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Copyright© 1988, American Society for Microbiology

Semiquantitative

Culture

Results

and Pathogenic Significance

of

Obligate

Anaerobes in Peritonsillar Abscesses

ANSSI M. M.

JOKIPII,'t*

LIISAJOKIPII,' PEKKA SIPILA,2 AND KALEVI JOKINEN2

Departmentof Serology and Bacteriology, University of Helsinki, Helsinki,' andDepartmentof Otolaryngology, University of Oulu, Oulu,2 Finland

Received 22October 1986/Accepted 25 January 1988

Westudied the bacteriain consecutive peritonsillarabscesses using semiquantitation of the primaryculture findings and correlated the resultstoclinicalparameters.Puncture-aspiratedpusfrom 42 abscesses yielded 133

isolates. Group Astreptococciwereisolated 10 times and, unlike other bacteria,wereisolated 4 timesinpure

culture; other beta-hemolytic streptococci werefound in 8 abscesses, and anaerobeswere found in 28. The

infections were polymicrobial, with two to seven bacteria in 83%. Anaerobes were more abundant than

nonanaerobes; members ofthegeneraStreptococcus,Bacteroides, Peptostreptococcus, and Fusobacterium were

the most important quantitatively, considering both frequency and abundance. In patients with ongoing antibiotic treatment, nonanaerobes (butnot anaerobes)were less abundant than in untreated patients. The

abundance ofobligate anaerobes (specifically cocci and gram-positive rods)correlatedtotheseverity ofillness as defined by fever and short duration before hospitalization. With other groups of bacteria, no such

correlationwasfound. The correlationwasnotexplained byadifferencebetween theantibiotic-treatedand the

untreated patients. Theresultsindicatethe value of the semiquantitation of culture data and the frequency and pathogenic significance of obligateanaerobesin peritonsillarabscesses.

Peritonsillar abscess isapotentially life-threatening

com-plication ofacutetonsillitis caused bygroupAstreptococci

and, according to a recent observation (10), of infectious mononucleosis. It requires immediatetreatment,which in its generally accepted form consists of drainage, antibiotics, andtonsillectomy; alternatively, needle aspiration and anti-bioticsmaysuffice (6, 7, 11). Propertreatmentthus relieson

microbiological statistics and shouldcoveressentially all the

bacteria thataresignificant causativeagents.Besides

Strep-tococcus pyogenes, a variety of organisms, notably

an-aerobes, commonly found in the normal pharyngeal flora havebeen culturedfrom peritonsillar abscesses (1, 4, 5, 12, 13). Owingtothe method of sample collection, such culture resultsincludeanunknown proportion of contaminants and

theclinical significance of the remaining organismsas

caus-ative agentsmay vary.

Thepurposeof thisstudywastorecord the bacteria found inaseries of 42peritonsillar abscesses and toestimate their relative significance by semiquantitating culture results and correlating bacteriological data with clinical parameters.

MATERIALSANDMETHODS

Patients. We studied 42 consecutive patients admittedto theDepartment of Otolaryngology, UniversityCentral Hos-pital, Oulu, Finland, and scheduled for tonsillectomy

be-causeofperitonsillarabscess. In additiontocommon demo-graphic information, the history of the present illness and previous episodes of tonsillitis,antimicrobialtreatment,and axillary temperature with an accuracy of 0.1°C were

re-corded (the standard procedure of the outpatient depart-ment).

* Correspondingauthor.

t Presentaddress:DepartmentofMedicalMicrobiology,

Univer-sityofTurku, Kiinamyllynkatu 13,20520Turku,Finland.

Samples. Standard culture media (3) were used, unless

stated otherwise, and all media for anaerobic incubation

wereprereduced in the GasPak system(BBLMicrobiology Systems, Cockeysville, Md.) for 24 horlonger.

Each abscess was punctured, andpus (>1 ml) was

aspi-rated intoasterile syringe. Daytime specimenswere

imme-diately (about 15 s) plated (0.1to0.2 ml)on chocolate agar

andnonselective enriched anaerobic bloodagar, and

night-time specimens stayed in the syringe, which was stored

anaerobically inaGasPakjaratroomtemperature,andwere

plated similarly in the morning. Anaerobic plates were

exposedtoaironly afew seconds before seeding andwere

immediately returned to anaerobic conditions at 37°C for incubation. Aerobic incubationtook place inacandle jarat 370C.

Bacteriology. Theprimary incubation continued for 3 days

or longer, after which the plates (in their anaerobic or

aerobic containers) were transferred to the bacteriological laboratory. For at least 7 days, the primary plates were

examined for distinct colony types to be isolated. The heaviness ofgrowthwasrecordedasthe numberof colonies

per plate: 0; +, 1 to 10; ++, 11 to 50; +++, 51 to 200; ++++, more than 200 or, usually, innumerable. The

or-ganisms were identified by standard procedures (3), the

Phadebact Streptococcus Test (Pharmacia, Uppsala, Swe-den) for grouping ofbeta-hemolytic streptococci, and the API 20A strip (API System S.A., Montalieu-Vercieu, France) and gas chromatography ofpeptone-yeast-glucose (PYG) brothcultureextracts(8)forcharacterizingthe

anae-robes. Wedefined obligate anaerobesas bacteriathatwere

unabletoform colonies duringa48-hcandlejar incubation; thus, microaerophilic streptococci were included in the

viridansgroup.

Statistical treatment. The significance of differences

be-tween frequency distributions was analyzed by the Fisher one-tailedexact test(14).Correlation between the heaviness ofbacterialgrowthand eitheraxillary temperatureor dura-957

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J. CLIN. MICROBIOL. TABLE 1. Organisms isolatedfrom 42 peritonsillarabscesses

Organism

Streptococcuspyogenes,

groupA

Streptococcus sp., beta-hemolytic, non-groupA Streptococcus sp.,viridans

group

Streptococcus faecalis Staphylococcusaureus

Staphylococcus sp., coagu-lase negative

NeisseriaorBranhamellasp. Moraxellasp. Haemophilus influenza Haemophilus sp. Eikenella corrodens Diphtheroidbacillus Bacillus subtilis Candidaalbicans Totalnonanaerobes Peptostreptococcus anaero-bius Peptostreptococcus asaccha-rolyticus Peptostreptococcus sp. Staphylococcus saccharoly-ticus Veillonellaparvula Fusobacterium necrophorum Fusobacterium nucleatum Bacteroidescapillosus Bacteroidesdistasonis Bacteroidesfragilis Bacteroidesmelaninogenicus Bacteroidessp. Propionibacterium sp. Arachnia propionica Bifidobacteriumsp. Lactobacillus sp. Nonsporeforming gram-positive rod Clostridium sp. Total anaerobes

No. ofisolationsa

+ ++ +++ ++++ Total

2 1 1 6 10

2 2 3 1 8

4 4 1 8 17

4 6 3 4 6 1 5 1 7 6 1

2 1 il

1

1 2

1 1

1 3

4 1 12

37 13 12

2 1 2

1

1 1 1

2 1

3

1 1

il 6 5

a Heavinessofgrowth(+ to+ + ++);semiquantitative estimate of numbers

oforganisms, basedonnumbersofcoloniesonprimary plate.

tion ofillness was assessedbySpearman'srank correlation

procedure givingthecoefficientr, andtheone-tailed

proba-bilityvalue (14).

TABLE 2. Multiplicityoforganisms isolated from each of 42

peritonsillarabscesses andfrequenciesof various combinations of anaerobes and nonanaerobes

No. ofabscesses with thefollowingno.of

No. of nonanaerobes:

anaerobes

0 1 2 3 4 5

0 2 5 6 1

1 6 3 3 1 1

2 2 3 2 1

3 2 2

4 i

5

6werenot, and thisinformationhadnotbeen recorded in 18 cases.

Culture results. All

growth

in aerobic and anaerobic cul-turesof punctureaspirateswasrecordedwithoutattempts at

a

priori judgement

ofclinical relevance. Amongthe aerobic orfacultative

bacteria,

variousstreptococciwerefound most

frequently, followed by members ofthe family Neisseria-ceae and gram-positive nonsporeforming bacilli (Table

1).

Among theobligate anaerobes, the members of the genera Bacteroides and Péptostreptococcus accounted formost of the

findings.

Of the non-group A beta-hemolytic

strepto-cocci, two were of group C (++ and +++) and the

remaining six were not groupable with the reagents for

groups

A,

B,

C, D,andG. If thebacteriaseenonlyasone or

few colonies (+) are ignored, anaerobes and nonanaerobes wereapproximately equally frequent and the

quantitatively

most

important

were members of the genera

Streptococcus

(isolated27times), Bacteroides (16 times),

Peptostreptococ-cus (13 times), and Fusobacterium (5 times) (Table

1).

Anaerobes were isolatedasconfluent growth

(+++

++)57%

(29of51)of thetime,ascomparedwith 24%(20 of 82) for the nonanaerobes. Members ofoneor more of the above four

generaoccurredas+ + + +growthin 27 of the abscesses and

asoneofthemostabundantisolates in 35 of the abscesses. Group A streptococciwere isolatedas a pureculturein4of the 10 cases; besides these, no other organism except one

viridans group streptococcus was seen in pure culture (on theprimary plates).

Anaverage of 3.2 organisms were isolated from 42

peri-tonsillar abscesses, 1.2 anaerobes and 2.0 nonanaerobes. Most or 83% (35 of 42) were mixed infections with up to

seven organisms per abscess (Table 2). In the 28 cases in

which anaerobes were found, an average of 1.8 of them

could be differentiated, and the corresponding number of nonanaerobes in 38 cases was 2.2. The distributions of the

multiplicities of infection with anaerobes versus

nonan-aerobeswerenotnotably different from each other (Table 2).

RESULTS

The study population consisted of29male and 13 female patients withperitonsillar abscesses.Theiragesrangedfrom

15to62yearswitha mean ageof 27.7years.Aretrospective analysis of their clinical records revealedthat 10patients had notexperienced tonsillitis before thepresent occurrence, 6

hadhadoneortwopreviousoccurrences, 11had hadmore

thantwopreviousoccurrences,andtheinformationhad not been recorded in 15cases. During the present episode, the tonsilsof18patientswerecovered with exudation, thoseof

TABLE 3. Heaviness ofgrowthofanaerobes and nonanaerobes invariouscombinations isolatedfrom 42peritonsillar abscesses

No.ofabscesses according to heaviness

Anaerobes ofgrowth of nonanaerobes:

(heaviness ofgrowth)

O + ++ +±+ ++++

0 2 2 2 8

+ 1 2

++ 2 2 i

+++ 1

+ ++ + 2 5 3 2 7

958 JOKIPII ET AL.

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TABLE 4. Comparison of bacterial findings from peritonsillar abscesses in 21 patients with and

withoutongoing antibiotic treatment

No.of abscesseswith

bacterialgrowth:

Bacteriological With With no

classification antibiotics antibiotics

+or ++or + or ++ or none heavier none heavier

Nonanaerobes 13 8 1 20 <0.0001

Streptococci 14 7 5 16 0.0061

Staphylococci 20 1 20 1 NS

Neisseriaceae 20 1 17 4 NS

Gram-negative rods 19 2 19 2 NS

Gram-positive rods 21 15 6 0.0103

Anaerobes 8 13 9 12 NS

Cocci 15 6 16 5 NS

Gram-negative rods 12 9 12 9 NS

Gram-positive rods 19 2 18 3 NS

Total growth 5 16 21 0.0239

a The Fisher exacttest;NS,P>0.05, onetailed.

Table 3describes the semiquantitative approach appliedto the 42culture results ignoring the taxonomicposition of the isolated organisms. Inall, + + + + growthwasfound in 71%

(30 of 42) of the abscesses and + + or heavier growth was

found in88%(37 of 42). Ifscantygrowth (+) isignored, the anaerobic and nonanaerobicfindingsperabscesswererather

similar with regard to both frequency and heaviness of growth (Table 3). The semiquantitative culture results

re-vealed no obvious dependence (antagonism or synergism)

betweenanaerobes and other bacteria.

Antibiotictreatment.No antimicrobialtreatmenthad been administered during the present illness of 21 patients, 17

were receiving penicillin, 3 were receiving erythromycin,

and 1wastreated withampicillin. In the latter21 cases,the treatment had continued for 1 to 10 days (mean, 3.6 days) before admission. In the treated group, bacterial growth from the abscesses was less heavy (Table 4). There was a

difference between anaerobes and other bacteria. Total nonanaerobic growth was less heavy in the antibiotic-re-ceiving group as compared with the untreated group, and thisfinding wasdue tothe relative lack ofstreptococci and diphtheroids; the amount of anaerobes showed no such correlation with ongoing antibiotic treatment (Table 4). Of the 10group Astreptococci, 5, including 1of thosein pure

culture, were found in patients receiving penicillin and 5, including 3 of those in pure culture, were found in the untreated group.

Clinical correlations. Measurements of axillary

tempera-ture atthe time of admissionwereavailablein the records of

36 patients. Fever correlated significantly with the semi-quantitatively assessed bacterialgrowth (Table 5). Thiswas

found withtotal anaerobic growth and withthe heaviness of growth of anaerobic cocci, but not with nonanaerobes or

with the othermorphologic classes of anaerobes.

Totalbacterial growthperabscesswasheavier the shorter

the duration of illness before admission (Table 6). More specifically, this correlation was found with the anaerobes

and among them with the cocci and gram-positive rods.

Similar correlations were found within the group of 21

antibiotic-treated patients: total growth,r, =0.403, P<0.05 (Spearman's rankcorrelation); total anaerobes,r, =0.524, P

< 0.01; anaerobic cocci, r, = 0.504, P < 0.025; anaerobic

gram-positive rods,r, = 0.294, 0.05 < P< 0.10.

DISCUSSION

The adoption of anaerobic technology and the ensuing bacteriological reevaluations have alteredourviews ofmany

infectious processes. That infections arederived from

nor-malflora has becomeanaccepted principle,and peritonsillar

abscess is anexample. Increased work load in the

microbi-ological diagnosis andambiguityofinterpretation whenever contamination from the normal floracannotbe excludedare

unfortunate by-products of theprogress. Thepresent inves-tigation showed thatsemiquantitative datamay be useful in themicrobiological work and that clinical relevancemay be

attributedtolaboratory findings inadifferentialmanner.

Nighttime specimens were kept in syringes in anaerobic

jars until morning to ensure anaerobiosis without

compro-mising the series of consecutive patients. The significance of the procedure was not investigated. There were no gross

differences between daytime and nighttime specimens as

regards the culture results, but we did not analyze subtle differences, as this would be unjustified in the absence of

parallel experiments with divided specimens.

Group A streptococci are implicated as pathogens in

peritonsillar abscesses, because thecomplication is usually

preceded by tonsillitis. Previous studies have revealed S.

pyogenesinnotmorethan39.3%or35 of 89cases(1, 4, 12,

13), and the present finding was even less (23.8%).

Non-group A beta-hemolytic streptococci were isolated twice (2.2%)by the previousgroups,whilewefoundeight (19.0%). Thismayreflectamoregeneralswitch fromgroupA toother

groups, notably C, which we have noticed in several other

infections recently (unpublished data), and the total

fre-quency of beta-hemolytic streptococci in peritonsillar

ab-scesses in both our series and the previous ones is very similar or about 40%. Finally, ourresults confirm that itis characteristic of S. pyogenes to occur in pure culture;

TABLE 5. Correlation betweenaxillarytemperature and heaviness of bacterialgrowthfromperitonsillarabscesses of 36 patients

Bacteriological Mean temp(°C) +SD (no. of patients)

classification________________________________r.j

classification + growth or none + +growthor heavier

Totalgrowth 37.5 ± 0.62(5) 37.6 ± 0.63 (31) 0.381 <0.025

Nonanaerobes 37.5 ± 0.56(13) 37.7 ± 0.67 (23) 0.168 NS

Anaerobes 37.5 ± 0.64(16) 37.7± 0.62 (20) 0.356 <0.025

Cocci 37.5 ± 0.60(27) 38.0± 0.63 (9) 0.351 <0.025

Gram-negativerods 37.6 ±0.64(22) 37.7± 0.63 (14) 0.239 NS

Gram-positive rods 37.6 ±0.63 (32) 37.7 ±0.70 (4) 0.225 NS

aSpearman'srankcorrelationcoefficient,usingthewholerangeofsemiquantitative growthreadingsfromOto++++;NS,P>0.05,onetailed.

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960 JOKIPII ET AL.

TABLE 6. Correlationbetweenacutenessof illness and heaviness of bacterialgrowthfromperitonsillarabscesses of 42 patients

Bacteriological Mean date of onset ofsymptoms+ SD (no. of patients) rb pb

classification +growthor none + +growthorheavier

Totalgrowth -7.0 ± 1.41 (5) -4.3 ± 2.93 (37) 0.265 <0.05

Nonanaerobes -5.6 ± 3.08(14) -4.1 ± 2.75 (28) 0.203 NS

Anaerobes -5.8 ± 3.11 (17) -3.8± 2.55(25) 0.381 <0.01

Cocci -5.1 ± 3.22(31) -3.3 ± 1.10 (11) 0.321 <0.025

Gram-negativerods -4.9 ± 3.01(24) -4.2± 2.84 (18) 0.204 NS

Gram-positiverods -4.8 ± 3.01(37) -3.0± 1.58 (5) 0.325 <0.025

a Date of admittance isday0.

b Spearman's rankcorrelationcoefficient,usingthe wholerangeofsemiquantitative growth readingsfrom to++++ +;NS,P>0.05,onetailed.

previous studies recorded this 17 times in 89patients (1,4, 12, 13).

Eventhough there isa subgroupofpatientswithgroup A

streptococciinpureculture,mostperitonsillarabscesses are causedbypolymicrobialinfections.Theaveragemultiplicity of culture resultsinearlier serieshas been2.3organismsper abscess (1, 5, 12, 13), and we found 3.2 per abscess.

Likewise, most peritonsillar abscesses are anaerobic infec-tions:66.1% on the average in 242 earlierpatients(1, 4, 5,12, 13) and 66.7% in our series (some authors included micro-aerophilic streptococci, butwe countedonly obligate

anae-robes). The individual variation of the culture results is great, andnearly alltheorganisms arecommon members of

thenormal flora. Sincetreatment

always

includesantibiotics

before culture results are

available,

the variation creates a

problemofchoice ofdrug. The similarity with normal flora creates aproblemofinterpretation ofculture results. Much of the presenteffortwas directed to thesetwoquestions.

The rationale behind the quantitation of culture results was twofold. Contaminating bacteria originating from the normalfloraatthe siteofpuncture orfromelsewhereduring handling ofthe sample orthe cultures are expected to be fewer innumberontheaverage than bacteria from thepus.

Second, it seems reasonable to suggest that abundant iso-lates are more likely causes of clinical illness than are

bacteria evidenced only by a few colonies. The present

approach was crude, and the semiquantitation was not

intended to refer to exact numbers of bacteria inside

ab-scesses, but to evaluate the possibilities of the normal procedures of a diagnostic laboratory. Dilution and the

calculation of CFU per volume ofpus is too tedious for routine diagnostic work. Furthermore, our method of

pro-viding anaerobiosis for the primary cultures has proved

efficient in revealing anaerobes in otolaryngological

infec-tions (9). We were unable simultaneously to adhere to the

method,tocollectunselected patientsconsecutively,and to carry outquantitative bacteriology. Therefore, our

compro-mise was toreplace the latterby

ils

approximation, colony

counts onprimary plates.With the crude butsimple method

it was possible to reduce the list ofsignificant bacteria to speciesof Streptococcus, Bacteroides, Peptostreptococcus,

and Fusobacterium. One or more species of these four genera wereamongthemostabundant isolatesin83% or 35

of 42 cases. In general terms, the weighted results empha-sized obligate anaerobes. These technical considerations

serve the purposes ofdescription and communcation, and thepossible clinical relevance remainsa suggestion.

Axillary temperatureand thedurationoftheillnessbefore admission were available for the

evaluation

of the clinical severity ofthe condition at the time of the microbiological

intervention.

These parameters correlated with the

abun-dance of anaerobes and more specifically with anaerobic

cocci

(and gram-positive rods)

intheperitonsillar abscesses.

Adifference betweentheantibiotic-treatedand theuntreated

groups was excluded as an explanation ofthe finding. The

probable

causality behind the correlation is that anaerobic cocci and

gram-positive

rods aggravate the symptoms and are thus to be regarded as clinically significant

laboratory

findings. Conceivably,

numerous other factors also deter-mine the

severity

of symptoms. The lack of sucha clinical

correlation in the case of other bacterial groups is no evidence

against

their

significance,

which remains to be evaluated infuture studies. While the importanceof anaer-obicinfections as awholeisgenerally accepted, that ofthe numerouscomponentsof normalflora-derived

polymicrobial

infectionsremainsdebatableinmost cases.Few attempts to sort out

pathogenic

significance in mixed infections have beenreported, and it isinterestingto note that such

impor-tancehas been ascribedtoanaerobic gram-positive cocci in amurine subcutaneous abscess model(2). The samegroup ofbacteria was emphasized in our work. The present

ap-proach to ascribe pathogenic significance to a component may bewidelyapplicable tomixedinfections.

ACKNOWLEDGMENTS

We thankIrjaJouhtenandMarjaKorvala forexcellenttechnical assistance.

This work was supported by a grant from the Sigrid Jusélius Foundation, Helsinki, Finland.

LITERATURE CITED

1. Brook,I. 1981. Aerobic and anaerobicbacteriologyof periton-sillarabscess in children. Acta Paediatr. Scand. 70:831-835. 2. Brook, I., and R. I. Walker. 1984. Pathogenicityofanaerobic

gram-positive cocci. Infect. Immun. 45:320-324.

3. Finegold,S. M.,W. J. Martin, and E. G. Scott. 1978. Baileyand Scott'sdiagnosticmicrobiology, 5thed. The C. V. MosbyCo. St. Louis.

4. Flodstrom, A., and H. O. Hallander. 1976. Microbiological aspects on peritonsillar abscesses. Scand. J. Infect. Dis. 8:157-160.

5. Hansen, A. U. 1950. Nogle

unders04gelser

over gram negative anaerobeikke-sporedannendebacterier isolerede fra peritonsil-loere abscesserhos mennesker. Ejnar Munksgaard, Copenha-gen.

6. Herzon,F. S. 1984.Permucosalneedle drainage ofperitonsillar abscesses.Afive-year experience.Arch. Otolaryngol. 110:104-105.

7. Herzon, F. S., and J. H.Aldridge. 1981. Peritonsillarabscess: needle aspiration. Otolaryngol. Head Neck Surg.89:910-911. 8. Holdeman, L.V., E. P. Cato, and W. E. C. Moore(ed.). 1977.

Anaerobe laboratorymanual, 4th ed. VirginiaPolytechnic In-stituteandState University, Blacksburg.

9. Jokipii, A. M. M., P. Karma, K. Ojala, and L. Jokipii. 1977. J. CLIN. MICROBIOL.

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Anaerobic bacteria in chronic otitis media. Arch. Otolaryngol. 12. Sprinkle, P. M., R. W. Veltri, and L. M. Kantor. 1974.

Ab-103:278-280. scessesof the head and neck. Laryngoscope84:1142-1148.

10. Portman, M., D. Ingall, G. Westenfelder, and R. Yogev. 1984. 13. Sugita, R., S. Kawamura, G. Icikawa, Y. Fujimaki, T. Oguri, Peritonsillar abscess complicatinginfectious mononucleosis. J. and K. Deguchi. 1982.Microorganisms isolated from peritonsil-Pediatr. 104:742-744. lar abscess and indicated chemotherapy. Arch. Otolaryngol. 11. Schechter, G. L., D. E. Sly, A. L. Roper, and R. T. Jackson. 108:655-658.

1982. Changing faceoftreatmentofperitonsillar abscess. La- 14. Zar, J. H. 1974. Biostatistical analysis. Prentice-Hall, lnc.,

ryngoscope92:657-659. Englewood Cliffs, N.J.

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