Lemierre's syndrome

Abstract

Lemierre's syndrome is characterized by thrombosis of the internal jugular vein that develops following an oropharyngeal infection. Sepsis and septic metastases frequently ensue and affect the lungs, the musculoskeletal system, and occasionally the liver. Most cases are caused by infection with Fusobacterium necrophorum. This infection responds to antibiotic therapy with beta-lactamaseresistant compounds that exert good anaerobic coverage. Anticoagulation and surgical intervention can be helpful in advanced cases. Fewer than 160 cases of classic Lemierre's syndrome have been described; approximately one-third of these reported cases have occurred since 1988. We describe a new case of Lemierre's syndrome that occurred in an otherwise healthy 27-year-old man. Thrombosis of both internal jugular veins extended through the subclavian system and into both upper extremities. The patient was treated with intravenous antibiotics and heparin during 14 days of hospitalization. He was discharged on oral clindamycin and warfarin sodium, and after 6 months he was able to return to full activity. To our knowledge, this is the first reported case of Lemierre's syndrome in which internal jugular vein thrombosis occurred bilaterally. By reporting this previously undescribed manifestation of Lemierre's syndrome, we hope to increase practitioner awareness of this disease entity.

Introduction

Internal jugular vein thrombosis is an uncommon disease that has been associated with central intravenous catheterization, IV drug abuse, hypereoagulability, infection, and atherosclerosis. (1) Virchow's triad (stasis, endothelial injury, and hypercoagulability) promotes clot development and propagation in the internal jugular vein (as it does in any other vascular bed), but fewer than 5% of deep venous thromboses occur in the head and neck. (2) Trauma from indwelling central venous catheterization or from the repeated use of the internal jugular vein by IV drug abusers is the most common cause of internal jugular vein thrombosis. (3) This has not always been the case; during the pre-antibiotic era, internal jugular vein thrombosis was a common sequela to oropharyngeal infection.

In 1936, Lemierre described a syndrome that was characterized by anaerobic septicemia, internal jugular vein thrombosis, and septic emboli that arose secondary to infections of the head and neck, particularly in the oropharynx. (4) (Lemierre was not the first to describe the syndrome that bears his name, but he is accorded the eponymous honor nonetheless.) Lemierre found that approximately 90% of patients with this illness had died within several weeks of its onset. Subsequent reports of this syndrome-which is also known as postanginal septicemia and a form of necrobacillosis-appeared intermittently in the literature until the 1950s. Most notably, Alston described 21 cases of classic Lemierre's syndrome in his review of 280 cases of necrobacillosis that had been published in the world literature between 1933 and 1955. (5)

Following the introduction of antibiotics, only a small number of cases was reported during the next 30 years. In 1989, Sinave et al published a thorough analysis of 38 cases that had occurred between 1974 and 1988. (6) In the same year, Eykyn commented on 45 cases of necrobacillosis in England and Wales, 29 of which exhibited the clinical characteristics of Lemierre's syndrome. (7) Since then, only sporadic case reports of Lemierre's syndrome have appeared in the English-language literature, and it came to be characterized as a "forgotten" disease. (8,9)

In order to raise awareness of this entity, we describe a new case of Lemierre's syndrome that featured a previously undocumented manifestation, and we provide an overview of those cases that have been reported since 1988.

Case report

A 27-year-old man (a soldier on active duty) was transferred to our institution for evaluation of bilateral internal jugular vein thrombosis, fever, and pharyngitis from a suspected occult malignancy. The patient had no significant medical history and denied IV drug abuse. He had been in his usual state of health until approximately 4 weeks prior to transfer, when he began experiencing fever and sore throat. He had received several courses of antibiotics--including erythromycin and ceftriaxone--and a tapered steroid regimen for culture-proven group A beta-hemolytic streptococcal pharyngitis, but he had failed to improve. The results of monospot tests were repeatedly negative. With the onset of anterior neck pain and tenderness, coupled with the persistence of his odynophagia, the patient had been admitted to an outside facility 5 days prior to transfer.

An outside otolaryngology service aspirated purulent matter from the anterior neck, diagnosed an infected thyroglossal duct cyst, and eventually incised the area and drained a large collection of fluid. However, despite IV antibiotic therapy with alternating clindamycin and ceftriaxone for 3 days, the patient's condition worsened and he began to evince right-sided facial and supraclavicular swelling in addition to left upper extremity swelling. Venous duplex ultrasonography documented the presence of bilateral internal jugular and subclavian venous thrombosis that extended to the axillary vein on the right and the basilic vein on the left (figure 1). Based on this finding, the patient was transferred to our facility.

Our otolaryngology--head and neck surgery service was consulted shortly after the patient's arrival. On initial evaluation, the patient had a temperature of 99.1[degree]F and appeared to be toxic. Examination of the oropharynx revealed an asymmetric tonsillar enlargement without erythema, exudates, or lesions. The patient's neck was marked by diffuse swelling and exquisite tenderness to palpation, and there was a distinct nodularity along the anterior aspect of both sternocleidomastoid muscles. A 1-cm transverse midline incision was noted at the level of the thyroid cartilage. The incision had been packed with NuGauze and the surrounding area was marked by edema and erythema; minimal mucopurulent drainage was noted. A palpable cord was noted in the right supraclavicular fossa, and there was obvious swelling of the left antecubital fossa and the medial aspect of the arm. No edema, asymmetry, erythema, or lesion was evident on flexible fiberoptic nasopharyngoscopy. On auscultation, the lungs were clear, but a I I/VI systolic ejection murmur was noted. The patient also had hepatosplenomegaly.

Results of initial laboratory evaluations were obtained (table 1). Among the significant findings were a normal leukocyte count, hypoalbuminemia, normal clotting, and elevated liver enzyme levels. Contrast-enhanced computed tomography (CT) of the neck (figure 2) and chest (figure 3) detected thrombosis of the right jugular, distal right subclavian, right brachiocephalic, and left jugular veins. The right jugular vein clot extended from the skull base to just above the aortic arch. The left internal jugular vein thrombus was only partially occlusive and limited to the area of the thyroid gland. A collection of fluid and surrounding inflammation occupied the anterior midline of the neck superior to the thyroid gland. Multiple pulmonary nodules (including a cavitary nodule in the anterior basal segment of the right lower lobe), bilateral lower lobe infiltrates, and bilateral pleural effusions were also evident.

A diagnosis of Lemierre's syndrome was made, and the patient was started on IV clindamycin (900 mg q8h) and IV ceftriaxone (2 g ql2h). Following an initial deterioration in his respiratory status (decreased oxygen saturations and pleuritic chest pain that did not require mechanical ventilation), the patient improved and began to experience less pain, swelling, and shortness of breath. However, a chest radiograph showed that his pulmonary disease was persistent (figure 4). After consultations with both the infectious disease and hematology services, the patient was started on IV heparin therapy. He required twice-daily dressing changes of the midline neck wound and received 14 days of IV antibiotics. After discharge, he continued on oral clindamycin for 4 weeks and warfarin sodium for 6 months. Venous duplex ultrasonography documented a gradual reduction in the size of the extensive bilateral thrombi (figure 5). At his last evaluation, the patient's warfarin was stopped, and he was able to return to active duty.

Review of the literature

Our examination of the English-language medical literature published since 1988 revealed that 54 patients were reported to have had clinical evidence of Lemierre's syndrome. However, in keeping with the criteria espoused by Sinave et al, (6) not all of these cases are included in this review. Classic Lemierre's syndrome is characterized by (1) primary infection in the oropharynx, (2) septicemia documented by at least one positive blood culture, (3) clinical or radiographic evidence of internal jugular vein thrombosis, and (4) at least one metastatic focus. (6) We determined that 40 of the 54 cases that were described by others since the publication of the report by Sinave et al were documented to have met all four criteria, and these are the cases that we discuss in this article, in addition to our own case (table 2). Although the clinical criteria for Lemierre's syndrome might have been met in the other 14 cases, (9-22) we did not include them in this review because there was either an absence of documented metastatic foci, absent or negative blood cultures, undocumented internal jugular vein thrombosis, or a primary infection that arose either outside the oropharynx or as a sequela to trauma. Moreover, another 29 patients were described in two series that examined necrobacillosis and septic internal jugular vein thrombosis, but insufficient data preclude these patients from consideration in this study. (23,24)

As was the case in the review by Sinave et al, (6) all 41 patients in our study were presumed to have had internal jugular vein thrombosis if they exhibited pleuropulmonary involvement. The 27 males (65.9%) and 14 females ranged in age from 8 to 49 years (mean: 20.6). Thirty-nine patients (95.1%) had developed Lemierre's syndrome following an episode of pharyngitis; the other two patients had evidence of gingivitis. Pleuropulmonary involvement--including infiltrates, nodular densities, pleural effusions, empyema, and adult respiratory distress syndrome--occurred in 38 patients (92.7%). (8-10,14,18,25-45)

Other sites of septic emboli or direct extension of thrombosis included the liver, (9,14,41) long bone and extremity joints, (25,32,34,36) the gluteal region, (9,46,47) the sternum, (32) and the cranial vault, (48) Patients also experienced systemic manifestations of illness, such as derangements of liver function with elevations of intracellular enzymes and bilirubin, (9,14,41) cytopenias, (32,43) and disseminated intravascular coagulation.37 Four patients manifested significant thrombosis beyond the internaijugular vein, including the external jugular vein, sigmoid sinus, and superior vena cava. (27,33,44,48)

Fusobacterium necrophorum was isolated from the blood of 36 patients (87.8%), including two who had polymicrobial infections. Fusobacterium nucleatum (37) and Streptococcus san guis (18) appeared in one patient each, and both Peptostreptococcus and group C Streptococcus spp. were isolated from a single patient. (10) Kiebsiella pneumoniae was isolated from both the sputum and blood of one patient who developed Lemierre's syndrome following a periodontal infection. (44)

All patients received intravenous antibiotics. The most common were metronidazole, penicillin, gentamicin, clindamycin, and various second- and third-generation cephalosporins. More than one antibiotic was administered to 35 patients; specific data on antibiotic selection and regimen are unavailable for two of these patients. (31, 46) Eleven patients (26.8%) required anticoagulation over a period of 1 week to 6 months. Thirty-nine of the 41 patients (95.1%) survived; of the two who did not, one died from fulminant pneumonia and the other from severe sepsis. (28, 46)

Our analysis revealed that there are striking similarities between our 41 cases and the cases of Lemierre's syndrome that were reported from 1974 through 1988 by Sinave et al with respect to patient demographics, sites of metastatic involvement, types of pathogen, treatment modalities, and outcomes. (6)

Discussion

We report the first case of bilateral internal jugular vein thrombosis in a patient with Lemierre's syndrome. When Lemierre first described the syndrome of postanginal sepsis, he noted that most cases developed in the setting of oropharyngeal infection. (4) Furthermore, he acknowledged that internal jugular vein thrombophlebitis could exhibit manifestations in the ear, mastoid, and sinuses, as well. (4)

Clinical features. Lemierre's syndrome is characterized by thrombosis of the internal jugular vein that develops following oropharyngeal infection. Sepsis and septic metastases frequently ensue, and they can affect the lungs, the musculoskeletal system, and on occasion the liver. Pharyngitis, tonsillitis, or gingivitis accounts for the initial infection and fever, which are typically followed in 1 to 3 weeks by the development of neck pain and swelling, respiratory decompensation, or myalgias and arthralgias. This pattern of events is fairly pathognomonic; in fact, Lemierre noted that this syndrome is so characteristic that "mistake is almost impossible." (4) Even so, delays in diagnosis are common.

The incidence of Lemierre's syndrome and associated mortality have decreased substantially since the dawn of the antibiotic age. (6) In fact, only two deaths have been documented since 1990. (28,46) Nevertheless, prolonged morbidity (and its attendant financial and social costs) can persist, as it did in our patient.

Although Streptococcus, Bacteroides, and Lactobacillus spp. as well as other Fusobacterium spp. have been implicated in the pathogenesis of Lemierre' s syndrome, F necrophorum is the most common pathogen isolated from blood cultures in these patients. The Fusobacterium organism is a normal component of the flora of the oral cavity, and it exists in large numbers in the gingival crevice and the subgingival plaque of adults. This genus also resides in the large bowel and in the female genital tract. An anaerobic, gram-negative bacillus, F necrophorum can be filamentous or fusiform in appearance. (49) In addition to oropharyngeal infections, Fusobacterium spp. have been implicated in the development of endocarditis, soft-tissue infections, and brain, hepatic, and intra-abdominal abscesses. Fusobacterium spp. have been associated with as many as 46% of all head and neck infections, frequently in conjunction with other organisms. (50)

A disruption of normal host mucosal defenses through trauma or hypoxia can provide a supportive environment for the proliferation of these bacteria. (50) Bacterial production of proteolytic enzymes, lipopolysaccharide endotoxin, leukocidin, and hemagglutinin accounts for the pathogenicity of F necrophorum, which then invade the regional veins. (36) The hemagglutinin moiety has been shown to aggregate bovine platelets, which might account for the internal jugular vein thrombosis of Lemierre's syndrome. (49)

The nomenclature of this class of bacteria has undergone significant evolution over the past 50 years. The current classification is based on selective culturing techniques and analysis of fatty-acid end products. Although other anaerobic bacilli such as Bacteroides spp. can be involved in oropharyngeal infections, Fusobacterium spp. can be differentiated by their production of n-butyric acid alone. (50)

The oropharynx--particularly the palatine tonsils--provides the source of infection in most cases of Lemierre's syndrome. The anatomy of the lateral pharyngeal space promotes invasion of the internal jugular vein in the retrostyloid compartment. An inverted cone extending from the skull base to the hyoid, the lateral pharyngeal space is bounded medially by the superior pharyngeal constrictor and laterally by the medial pterygoid. The styloid process divides this anatomic space into anterior and posterior compartments; the contents of the carotid sheath and cranial nerves IX through XII reside in the posterior compartment. Tonsillar infection can involve the jugular vein by direct extension through this fascial space or by hematogenous or lymphatic spread from peritonsillar vessels. (32)

After the development of internal jugular vein thrombosis, septic emboli can emerge and affect distant sites. Numerous reports of pulmonary involvement--ranging from discrete nodularity to empyema thoracis and adult respiratory distress syndrome--have been published. (8-10,14,18,25-45) Patients can experience decreased oxygen saturation, pleuritic chest pain, or hemoptysis. Liver abscesses can occur, but elevations in both intra- and extra-cellular liver enzyme levels appear to be more common, (9,10) as was evident in our patient. The long bones can be affected by osteomyelitis, and joints such as the elbow, knee, and ankle can also be affected. (25,32,34,36) Soft-tissue abscesses have also been described, and they often required drainage before systemic improvement was noted. (9,34,46,47) Multiple hematologic abnormalities have been reported, including thrombocytopenia and disseminated intravascular coagulation. (9,10,21) Neurologic and intracranial complications such as meningitis and cranial nerve palsies can even occur. (48)

The myriad manifestations of Lemierre's syndrome often complicate its diagnosis and cause a delay in appropriate therapy. Evaluation of the patient with suspected Lemierre's syndrome should begin with a thorough history and physical examination, because abnormalities can be present in more than one organ system.

Chest radiography is indicated when pulmonary symptoms are present, and appropriate laboratory studies--including measurements of the complete blood count and electrolyte and liver enzyme levels--can provide insight into the extent of disease. Blood culture results, both aerobic and anaerobic, should be obtained prior to initiating antibiotic therapy.

Imaging studies. Radiographic evaluation of the neck and internal jugular veins can be accomplished in several ways: via venous duplex ultrasonography, CT with IV contrast (in patients with adequate renal function), magnetic resonance imaging (MRI), magnetic resonance venography, nuclear scintigraphy, and gallium-67 scanning.

Although contrast venography is the gold standard, the attendant radiation exposure, invasiveness, and risk of perforation or embolic events might outweigh its utility. Venous duplex ultrasonography is accurate and provides reproducible detection of intraluminal thrombosis or abscess, but its application can be limited by the anatomic location of the clavicle and mandible, as well as variability in the skill level of the technician. Although acute thrombus can be missed because of its low degree of echogenicity, thrombosed veins are typically dilated and incompressible, and they feature either a lack of venous pulsations or a flow that does not vary during sniffing or Valsalva's maneuver. (51) Venous duplex ultrasonography is an inexpensive method of documenting improvement or resolution of thrombosis (figure 5).

The most common modality employed to diagnose internal jugular vein thrombosis is CT with IV contrast. (16) Radiographically, the internal jugular vein will be dilated and there will be a low-attenuation intraluminal content and enhancement of the vessel wall and surrounding tissue. The wall enhancement has been attributed to the uptake of the contrast material by the vasa vasorum.

Although CT does involve radiation exposure and the administration of intravenous contrast, it is rapid and reliable. (51)

MRI provides an excellent delineation of soft tissues without radiation exposure and with the benefit of multiplanar viewing. Some authors attest that magnetic resonance venography is the most accurate and reliable method of detecting the presence and extension venous thrombosis, and its correlation to contrast venography has been reported to be as high as 97%. (12) Neither nuclear scintigraphy nor gallium-67 scanning approaches the reliability and ease of CT, MRI, or magnetic resonance venography. (22, 51)

Treatment. Antibiotic therapy--particularly with a beta-lactamase-resistant compound that provides excellent anaerobic coverage--is the mainstay of treatment. Metronidazole, penicillin, and clindamycin are the most frequently used drug therapies. However, the emergence of beta-lactamase-producing strains can minimize the efficacy of penicillin. Therefore, beta-lactamase-resistant antibiotics are becoming more popular because they typically overcome this type of bacterial resistance. (52) Depending on the severity of the infection, antibiotics should be administered intravenously for 7 to 14 days, followed by an additional 2 to 4 weeks of oral antibiotics. (10)

The use of additional measures--such as surgical drainage of abscesses, ligation of thrombosed vessels, and administration of an anticoagulant--depends on both the severity of the illness and its response to antibiotic treatment. Surgical intervention is indicated if there is a lack of improvement after 48 to 72 hours of intravenous antibiotic therapy, a worsening of systemic illness, or the development of sepsis. Our patient likely benefited from the incision and drainage of his midline neck mass, which was initially presumed to be a thyroglossal duct cyst. Other authors have documented improvement following surgical intervention. (10, 44)

The fact that 11 of the 41 patients (26.8%) in this review improved following the addition of anticoagulation therapy supports its use in cases of extensive thrombosis. (8, 12, 25, 32, 33, 44, 48)

In conclusion, Lemierre's syndrome is less common now than it was during the pre-antibiotic era, but it remains a serious entity. It carries significant morbidity and a low but consistent risk of mortality. Despite intermittent reports of this illness, delays in diagnosis continue to occur. It is our hope that this article will increase awareness of this rare clinical entity and minimize diagnostic and therapeutic delay.

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From the Department of Otolaryngology-Head and Neck Surgery, the Vanderbilt Bill Wilkerson Center for Otolaryngology and Communication Sciences (Dr. Moore and Dr. Werkhaven), and the Department of Medicine (Dr. Dekle), Vanderbilt University Medical Center, Nashville, Tenn.

Reprint requests: Brian A. Moore, MD, Department of Otolaryngology-Head and Neck Surgery, Suite 2900 TVC, Vanderbilt University Medical Center, Nashville, TN 37232-5555. Phone: (615) 322-7267; fax: (615) 343-7604; e-mail: brian.moore@mcmail.vanderbilt.edu

Originally presented at the Southern Section meeting of the Triological Society; Marco Island, Fla.; Jan. 11-13, 2001.

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