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Prevalence of Fusobacterium necrophorum in

tonsils from patients with chronic tonsillitis

Anna Dapefrid, Birgitta Lundström & Krister Tano

To cite this article: Anna Dapefrid, Birgitta Lundström & Krister Tano (2016): Prevalence
of Fusobacterium necrophorum in tonsils from patients with chronic tonsillitis, Acta Oto-
Laryngologica, DOI: 10.1080/00016489.2016.1229024

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Published online: 23 Sep 2016.

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Download by: [Cornell University Library] Date: 25 September 2016, At: 21:21


Prevalence of Fusobacterium necrophorum in tonsils from patients with

chronic tonsillitis
€mb and Krister Tanoa
Anna Dapefrida, Birgitta Lundstro
Department of Clinical Sciences, Otorhinolaryngology, Umeå University, Umeå, Sweden; bDepartment of Clinical Microbiology, Sunderby
Hospital, Umeå University, Umeå, Sweden


Conclusion: There was a high prevalence of Fusobacterium necrophorum (FN) in patients with chronic Received 21 June 2016
tonsillitis in the age group 15–23 years. This indicates that FN might play an important role in the Revised 11 August 2016
pathogenesis of chronic tonsillitis in this age group, which is also the age group in which chronic or Accepted 15 August 2016
recurrent tonsillitis is most common. Published online 22 Septem-
ber 2016
Objectives: The role of FN in patients with acute and chronic tonsillitis is unclear. Thus, this study
investigated the occurrence of FN in tonsils of patients with chronic tonsillitis. The aim of the study KEYWORDS
was to determine the prevalence of FN in patients that underwent tonsillectomy due to chronic tonsil- Tonsillectomy; human
litis. This study also investigated if FN was found at different areas in the tonsils. tonsils; bacterial culture;
Method: One hundred and twenty-six consecutive patients undergoing tonsillectomy due to chronic streptococci
tonsillitis were included from the ENT clinics at Sunderby Hospital and G€allivare Hospital, Sweden. Both
children and adults were included to encompass various age groups (age ¼2–57 years). Culture swabs
were taken from three different levels of the tonsils – the surface, the crypts, and the inner core of the
tonsils. Selective agar plates for detecting FN were used for culture. Culture was also made for detect-
ing b-hemolytic streptococci, Haemophilus influenzae, and Arcanobacterium.
Results: FN was the most common pathogen (19%). The highest prevalence of FN was found in the
age group 15–23 years (in 34% of the patients). FN was detected both at the surface and in the core
of the tonsils. Furthermore, in the few patients where FN was not detected in all three areas, FN was
always detected at the tonsillar surface, in spite of being an anaerobic bacterium. Streptococci group
G and C also occurred most frequently (30%) in the same age group as FN (15–23 years), whereas
Streptococci group A was more evenly spread among the age groups.

Introduction peritonsillar abscess development, and to prevent the infec-

tion from spreading deep into the tissues in the neck to
Fusobacterium necrophorum (FN) is a gram-negative bacter-
thereby cause Lemierre’s syndrome; in other words attempts
ium that causes the life threatening disease Lemierre’s syn-
are made to limit it to a local throat infection [9,10].
drome that refers to thrombosis of the internal jugular vein Patients with long-term symptoms of chronic/recurrent
and septic embolies to other organs such as the lungs [1]. tonsillitis are commonly young adults, and one of the most
The disease is often preceded by a throat infection. common surgical procedures at an ENT department is ton-
Nowadays, FN is reported in patients with acute throat sillectomy due to chronic symptoms from the throat.
infections [2,3], patients with chronic/recurrent tonsillitis Tonsillectomies due to chronic/recurrent tonsillitis are per-
[4], patients with peritonsillar abscesses [5], as well as in formed in all age groups, which allow the opportunity to
healthy persons [3,6]. It also appears that FN may be more study the prevalence of FN over age groups. In addition, it
frequent in patients with chronic disease than in those with is possible to examine the tonsils more thoroughly with a
acute throat infections [4]. Several studies have reported that tonsillectomy than with a normal throat swab. Since FN is
the prevalence of FN is highest among young adults an anaerobic bacterium, one would suspect that it is easier
[3,4,7,8]; however, evidence is still lacking regarding the to find the bacterium deep in the core of the tonsils, and
importance of FN among young people with acute or not primarily on the surface of the tonsils, which in turn
chronic tonsillitis. In the clinical situation, doctors meeting could make it difficult to perform comparisons with control
patients with tonsillitis are mostly concerned with Group A groups where the sampling is only performed superficially
Streptococci (GAS), and, thus, rapid detection tests are in the throat.
focused primarily on GAS. In the present study we took FN samples from three dif-
The rationale of treating FN in throat infections would ferent levels – the surface, deep in the crypts, and in the
be to shorten the duration of symptoms, to prevent core of the tonsils, in order to detect where in the tonsils

CONTACT Anna Dapefrid, MD Department of Clinical Sciences, Otorhinolaryngology, Umeå University, Sunderby Hospital, SE 971 80
Luleå, Sweden
ß 2016 Acta Oto-Laryngologica AB (Ltd)

one could find FN and also to determine how common FN the surgeon divided the tonsils with a knife and swept a
is among patients undergoing surgery due to chronic swab over the core of the tonsils, carefully avoiding the sur-
tonsillitis. face of the tonsil. All three swabs were placed in Amies Gel
medium with charcoal for transport (Copan Brescia, Italy)
and sent immediately to the Microbiological Laboratory at
Materials and method Sunderby Hospital for detection of FN (ssp. funduliforme),
Patients at the ENT Department in the County of Arcanobacterium haemolyticum, Non-typeable H. influenzae
Norrbotten that were scheduled for tonsillectomy due to and b-hemolytic streptococci. The samples were cultured
chronic or recurrent tonsillitis (ICD 10 ¼ J 35.0) were con- within the same day if they were sampled at Sunderby
secutively included. The diagnosis was made by the surgeon Hospital and within 24 hours if they were sampled at
and was based on the patient history and medical records. G€allivare Hospital.
The inclusion period was January 30, 2012–December 18,
2012. During this time period 139 tonsillectomies (TE) were Method of culture
performed in the County of Norrbotten, and out of these
126 were included in the present study. The surgery was The swabs were cultured on Fusobacterium necrophorum
performed by different surgeons at two hospitals – Sunderby selective agar made of Fastidious anaerobe agar (Lab M),
Hospital in Luleå and G€allivare Hospital in G€allivare. All of defibrinated horse blood (Håtuna lab, Sweden), vancomycin
the surgeons had been introduced in how to perform sam- 4 mg/L (Xellia Pharmaceuticals, Copenhagen, Denmark) and
plings for the study. To avoid bleeding during the proced- nalidixic acid 5 mg/L (Sigma-Aldrich, St Louis, MO) (modi-
ure, the tonsillectomy was performed carefully with either fied from Bank et al. [11]). To support identification, a
the coblation technique or with blunt dissection using bipo- 500 lg Kanamycin (ROSCO) disc was placed on the agar
lar diathermy. All patients had signed an informed consent plate after streaking the sample. Agar plates were incubated
anaerobically in a Tritrainer jar with catalyst, TrilabVSystem.
form before inclusion. Patients with ongoing antibiotics or
those with an antibiotic treatment within 2 weeks before the The jar was incubated for 2 days at 35  C before the first
tonsillectomy were excluded from the study. evaluation, and for 1 additional day before the final
Thus, 126 patients were originally included; however, evaluation.
three of these were later found to have been on antibiotics Presumptive FN colonies were sub-cultured on selective
when the patient reports were analysed. This meant that 123 Fusobacteria agar for identification according to Bank et al.
patients (88% inclusion rate considering all receiving TE for [11]. Criteria for identification of FN were: b-hemolysis,
this diagnosis) fulfilled the inclusion criteria. Table 1 exhib- grey-to-light yellow and waxy colonies that slides on the
its demographic data and culture results. agar surface when picked, characteristic Gram-negative pleo-
morphic rods (Gram Stain; BD, BBLTM), a positive spot-
indole test (in house; p-Dimetylaminocinnamaldehyde,
Bacterial sampling and culture Sigma), and yellow fluorescence in Wood’s light (365 nm).
Prior to removal of the tonsils during general anesthesia, the Furthermore, testing was done for susceptibility (S) to
surgeon swiped over the surface of the tonsils with a cotton Kanamycin disc 500 lg (S), Vancomycin disc 5 lg (R), and
swab. Thereafter, the surgeon swiped another swab deep Colistine (Oxoid) disc 25 lg (S).
Identification with Vitek 2 System, Biomerieux was also
into crypts of the tonsils. After the removal of the tonsils,
All of the purified Fusobacterium necrophorum isolates
Table 1. Demographic data and culture results. were frozen at 80  C.
Total Men Women In addition, swabs were also cultured regarding ß-hemo-
Included N ¼ 123 N ¼ 52 (42%) N ¼ 71 (58%) lytic streptococci (Blood Agar Base No.2, Acumedia, defibri-
Age range 2–57 yrs 3–57 yrs 2–55 yrs
Mean age 19 yrs 19.5 yrs 18.8 yrs
nated horse- and sheep blood, Håtuna lab), Non-typeable
Pos culture N ¼ 50 (41%) N ¼ 20 (40%) N ¼ 30 (60%) H. influenzae in pure culture (GC-agar, Hemoglobin,
Neg culturea N ¼ 73 (59%) N ¼ 32 (44%) N ¼ 41 (56%) Acumedia, IsoVitox Enrichment, Dalynn) and
FN positive N ¼ 23 (19%) N ¼ 9 (39%) N ¼ 14 (61%)
Strep positive N ¼ 35 (28%) N ¼ 16 (46%) N ¼ 19 (54%) Arcanobacterium haemolyticum (Columbia Blood Agar Base,
FN positive Strep positive human blood) incubated and examined in accordance with
Sub-group “rec”b N ¼ 91 (74%) 17/91 (19%) 25/91 (27%) the standard routines at the laboratory. The ß-hemolytic
Sub-group “chron”c N ¼ 32 (26%) 6/32 (19%) 10/32 (31%)
streptococci were identified by latex agglutination test,
Demographic data and culture results.
Growth of only normal bacterial flora, mostly a-haemolytic streptococci. Streptococcal Grouping Kit (Oxoid).
Number of patients with a history of recurrent episodes of acute tonsillitis or The study was approved by the Regional Ethics
previous peritonsillar abscess. Committee, Umeå, dnr 2012-104-31M.
Number of patients with more diffuse persistent problems from the throat
with recurrent pain, episodes of fever, or sporadic episodes of tonsillitis.
FN positive ¼ Number of patients with a positive culture of Fusobacterium nec-
rophorum; Strep positive ¼ Number of patients with a positive culture of Statistics
ß-haemolytic streptococci (GAS/GGS/GCS).
There were no significant differences between the sexes neither between the The Chi-square test was used to test equality between pro-
“rec” or the “chron” groups. portions, and the calculations were made with the OpenEpi

FN positive cultures (a)

GCS/GGS positive cultures

No of patients
No of samples

10 2 pos
8 1
6 0
FN pos


FN neg Age
0 (b) GAS positive cultures

GAS pos

No of patients
Age 3
Figure 1. Black staples ¼ Number of patients with positive culture of F necro- 2
phorum (FN). Grey staples ¼ number of patients with negative culture of 1
F necrophorum. Y-axis ¼ Number of patients. X-axis ¼ Age (years). Most of the 0
FN positive patients were found between 15–23 years.



Figure 2. (a-b) Y-axis ¼ Number of patients. X-axis ¼ Age (years). Both FN

Table 2. Specification of the pathogens found from the (Figure 1) and GGS þ GCS showed a significant accumulation of positive cul-
sampling of the tonsils. tures in the age group 15–23 years. There was no such accumulation regarding
Bacteria Pos culture (n) the GAS positive cultures. Most of the GAS positive patients were found in the
younger age groups (0–14 years). GCS ¼ ß-haemolytic streptococci group C,
FN 15 GGS ¼ ß-haemolytic streptococci group G, GAS ¼ ß-haemolytic streptococci,
FN þ GCS 3 group A.
FN þ GGS 4
FN þ GCS þ GGS 1
GAS 10 together with FN. None of the patients had growth of group
GCS 10
GGS 6 A streptococci (GAS) together with FN. In total, 35 patients
GCS þ GGS 1 (28%) had growth of b-hemolytic streptococci, for which
H. influenzae 0 eight of these had simultaneous growth of FN (see above).
Arcanobacteria 0
In 73 patients (59%) we found no growth of either FN or
Specification of the pathogens found from the sampling
of the tonsils. b-hemolytic streptococci. In no patients did we find growth
n ¼ number of patients with positive culture; of H. influenzae in pure culture or Arcanobacterium haemo-
FN ¼ Fusobacterium necrophorum; GCS ¼ ß-hemolytic lyticum (Table 2).
streptococci, group C; GGS ¼ ß-hemolytic streptococci,
group G; GAS ¼ ß-hemolytic streptococci, group A. Regarding the positive cultures in relation to age groups,
FN were found mostly in the age group between 15–23
years. The distribution by age group of FN positive cultures
were 3/38 (8%) for 0–14 years, 19/56 (34%) for 15–23 years
web site ( The significance level was (p ¼ 0.0004 in comparison to the other age groups), and
defined as a p-value below 0.05. 1/29 (4%) in the age group for 24–60 years (Figure 1).
Regarding GCS and/or GGS positive (GCS ¼ 18%,
GGS ¼ 16%) cultures we found similar distributions by age
Results groups as for the FN positive cultures: 3/38 (8%) for 0–14
The mean age in the study material was 19 years years, 17/56 (30%) for 15–23 years (p ¼ .001), and 1/29 (4%)
(range ¼ 2–57 years) and 42% of the patients were male for 24–60 years (Figure 2).
GAS positive cultures were more evenly distributed
(Table 1). By examining the medical records, a further sub-
among the age groups: 7/38 (18%) for 0–14 years, 2/56 (4%)
division of the patients was made into two groups – a group
for 15–23 years, and 1/29 (4%) for 24–60 years. In the inter-
of recurrent tonsillitis episodes (n ¼ 91) and a group of
val between 15–23 years of age (that included most of the
more ‘chronic’ character (n ¼ 32) with only sporadic epi-
patients), there were, thus, only two GAS positive patients
sodes of fulminant infection. However, we found no signifi- (4%) and in the total material only 10/123 (8%) patients
cant group differences regarding the frequency of FN or were GAS positive. GAS positive patients tended to be more
streptococci (19% FN positive cultures in both sub-groups, common in the youngest age group (18%), but test of equal-
27% b-hemolytic streptococci in the recurrent group and ity between proportions could not be made for the GAS
31% b-hemolytic streptococci in the ‘chronic’ group) and, positive cultures since the distribution of observations made
thus, the results below are presented for the whole group of the Chi-square test not trustworthy.
123 patients. There was no significant (statistics calculated quarterly)
In the total material we found growth of FN in 23 peak of FN or streptococcal positive (GAS/GGS/GCS) cul-
patients (19%) (Figure 1). There was no significant differ- tures around any specific time of the year (Figure 3). The
ence between sexes (17.3% of the males vs 19.7% of the reason for the low incidences during June–July and
women). Seven patients had simultaneous growth of either December–January was that nearly no elective surgeries
streptococci group C (GCS) or group G (GGS) together were done during the summer months and around the holi-
with FN, and one patient had growth of both GCS and GGS days at Christmas and New Year.

Seasonal variation of cultures morbidity of FN acute tonsillitis infections among young

14 adults, especially because the management of these infections
12 so far is almost exclusively directed to detect GAS infections.
10 According to Centor et al. [14], acute FN pharyngitis infec-
No of patients

8 tions were more common among students than acute GAS
positive pharyngitis. Perhaps detection of FN with quantita-
tive PCR methods could be a way to discriminate between
significant and non-significant growth of FN [3,6].
It is possible that more FN positive patients would
Jan Feb Mar Apr May June July Aug Sept Oct Nov Dec
have been detected if we had used a PCR method instead
of the culture method we employed. However, the fact
that the swabs could be taken thoroughly, since the
Figure 3. FN ¼ Number of patients with positive cultures of Fusobacterium nec- patients were under general anesthesia, and also from dif-
rophorum; Strep ¼ Number of patients with positive cultures of streptococci
(GAS/GGS/GCS); Neg ¼ Number of patients with negative cultures. ferent parts of the tonsils, it is not likely that a PCR
Y-axis ¼ Number of patients. X-axis ¼ Month of the year. There was no signifi- method would have detected more FN positive patients of
cant variation over the year regarding the prevalence of positive FN or strepto- clinical significance.
coccal cultures. In July there were no samplings and in January, June, and
December there were only a few samplings due to the decrease in elective Our finding that FN always showed growth at the sur-
surgery. face of the tonsils, in spite of being an anaerobic bacter-
ium, suggests that it would be possible to find FN in
ordinary bacterial sampling from throat swabs. Klug et al.
In two FN positive patients only the surface sample was [15], however, found most of the FN preferably deep into
positive, and in one of the FN positive patients only the sur- the tonsils, which is not in accordance with the present
face and the core samples were positive. In all the other 20 study.
FN positive patients the sampling was positive from all three The surface sampling was performed before the removal
sampling sites (surface, crypts, and core). of the tonsils in order to mimic a normal throat culture.
However, since it was performed under general anesthesia in
the present study, it is possible that it could be made more
Discussion thoroughly than in a clinical situation. The samplings from
In the present study we investigated the occurrence of FN in the crypts were also made before the removal of the tonsils
consecutive patients encompassing various age groups that in order to preserve the anatomy. An advantage of removing
were scheduled for elective tonsillectomy due to chronic or the tonsils before performing the core sampling was to
facilitate that the sampling pin was not contaminated from
recurrent tonsillitis (ICD 10 ¼ J 35.0). We found growth of
the tonsillar surface. The drawback with this could be that
FN in 19% of the total material and in 34% of the patients
the tonsils were affected by the surgical procedure. The
for the age group 15–23 years. GCS and GGS positive
coblation technique and the use of bipolar diathermy during
patients were also concentrated to the same age group
the tonsillectomy procedure, however, made it possible to
(15–23 years) with a prevalence of 30%. GAS positive
remove the tonsils carefully and without any significant
patients did not show a significant concentration to any spe-
bleeding. There is a potential risk of damaging bacteria
cific age group, although 18% of the GAS positive patients
when using diathermy, but the diathermy was only used
were found in the youngest age group (0–14 years). Only
outside the capsule of the tonsils, why this risk probably
8% of the total included patients were GAS positive. Thus, is low.
in the age group 15–23 years FN was the single most com- In our study, we did not find any H. influenzae in pure
mon pathogen and as common as any ß-hemolytic culture or Arcanobacteria in the tonsils. This is in contrast
streptococci. to the study of Stjernquist-Desatnik et al. [16] who detected
The concentration of FN-positive cultures to the age a substantial amount of H. influenzae in tonsils from
group of 15–23 years was interesting, and is also in accord- patients with recurrent tonsillitis.
ance with the results of other studies [3,4,8]. This is also the As has been described previously [17], we found no sea-
same age group where most of the Lemierre’s patients are sonal variation regarding the detection of FN, which also
found [12]. It is, thus, possible that FN is a significant cause pertained to the detection rates of ß-hemolytic streptococci.
of chronic tonsillitis in young adults and has the same clin- Furthermore, FN was often cultured together with GCS
ical significance in this disease as the ß-hemolytic strepto- or GGS (35%), but this was not the case for GAS.
cocci [13]. However, it would be of interest to make Also, Hagelskjaer Kristensen and Prag [18] found an
bacterial cultures also among healthy young adults to evalu- increased co-prevalence of FN and GCS in FN infections.
ate the presence of FN among healthy individuals in the Further studies could be of interest to investigate if there are
same age group (i.e. 15–23 years). There are studies indicat- interactions between these species in chronic or recurrent
ing the presence of FN among healthy young adults without tonsillitis.
any throat symptoms [3,8], so the asymptomatic carriership There are studies suggesting that FN is an important
in relation to throat disease needs to be further investigated. pathogen also in patients with peritonsillar abscess [5],
Furthermore, it would be of interest to investigate the which would not be surprising since most patients with

peritonsillar abscess are also in the same age group as the [5] Klug TE, Rusan M, Fuursted K, Ovesen T. Fusobacterium nec-
majority of chronic tonsillitis patients [19]. rophorum: most prevalent pathogen in peritonsillar abscess in
Denmark. Clin Infect Dis 2009;49:1467–72.
In conclusion, we found a high prevalence (19%) of the [6] Jensen A, Hagelskjaer Kristensen L, Prag J. Detection of
anaerobic bacteria F necrophorum in a patient material of Fusobacterium necrophorum subsp funduliforme in tonsillitis in
chronic tonsillitis, especially in the age group between 15–23 young adults by real-time PCR. Clin Microbiol Infect
years (34%). We also found that it was possible to detect FN 2007;13:695–701.
Amess JA, Oneill W, Giollariabhaigh CN, Dytrych JK. A six-
from the surface of the tonsils with a COPAN throat swab, month audit of the isolation of Fusobacterium necrophorum
which is often used routinely in the clinics; this is in spite of from patients with sore throat in a district general hospital. Br J
FN being an anaerobic bacterium. Biomed Sci 2007;64:63–5.
[8] Bj€ork H, Bieber L, Hedin K, Sundqvist M. Tonsillar colonisa-
tion of Fusobacterium necrophorum in patients subjected to ton-
Acknowledgments sillectomy. BMC Infect Dis 2015;15:264.
[9] Sherer Y, Mishal J, Leibovici O. Early antibiotic treatment may
We especially thank Mats Sellin, Umeå, and Peter Cettner, Sunderby prevent complete developement of Lemierres syndrome: experi-
Hospital, for their co-operation regarding the FN culture method and ence from 2 cases. Scand J Infect Dis. 2000;32:706–7.
Robert Lundqvist for assistance with the statistical analysis. [10] Bank S, Christensen K, Kristensen LH, Prag J. A cost-effective-
ness analysis of identifying Fusobacterium necrophorum in
throat swabs followed by antibiotic treatment to reduce the
Disclosure statement incidence of Lemierres syndrome and peritonsillar abscesses.
Eur J Microbial Infect Dis. 2013;32:71–8.
The authors report no conflicts of interest. The authors alone are [11] Bank S, Nielsen HM, Hoyer Mathiasen B, Christiansen Leth D,
responsible for the content and writing of the paper. Hagelskjær Kristensen L, Prag J. Fusobacterium necrophorum-
detection and identification on a selective agar. Apmis
Funding [12] Karkos PD, Asrani S, Karkos CD, Leong SC, Theochari EG,
Alexopoulou TD, et al. Lemierre's syndrome: a systematic
The present study was financed by Umeå University, Akademisk milj€o, review. Laryngoscope 2009;119:1552–9.
Sunderby Hospital and the Research Unit at the County of Norrbotten. [13] Eaton C, Swindells J. The significance and epidemiology of
Fusobacterium necrophorum in sore throats. J Infection
ORCID [14] Centor RM, Atkinson TP, Ratliff AE, Xiao L, Crabb DM,
Estrada CA, et al. The clinical presentation of Fusobacterium-
Krister Tano positive and streptococcal-positive pharyngitis in a university
health clinic. Ann Intern Med 2015;162:241–7.
[15] Klug TE, Henriksen JJ, Fuursted K, Ovesen T. Similar recovery
rates of Fusobacterium necrophorum from recurrently infected
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