the right piriform sinus. There was obvious thrombosis of the right IJV (Figure 1A and B). A chest X-ray was unremarkable (Figure 1C).
On the basis of these findings, a diagnosis of Lemierre syndrome was made. The patient was started on clindamycin 900 mg intravenous every 8 hours. Blood cultures performed on admission were negative. The neck tenderness and dysphagia rapidly resolved over the next day. He continued spiking fevers as high as 102 °F for the next 5 days. The patient’s mass slowly decreased in size over 9 days, after which the patient was discharged on oral clindamycin, with subsequent complete recovery.
A 45-year-old man was admitted with a 3-day history of right-sided neck tenderness and facial “puffiness.” His past medical history was remarkable for multiple substance abuse, congestive heart failure diagnosed 3 months before admission, irondeficiency anemia, and hyperthyroidism. The patient also described orthopnea and dry cough, which had been present for several months. There was no history of fever, chills, chest pain, lower extremity edema, weight loss, or night sweats.
On physical examination, the patient was in no acute distress. He was afebrile and jaundiced; he had mild periorbital edema and poor dentition. His neck did not show any track marks. There was jugular venous distention, mild thyromegaly (particularly on the right side) but no discrete masses. The right side of the neck was tender to palpation. The rest of the physical examination was normal.
Laboratory analysis revealed a white blood cell count of 8,300 with 63% neutrophils, 25% lymphocytes, 10% monocytes, and 2% eosinophils. Prothrombin time was 15 seconds, and partial thromboplastin time was 29 seconds. A chest X-ray was remarkable for a markedly enlarged cardiac silhouette and a right subpulmonic pleural effusion. Urine toxicologic screen was negative. He was human immunodeficiency virus (HIV)-negative by ELISA. Total bilirubin was 2.6 mg/dL and direct bilirubin 0.6 mg/dL. Creatinine was 1.1 mg/dL.
The following morning, the patient’s right neck tenderness had increased and there was a new area of soft tissue swelling that was nonerythematous and measured 2 × 4 × 1 cm. A CT scan of the neck and chest demonstrated thrombosis of the right IJV down to the level of the right subclavian vein. It also showed multiple small jugular and spinal accessory chain lymph nodes on the right, and a moderate right pleural effusion. Aspiration biopsy of the area was attempted, but only blood was obtained. The patient had fever during the first 3 days of hospitalization; with a peak temperature of 101.7 °F. The diagnosis of Lemierre syndrome was made and the patient was started on heparin, ibuprofen, and clindamycin. Blood cultures drawn on admission were negative. Thoracentesis was performed, revealing an exudate. Gram stain, culture, and cytology of the pleural fluid were negative. The patient’s right-sided neck pain slowly improved. A follow-up CT of the neck and chest showed no significant change in the IJV thrombus and a slight decrease in the right pleural effusion. The patient was discharged on anticoagulation, an antiinflammatory agent, and oral clindamycin and levofloxacin to complete a total course of 4 weeks.
Patient Characteristics and Etiology
Most cases (73.4%) occurred in patients aged 16–25 years, but cases occasionally occurred in younger patients and older patients as well. Most patients were previously healthy individuals. The etiology of Lemierre syndrome was found to be Fusobacterium necrophorum in 81.7% of the cases, as demonstrated by positive cultures from clinical specimens, usually blood (Table 1). However, several other organisms were found to be reported, alone (5.5%) or in combination with F. necrophorum (10.1%). These include Bacteroides asaccharolyticus, Bacteroides fragilis, Bacteroides gracilis, Bacteroides melaninogenicus, Bacteroides distasonis, Bacteroides uniformis, Peptostreptococcus, Group B and C Streptococcus, Streptococcus oralis, Staphylococcus epidermidis, Enterococcus sp., Proteus mirabilis, Eubacterium sp., Eikenella corrodens, lactobacilli, and Candida sp. Cultures were negative in 12.8% of cases.
F. necrophorum has an unusual ability to cause severe disease as a primary pathogen in previously healthy people with intact anatomical barriers (35,38,41,50,57,73), unlike other anaerobic bacteria. Its microbiology and virulence factors have been extensively reviewed elsewhere (38). The disease progresses in several steps (Figure 2). The first stage is the primary infection, which is usually pharyngitis (35,38,41,50,57,73). This is followed by local invasion to the lateral pharyngeal space and IJV septic thrombophlebitis, and finally, the occurrence of metastatic complications. In the majority of cases reviewed, a temporal pattern was obvious in that these stages occurred in an orderly fashion and corresponded to distinct clinical manifestations. Below, we describe the pathophysiology of each stage as we review the corresponding clinical findings.
The palatine tonsils and peritonsillar tissue were found to be the primary source of infection in most cases (87.1%). Odontogenic infections (1.8%) and mastoiditis (2.7%) also occurred in some patients. Additional sources have been reported in other series, including parotitis, sinusitis, and primary infection in the skin or subcutaneous tissues of the head and neck.
The clinical findings in this stage depend on the primary site of infection. Since pharyngitis made up the vast majority of cases, a sore throat and evidence of pharyngeal inflammation were the primary findings. Fever occurred in about 82.5% of cases, but not necessarily at the time of initial presentation. Gastrointestinal complaints such as abdominal pain, nausea, and vomiting were present in 49.5% of cases. At this point in presentation, there are no “red flags” that would suggest the etiology. Many patients had only subtle findings, such as hyperemia of the pharynx. The percentage of cases of F. necrophorum pharyngitis that progress to invasion of the lateral pharyngeal space and IJV septic thrombophlebitis is unknown. In a report (40) of 3 patients with documented F. necrophorum pharyngitis who received antibiotic therapy, 1 case progressed to IJV thrombophlebitis.
The time interval between the oropharyngeal infection and the onset of the second stage was usually less than 1 week. In some cases, signs and symptoms related to oropharyngeal infection had cleared (at times without antibiotic therapy) by the time IJV thrombosis developed.
Invasion of the Lateral Pharyngeal Space and IJV Thrombophlebitis
In the past, it was thought that IJV thrombophlebitis was initiated in the tonsillar and peritonsillar veins with subsequent spread to the IJV. However, it is likely that the most common mechanism involves spread of infection from peritonsillar tissue to the adjacent lateral pharyngeal space, mainly via lymphatic vessels (31). It is the infection of this compartment that can cause complications such as thrombophlebitis of the IJV and severe sepsis with metastatic infections (35,38,41,50,57,73).
The lateral pharyngeal space is divided by the styloid process into an anterior (muscular) and a posterior (neurovascular) compartment. The posterior neurovascular compartment includes the IJV, the carotid artery, the vagus nerve, lymph nodes, cranial nerves X-XII, and the cervical sympathetic trunk. The clinical findings of the invasion of this compartment result from compromise of these vital structures. Carotid artery rupture has occurred and is the most catastrophic complication of this stage; Horner syndrome may occur if the sympathetic trunk is involved. Paralysis of the trapezius muscle has been reported in 1 case, most likely secondary to compromise of the spinal accessory nerve (3). Dysphagia occurred in 17.4% of patients. The most frequent finding (52.2% of cases) at this stage is a tender and/or swollen neck, and this should be considered a warning sign in a patient with pharyngitis. The pain and swelling may extend from the angle of the jaw and along the sternocleidomastoid muscle, sometimes with associated trismus (9.1% of cases) (16,21,26,66,83,89,90). Pain when turning the head away from the involved site may occur as a consequence of irritation of the sternocleidomastoid muscle. Spasm of the sternocleidomastoid muscle may occur as well. The thrombosed jugular vein is rarely palpable. It must be remembered that local findings may be subtle or absent, particularly if the infection selectively affects the posterior compartment of the lateral pharyngeal space. No significant neck findings were found in 47.7% of the patients.
Once the infection involves the IJV, it may cause bacteremia with hematogenous spread to other sites. The first sign of this complication may be fever, soon thereafter accompanied by intense rigor. The lungs are by far the most common metastatic target (79.8% of cases), followed by the joints (16.5% of cases). The typical pulmonary findings in Lemierre syndrome reported previously were those resembling septic pulmonary embolism with chest X-ray findings of cavitating pneumonia, similar to what is seen in right-sided bacterial endocarditis with septic embolization. In our review, the most common finding on chest X-ray at presentation was the presence of pulmonary infiltrates in the absence of cavitation. Associated pleural effusions are common (43.1% of patients) and may precede the appearance of pulmonary infiltrates. A normal chest X-ray was present in 19.2% of cases, and only 31.1% of patients had radiologic evidence of cavitation. Moreover, almost half (44.2%) of these cases of cavitation were not evident on follow-up plain chest films, and were demonstrated only by CT scans of the chest. Empyema and lung abscess may be seen, and both pneumatoceles and pneumothorax have been described. Frank respiratory failure requiring ventilatory support occurred in 15.5% of cases.
The second most common site of septic embolization are the joints, with the hip, shoulders, and knees most frequently involved (10,21,36,47,50,87,91,92). The frequency of joint involvement in our series was 16.5%, which is significantly lower than that reported in the preantibiotic era (66.6%). Other sites of septic dissemination reported include hepatic or splenic abscesses (2.7% of cases). However, splenomegaly and hepatomegaly are common (15.5%) and are not necessarily associated with liver or hepatic abscesses (47). Mild hyperbilirubinemia with slight elevation of liver enzyme levels has been reported to be a common finding (8), which has been confirmed in our series (32.1%). In contrast to what occurred in the preantibiotic era, frank jaundice was present in only a minority (12.8%) of patients. Hematuria has also been described (5.5% of cases). Renal involvement with proteinuria and hematuria has been described as the predominant manifestation in a patient (17). When renal complications develop, the syndrome may be mistaken for poststreptococcal glomerulonephritis.
Metastatic spread of infection through embolization complicated all the cases described by Lemierre. However, this seems to be preventable by early antibiotic treatment. Both of our patients had documented IJV thrombosis, but neither showed evidence of metastatic infection. As the syndrome becomes more familiar to practicing physicians, the incidence of these complications should decrease.
In the cases described by Lemierre in the preantibiotic era, the outcome was fatal with rapidly progressing septicemia (22,49). The outcome of the syndrome after appropriate therapy has been instituted is favorable in most patients, although adult respiratory distress syndrome has been reported, and fatal cases have been seen even in the antibiotic era. The mortality in our series was 6.4%. Clearly, however, if it is recognized and appropriately treated, Lemierre syndrome has a good prognosis in most cases.
Clues to Diagnosis
Lemierre himself stated (49) that:
The appearance and repetition several days after the onset of a sore throat (and particularly of a tonsillar abscess) of severe pyrexial attacks with an initial rigor, or still more certainly the occurrence of pulmonary infarcts and arthritic manifestations, constitute a syndrome so characteristic that mistake is almost impossible.
In fact, the diagnosis of Lemierre syndrome on the basis of clinical grounds should be considered if the physician is aware of the existence of the disease. However, it is rare today and has been said to be “forgotten” by the medical community (16,47,57,66,89). The first clue to the diagnosis in 69.7% of the cases we reviewed was the finding of F. necrophorum in blood culture results rather than the clinical signs or symptoms. A microbiologic rather than clinical diagnosis may result in failure to institute early anaerobic coverage. Significant mortality and morbidity occurred, which was likely preventable. Most patients (89.8%) had evidence of metastatic complications by the time of diagnosis. In some cases, interventions such as chest tube thoracostomy, intubation and ventilatory support, and major surgery such as debridement of necrosed bone, were required. Nine cases required thrombectomy with IJV ligation.
The approach to a patient with pharyngitis and a tender/swollen neck should be aggressive. Blood cultures should be obtained, evidence of IJV thrombophlebitis should be sought, and anaerobic coverage with metronidazole or clindamycin should be initiated. Diagnostic methods to detect IJV thrombophlebitis include CT, MRI, and ultrasound. Ultrasound, the least expensive, may reveal an echogenic region within a dilated jugular vein, or a complex mass of solid and cystic components. However, it may miss a fresh thrombus with low echogenicity, and imaging the area beneath the clavicle may be technically difficult. CT scans are better able to demonstrate the anatomy and the presence of abscesses that need to be drained. This method may also reveal low attenuation intraluminal filling defects, and adjacent soft tissue swelling (see Figures 1A and 1B). Some authors have recommended CT as the primary diagnostic method, with ultrasound being the best test for follow-up once the anatomy has been well defined. If the patient has infection arising from the mastoid, the presence of intracerebral vein thrombosis specifically needs to be excluded (usually with MRI). In our series, most patients who had mastoiditis as the primary site developed intracerebral sinus vein thrombosis that required surgery.
For the treatment of Lemierre syndrome today, we certainly have more tools than Lemierre had at his disposal. The only recognized treatment in the preantibiotic era was ligation of the IJV on the affected side in an attempt to prevent septicemic spread. Today, the mainstay of treatment is prolonged antibiotic therapy (3–6 weeks), which seems necessary to eradicate the infection, probably because of its endovascular nature. The role of anticoagulant therapy in Lemierre syndrome remains controversial. The outcome of most patients in 1 review (90) was good without it. There have been no controlled studies, however, to assess its value in septic thrombophlebitis of the IJV. Finally, in patients with uncontrolled sepsis and ongoing evidence of septic emboli despite appropriate medical therapy, surgical ligation or excision of the IJV should be considered. Fortunately, this treatment is rarely needed today (8.2% of cases in our series).
We are indebted to Dr. Alan Bisno for his critical review of the manuscript and thoughtful suggestions.
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