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Eur Arch Otorhinolaryngol
Eur Arch Otorhinolaryngol
European Archives of Oto-Rhino-Laryngology
0937-4477
1434-4726
Springer Berlin Heidelberg Berlin/Heidelberg

38839700
8767
10.1007/s00405-024-08767-x
Head and Neck
Epstein-Barr virus as promoter of Lemierre syndrome: systematic literature review
Delcò Alessia A. 1
Montorfani Sara M. M. A. 1
Gualtieri Renato 1
Lava Sebastiano A. G. 23
http://orcid.org/0000-0003-3829-4254
Milani Gregorio P. gregorio.milani@unimi.it

45
Bianchetti Mario G. 1
Bronz Gabriel 1
Faré Pietro B. 16
Kottanattu Lisa 78
1 https://ror.org/03c4atk17 grid.29078.34 0000 0001 2203 2861 Family Medicine, Faculty of Biomedical Sciences, Università Della Svizzera Italiana, Lugano, Switzerland
2 https://ror.org/05a353079 grid.8515.9 0000 0001 0423 4662 Pediatric Cardiology Unit, Department of Pediatrics, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
3 https://ror.org/05a353079 grid.8515.9 0000 0001 0423 4662 Clinical Pharmacology Service, Centre Hospitalier Universitaire Vaudois and University of Lausanne, Lausanne, Switzerland
4 https://ror.org/016zn0y21 grid.414818.0 0000 0004 1757 8749 Pediatric Unit, Fondazione IRCCS Ca’ Granda Ospedale Maggiore Policlinico, Via Della Commenda 9, 20122 Milan, Italy
5 https://ror.org/00wjc7c48 grid.4708.b 0000 0004 1757 2822 Department of Clinical Sciences and Community Health, Università Degli Studi Di Milano, Milan, Italy
6 https://ror.org/01462r250 grid.412004.3 0000 0004 0478 9977 Department of Infectious Diseases and Hospital Epidemiology, University Hospital Zurich, Zurich, Switzerland
7 https://ror.org/00sh19a92 grid.469433.f 0000 0004 0514 7845 Pediatric Institute of Southern Switzerland, Ente Ospedaliero Cantonale, Bellinzona, Switzerland
8 https://ror.org/03c4atk17 grid.29078.34 0000 0001 2203 2861 Faculty of Biomedical Sciences, Università Della Svizzera Italiana, Lugano, Switzerland
5 6 2024
5 6 2024
2024
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26 5 2024
© The Author(s) 2024
2024
https://creativecommons.org/licenses/by/4.0/ Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
Purpose

To investigate a possible link between acute Epstein-Barr virus infection and Lemierre syndrome, a rare yet life-threatening infection.

Methods

A systematic review was conducted adhering to the 2020 Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. Diagnosis criteria for Lemierre syndrome were established, and data extraction encompassed demographic data, clinical, and laboratory information.

Results

Out of 985 initially identified papers, 132 articles were selected for the final analysis. They reported on 151 cases of Lemierre syndrome (76 female and 75 male patients with a median of 18 years) alongside interpretable results for Epstein-Barr virus serology. Among these, 38 cases (25%) tested positive for acute Epstein-Barr virus serology. There were no differences in terms of age, sex, or Fusobacterium presence between the serologically positive and negative groups. Conversely, instances of cervical thrombophlebitis and pulmonary complications were significantly higher (P = 0.0001) among those testing negative. The disease course was lethal in one case for each of the two groups.

Conclusions

This analysis provides evidence of an association between acute Epstein-Barr virus infection and Lemierre syndrome. Raising awareness of this link within the medical community is desirable.

Supplementary Information

The online version contains supplementary material available at 10.1007/s00405-024-08767-x.

Keywords

Epstein-Barr virus
Human herpesvirus 4
Lemierre syndrome
Necrobacillosis
Postanginal sepsis
http://dx.doi.org/10.13039/501100003196 Ministero della Salute Ricerca Corrente Milani Gregorio P. Università degli Studi di MilanoOpen access funding provided by Università degli Studi di Milano within the CRUI-CARE Agreement.

issue-copyright-statement© Springer-Verlag GmbH Germany, part of Springer Nature 2024
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pmcIntroduction

Lemierre syndrome, also known as postanginal sepsis or necrobacillosis, is an infrequent yet potentially fatal infection, that usually affects immunocompetent individuals. It is characterized by an acute oropharyngeal inflammation, which is followed by a septic cervical (mostly jugular) thrombophlebitis, which, in turn, leads to the dissemination of septic emboli [1–4]. Fusobacterium species, part of the oral microbiota, are the primary causative agents [1–4]. The condition was initially documented in 1900 by Paul Courmont [5], followed by Mark S. Reuben in 1936 [6]. However, André Lemierre in France provided the most detailed description in 1936 [7].

Viral agents may compromise mucous membrane integrity, providing an entry point for bacterial pathogens and increasing the susceptibility to various invasive infections, including those caused by meningococci [8, 9]. A link between acute infection caused by the human herpes virus 4, also known as Epstein-Barr virus [10, 11], and Lemierre syndrome has been suggested [3]. This report aims to systematically explore this association.

Methods

This systematic review (registered on INPALSY, number 202410102) adhered to the 2020 edition of the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [12]. The data were sourced from Web of Science, the United States National Library of Medicine, and Excerpta Medica. The search strategy focused on the term "Lemierre syndrome" across the three databases. Additionally, articles identified in the references of retrieved records, reports available in Google Scholar, and articles already familiar to the authors were included [13]. The searches were conducted in July 2023 and repeated prior to submission (February 28, 2024).

Eligible were reports of apparently immunocompetent patients with a diagnosis of Lemierre syndrome and with either a positive or negative serology for Epstein-Barr virus.

Since a formal case definition for Lemierre syndrome has not yet been established [1–4], we established this diagnosis in patients with an acute onset pharyngeal inflammation associated with (a) isolation of Fusobacterium species from a blood culture or a normally sterile site, or (b) a cervical thrombophlebitis associated with one of the following features: pulmonary involvement (infiltrates, septic emboli, abscesses, or empyema; an isolated pleural effusion was not considered sufficient to define lung impairment); metastatic extra-pulmonary involvement such as abscesses or septic emboli; or isolation of a germ other than Fusobacterium from a blood culture or a normally sterile site. Cases of Lemierre syndrome temporally associated with a urogenital infection, or surgery were excluded. Cases related to a significant odontogenic infection were also not included [14]. A local spread of the oropharyngeal infection was not regarded as systemic involvement in the diagnosis of Lemierre syndrome.

Patients with a positive Paul-Bunnell-Davidsohn heterophile test, IgM and IgG antibodies to the Epstein-Barr viral capsid, or IgG antibodies to the early Epstein-Barr viral antigen were deemed to have a positive serology for acute Epstein-Barr Virus infection [10, 11]. Conversely, the serology for acute Epstein-Barr Virus infection was considered negative in cases with isolated IgG antibodies to the Epstein-Barr viral capsid; negativity for IgM antibodies to the Epstein-Barr viral capsid; positivity for IgG to Epstein-Barr virus nuclear antigen; or negative Paul-Bunnell-Davidsohn test [10, 11]. Cases that were reported as serologically positive respectively negative for an acute Epstein-Barr virus infection but lacked information regarding the performed serological tests were also included. For both Epstein-Barr virus positive and negative cases, demographic details, clinical and laboratory data, and outcomes were collected.

Two authors in duplicate conducted the literature search, selected eligible studies, extracted data, and assessed the comprehensiveness of each included case. Disagreements were resolved through discussions, involving a senior author if needed. One author inputted data into a worksheet, and the second author verified data accuracy.

The omnibus normality test disclosed that continuous variables were not normally distributed [15]. Hence, the latter are presented as median and interquartile range, and their analysis was conducted using the Mann–Whitney-Wilcoxon test for two independent samples [16]. Categorical variables are expressed as counts and were analyzed by means of the Fisher exact test [16]. A significance level was assigned at < 0.05 for a two-sided P-value.

Results

The literature search process is outlined in Fig. 1. The full-text of 1001 papers was assessed. For the final analysis, we included 132 articles [see: supplementary document] published after 1979: 70 from America (United States of America, N = 64; Canada, N = 5; Jamaica, N = 1), 53 from Europe (United Kingdom, N = 15; Germany, N = 6; France, N = 5; Greece, N = 5; Spain, N = 4; Denmark, N = 3; Netherlands, N = 3; Belgium, N = 2; Italy, N = 2; Portugal, N = 2; Sweden, N = 2; Switzerland, N = 2; Austria, N = 1; Norway, N = 1) and 9 from Asia (Türkiye, N = 3; Israel, N = 2; Japan, N = 2; Pakistan, N = 1; Sri Lanka, N = 1). One hundred twenty-two articles were written in English, three in French, three in German, two in Spanish, and each one in Norwegian and Swedish. The mentioned 132 articles [15–146] described subjects with a Lemierre syndrome and an interpretable serology for Epstein-Barr virus.Fig. 1 Epstein-Barr virus as promoter of Lemierre syndrome. Flowchart of the literature search

The mentioned reports provided information about 151 cases of Lemierre syndrome (76 female and 75 male individuals 18 [16–23] years of age) with an interpretable serology for Epstein-Barr virus infection (Table 1). The acute Epstein-Barr virus serology was positive in 38 (25%) and negative in 113 (75%) cases. Cases with and without serological evidence of acute Epstein-Barr virus infection did not significantly differ with respect to female-male-ratio, age, positivity for Fusobacterium species or extrapulmonary involvement. A cervical thrombophlebitis (75% versus 39%) and a pulmonary involvement (87% versus 55%) were more frequently (P = 0.0001) observed in cases with a negative acute Epstein-Barr virus serology. The disease course was lethal in one case for each of the two groups.Table 1 Clinical features in 151 patients (ranging in age from 3.5 to 70 years) affected by Lemierre syndrome with and without laboratory features consistent with an acute Epstein-Barr virus infection

	All cases	Serology for Acute Epstein-Barr Virus Infection	P–values&	
Positive	Negative	
N (%)	151 (100)	38 (25)	113 (75)		
Demographics	
 Females: males, N (%)	76 (50): 75 (50)	23 (61): 15 (39)	53 (47): 60 (53)	0.1894	
 Age, years	18 [16–23]	19 [17–21]	18 [16–23]	0.7864	
Fusobacterium species positivity, N (%)	121 (80)	33 (87)	88 (78)	0.3468	
Cervical vessel thrombophlebitis, N (%)	100 (66)	15 (39)	85 (75)	0.0001	
Pulmonary involvement, N (%)	119 (79)	21 (55)	98 (87)	0.0001	
 Pneumonia, N (%)	91 (60)	12 (32)	79 (70)	0.0001	
 Abscess, N (%)	46 (30)	7 (18)	39 (36)	0.0694	
 Septic emboli, N (%)	44 (29)	7 (18)	37 (33)	0.1031	
 Empyema, N (%)	6 (4.0)	2 (5.3)	4 (3.5)	0.6417	
Extrapulmonary involvement, N (%)	41 (27)	12 (32)	29 (26)	0.5290	
 Central nervous system, N (%)	16 (11)	6 (16)	10 (8.8)	0.2345	
 Musculoskeletal system, N (%)	16 (11)	6 (16)	10 (8.8)	0.2345	
 Hepatobiliary system, N (%)	10 (6.6)	2 (5.3)	8 (7.1)	 > 0.9999	
 Further systems, N (%)**	7 (4.6)	2 (5.3)	5 (4.4)	 > 0.9999	
Death, N (%)	2 (1.3)	1 (2.6)	1 (0.9)	0.4412	
Data are presented either as frequency (with percentage) or as median (with interquartile range)

**splenic abscess (N = 3), endocarditis (N = 3), renal abscess (N = 1), skin emboli (N = 1). &Significant p-values are in bold

The serology for acute Epstein-Barr virus infection was never positive in individuals ≤ 10 and ≥ 41 years of age (Fig. 2).Fig. 2 Age distribution of patients with Lemierre syndrome and positive serology for an acute Epstein-Barr virus infection

Discussion

Lemierre syndrome [1–4] and Epstein-Barr virus [10, 11] infectious mononucleosis predominantly occur in otherwise healthy teenagers and young adults. A link between Lemierre syndrome and serological evidence of acute Epstein-Barr virus infection was first proposed in the eighties of last century [3]. In this analysis of the literature, we identified a positive serology for an acute Epstein-Barr virus infection in 38 (25%) out of 151 patients diagnosed with Lemierre syndrome. Hence, these data allow to infer that Epstein-Barr virus infection may sporadically predispose individuals to develop Lemierre syndrome.

At least two mechanisms might underly the link between Epstein-Barr virus infection and Lemierre syndrome. Firstly, there is a higher prevalence of Fusobacterium positivity in individuals with infectious mononucleosis as opposed to those who are healthy [17]. Furthermore, in instances where the Fusobacterium swab yields positive results, the bacterial load is elevated in patients with infectious mononucleosis [17]. Secondly, the infiltration of bacteria into the tonsillar epithelium is increased in individuals with Epstein-Barr virus infectious mononucleosis [18].

Cervical thrombophlebitis and pulmonary involvement occurred more frequently in instances where there was a negative acute Epstein-Barr virus serology. The reasons behind this observation remain unexplained.

This analysis exhibits both limitations and strengths. The main weakness is the limited dataset: only 151 instances of Lemierre syndrome with associated Epstein-Barr virus serology were detected, highlighting the need for broader, prospective research. However, the rarity of this condition, evidenced by a Danish report of an incidence rate of 3.6 per million annually [19], complicates such research efforts. In contrast, the study’s strengths include adherence to established methodologies and the comprehensive analysis of data from three distinct databases.

Conclusion

This literature review, taken together with experimental data [127, 18], support the link between Epstein-Barr virus infectious mononucleosis and Lemierre syndrome, highlighting the importance of increasing awareness within the medical community. Even though it is rare, healthcare providers should keep Lemierre syndrome in mind when infectious mononucleosis patients acutely present with high fever, deterioration of general well-being, unilateral neck pain, or shortness of breath.

Supplementary Information

Below is the link to the electronic supplementary material.Supplementary file1 (DOCX 38 KB)

Acknowledgements

We gratefully dedicate this work to the memory of Professor Jürg Pfenninger (15 October 1943 – 25 August 2014), who made us aware of the possible connection between Epstein-Barr mononucleosis and Lemierre syndrome.

Author contributions

Conceptualization: AAD, SMMAM, RG, SAGL, GPM, MGB, GB; Formal analysis: AAD, SMMAM; Project administration: SAGL, GPM, MGB; Supervision: PBF, LK; Original draft of the manuscript: AAD, SMMAM, MGB, PBF, LK; Review and editing of the manuscript: all authors.

Funding

Open access funding provided by Università degli Studi di Milano within the CRUI-CARE Agreement. The study was partially funded by the Italian Ministry of Health (Ricerca Corrente).

Data availability

Data sharing is not applicable to this article as no new data were generated in this study.

Declarations

Conflict of interest

The authors declare that there are no competing interests relevant to the content of this article. The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Ethical approval.

The study was performed in accordance with ethical standards as laid down in the 1964 Helsinki Declaration.

Consent for participation

Not applicable (literature review).

Consent for publication

Not applicable (literature review).

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Alessia A. Delcò and Sara M. M. A. Montorfani have contributed equally to the work (co-first authors).

Pietro B. Faré and Lisa Kottanattu have contributed equally to the work (co-last authors).
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References

1. Sinave CP Hardy GJ Fardy PW The Lemierre syndrome: suppurative thrombophlebitis of the internal jugular vein secondary to oropharyngeal infection Medicine (Baltimore) 1989 68 2 85 94 10.1097/00005792-198903000-00002 2646510
Sinave CP, Hardy GJ, Fardy PW (1989) The Lemierre syndrome: suppurative thrombophlebitis of the internal jugular vein secondary to oropharyngeal infection. Medicine (Baltimore) 68(2):85–942646510
2. Chirinos JA Lichtstein DM Garcia J Tamariz LJ The evolution of Lemierre syndrome: report of 2 cases and review of the literature Medicine (Baltimore) 2002 81 6 458 465 10.1097/00005792-200211000-00006 12441902
Chirinos JA, Lichtstein DM, Garcia J, Tamariz LJ (2002) The evolution of Lemierre syndrome: report of 2 cases and review of the literature. Medicine (Baltimore) 81(6):458–465. 10.1097/00005792-200211000-0000612441902
3. Riordan T Human infection with Fusobacterium necrophorum (Necrobacillosis), with a focus on Lemierre's syndrome Clin Microbiol Rev 2007 20 4 622 659 10.1128/CMR.00011-07 17934077
Riordan T (2007) Human infection with Fusobacterium necrophorum (Necrobacillosis), with a focus on Lemierre’s syndrome. Clin Microbiol Rev 20(4):622–659. 10.1128/CMR.00011-0717934077
4. Wright WF Shiner CN Ribes JA Lemierre syndrome South Med J 2012 105 5 283 288 10.1097/SMJ.0b013e31825581ef 22561543
Wright WF, Shiner CN, Ribes JA (2012) Lemierre syndrome. South Med J 105(5):283–288. 10.1097/SMJ.0b013e31825581ef22561543
5. Courmont P Cade A Sur une septico-pyohémie de l’homme simulant la peste et causée par un strepto-bacille anaérobie Arch Med Exp Anat Pathol 1900 12 4 393 418
Courmont P, Cade A (1900) Sur une septico-pyohémie de l’homme simulant la peste et causée par un strepto-bacille anaérobie. Arch Med Exp Anat Pathol 12(4):393–418
6. Reuben MS Post-anginal sepsis: sepsis of oro-naso-pharyngeal origin Arch Dis Child 1931 6 32 115 128 10.1136/adc.6.32.115 21031841
Reuben MS (1931) Post-anginal sepsis: sepsis of oro-naso-pharyngeal origin. Arch Dis Child 6(32):115–128. 10.1136/adc.6.32.11521031841
7. Lemierre A On certain septicaemias du to anaerobic organisms Lancet 1936 227 5874 701 703 10.1016/S0140-6736(00)57035-4
Lemierre A (1936) On certain septicaemias du to anaerobic organisms. Lancet 227(5874):701–703. 10.1016/S0140-6736(00)57035-4
8. Cartwright KA Jones DM Smith AJ Stuart JM Kaczmarski EB Palmer SR Influenza A and meningococcal disease Lancet 1991 338 8766 554 557 10.1016/0140-6736(91)91112-8 1678811
Cartwright KA, Jones DM, Smith AJ, Stuart JM, Kaczmarski EB, Palmer SR (1991) Influenza A and meningococcal disease. Lancet 338(8766):554–557. 10.1016/0140-6736(91)91112-81678811
9. Salomon A Berry I Tuite AR Drews S Hatchette T Jamieson F Johnson C Kwong J Lina B Lojo J Mosnier A Ng V Vanhems P Fisman DN Influenza increases invasive meningococcal disease risk in temperate countries Clin Microbiol Infect 2020 26 9 1257.e1 1257.e7 10.1016/j.cmi.2020.01.004 31935565
Salomon A, Berry I, Tuite AR, Drews S, Hatchette T, Jamieson F, Johnson C, Kwong J, Lina B, Lojo J, Mosnier A, Ng V, Vanhems P, Fisman DN (2020) Influenza increases invasive meningococcal disease risk in temperate countries. Clin Microbiol Infect 26(9):1257.e1-1257.e7. 10.1016/j.cmi.2020.01.00431935565
10. Jenson HB Epstein-Barr virus Pediatr Rev 2011 32 9 375 384 10.1542/pir.32-9-375 21885661
Jenson HB (2011) Epstein-Barr virus. Pediatr Rev 32(9):375–384. 10.1542/pir.32-9-37521885661
11. Balfour HH Jr Dunmire SK Hogquist KA Infectious mononucleosis Clin Transl Immunol 2015 4 2 33 10.1038/cti.2015
Balfour HH Jr, Dunmire SK, Hogquist KA (2015) Infectious mononucleosis. Clin Transl Immunol 4(2):33. 10.1038/cti.2015
12. Page MJ McKenzie JE Bossuyt PM Boutron I Hoffmann TC Mulrow CD Shamseer L Tetzlaff JM Akl EA Brennan SE Chou R Glanville J Grimshaw JM Hróbjartsson A Lalu MM Li T Loder EW Mayo-Wilson E McDonald S McGuinness LA Stewart LA Thomas J Tricco AC Welch VA Whiting P Moher D The PRISMA 2020 statement: an updated guideline for reporting systematic reviews J Clin Epidemiol 2021 134 178 189 10.1016/j.jclinepi.2021.03.001 33789819
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, Shamseer L, Tetzlaff JM, Akl EA, Brennan SE, Chou R, Glanville J, Grimshaw JM, Hróbjartsson A, Lalu MM, Li T, Loder EW, Mayo-Wilson E, McDonald S, McGuinness LA, Stewart LA, Thomas J, Tricco AC, Welch VA, Whiting P, Moher D (2021) The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. J Clin Epidemiol 134:178–189. 10.1016/j.jclinepi.2021.03.00133789819
13. Haddaway NR Collins AM Coughlin D Kirk S The role of Google Scholar in evidence reviews and its applicability to grey literature searching PLoS ONE 2015 10 9 e0138237 10.1371/journal.pone.0138237 26379270
Haddaway NR, Collins AM, Coughlin D, Kirk S (2015) The role of Google Scholar in evidence reviews and its applicability to grey literature searching. PLoS ONE 10(9):e0138237. 10.1371/journal.pone.013823726379270
14. Ogle OE Odontogenic infections Dent Clin North Am 2017 61 2 235 252 10.1016/j.cden.2016.11.004 28317564
Ogle OE (2017) Odontogenic infections. Dent Clin North Am 61(2):235–252. 10.1016/j.cden.2016.11.00428317564
15. Poitras G More on the correct use of omnibus tests for normality Econ Lett 2006 90 3 304 309 10.1016/j.econlet.2005.08.016
Poitras G (2006) More on the correct use of omnibus tests for normality. Econ Lett 90(3):304–309. 10.1016/j.econlet.2005.08.016
16. Brown GW Hayden GF Nonparametric methods. Clinical applications Clin Pediatr (Phila) 1985 24 9 490 498 10.1177/000992288502400905 4017399
Brown GW, Hayden GF (1985) Nonparametric methods. Clinical applications. Clin Pediatr (Phila) 24(9):490–498. 10.1177/0009922885024009054017399
17. Jensen A Hagelskjaer Kristensen L Prag J Detection of Fusobacterium necrophorum subsp. funduliforme in tonsillitis in young adults by real-time PCR Clin Microbiol Infect. 2007 13 7 695 701 10.1111/j.1469-0691.2007 17403128
Jensen A, Hagelskjaer Kristensen L, Prag J (2007) Detection of Fusobacterium necrophorum subsp. funduliforme in tonsillitis in young adults by real-time PCR. Clin Microbiol Infect. 13(7):695–701. 10.1111/j.1469-0691.200717403128
18. Stenfors LE Bye HM Räisänen S Myklebust R Bacterial penetration into tonsillar surface epithelium during infectious mononucleosis J Laryngol Otol 2000 114 11 848 852 10.1258/0022215001904149 11144834
Stenfors LE, Bye HM, Räisänen S, Myklebust R (2000) Bacterial penetration into tonsillar surface epithelium during infectious mononucleosis. J Laryngol Otol 114(11):848–852. 10.1258/002221500190414911144834
19. Hagelskjaer LH Prag J Malczynski J Kristensen JH Incidence and clinical epidemiology of necrobacillosis, including Lemierre's syndrome, in Denmark 1990–1995 Eur J Clin Microbiol Infect Dis 1998 17 8 561 565 10.1007/BF01708619 9796654
Hagelskjaer LH, Prag J, Malczynski J, Kristensen JH (1998) Incidence and clinical epidemiology of necrobacillosis, including Lemierre’s syndrome, in Denmark 1990–1995. Eur J Clin Microbiol Infect Dis 17(8):561–565. 10.1007/BF017086199796654
