Bacteria in Chronic Pekka Jukka
Maxillary Sinusitis
Karma, MD; Liisa Jokipii, MD; Pekka Sipil\l=a"\,MD; Luotonen, MD; Anssi M. M. Jokipii, MD
\s=b\ Sixty-one chronically inflamed maxillary sinuses produced 131 bacterial strains from mucosal pieces that were taken during a Caldwell-Luc operation and cultured aerobically and anaerobically. Sinus secretions showed only 62 and
nasal secretions 106 bacterial strains. Fourteen mucosal strains, including 11 Haemophilus influenzae, grew heavily. None of 24 mucosal anaerobes showed heavy growth. Of 52 antral mucosae with culturable bacteria, 37 disclosed mixed and 15 pure growth. The bacteriological characteristics of the diseased sinus and the nose did not correlate. The duration or extent of the disease, the macroscopic appearance of the diseased sinus, or the presence or absence of allergy were unrelated to bacteriological findings, except that H influenzae was concentrated in purulent sinuses. Intraoperative culture of antral mucosa seems to give the most reliable picture of the bacteriological condition in chronic maxillary sinusitis.
(Arch Otolaryngol 105:386-390, 1979)
characteristics sinusitis of chronic have been widely studied with vary¬ ing results. Although the reason for this variability has been admittedly more in different bacteriological sam¬ pling transportation and culture tech¬ niques than in real differences of bacterial flora,' - this has not led to clarification of the concepts with regard to the role of bacteria in the course of the disease. On the contrary, newer and more sensitive bacteriolog¬ ical methods, especially those that disclose anaerobic bacteria, have still increased the confusion.3 To avoid nasal contamination, which is inevitable in various antral puncture techniques, the bacterial specimen should be taken directly from the diseased maxillary sinus. Some of the latest investigators1'4" have done this by obtaining the speci¬ mens during the Caldwell-Luc opera-
The bacteriological maxillary
4
Accepted
for publication Jan 22, 1978. From the Institute of Clinical Sciences, University of Tampere, Finland (Dr Karma), the Department of Serology and Bacteriology, University of Helsinki (Dr L. Jokipii), and the Departments of Otolaryngology (Drs Sipil\l=a"\and Luotonen) and Medical Microbiology (Dr A. M. M. Jokipii), University of Oulu, Finland. Reprint requests to Institute of Clinical Sciences, University of Tampere, Teiskontie 35, 33520 Tampere 52, Finland (Dr Karma).
tion. Poor drainage of the chronically inflamed maxillary sinus reduces the antral Po27; thus, this encourages the growth of anaerobic bacteria. Howev¬ er, there are only a few studies that have made serious efforts to show anaerobic bacteria.3's Only one of these studies used an intraoperative technique' but combined the samples that were taken from three different paranasal sinuses during two differ¬ ent kinds of operations, which may reflect in their bacteriological re¬ sults. Mucosa is the real site of infection in chronic maxillary sinusitis. To our knowledge, the culture of mucosal pieces and the comparison of the results with those of simultaneously taken and cultured maxillary and nasal secretions has not been done. Further, to distinguish between sig¬ nificant bacteria and less important findings in individual cases, it is important, in addition to Gram's stain of the original specimen, to quantitate the growth results; this is a bacterio¬ logical principle that is very rarely included in previous studies.' To get a realistic picture of the bacteria and their role in chronic maxillary sinusitis we applied tech¬ niques and methods that followed the lines we have just described.
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Table 1.—Bacteria Isolated From 61 Consecutive Cases of Chronic
Maxillary Sinusitis
Secretion*
Nose4 Total No.
Organism
15
With Secretion
50
of Strains
10
13
19
20
Mucosa* Total No. of Strains
50
22
23
50
Total No. of Strains
36
38
13
13
dis S aureus Neisseria meningitidis Neisseria sp Bacillus subtilis
10
Diphtheroid bacillus Haemophilus influenzae Haemophilus sp Proteus morganii vulgaris Pseudomonas aeruginosa
13
Total
66
11
15
85
11
13 19
14
107
12
21
39
51
87
6
Anaerobic
Peptostreptococcus sp Peptococcus sp Veiltonella sp Anaerobic diphtheroid
14
14
10
Propionibacterium acnes Bacteroides fragilis melaninogenicus Bacteroides sp Fusobacterium sp Total Bacteria total
19
18 84
"Number of bacterial colonies per
16
primary plate
106
6
Table
Specimens
No
growth 1 2
3 4
5
6
3.—Bacteriological Category
Bacteriological Category
No. of Nose 14
15
13 14 3 1 1
Secretion 28 17 6 7 3 ...
Mucosa 9 15 15 10 7 2 3
24
19
106
11
Types
of
14
131
is indicated.
Table 2.—Number of Bacterial Strains in Various Types of
Strains
11 62
48
in Various
Secretion
Nose
Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth
Specimens
16
12
Mucosa 13
22
20
15
12 14
28
...
SUBJECTS
study consisted of 40 consecutive patients who were subjected to the Caldwell-Luc operation because of chronic maxillary sinusitis. There were 26 men and 14 women. The age of the patients ranged from 21 to 79 years (mean, 48 years). Twenty-one of the patients were operated on bilaterally; thus, 61 sinuses were stud¬ ied. Dry antra were not included in the study, and in every case, the diagnosis was confirmed also histologically. Clinically, Our
the disease had lasted for three to five months in 17 patients, for six to 11 months in 16, and for a year or longer in seven
patients.
The disease had usually been treated with repeated antral punctures and washings, but none of the patients had received antimicrobial agents during the week preceding the operation. Two antra had been operated on previously and were now subjected to revision. Clinical (asthma or rhinitis) and/or histological (eosinophils) allergic manifes¬ tations could be verified in nine patients (17 antra); all six patients (nine antra) with polyps belonged to this group. Antral secretions were macroscopically classified purulent in 43 and mucoid in 18 cases. In one case, the secretion had a fetid odor, but
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this infection could not be clinically defined dentogenous. even
METHODS
During the operation, immediately after opening the antral wall through the canine fossa, carefully avoiding gingival and oral contamination, an antral secretion was collected with a silver probe and spread on an enriched blood agar plate for anaerobic culture and on a chocolate agar plate for aerobic culture. Also two tubes of Schaedler broth (BBL), one for anaerobic culture and another for aerobic culture, were inoculated simultaneously. The plate and
Table
4.—Comparison
of
Three
Bacteriological Findings Between Specimens NoseSecretion
Bacteriological Finding All cultures according to bacterial species Both sterile in culture Same bacteriology in culture One strain different Two or more strains different All cultures according to
Types
the tube for anaerobic culture had been
of
NoseMucosa
SecretionMucosa
35
14 41
17 29
40
42
37
52
48
48
10
were
*Haemophilus influenzae
in six
cases
nasal secretion were taken with a silver probe from the middle meatus, strictly avoiding contamination from the nasal vestibulum. Incubation of all the specimens at 37 °C was immediately started at the Department of Otolaryngology, University of Oulu, Finland, and later the specimens were handled, analyzed and semiquantitated as described earlier." Further, a Gram's stain was taken of each specimen. The bacteriologist (L. J. and A. M. M. J) did not know anything about clinical find¬ ings before the completion of the study. For statistical analyses between clinical and bacteriological data, the - test and Fisher's exact test were used.
13
and
Diplococcus pneumoniae
in
then immersed into the two tubes.
Still, the respective specimens from the
bacteriological category
Pure culture in both Aerobic or facultative Anaerobic Mixed culture in both Aerobic or facultative only Anaerobic plus facultative "Category" different Cultures with heavy growth Neither showing heavy growth Same bacteriology Strain different
prereduced in an anaerobic system (GasPak), removed a few seconds before, and placed back immediately after inoculation. Aerobic cultures were put in a candle jar. Thereafter, two small pieces of antral mucosa were cultured similarly. The plates were first streaked with the pieces, which
one.
RESULTS Table
5.—Comparison of Bacteriological Findings
Bacteriological Finding
in 21 Bilateral Cases
Nose
All cultures according to bacterial species Both sterile in culture Same bacteriology in culture One strain different Two or more strains different All cultures according to bacteriological category Pure culture in both Mixed culture in both Aerobic or facultative only Anaerobic plus facultative
Mucosa
Secretion
2 6
5
1 1
6
3 16
...
...
13
10
_"Category" different_12_15_15 Cultures with heavy growth Both negative for heavy growth Same bacteriology Strain different
18
16
15
5
3
3f 3
...
...
*Both aerobic.
fAII Haemophilus influenzae.
Table 6—Mucosal
Bacteriological Category
in Relation to Duration of Disease Duration
Bacteriological Category Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth* Total "Number of cultures with
3-5
6-11
mo
1 yr
or more
bacterial strains and sinus secretions 62 strains. Ipsilateral nasal samples grew 106 strains. The occurrence of different bacterial strains and the quantitation of bacterial isolations in the three types of specimens can be seen in Table 1. The most commonly cultured bacteria in sinus specimens were Streptococcus viridans and Hae¬ mophilus influenzae (38 [62%] and 19 [31%], respectively, of mucosal cul¬ tures), and in nasal samples, diphtheroids and Staphylococcus epidermidis (21 [34%] and 20 [33%], respectively, of cultures). Eighteen percent of the bacterial strains were anaerobic in each of the three sites. Usually, the number of bacteria in each type of specimen was small. However, in ei¬ ther type of sinus specimens, influenzae grew in abundant numbers significantly more often than other bacteria ( - test, < .001) and signif¬ icantly more often than in the nose
(Fisher's exact test, mucosa, .024; secretion, .004). Nine (15%) of mucosae, 14 (23%) of nasal secretions, and 28 (46%) of sinus secretions did =
=
10
3(6) 25
heavy growth
mo
From 61 chronically inflamed max¬ illary sinuses mucosal pieces grew 131
5(7) 27
is indicated in parentheses.
1(...)
not grow any bacteria. Gram's stain confirmed the bacteriological finding in two thirds of the cases with heavy
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Signs
Table 7.—Mucosal Bacteriological Category in Relation to of Allergy, Appearance of Maxillary Sinus, and Extent of Disease Mucosa
Allergy Bacteriological Category
Yes
No
Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth* Total
Ethmoid Sinuses
Secretion
Polypous
Only
Purulent
Thick
Mucoid
Diseased
Healthy
10
15
10
12
19
8
1(2)
8(11)
17
44
2(3) 23
7(10) 38
5(12)
4(1)
43
2(3)
18
21
7(10) 40
*Number of cultures with heavy growth is indicated in parentheses.
growth, but usually did not show any bacteria in specimens with negative
culture. Pure culture was found in 15 (25%) of mucosal and nasal specimens (Ta¬ bles 2 and 3), and they usually grew aerobic bacteria. Mixed infections with two or three and sometimes even six strains were found in 37 mucosae (61%). Fifteen of them showed the mixture of anaerobic and facultative bacteria. Nasal samples had almost similar bacteriological distribution, but sinus secretions were highly significantly more seldom polymicrobic ( 2 test, < .001) and more often < .001) than negative ( 2 test, mucosal cultures. Bacteriological findings between the three different specimens in each case usually differed from each other
(Table 4). Only very rarely (in two [3%] to six [10%] of the cases, depend¬ ing on the pairs of specimens exam¬ ined) could we find exactly the same bacterial strains in two, and only once (2%) in all three specimens. When the bacteriological categorization de¬ scribed in Table 3 was used, the cate¬ gory was different in 37 (61%) to 42 (69%) of the cases between two types of specimens. When the most common bacteria of the sinuses were consid¬ ered, most coincidences were found with influenzae. If it was found from the nose, sinus secretion grew it in two thirds of cases, and if it was found from the secretion, sinus muco¬ sa grew it in ten of 11 cases. However, 19 sinus mucosae grew influenzae. When only bacterial strains with heavy growth were correlated, the same strain could be found in seven of
the 13 cases (54%) when secretion and/ or mucosa grew heavy growth. Nasal and sinus specimens never showed the same
heavy growth.
In 21 bilateral cases, the bacterio¬ logical characteristics also remarkably differed from side to side, regardless of the type of bacterial sample (Table 5). Only once did the mucosal samples grow the same bacteria, and 16 times, there was a difference of at least two bacterial strains between the two sides. The bacteriological category was different in 12 (57%) to 15 (71%) of pairs of specimens. Haemophilus in¬ fluenzae was found both bilaterally and unilaterally from five mucosae; in the nose and secretion it usually only grew unilaterally. Except for S viri· dans, often (in ten of the 16 cases with positive cultures) bilateral mucosally, other bacteria, irrespective of the type of specimen, rarely grew bilaterally. The same species showed heavy growth only in three pairs of mucosae, and it was H influenzae in every case.
bacteriological finding was essentially the same, irrespective of whether the disease had lasted only few months
same was
true for bacterial
for H
influenzae,
which favored purulent cases in all types of specimens ( 2 test, < .01). COMMENT
Simultaneous collection and similar
bacteriological processing of three different types of specimens in the present study of chronic maxillary sinusitis made possible their reliable bacteriological comparison. Because mucosal samples more than doubled the bacteriological yield of the sam¬ ples that were taken from sinus secre¬ tions, and because healthy mucosa is known to be sterile,1" it must be concluded that the samples that were taken from sinus mucosa most reliably reflect the bacteriological characteris¬ tics in chronic maxillary sinusitis. On the other hand, when correlations between the bacteriological character¬ istics of the nose and diseased sinus are looked for, the two secretions are the best comparable types of speci¬ men.
The mucosal
a
7). The
species, except
or even one
year
or
longer (Table 6). If, instead of bacteri¬ ological categories, most common mu¬
cosal bacteria were studied, the find¬ ings followed the same lines. When we tried to relate the mucosal bacterio¬ logical conditions to the cases with or without signs of allergy, to the extent of the disease and to the macroscopic appearance of the diseased sinus, again, the distribution of bacteriologi¬ cal categories was similar in all clini¬ cal groups that were compared (Table
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Our intraoperative mucosal culture method yielded more bacteria than found in earlier studies and showed the bacteriological characteristics of the diseased sinus to be more often
polymicrobic.1'2"11"12 However, only
14
strains (11%) in 13 cases (21%) showed heavy growth, which in 11 sinuses (85%) turned out to be influenzae. Consequently, if heavy growth per primary plate is regarded as a sign of a causal relationship between the inflammatory process and the bacteri¬ ological finding, influenzae should be regarded as the most important bacterial species in chronic maxillary
sinusitis. If nasal
findings
are
taken
to indicate the probability of nasal contamination among the sinus find¬ ings, then S viridans also seems to be
than a nasal contaminant, since it was more frequent in the sinus than in the nose. In many series,121013 Diplococcus pneumoniae is one of the most common bacteria. In the present study, its role was negligible. Our mucosal cultures disclosed 24 anaerobic bacterial strains in 17 (28%) sinuses, but they never grew heavily. For comparison, with the same meth¬ od, we cultured anaerobic bacteria in 33% of chronic middle ear discharges," and two thirds of them showed heavy growth. Thus, the lack of heavy anae¬ robic growth in chronically inflamed maxillary sinus cannot be only meth¬ odological. Urdal and Berdals found anaerobes in six of 36 cases (17%) of chronic maxillary sinusitis, but they did not quantitate their results, which were achieved by the puncture-aspira¬ tion method. Frederick and Braude,4 with their scrupulous anaerobic tech¬ niques, concluded that anaerobic bac¬ teria were the most important compo¬ nent of bacterial flora in chronic paranasal sinusitis. However, their cases were not restricted to maxillary sinus¬ itis, and they did not detail their material. Consequently, direct com¬ parisons with our contradictory re¬ sults are not possible. Success in culturing fastidious organisms is of¬ ten judged by the frequency of sterile cultures in the series. This was 15% in our study and 25% in the series reported by Frederick and Braude,4 thus providing no explanation for their better anaerobic success. Earlier communications have stressed the dominance of monomicrobial infections in chronic maxillary sinusitis1'281" and have shown 61% to 82% of positive cultures to be pure.1·2·401"1214 However, our cultures of mucosal pieces revealed 71% of the growths (37/52) to be mixed as could more
be supposed in the case of mucosal infections.1"' Fifteen pure cultures were evenly divided between differ¬ ent bacterial species; only two of them were anaerobic, and only three of them showed heavy growth, which again contrasted with the findings of Frederick and Braude,4 who found that among 83 specimens, there were 23 pure heavy anaerobic growths. Although nasal bacteriological find¬ ings were different from that of the healthy nose,10"418 in most cases it was also different from that of the diseased sinus. Consequently, we agree"1*1" that the bacteriological characteristics of maxillary sinusitis cannot be predicted from nasal sam¬ ples. Similar bacterial growth was found only in two of 21 bilateral muco¬ sal samples. This is far less than in earlier studies (52% to 72%)·112·2" and probably reflects the abundance of bacterial isolations found in this study. Thus, in bilateral cases, the bacteriological characteristics of both sinuses must be examined separate-
ly.
When
considering the clinical fac¬
studied, ie, duration of the disease, extent of the disease, signs of
tors
allergy, and appearance of the maxil¬ lary sinus, the bacteriological charac¬ teristics could not be shown to obey any certain clinical patterns, except for the quality of the sinus secretion. Purulent secretion grew H influenzae
significantly more often, and cultures with heavy growth tended to concen¬ trate in purulent cases. Other bacteria were relatively evenly distributed in
the various groups and classifications of the present material, and these bacteria usually showed only light or moderate growth. Thus, their clinical significance in chronic maxillary sinusitis is questionable. Irja Jouhten, Maisa Korvala, and Anita Mutanprovided technical assistance, and Terttu Jokinen provided secretarial assistance. en
References 1. Palva T, Gr\l=o"\nroosJA, Palva A: Bacteriology and pathology of chronic maxillary sinusitis. Acta Otolaryngol 54:159-175, 1962. 2. Lystad A, Berdal P, Lund-Iversen L: The bacterial flora of sinusitis with an in vitro study of the bacterial resistance to antibiotics. Acta Otolaryngol Suppl 188:390-400, 1964. 3. Fredette V, Auger A, Forget A: Anaerobic flora of chronic nasal sinusitis in adults. Can Med Assoc J 84:164-165, 1961. 4. Frederick J, Braude AI: Anaerobic infection of paranasal sinuses. N Engl J Med 290:135-137, 1974. 5. Catlin FI, Cluff LE, Reynolds RC: The bacteriology of acute and chronic sinusitis. South Med J 58:1497-1502, 1965. 6. Kessler L: Die Bakterienflora der Nasenhaupt-und Nasennebenh\l=o"\hlenbei chronischen Sinuitiden und ihre Beziehung zueinender. HNO 16:36-39, 1968. 7. Aust R, Drettner B: Ventilatory studies of the maxillary sinus. Int Rhinol 9:69-78, 1971. 8. Urdal K, Berdal P: The microbial flora in 81 cases of maxillary sinusitis. Acta Otolaryngol 37:20-25, 1949. 9. Jokipii AMM, Karma P, Ojala K, et al: Anaerobic bacteria in chronic otitis media. Arch Otolaryngol 103:278-280, 1977. 10. Bj\l=o"\rkwallT: Bacteriological examinations in maxillary sinusitis. Acta Otolaryngol Suppl 83:1-58, 1950. 11. Sparrevohn UR, Buch A: The bacteriology of maxillary sinusitis. Acta Otolaryngol 34:425\x=req-\ 436, 1946. 12. Kinnman J, Lee CW, Park SH: Bacterial flora in chronic, purulent maxillary sinusitis. Acta Otolaryngol 64:37-44, 1967. 13. Van Dishoeck HAE, Franssen MGC: The incidence and correlation of allergy and chronic maxillary sinusitis. Pract Otorhinolaryngol 19:502-506, 1957. 14. Majapuro T: Results from the Caldwell-Luc operation: A clinical follow-up study of 448 patients. Acta Univ Oul, series D, 13:1-66, 1976. 15. Gorbach SL, Bartlett JG: Anaerobic infections. N Engl J Med 290:1177-1184, 1237-1245, 1289-1294, 1974. 16. Rippon JE, Vogelsang TM: Carriage of pathogenic staphylococci in the upper respiratory tract of children. Acta Pathol Microbiol Scand B 39:284-296, 1956. 17. Cetin ET, T\l=o"\reciK, Agbaba \l=O"\,et al: Study of oral, nasal and skin flora in an investigation on hospital infection. Pathol Microbiol 37:324-332, 1971. 18. Axelsson A, Brorson JE: The correlation between bacteriological findings in the nose and maxillary sinus in acute maxillary sinusitis. Laryngoscope 83:2003-2011, 1973. 19. Krajina Z, Koskovic F, Babic I: The bacteriology of the respiratory tract in various pathological conditions. Acta Otolaryngol 67:453-459, 1969. 20. Kortekangas AE: Antibiotics in the treatment of maxillary sinusitis. Acta Otolaryngol Suppl 188:379-389, 1964.
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Maxillary Sinusitis
Karma, MD; Liisa Jokipii, MD; Pekka Sipil\l=a"\,MD; Luotonen, MD; Anssi M. M. Jokipii, MD
\s=b\ Sixty-one chronically inflamed maxillary sinuses produced 131 bacterial strains from mucosal pieces that were taken during a Caldwell-Luc operation and cultured aerobically and anaerobically. Sinus secretions showed only 62 and
nasal secretions 106 bacterial strains. Fourteen mucosal strains, including 11 Haemophilus influenzae, grew heavily. None of 24 mucosal anaerobes showed heavy growth. Of 52 antral mucosae with culturable bacteria, 37 disclosed mixed and 15 pure growth. The bacteriological characteristics of the diseased sinus and the nose did not correlate. The duration or extent of the disease, the macroscopic appearance of the diseased sinus, or the presence or absence of allergy were unrelated to bacteriological findings, except that H influenzae was concentrated in purulent sinuses. Intraoperative culture of antral mucosa seems to give the most reliable picture of the bacteriological condition in chronic maxillary sinusitis.
(Arch Otolaryngol 105:386-390, 1979)
characteristics sinusitis of chronic have been widely studied with vary¬ ing results. Although the reason for this variability has been admittedly more in different bacteriological sam¬ pling transportation and culture tech¬ niques than in real differences of bacterial flora,' - this has not led to clarification of the concepts with regard to the role of bacteria in the course of the disease. On the contrary, newer and more sensitive bacteriolog¬ ical methods, especially those that disclose anaerobic bacteria, have still increased the confusion.3 To avoid nasal contamination, which is inevitable in various antral puncture techniques, the bacterial specimen should be taken directly from the diseased maxillary sinus. Some of the latest investigators1'4" have done this by obtaining the speci¬ mens during the Caldwell-Luc opera-
The bacteriological maxillary
4
Accepted
for publication Jan 22, 1978. From the Institute of Clinical Sciences, University of Tampere, Finland (Dr Karma), the Department of Serology and Bacteriology, University of Helsinki (Dr L. Jokipii), and the Departments of Otolaryngology (Drs Sipil\l=a"\and Luotonen) and Medical Microbiology (Dr A. M. M. Jokipii), University of Oulu, Finland. Reprint requests to Institute of Clinical Sciences, University of Tampere, Teiskontie 35, 33520 Tampere 52, Finland (Dr Karma).
tion. Poor drainage of the chronically inflamed maxillary sinus reduces the antral Po27; thus, this encourages the growth of anaerobic bacteria. Howev¬ er, there are only a few studies that have made serious efforts to show anaerobic bacteria.3's Only one of these studies used an intraoperative technique' but combined the samples that were taken from three different paranasal sinuses during two differ¬ ent kinds of operations, which may reflect in their bacteriological re¬ sults. Mucosa is the real site of infection in chronic maxillary sinusitis. To our knowledge, the culture of mucosal pieces and the comparison of the results with those of simultaneously taken and cultured maxillary and nasal secretions has not been done. Further, to distinguish between sig¬ nificant bacteria and less important findings in individual cases, it is important, in addition to Gram's stain of the original specimen, to quantitate the growth results; this is a bacterio¬ logical principle that is very rarely included in previous studies.' To get a realistic picture of the bacteria and their role in chronic maxillary sinusitis we applied tech¬ niques and methods that followed the lines we have just described.
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Table 1.—Bacteria Isolated From 61 Consecutive Cases of Chronic
Maxillary Sinusitis
Secretion*
Nose4 Total No.
Organism
15
With Secretion
50
of Strains
10
13
19
20
Mucosa* Total No. of Strains
50
22
23
50
Total No. of Strains
36
38
13
13
dis S aureus Neisseria meningitidis Neisseria sp Bacillus subtilis
10
Diphtheroid bacillus Haemophilus influenzae Haemophilus sp Proteus morganii vulgaris Pseudomonas aeruginosa
13
Total
66
11
15
85
11
13 19
14
107
12
21
39
51
87
6
Anaerobic
Peptostreptococcus sp Peptococcus sp Veiltonella sp Anaerobic diphtheroid
14
14
10
Propionibacterium acnes Bacteroides fragilis melaninogenicus Bacteroides sp Fusobacterium sp Total Bacteria total
19
18 84
"Number of bacterial colonies per
16
primary plate
106
6
Table
Specimens
No
growth 1 2
3 4
5
6
3.—Bacteriological Category
Bacteriological Category
No. of Nose 14
15
13 14 3 1 1
Secretion 28 17 6 7 3 ...
Mucosa 9 15 15 10 7 2 3
24
19
106
11
Types
of
14
131
is indicated.
Table 2.—Number of Bacterial Strains in Various Types of
Strains
11 62
48
in Various
Secretion
Nose
Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth
Specimens
16
12
Mucosa 13
22
20
15
12 14
28
...
SUBJECTS
study consisted of 40 consecutive patients who were subjected to the Caldwell-Luc operation because of chronic maxillary sinusitis. There were 26 men and 14 women. The age of the patients ranged from 21 to 79 years (mean, 48 years). Twenty-one of the patients were operated on bilaterally; thus, 61 sinuses were stud¬ ied. Dry antra were not included in the study, and in every case, the diagnosis was confirmed also histologically. Clinically, Our
the disease had lasted for three to five months in 17 patients, for six to 11 months in 16, and for a year or longer in seven
patients.
The disease had usually been treated with repeated antral punctures and washings, but none of the patients had received antimicrobial agents during the week preceding the operation. Two antra had been operated on previously and were now subjected to revision. Clinical (asthma or rhinitis) and/or histological (eosinophils) allergic manifes¬ tations could be verified in nine patients (17 antra); all six patients (nine antra) with polyps belonged to this group. Antral secretions were macroscopically classified purulent in 43 and mucoid in 18 cases. In one case, the secretion had a fetid odor, but
Downloaded From: http://archotol.jamanetwork.com/ by a Michigan State University User on 06/08/2015
this infection could not be clinically defined dentogenous. even
METHODS
During the operation, immediately after opening the antral wall through the canine fossa, carefully avoiding gingival and oral contamination, an antral secretion was collected with a silver probe and spread on an enriched blood agar plate for anaerobic culture and on a chocolate agar plate for aerobic culture. Also two tubes of Schaedler broth (BBL), one for anaerobic culture and another for aerobic culture, were inoculated simultaneously. The plate and
Table
4.—Comparison
of
Three
Bacteriological Findings Between Specimens NoseSecretion
Bacteriological Finding All cultures according to bacterial species Both sterile in culture Same bacteriology in culture One strain different Two or more strains different All cultures according to
Types
the tube for anaerobic culture had been
of
NoseMucosa
SecretionMucosa
35
14 41
17 29
40
42
37
52
48
48
10
were
*Haemophilus influenzae
in six
cases
nasal secretion were taken with a silver probe from the middle meatus, strictly avoiding contamination from the nasal vestibulum. Incubation of all the specimens at 37 °C was immediately started at the Department of Otolaryngology, University of Oulu, Finland, and later the specimens were handled, analyzed and semiquantitated as described earlier." Further, a Gram's stain was taken of each specimen. The bacteriologist (L. J. and A. M. M. J) did not know anything about clinical find¬ ings before the completion of the study. For statistical analyses between clinical and bacteriological data, the - test and Fisher's exact test were used.
13
and
Diplococcus pneumoniae
in
then immersed into the two tubes.
Still, the respective specimens from the
bacteriological category
Pure culture in both Aerobic or facultative Anaerobic Mixed culture in both Aerobic or facultative only Anaerobic plus facultative "Category" different Cultures with heavy growth Neither showing heavy growth Same bacteriology Strain different
prereduced in an anaerobic system (GasPak), removed a few seconds before, and placed back immediately after inoculation. Aerobic cultures were put in a candle jar. Thereafter, two small pieces of antral mucosa were cultured similarly. The plates were first streaked with the pieces, which
one.
RESULTS Table
5.—Comparison of Bacteriological Findings
Bacteriological Finding
in 21 Bilateral Cases
Nose
All cultures according to bacterial species Both sterile in culture Same bacteriology in culture One strain different Two or more strains different All cultures according to bacteriological category Pure culture in both Mixed culture in both Aerobic or facultative only Anaerobic plus facultative
Mucosa
Secretion
2 6
5
1 1
6
3 16
...
...
13
10
_"Category" different_12_15_15 Cultures with heavy growth Both negative for heavy growth Same bacteriology Strain different
18
16
15
5
3
3f 3
...
...
*Both aerobic.
fAII Haemophilus influenzae.
Table 6—Mucosal
Bacteriological Category
in Relation to Duration of Disease Duration
Bacteriological Category Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth* Total "Number of cultures with
3-5
6-11
mo
1 yr
or more
bacterial strains and sinus secretions 62 strains. Ipsilateral nasal samples grew 106 strains. The occurrence of different bacterial strains and the quantitation of bacterial isolations in the three types of specimens can be seen in Table 1. The most commonly cultured bacteria in sinus specimens were Streptococcus viridans and Hae¬ mophilus influenzae (38 [62%] and 19 [31%], respectively, of mucosal cul¬ tures), and in nasal samples, diphtheroids and Staphylococcus epidermidis (21 [34%] and 20 [33%], respectively, of cultures). Eighteen percent of the bacterial strains were anaerobic in each of the three sites. Usually, the number of bacteria in each type of specimen was small. However, in ei¬ ther type of sinus specimens, influenzae grew in abundant numbers significantly more often than other bacteria ( - test, < .001) and signif¬ icantly more often than in the nose
(Fisher's exact test, mucosa, .024; secretion, .004). Nine (15%) of mucosae, 14 (23%) of nasal secretions, and 28 (46%) of sinus secretions did =
=
10
3(6) 25
heavy growth
mo
From 61 chronically inflamed max¬ illary sinuses mucosal pieces grew 131
5(7) 27
is indicated in parentheses.
1(...)
not grow any bacteria. Gram's stain confirmed the bacteriological finding in two thirds of the cases with heavy
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Signs
Table 7.—Mucosal Bacteriological Category in Relation to of Allergy, Appearance of Maxillary Sinus, and Extent of Disease Mucosa
Allergy Bacteriological Category
Yes
No
Pure culture Aerobic or facultative Anaerobic Mixed culture Aerobic or facultative only Anaerobic plus facultative No growth* Total
Ethmoid Sinuses
Secretion
Polypous
Only
Purulent
Thick
Mucoid
Diseased
Healthy
10
15
10
12
19
8
1(2)
8(11)
17
44
2(3) 23
7(10) 38
5(12)
4(1)
43
2(3)
18
21
7(10) 40
*Number of cultures with heavy growth is indicated in parentheses.
growth, but usually did not show any bacteria in specimens with negative
culture. Pure culture was found in 15 (25%) of mucosal and nasal specimens (Ta¬ bles 2 and 3), and they usually grew aerobic bacteria. Mixed infections with two or three and sometimes even six strains were found in 37 mucosae (61%). Fifteen of them showed the mixture of anaerobic and facultative bacteria. Nasal samples had almost similar bacteriological distribution, but sinus secretions were highly significantly more seldom polymicrobic ( 2 test, < .001) and more often < .001) than negative ( 2 test, mucosal cultures. Bacteriological findings between the three different specimens in each case usually differed from each other
(Table 4). Only very rarely (in two [3%] to six [10%] of the cases, depend¬ ing on the pairs of specimens exam¬ ined) could we find exactly the same bacterial strains in two, and only once (2%) in all three specimens. When the bacteriological categorization de¬ scribed in Table 3 was used, the cate¬ gory was different in 37 (61%) to 42 (69%) of the cases between two types of specimens. When the most common bacteria of the sinuses were consid¬ ered, most coincidences were found with influenzae. If it was found from the nose, sinus secretion grew it in two thirds of cases, and if it was found from the secretion, sinus muco¬ sa grew it in ten of 11 cases. However, 19 sinus mucosae grew influenzae. When only bacterial strains with heavy growth were correlated, the same strain could be found in seven of
the 13 cases (54%) when secretion and/ or mucosa grew heavy growth. Nasal and sinus specimens never showed the same
heavy growth.
In 21 bilateral cases, the bacterio¬ logical characteristics also remarkably differed from side to side, regardless of the type of bacterial sample (Table 5). Only once did the mucosal samples grow the same bacteria, and 16 times, there was a difference of at least two bacterial strains between the two sides. The bacteriological category was different in 12 (57%) to 15 (71%) of pairs of specimens. Haemophilus in¬ fluenzae was found both bilaterally and unilaterally from five mucosae; in the nose and secretion it usually only grew unilaterally. Except for S viri· dans, often (in ten of the 16 cases with positive cultures) bilateral mucosally, other bacteria, irrespective of the type of specimen, rarely grew bilaterally. The same species showed heavy growth only in three pairs of mucosae, and it was H influenzae in every case.
bacteriological finding was essentially the same, irrespective of whether the disease had lasted only few months
same was
true for bacterial
for H
influenzae,
which favored purulent cases in all types of specimens ( 2 test, < .01). COMMENT
Simultaneous collection and similar
bacteriological processing of three different types of specimens in the present study of chronic maxillary sinusitis made possible their reliable bacteriological comparison. Because mucosal samples more than doubled the bacteriological yield of the sam¬ ples that were taken from sinus secre¬ tions, and because healthy mucosa is known to be sterile,1" it must be concluded that the samples that were taken from sinus mucosa most reliably reflect the bacteriological characteris¬ tics in chronic maxillary sinusitis. On the other hand, when correlations between the bacteriological character¬ istics of the nose and diseased sinus are looked for, the two secretions are the best comparable types of speci¬ men.
The mucosal
a
7). The
species, except
or even one
year
or
longer (Table 6). If, instead of bacteri¬ ological categories, most common mu¬
cosal bacteria were studied, the find¬ ings followed the same lines. When we tried to relate the mucosal bacterio¬ logical conditions to the cases with or without signs of allergy, to the extent of the disease and to the macroscopic appearance of the diseased sinus, again, the distribution of bacteriologi¬ cal categories was similar in all clini¬ cal groups that were compared (Table
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Our intraoperative mucosal culture method yielded more bacteria than found in earlier studies and showed the bacteriological characteristics of the diseased sinus to be more often
polymicrobic.1'2"11"12 However, only
14
strains (11%) in 13 cases (21%) showed heavy growth, which in 11 sinuses (85%) turned out to be influenzae. Consequently, if heavy growth per primary plate is regarded as a sign of a causal relationship between the inflammatory process and the bacteri¬ ological finding, influenzae should be regarded as the most important bacterial species in chronic maxillary
sinusitis. If nasal
findings
are
taken
to indicate the probability of nasal contamination among the sinus find¬ ings, then S viridans also seems to be
than a nasal contaminant, since it was more frequent in the sinus than in the nose. In many series,121013 Diplococcus pneumoniae is one of the most common bacteria. In the present study, its role was negligible. Our mucosal cultures disclosed 24 anaerobic bacterial strains in 17 (28%) sinuses, but they never grew heavily. For comparison, with the same meth¬ od, we cultured anaerobic bacteria in 33% of chronic middle ear discharges," and two thirds of them showed heavy growth. Thus, the lack of heavy anae¬ robic growth in chronically inflamed maxillary sinus cannot be only meth¬ odological. Urdal and Berdals found anaerobes in six of 36 cases (17%) of chronic maxillary sinusitis, but they did not quantitate their results, which were achieved by the puncture-aspira¬ tion method. Frederick and Braude,4 with their scrupulous anaerobic tech¬ niques, concluded that anaerobic bac¬ teria were the most important compo¬ nent of bacterial flora in chronic paranasal sinusitis. However, their cases were not restricted to maxillary sinus¬ itis, and they did not detail their material. Consequently, direct com¬ parisons with our contradictory re¬ sults are not possible. Success in culturing fastidious organisms is of¬ ten judged by the frequency of sterile cultures in the series. This was 15% in our study and 25% in the series reported by Frederick and Braude,4 thus providing no explanation for their better anaerobic success. Earlier communications have stressed the dominance of monomicrobial infections in chronic maxillary sinusitis1'281" and have shown 61% to 82% of positive cultures to be pure.1·2·401"1214 However, our cultures of mucosal pieces revealed 71% of the growths (37/52) to be mixed as could more
be supposed in the case of mucosal infections.1"' Fifteen pure cultures were evenly divided between differ¬ ent bacterial species; only two of them were anaerobic, and only three of them showed heavy growth, which again contrasted with the findings of Frederick and Braude,4 who found that among 83 specimens, there were 23 pure heavy anaerobic growths. Although nasal bacteriological find¬ ings were different from that of the healthy nose,10"418 in most cases it was also different from that of the diseased sinus. Consequently, we agree"1*1" that the bacteriological characteristics of maxillary sinusitis cannot be predicted from nasal sam¬ ples. Similar bacterial growth was found only in two of 21 bilateral muco¬ sal samples. This is far less than in earlier studies (52% to 72%)·112·2" and probably reflects the abundance of bacterial isolations found in this study. Thus, in bilateral cases, the bacteriological characteristics of both sinuses must be examined separate-
ly.
When
considering the clinical fac¬
studied, ie, duration of the disease, extent of the disease, signs of
tors
allergy, and appearance of the maxil¬ lary sinus, the bacteriological charac¬ teristics could not be shown to obey any certain clinical patterns, except for the quality of the sinus secretion. Purulent secretion grew H influenzae
significantly more often, and cultures with heavy growth tended to concen¬ trate in purulent cases. Other bacteria were relatively evenly distributed in
the various groups and classifications of the present material, and these bacteria usually showed only light or moderate growth. Thus, their clinical significance in chronic maxillary sinusitis is questionable. Irja Jouhten, Maisa Korvala, and Anita Mutanprovided technical assistance, and Terttu Jokinen provided secretarial assistance. en
References 1. Palva T, Gr\l=o"\nroosJA, Palva A: Bacteriology and pathology of chronic maxillary sinusitis. Acta Otolaryngol 54:159-175, 1962. 2. Lystad A, Berdal P, Lund-Iversen L: The bacterial flora of sinusitis with an in vitro study of the bacterial resistance to antibiotics. Acta Otolaryngol Suppl 188:390-400, 1964. 3. Fredette V, Auger A, Forget A: Anaerobic flora of chronic nasal sinusitis in adults. Can Med Assoc J 84:164-165, 1961. 4. Frederick J, Braude AI: Anaerobic infection of paranasal sinuses. N Engl J Med 290:135-137, 1974. 5. Catlin FI, Cluff LE, Reynolds RC: The bacteriology of acute and chronic sinusitis. South Med J 58:1497-1502, 1965. 6. Kessler L: Die Bakterienflora der Nasenhaupt-und Nasennebenh\l=o"\hlenbei chronischen Sinuitiden und ihre Beziehung zueinender. HNO 16:36-39, 1968. 7. Aust R, Drettner B: Ventilatory studies of the maxillary sinus. Int Rhinol 9:69-78, 1971. 8. Urdal K, Berdal P: The microbial flora in 81 cases of maxillary sinusitis. Acta Otolaryngol 37:20-25, 1949. 9. Jokipii AMM, Karma P, Ojala K, et al: Anaerobic bacteria in chronic otitis media. Arch Otolaryngol 103:278-280, 1977. 10. Bj\l=o"\rkwallT: Bacteriological examinations in maxillary sinusitis. Acta Otolaryngol Suppl 83:1-58, 1950. 11. Sparrevohn UR, Buch A: The bacteriology of maxillary sinusitis. Acta Otolaryngol 34:425\x=req-\ 436, 1946. 12. Kinnman J, Lee CW, Park SH: Bacterial flora in chronic, purulent maxillary sinusitis. Acta Otolaryngol 64:37-44, 1967. 13. Van Dishoeck HAE, Franssen MGC: The incidence and correlation of allergy and chronic maxillary sinusitis. Pract Otorhinolaryngol 19:502-506, 1957. 14. Majapuro T: Results from the Caldwell-Luc operation: A clinical follow-up study of 448 patients. Acta Univ Oul, series D, 13:1-66, 1976. 15. Gorbach SL, Bartlett JG: Anaerobic infections. N Engl J Med 290:1177-1184, 1237-1245, 1289-1294, 1974. 16. Rippon JE, Vogelsang TM: Carriage of pathogenic staphylococci in the upper respiratory tract of children. Acta Pathol Microbiol Scand B 39:284-296, 1956. 17. Cetin ET, T\l=o"\reciK, Agbaba \l=O"\,et al: Study of oral, nasal and skin flora in an investigation on hospital infection. Pathol Microbiol 37:324-332, 1971. 18. Axelsson A, Brorson JE: The correlation between bacteriological findings in the nose and maxillary sinus in acute maxillary sinusitis. Laryngoscope 83:2003-2011, 1973. 19. Krajina Z, Koskovic F, Babic I: The bacteriology of the respiratory tract in various pathological conditions. Acta Otolaryngol 67:453-459, 1969. 20. Kortekangas AE: Antibiotics in the treatment of maxillary sinusitis. Acta Otolaryngol Suppl 188:379-389, 1964.
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