Abstract
Lemierre’s syndrome, a forgotten clinical entity, is characterised by septic thrombophlebitis of the internal jugular vein due to oropharyngeal infection. In the past, it was mainly associated with Fusobacterium necrophorum infections. We present a unique case report of Lemierre’s syndrome due to Klebsiella pneumoniae. Patient reported with progressive swelling involving right side of the neck that eventually increased in size. After confirming the diagnosis through CECT, patient was managed through combined medical and surgical therapy in the form of incision and drainage, targeted antibiotic therapy, glycaemic control and anticoagulation therapy. This case report highlights the association of poor glycaemic control in the pathogenesis and the isolation of Klebsiella pneumoniae as the rare organism of Lemierre’s syndrome.
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Introduction
Lemierre’s syndrome, also known as human necrobacillosis, is an anaerobic post-anginal septicaemia. Characterised by septic thrombophlebitis of the internal jugular vein due to oropharyngeal infection, this clinical entity is also complicated by presence of bacteraemia and haematogenous spread of infection via septic emboli [1, 2]. Although the first description of a case of oropharyngeal infection along with jugular vein thrombosis was by Courmont and Cade in 1900 [3], the syndrome was named much later after Andre-Alfred Lemierre in 1936. In the pre-antibiotic era, patients succumbed to the disease within 7–15 days [4]. But the antibiotic era witnessed a decrease in its incidence rate [2, 4], resulting in fewer cases being reported and eventually being recognised as ‘forgotten disease’. Although a synergic infection due to aerobic and anaerobic bacteria has been held accountable for Lemierre syndrome [5, 6], the non-spore forming anaerobe, Fusobacterium necrophorum, has been regarded as the typical pathogen behind Lemierre syndrome [1, 2]. Nevertheless, many clinical studies have isolated other bacteria as well, such as Staphylococcus aureus, Bacteroides species or Klebsiella pneumoniae [1, 2, 7,8,9,10]. Very few cases have been reported till date wherein Klebsiella has been isolated as the causative organism. We present one such extremely rare case report of Lemierre syndrome in an adult with poorly controlled diabetes.
Case presentation
A 48-year-old male diabetic with suboptimal glycaemic control (Hb1ac 11.1%) and no past history of odontogenic infection, initially developed flu like symptoms and sore throat, which was managed with oral antibiotics and supportive therapy. Thereafter, over a period of 1 week, he noticed a progressively increasing swelling, involving right side of neck, causing odynophagia. However, he did not experience fever spikes, productive cough, breathlessness or chest pain. As the swelling worsened, he reported at our tertiary care centre. On examination, he was afebrile, with a unilateral swelling on right side of neck, roughly ovoid in shape with well circumscribed borders, measuring approximately 8 cm × 5 cm in its maximum dimensions. The swelling was extending till the anterior border of sternocleidomastoid, superiorly 2 cm below the lower border of mandible and about 2 cm posterior to midline of neck, and inferiorly, 3 cm above the clavicular region. The overlying skin was normal, with no discharging sinus or local rise of temperature. Swelling was soft and fluctuant in consistency. However, as the disease progressed, the swelling became tender, with firm to hard consistency, accompanied by erythematous changes of the overlying skin and local rise in temperature. Regional lymph nodes examination revealed solitary, non-tender and freely mobile level IB lymph nodes, bilaterally (Fig. 1). The swelling was non-mobile during deglutition and coughing.
Intraorally (Fig. 2), there was mildly erythematous post pharyngeal wall with centrally positioned uvula and multiple infected root stumps of mandible. Bimanual palpation of ipsilateral submandibular and parotid glands was normal, with no clinical features suggestive of facial nerve weakness or dry mouth. The ear lobule was not elevated on frontal view. His haematological investigations showed neutrophilic leucocytosis (total leucocyte count of 12,800 cell/mm3), positive C reactive protein and a positive urine dipstick for ketone bodies.
Ultrasound of neck revealed an ill-defined heterogeneously enhancing hypoechoic lesion, measuring approximately 8.6 cm × 8.9 cm × 9.0 cm in right carotid triangle region of neck, involving level II and III lymph nodes, and encasing right internal jugular vein and thrombus within (4).
Suspecting LS, we proceeded ahead with the gold standard—contrast-enhanced computed tomography (CECT) of neck (5) which revealed central filling defect in internal jugular vein suggestive of thrombosis (Fig. 3a, b), along with medial deviation of right internal carotid artery and homogenously enhancing lymph nodes at level Ia, bilateral Ib, level II and III. The chest roentgenogram did not show any pulmonary infiltrates, which was further confirmed on computed tomography (CT) and contrast angiography was also performed to rule out emboli elsewhere (Fig. 4).
The patient was taken up for incision and drainage of an abscess in the right carotid triangle under general anaesthesia along with management with therapeutic anticoagulant—enoxaparin (to prevent thrombo-embolic complications), parenteral antibiotics, fluid resuscitation, potassium supplementation and insulin infusion. Corrugated rubber drain was secured for irrigation and drainage of exudates. Irrigation and dressing were carried out every 8 hourly till the third post-operative day. The pus samples that were taken intraoperatively revealed pyogenic growth of Klebsiella pneumoniae spp. pneumoniae (Fig. 5), which were sensitive to piperacillin/tazobactam, amikacin, imipenem and meropenem. Following culture report, the patient was subjected to targeted antibiotic therapy and on significant clinical improvement, was discharged on oral antibiotics. On subsequent post-operative follow-up, the patient was asymptomatic and had resolution of his signs and symptoms.
Discussion
Epidemiology
Earlier thought to be a rare disease, Lemierre’s syndrome has witnessed a resurgence of late. This notorious behaviour could possibly be attributed to restriction in the use of antibiotics to treat upper respiratory tract infections, overconsumption of non-steroidal anti-inflammatory drugs during ear, nose and throat (ENT) infections, increasing antibiotic resistance, and injudicious use of corticosteroids [11]. In a prospective epidemiological and clinical survey carried out in Denmark in 2008, an annual incidence of 3–6 cases per million people from 1998 to 2001, with a substantially higher annual rate of 14.4 cases per million people aged 14–24 years, was reported [4, 11, 12]. It has a male predilection with a 2:1 male:female ratio described in literature [11,12,13,14]. It primarily affects adolescents and young adults, with the majority affected (89%) aged between 10 and 35 years [15].
Microbiology
Fusobacterium Necrophorum, which is a part of the normal flora in the oropharynx, genitourinary tract and gastrointestinal tract, has been long regarded as the standing culprit of Lemierre’s syndrome. Other microbes that can be linked are groups A, B, and C Streptococcus, Staphylococcus aureus, Proteus mirabilis, Klebsiella pneumoniae, Pseudomonas aeruginosa, Bacteroids, Eikenella corrodens, Leptotrichia buccalis, Porphyromonas or Prevotella bivia [5] as highlighted in undermentioned table (Table 1).
In previous case reports, K. pneumonia has rarely been reported. Based on few retrospective studies, only 2.5% cases have been reported with K. pneumonia as the causative agent [8]. Similar to our case report, in a study of 2015, eight out of nine patients with Lemierre’s syndrome were associated with K. pneumonia and had poor glycaemic control [17].
Associated pathophysiology
The invasion in the oropharynx due to either of the plethora of microbes highlighted previously result in weakening and mucosal disruption. This can lead to direct local invasion through connective tissue and further inflammation of local lymph nodes, along with hematogenous spread to distant sites. The presence of tonsils seems to be a prerequisite for the anatomical passage of the micro-organisms [16]. In our case, the possible foci are multiple infected root stumps coupled with mucosal breach. The endotoxic lipopolysaccharide (LPS) in the cell wall of F. necrophorum not only causes tissue necrosis but also simulates encapsulation of the infection focus by fibrous connective tissue [18]. Moreover, it sticks to epithelial cells and gains access to tissues through plasmin (fibrinolytic enzyme) [19]. Through factor H and a protein that impairs the recruitment of white blood cells (WBCs) to the site of infection, F. necrophorum has the potential of deceiving the innate immunity of the infected individual. To relate to our case report, patients with poor glycemic control have decreased neutrophilic activity, thereby increasing the susceptibility to various infections [20]. Moreover, the hypermucoviscosity phenotype of K. pneumoniae, especially K1/K2 isolates, are resistant to phagocytosis [21]. The phagocytosis of virulent K1/K2 K. pneumonia is reduced significantly in patients with poor glycemic control [22]. Elaboration of hemagglutinin by the causative bacteria results in formation of thrombus, another pathognomic feature of Lemierre’s syndrome. Russo et al [23] highlighted more frequent metastatic spread in the K1/K2 group of K. pneumonia. Hypervirulent Klebsiella pneumoniae (hvKp) is an increasingly recognized pathotype of Klebsiella pneumoniae, characterized clinically in causing various life-threatening infections in healthy hosts [23]. The hypervirulent strain is differentiated from classical K. pneumoniae (cKp), which is most common in Western countries, by its acquisition of a few virulence factors encoded on a virulence plasmid and other mobile chromosomally integrated genetic elements. Clinically, cKp primarily affects people in the hospital setting with comorbid conditions rather than healthy individuals [23]. The mucoviscosity of the strain’s thick capsules persist in the bloodstream, resulting in greater aggregation of bacterial cells to form thrombi [23]. The pathophysiology along with contributing factors is highlighted in Flow Chart 1.
Signs and symptoms
The clinical presentation of Lemierre’s syndrome can be broadly explained in three phases:
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1.
Oropharynx involvement: Sore throat is usually the most common clinical presentation, often preceded to the symptoms of jugular thrombophlebitis by at least 3–4 days. Dysphagia, tonsillitis, pharyngitis, loss of appetite or nausea has been commonly reported. Due to ongoing bacteraemia, fever with chills usually accompanies [1, 2]. While our case did not report any febrile episodes, there was a positive history of contracting sore throat which was managed through empirical antibiotics.
-
2.
Internal jugular vein thrombophlebitis: Similar to our case, a painful, tender neck mass follows the thrombophlebitis of internal jugular vein and inflammation of the surrounding soft tissues. An area of induration, oedema and erythema can present over or parallel to sternocleidomastoid muscle [23]. Cord sign, identified by swelling and tenderness over one side at the mandibular angle, is noted in 25 to 40% of cases [24].
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3.
Distant septic metastasis: Lungs are primarily affected by this spread. These patients usually present with symptoms of productive cough, chest pain, contaminated breath, along with haemoptysis [25]. Involvement of various joints presents with arthralgias of knee or shoulder joints and sometimes even as osteomyelitis. Hepatic involvement is presented as jaundice, hepatomegaly and liver abscess [26]. Further spread to the brain presents with palsies of VI and XII cranial nerves, and in its most complicated forms, cases of epidural abscess have also been reported in literature [7,8,9,10]. Fortunately, due to prompt diagnosis and timely intervention through incision and drainage, coupled with targeted antibiotic therapy, our patient was spared of such potentially lethal consequences.
Diagnostic modalities
A detailed clinical history coupled with thorough clinical examination forms the cornerstone in the diagnosis of Lemierre’s syndrome. The diagnostic criteria were suggested by Sinave et al in 1989 [28]: (1) Primary infection of the oropharynx; (2) Sepsis with at least one bacteria identified on a blood culture; (3) Clinical or imaging findings of IJV thrombosis; and (4) At least one metastasis.
Various laboratory tests can be employed in further assessing and confirming the diagnosis include haematology (CRP, ESR, CBC for leukopenia or leucocytosis, thrombocytopenia), LFT/RFT (elevated hepatic enzymes, bilirubin, creatininemia, lactate assay), coagulation studies, blood cultures for isolation of etiological bacteria, etc. The technological advancement in the field of medical diagnostic aids have further contributed in precise understanding of the anatomical location and clear visualization of the condition. Computed tomography (CT) scans with contrast enable the treating surgeon to access the location of infection, evaluate the presence of septic thrombosis of various veins involved, presence of pulmonary emboli, empyema, osteomyelitis, and brain or epidural abscess; hence considered as investigation of choice [29]. Ultrasound Doppler, an extremely fast and non-invasive procedure, provides clear image of blood clots around IJV (shown as an echogenic region with dilated IJV or a complex mass of cystic and solid components) [30, 31] and allows the evaluation of rate of blood flow inside vessels to detect any stasis. MRI, another very sensitive diagnostic modality, can be used for ruling out if any thrombi is present along and inside the IJV and in suspected cases of osteomyelitis due to distant septic thrombosis [26]. Since lungs are the most common target organs for distant emboli, chest radiographs are useful in assessing any consolidation, abscess formation or emphysema.
Management
Treatment of Lemierre’s syndrome warrants a multidisciplinary approach. Association with pharmacologists, infectious disease experts, radiologists, otolaryngologists and thoracic surgeons is crucial to aid in prompt diagnosis and formulate the best treatment plan [4, 29]. The management centres around use of appropriate antibiotics along with surgical drainage of the formed abscess.
Empirical antibiotics include penicillin/beta-lactamase inhibitors, penicillin plus metronidazole or a carbapenem. On subsequent antibiotic sensitivity reports, targeted therapy should be initiated. We used piperacillin-tazobactam along with metronidazole and amikacin. Our antibiotic sensitive test was suggestive of Klebsiella pneumoniae growth, which was sensitive to piperacillin-tazobactam, amikacin, imipenem and meropenem.
The role of anticoagulants in the management of Lemierre’s syndrome has not been very well explained. Main rationale behind advocating the use of anticoagulants is to stop the spread of thrombi, especially inside central nervous system to prevent lethal complications. Low molecular weight heparin and also warfarin are used in anticoagulation therapy. The most common indications enumerating use of anticoagulation is highlighted in Table 2. Not only it helps to prevent the spread, but also stops the formation of new thrombus [31]. But the use of anticoagulants is also linked with increased risk of haemorrhagic complications, which further explains it as being a long-debated topic. Few anecdotal reports suggest that anticoagulation plays a part in preventing septic embolic events originating from IJV thrombosis [29, 32,33,34,35]. An observational study of cases treated with heparin for septic pelvic thrombophlebitis showed clinical resolution within a week in 42 out of 46 patients [33].
Surgical decompression by incision and drainage, as employed in our case, helps reduce bacterial load and prevents further spread of infection.
Our management strategy was based on sound review of literature which addressed cases with similar presenting signs and symptoms that were managed with combined medical therapy and surgical drainage with a favourable outcome over longest follow-up of 6 months as highlighted in Table 3.
Conclusion
Lemierre’s syndrome is a potentially lethal bacterial infection, initially involving the oropharynx with progressive involvement of IJV in the form of thrombophlebitis. Prompt diagnosis and early intervention in the form of appropriate antibiotics, surgical decompression and anticoagulation therapy is crucial in preventing the associated morality. While majority of cases in literature have targeted F. necrophorum as the most isolated causative microbe, atypical Lemierre’s syndrome due to K. pneumoniae must be suspected when this typical strain is not isolated. This rare case report highlights and supports the literature (Table 3) in isolation of Klebsiella pneumoniae as the rare and emerging causative species of Lemierre’s syndrome, its prompt diagnosis with inter-disciplinary team approach and targeted antibiotic therapy with a favourable outcome on long-term follow-up.
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Rangan, N.M., Singh, A.K., Yadav, R.C. et al. Lemierre syndrome due to Klebsiella pneumoniae: a rare case report with review of literature. J Rare Dis 3, 30 (2024). https://doi.org/10.1007/s44162-024-00054-x
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DOI: https://doi.org/10.1007/s44162-024-00054-x