Secondary Logo

Journal Logo

The Evolution of Lemierre Syndrome

Report of 2 Cases and Review of the Literature

CHIRINOS, JULIO A. M.D.; LICHTSTEIN, DANIEL M. M.D.; GARCIA, JAVIER M.D.; TAMARIZ, LEONARDO J. M.D., M.P.H.

Article
Free

Lemierre syndrome (postanginal septicemia) is caused by an acute oropharyngeal infection with secondary septic thrombophlebitis of the internal jugular vein and frequent metastatic infections. A high degree of clinical suspicion is necessary for diagnosis. Fusobacterium necrophorum is the usual etiologic agent. The disease progresses in several steps. The first stage is the primary infection, which is usually a pharyngitis (87.1% of cases). This is followed by local invasion of the lateral pharyngeal space and IJV septic thrombophlebitis (documented in 71.5% of cases), and finally, the occurrence of metastatic complications (present in 90% of cases at the time of diagnosis). A sore throat is the most common symptom during the primary infection (82.5% of cases). During invasion of the lateral pharyngeal space and IJV septic thrombophlebitis, a swollen and/or tender neck is the most common finding (52.2% of patients) and should be considered a red flag in patients with current or recent pharyngitis. The most common site of metastatic infection is the lungs (79.8% of cases). In contrast to the preantibiotic era, cavitating pneumonia and septic arthritis are now uncommon. Most patients (82.5%) had fever at some stage during the course of the disease. Gastrointestinal complaints such as abdominal pain, nausea, and vomiting were common (49.5% of cases). An elevated white blood cell count occurred in 75.2% of cases. Hyperbilirubinemia with slight elevation of liver enzyme levels occurred in one-third of patients, but frank jaundice was uncommon, in contrast to its high frequency reported in the preantibiotic era. We conclude that, most likely as a consequence of widespread antibiotic use for pharyngeal infections, the typical course of the disease has changed since Lemierre’s original description. The typical triad in our series was: pharyngitis, a tender/swollen neck, and noncavitating pulmonary infiltrates. The previous classical description of severe sepsis with cavitating pneumonia and septic arthritis was not commonly seen in our review. Mortality was low in our series (6.4%), but significant morbidity occurred, which was likely preventable by early diagnosis and treatment. The pathophysiology, natural history, diagnostic methods for internal jugular vein thrombosis, and management are discussed.

From Department of Medicine, University of Miami School of Medicine, Miami, Florida.

Address reprint requests to: Leonardo Tamariz, MD, MPH, Johns Hopkins University School of Medicine, Welch Center for Prevention, Epidemiology and Clinical Research, 2024 East Monument Street, Room 2–516, Baltimore, MD 21205. Fax: 410-614-0588; e-mail: ltamari1@jhmi.edu.

Accessible online at “http://www.md-journal.com.” To search for Medicine articles in PubMed, use the journal name “Medicine Baltimore.”

Back to Top | Article Outline

Introduction

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.

Back to Top | Article Outline

Methods

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.

Back to Top | Article Outline

Case Reports

Case 1

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).

Fig. 1

Fig. 1

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.

Back to Top | Article Outline

Case 2

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.

Back to Top | Article Outline

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.

TABLE 1

TABLE 1

Back to Top | Article Outline

Pathogenesis

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.

Fig. 2

Fig. 2

Back to Top | Article Outline

Primary Infection

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.

Back to Top | Article Outline

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.

Back to Top | Article Outline

Metastatic Complications

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.

Back to Top | Article Outline

Outcome

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.

Back to Top | Article Outline

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.

Back to Top | Article Outline

Management

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).

Back to Top | Article Outline

Acknowledgment

We are indebted to Dr. Alan Bisno for his critical review of the manuscript and thoughtful suggestions.

Back to Top | Article Outline

References

1. Abele-Horn M, Emmerling P, Mann JF. Lemierre’s syndrome with spondylitis and pulmonary and gluteal abscesses associated with Mycoplasma pneumoniae pneumonia. Eur J Clin Microbiol Infect Dis 20: 263–6, 2001.
2. Adams J, Capistrant T, Crossley K, Johanssen R, Liston S. Fusobacterium necrophorum septicemia [letter]. JAMA 250: 35, 1983.
3. Agarwal R, Arunachalam PS, Bosman DA. Lemierre’s syndrome: A complication of acute oropharyngitis. J Laryngol Otol 114: 545–7, 2000.
4. Ahkee S, Srinath I, Huang A, Raff MJ, Ramirez JA. Lemierres syndrome: Postanginal sepsis due to anaerobic oropharyngeal infection. Ann Otol Rhinol Laryngol 103: 308–10, 1994.
5. Alifano M, Venissac N, Guillot F, Mouroux J. Lemierre’s syndrome with bilateral empyema thoracis. Ann Thorac Surg 69: 930–1, 2000.
6. Alvarez A, Schreiber JR. Lemierre’s syndrome in adolescent children—anaerobic sepsis with internal jugular vein thrombophlebitis following pharyngitis. Pediatrics 96: 354–9, 1995.
7. Avinash K, et al. Lemierre’s syndrome following mastoiditis. Infect Med 15: 323–5, 1998.
8. Baddour LM, Land MA, Barrett FF, Rivara FP, Bruce WM, Bisno AL. Hepatobiliary abnormalities associated with postanginal sepsis. Common manifestations of an uncommon disease. Diagn Micriobiol Infect Dis 4: 19–28, 1986.
9. Baker J, Winer-Muram HT, Grey SW. Lemierre syndrome. South Med J 89: 1021–3, 1996.
10. Beldman TF, Teunisse HA, Schouten TJ. Septic arthritis of the hip by Fusobacterium necrophorum after tonsillectomy: A form of Lemierre syndrome? Eur J Pediatr 156: 856–7, 1997.
11. Bielecki JW. [Septic syndrome with a pulmonary focus]. Schweiz Rundsch Med Prax 80: 1030–3, 1991.
12. Bouvier DP, Armstrong RD, Bradshaw DM, Hoenzsch RE. Fusobacterium necrophorum septicemia without a primary focus. South Med J 78: 1521–2, 1985.
Brown R, Lough HG, Poxton IR. Phenotypic characteristics and lipopolysaccharides of human and animal isolates of Fusobacterium necrophorum. J Med Microbiol 46: 873–8, 1997.
    14. Busch N, Mertens PR, Schonfelder T, Nguyen H, Marschall HU, Kierdorf H, Haase G, Urhahn R, Sieberth HG, Matern S. [Lemierre’s post-tonsillitis sepsis with meningitis and intravascular consumption coagulopathy as complication of infectious mononucleosis with pansinusitis.] Dtsch Med Wochenschr 12: 94–8, 1996.
    15. [Deleted.]
    16. Carlson ER, Bergamo DF, Coccia CT. Lemierre’s syndrome: Two cases of a forgotten disease. J Oral Maxillofac Surg 52: 74–8, 1994.
    17. Carrie S, Fenton PA. Necrobacillosis—an unusual case of pharyngotonsillitis. J Laryngol Otol 108: 1097–8, 1994.
    18. Celikel TH, Muthuswamy PP. Septic pulmonary emboli secondary to internal jugular vein phlebitis (postanginal sepsis) caused by Eikenella corrodens. Am Rev Respir Dis 130: 510–3, 1984.
    19. Chalstrey SE, Williams HO, Reilly G. Necrobacillosi—an unusual cause of cervical abscess. J Laryngol Otol 106: 374–5, 1992.
    20. Chippindale AJ, Patel B, Mamtora H. A case of necrobacillosis. Thorax 45: 74–5, 1990.
    21. Cosgrove EF, Colodny SM, Pesce RR. Adult respiratory distress syndrome as a complication of postanginal sepsis. Chest 103: 1628–9, 1993.
    22. Courmont P, Cade A. Sur une septico-pyohemie de l’homme simulant la peste et causee par un streptobacille anaerobie. Arch Med Exp Anat Pathol no. 4, 1900.
    23. Dagan O, Powell KR. Postanginal sepsis following infectious mononucleosis. Arch Intern Med 147: 1581–3, 1987.
    24. De Vos AI, van Rossem RN, van Elzakker EP, Nijhuis-Heddes JM, Maartense E. Lemierre’s syndrome. Sepsis complicating an anaerobic oropharyngeal infection. Neth J Med 59: 181–3, 2001.
    25. Dellamonica P, Bernard E. “Deep throat” cellulites. J Infect 38: 134, 1999.
    26. Dykhuizen RS, Olson ES, Clive S, Douglas JG. Necrobacillosis (Lemierre’s syndrome): A rare cause of necrotizing pneumonia. Eur Respir J 7: 2246–8, 1994.
    27. Ellis GR, Gozzard DI, Looker DN, Green GJ. Postanginal septicaemia (Lemierre’s disease) complicated by haemophagocytosis. J Infect 36: 340–1, 1998.
    28. Ely EW, Stum TE, Hudspeth AS, Haponik EF. Thoracic complications of dental surgical procedures: Hazards of the dental drill. Am J Med 95: 456–65, 1993.
    29. Enwonwu CO, Falkler Jr, WA Idigbe EO, Afolabi BM, Meeks VI. Pathogenesis of cancrum oris (noma): Confounding interactions of malnutrition with infection. Am J Trop Med Hyg 60: 223–32, 1999.
    Enwonwu CO, Falkler Jr, WA Savage KO. Noma (cancrum oris): Questions and answers. Oral Dis 5: 144–9, 1999.
      31. Falkler Jr, WA Enwonwu CO. Microbiological understandings and mysteries of noma. Oral Dis 5: 150–5, 1999.
      32. Fiesseler FW, Richman PB, Riggs RL. Pharyngitis followed by hypoxia and sepsis: Lemierre syndrome. Am J Emerg Med 19: 320–2, 2001.
      33. Gerst C, Primrose JM. Septic arthritis of the ankle from Fusobacterium necrophorum. Acad Emerg Med 4: 1172–3, 1997.
      34. Golledge CL, Beaman MH, Weeramanthri T, Riley TV. Necrobacillosis—primary anaerobic septicaemia due to Fusobacterium necrophorum. Aust N Z J Med 20: 152–3, 1990.
      35. Golpe R, Marin B, Alonso M. Lemierre’s syndrome (necrobacillosis). Postgrad Med J 75: 141–4, 1999.
      36. Gong J, Garcia J. Lemierre’s syndrome. Eur Radiol 9: 672–4, 1999.
      37. Gudinchet F, Maeder P, Neveceral P, Schnyder P. Lemierre’s syndrome in children: High-resolution CT and color Doppler sonography patterns. Chest 112: 271–3, 1997.
      38. Hagelskjaer Kristensen L, Prag J. Human necrobacillosis, with emphasis on Lemierre’s syndrome. Clin Infect Dis 31: 524–32, 2000.
      Hall V, Duerden BI, Magee JT, Ryley HC, Brazier JS. A comparative study of Fusobacterium necrophorum strains from human and animal sources by phenotypic reactions, pyrolysis mass spectrometry and SDS-PAGE. J Med Microbiol 46: 865–71, 1997.
        40. Harar RP, MacDonald A, Pullen D, Ganesan S, Prior AJ. Lemierre’s syndrome: Are we underdiagnosing this life-threatening infection? J Otorhinolaryngol Relat Spec 58: 178–81, 1996.
        41. Henry S, deMaria A, McCabe WR. Bacteremia due to Fusobacterium species. Am J Med 75: 225–32, 1983.
        42. Holland BW, McGuirt Jr. WF Imaging quiz case 2. Lemierre syndrome: Septic thrombophlebitis of the internal jugular vein, or “postanginal” sepsis. Arch Otolaryngol Head Neck Surg 126: 1500–4, 2000.
        43. Hughes CE, Spear RK, Shinabarger CE, Tuna IC. Septic pulmonary emboli complicating mastoiditis: Lemierre’s syndrome revisited. Clin Infect Dis 18: 633–5, 1994.
        44. Ieven M, Vael K, De Mayer M, De Schepper A, Pattyn S. Three cases of Fusobacterium necrophorum septicemia. Eur J Clin Microbiol Infect Dis 12: 705–6, 1993.
        45. Kasaranas YL, Yim KK, Shuster BB, Lineaweaver WC. Lemierre’s syndrome: A case of postanginal septicemia and bilateral flank abscess. Ann Plast Surg 35: 525–8, 1995.
        46. Kern W, Dolderer M, Krieger D, Buchler M, Kern P. [Lemierre’s syndrome with splenic abscesses.] Dtsch Med Wochenschr 117: 1513–7, 1992.
        47. Koay CB, Heyworth T, Burden P. Lemierre syndrome—a forgotten complication of acute tonsillitis. J Laryngol Otol 109: 657–61, 1995.
        48. Lau ES, Shuckett R. Fusobacterium septic arthritis of the sternoclavicular joint. J Rheumatol 20: 1979–81, 1993.
        48a. Lee BK, Lopez F, Genovese M, Loutit JS. Lemierre’s syndrome. South Med J 90: 640–3, 1997.
        49. Lemierre A. On certain septicemias due to anaerobic organisms. Lancet 1: 701–3, 1936.
        50. Leugers CM, Clover R. Lemierre’s syndrome: Postanginal sepsis. J Am Board Fam Pract 8: 384–91, 1995.
        51. Lustig RL, Cusick BC, Cheung SW, Lee KC. Lemierre’s syndrome: Two cases of postanginal sepsis. Otolaryngol Head Neck Surg 112: 767–72, 1995.
        52. Mane S, Torres M, Buges J, Rivas A, Bruno C, Rodriguez E, Martinez JA, Nubiola A. Scintigraphic demonstration of jugular obstruction in a case of Lemierre syndrome. Clin Nucl Med 17: 233–5, 1992.
        53. Marangos MN, Fuchs-Ertman DA, Kourea HP, Meureer KJ, Lerwick PA, Zimmerman SH, Valenti AJ. Cerebral infarct and adult respiratory distress syndrome in a patient with postanginal sepsis. Clin Microbiol Infect 6: 337–9, 2000.
        54. Martin MJ, Wrigth ED. A case of Fusobacterium necrophorum sepsis. J Infect 31: 151–2, 1995.
        55. McLean AS, Tyler K. Cardiac tamponade in a postpartum woman with Lemierre’s syndrome. Anaesth Intensive Care 26: 582–3, 1998.
        56. Moller K, Dreijer B. Post-anginal sepsis (Lemierre’s disease): A persistent challenge. Presentation of 4 cases. Scand J Infect Dis 29: 191–4, 1997.
        57. Moore-Gillon J, Lee TH, Eykyn SJ, Phillips I. Necrobacillosis: A forgotten disease. Br Med J (Clin Res Ed) 288: 1526–7, 1984.
        58. Mukau L. Dissecting retropharyngeal abscess due to Fusobacterium necrophorum in an adult. South Med J 78: 476–8, 1985.
        59. Nakamura S, Sadoshima S, Doi Y, Yoshioka M, Yamashita S Gotoh H, Onoyama K. Internal jugular vein thrombosis, Lemierre’s syndrome; oropharyngeal infection with antibiotic and anticoagulation therapy—a case report. Angiology 51: 195–9, 2000.
        60. Narsinghani U, Schmidt MB, Jacobs PF, Anand KS. Radiological case of the month: Lemierre syndrome. Arch Pediatr Adolesc Med 155: 965–6, 2001.
        61. Nuermberger E. Case Rounds. Case 17: A previously healthy 23 year-old woman with sepsis. http://hopkins-id.edu/education/id_caserounds/caserounds17.html; posted 4/7/2000.
        62. Ockrim J, Kettlewell S, Gray GR. Lemierre’s syndrome. Curr Infect Dis Rep 2: 168–73, 2000.
        63. Page Y, Comtet C, Tardy B, Zeni F, Thevenet D, Lucht F, Bertrand JC. Disseminated intravascular coagulation in fusobacterium nacrophorum septicemia. Scand J Infect Dis 22: 743–7, 1990.
        64. Pickering MC, Barkham T, Mason JC, Shaunak S, Davies KA. Bilateral gluteal abscesses as a unique manifestation of Fusobacterium septicemia. Rheumatology (Oxford) 39: 224–5, 2000.
        65. Ray J, O’Gradaigh D, Tighe R. A young man with a characteristic syndrome. Postgrad Med J 76: 51–2, 2000.
        66. Screaton NJ, Ravenel JG, Lehner PJ, Heitzman ER, Flower CD. Lemierre syndrome: Forgotten but not extinct—report of four cases. Radiology 213: 369–74, 1999.
        67. Seidenfeld SM, Sutker WL, Luby JP. Fusobacterium necrophorum septicemia following oropharyngeal infection. JAMA 248: 1348–50, 1982.
        68. Sena S, Rosenfeld DL, Santos S, Keller I. Jugular thrombophlebitis complicating bacterial pharyngitis (Lemierre’s syndrome). Pediatr Radiol 26: 141–4, 1996.
        69. Shadowen RD, Trevor RP. Lemierre’s postanginal septicemia: Internal jugular vein thrombosis related to pharyngeal infection. South Med J 82: 1583–4, 1989.
        70. Shaham D, Sklair-Levy M, Weinberger G, Gomori JM. Lemierre’s syndrome presenting as multiple lung abscesses. Clin Imaging 24: 197–9, 2000.
        71. Shaman D, Sklair-Levy M, Weinberger G, Gomori JM. Lemierre’s syndrome presenting as multiple lung abscesses. Clin Imaging 24: 197–9, 2000.
        Shinjo T, Misawa N, Goto Y. Comparison of haemolytic activity between Fusobacterium necrophorum subsp. necrophorum subsp. funduliforme in vitro and in vivo. APMIS 104: 75–8, 1996.
          73. Sinave CP, Hardy GJ, Fardy PW. The Lemierre syndrome: Suppurative thrombophlebitis of the internal jugular vein secondary to oropharyngeal infection. Medicine (Baltimore) 68: 85–94, 1989.
          74. Singhal A, Kerstein MD. Lemierre’s syndrome. South Med J 94: 886–7, 2001.
          75. Sinnott 4th, JT Wheedon C, Schwartz M, Villanueva L. Postanginal sepsis: A pain in the neck. Postgrad Med 86: 77–8, 81–2, 1989.
          Smith GR, Thornton EA. Classification of human and animal strains of Fusobacterium necrophorum by their pathogenic effects in mice. J Med Microbiol 46: 879–82, 1997.
            77. Smith SA. Respiratory failure as a complication of pharyngitis: Lemierre’s syndrome. Pediatr Emerg Care 159: 402–3, 1999.
            78. Soave RL, Kuchar DJ. Bilateral forefoot gangrene secondary to Lemierre’s disease. J Am Podiatr Med Assoc 91: 147–9, 2001.
            Spelman D. Suppurative (septic) thrombophlebitis. Up To Date Feb. 28, 2000.
              80. Stahlman GC, DeBoer DK, Green NE. Fusobacterium osteomyelitis and pyarthrosis: A classic case of Lemierre’s syndrome. J Pediatr Orthop 16: 529–32, 1996.
              81. Stallworth JR, Carroll JM. Lemierre’s syndrome: New insights into an old disease. Clin Pediatr (Phila) 36: 5–9, 1997.
              82. Stokroos RJ, Manni JJ, de Kruijk JR, Soudijin ER. Lemierre syndrome and acute mastoiditis. Arch Otolaryngol Head Neck Surg 125: 589–91, 1999.
              83. Tewfik TL, Husein M, Shapiro RS, Oudjhane K. Lemierre syndrome in an immunocompromised patient. Int J Pediatr Otorhinolaryngol 51: 195–9, 1999.
              84. Turay UY, Erdogan Y, Ergun P, Biber C, Ciftci B, Ayaz A. Lemierre’s syndrome. Respirology 6: 171–3, 2001.
              85. Vandenberg SJ, Harting GK. Lemierre’s syndrome. Otolaryngol Head Neck Surg 119: 516–8, 1998.
              86. Venkatamaran MT, Policar M. Fever, sore throat, and pulmonary infiltrates in a 20-year old man. Chest 112: 268–70, 1997.
              87. Vogel LC, Boyer KM. Metastatic complications of Fusobacterium necrephorum sepsis. Am J Dis Child 134: 356–8, 1980.
              88. Vohra A, Saiz E, Ratzan KR. A young woman with a sore throat, septicaemia, and respiratory failure. Lancet 350: 928, 1997.
              89. Weesner CL, Cisek JE. Lemierre syndrome: The forgotten disease. Ann Emerg Med 22: 256–8, 1993.
              90. Williams A, Nagy M, Wingate J, Bailey L, Wax M. Lemierre syndrome: A complication of acute pharyngitis. Int J Pediatr Otorhinolaryngol 45: 51–7, 1998.
              91. Wolf RF, Konings JG, Prins TR, Weits J. Fusobacterium pyomyositis of the shoulder after tonsillitis. Report of a case of Lemierre’s syndrome. Acta Orthop Scand 62: 595–6, 1991.
              92. Zapor M, Fraser SL. A 47-year old man with a sore throat. Cleve Clin J Med 68: 605–6, 2001.

              Cited By:

              This article has been cited 5 time(s).

              The American Journal of the Medical Sciences
              An Unusual Case of Lemierre's Syndrome Presenting as Pyomyositis
              CRUM-CIANFLONE, N; MAYER, R
              The American Journal of the Medical Sciences, 335(6): 499-501.
              10.1097/MAJ.0b013e318157d3c7
              PDF (181) | CrossRef
              The American Journal of the Medical Sciences
              Community-Acquired Methicillin-Resistant Staphylococcus aureus and Lemierre Syndrome
              Bilal, M; Cleveland, KO; Gelfand, MS
              The American Journal of the Medical Sciences, 338(4): 326-327.
              10.1097/MAJ.0b013e3181a9302b
              PDF (131) | CrossRef
              Pediatric Critical Care Medicine
              Lemierre-like syndrome caused by community-associated methicillin-resistant Staphylococcus aureus complicated by hemorrhagic pericarditis
              Hoehn, KS; Capouya, JD; Daum, RS; Glikman, D; Gossett, JG; Hafzalah, M; Johnson, D; Marcinak, J
              Pediatric Critical Care Medicine, 11(3): e32-e35.
              10.1097/PCC.0b013e3181b806cb
              PDF (1129) | CrossRef
              Pediatric Emergency Care
              Lemierre Syndrome: A Case Report
              Waterman, JA; Balbi, HJ; Vaysman, D; Ayres, RA; Caronia, CG
              Pediatric Emergency Care, 23(2): 103-105.
              10.1097/PEC.0b013e3180302c0f
              PDF (217) | CrossRef
              Pediatric Emergency Care
              Lemierre Syndrome: Unusual Cause and Presentation
              Aouad, R; Melkane, A; Rassi, S
              Pediatric Emergency Care, 26(5): 376-377.
              10.1097/PEC.0b013e3181db235b
              PDF (193) | CrossRef
              Back to Top | Article Outline
              © 2002 Lippincott Williams & Wilkins, Inc.