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Streptococcus milleri head and neck abscesses: a case series.

Abstract

Streptococcus milleri infections and abscesses in the head and neck region have been previously reported, but there is still a dearth of clinical literature on this topic. To add to the available reports and to promote a better understanding and awareness of this clinically important entity, we present this retrospective review of 7 cases of head and neck abscess caused by S milleri infection. We have placed particular emphasis on antibiotic sensitivity patterns. These patients--6 men and 1 woman, aged 28 to 73 years (mean: 42.7)--had been seen at a district general hospital in Gosford, Australia, over a 6-month period. All patients had undergone surgical intervention and had been treated with intravenous antibiotics. All the S milleri cultures were sensitive topenicillin G, cephalexin, and erythromycin. Six of these patients experienced a resolution of their abscess, while 1 patient died from overwhelming sepsis. We believe that the initiation of penicillin G, cephalexin, or erythromycin is a good starting point for empiric therapy. S milleri should be considered as a causative organism in a patient who presents with a head and neck abscess, especially in the presence of a dental infection. Such a patient should be monitored closely for airway obstruction and distal infective sequelae. Also in this article, we compare our findings with those reported in two other published series.

Introduction

Streptococcus milleri comprises a group of three distinct gram-positive species: Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus. The

identification and classification of this group of bacteria have been historically complicated, and hence recognition of S milleri infections may be under-reported. (1)

Guthof coined the term Streptococcus milleri in 1956 to describe nonhemolytic streptococci that were isolated from oral infections; his intention was to honor oral microbiologist W.D. Miller (1853-1907). (2) S milleri is a common commensal organism found in the oral cavity, gingival crevices, dental plaque, dental root canals, throat, oropharynx, gastrointestinal tract, appendix, stool, and the vaginal canal. (3)

S milleri is well known for its ability to cause purulent infections and abscesses at various sites in the body. Infections caused by this organism usually occur in the abdominal/hepatobiliary system and in the thoracic cavity, while abscesses usually occur in the liver, abdomen, pelvis, lung, and brain. (4)

A number of cases of S milleri infections and abscesses of the head and neck region have been previously reported, but there is still a dearth of clinical literature about these pathologies. Han and Kerschner (5) in Milwaukee published a series of 26 cases in 2001, and Hirai et al (6) in Hiroshima reviewed 17 cases in 2005. We describe a small series of patients with an abscess of the head and neck caused by S milleri infection, and we pay particular attention to antibiotic sensitivities in comparison with the two previous case series. It is our wish to add to the available literature and to promote a better understanding and awareness of this clinically important entity.

Patients and methods

We retrospectively reviewed 7 cases of head and neck abscess secondary to S milleri infection that had been treated over a 6-month period in the Department of Otolaryngology at Gosford Hospital in New South Wales, Australia. The 7 patients included 6 men and 1 woman, aged 28 to 73 years (mean: 42.7).

In addition to demographic data, we compiled information on the site of the abscess, comorbidities, the clinical presentation and treatment, outcomes, and inpatient and discharge antibiotic regimens. We also paid particular attention to culture sensitivity patterns. Pus cultured from each of the 7 patients had grown S milleri. Identification of the causative pathogen had been made by the hospital's microbiology service. (At Gosford Hospital microbiologic cultures are reported only as S milleri; they are not further subclassified as either S intermedius, S constellatus, or S anginosus.)

Once our data were complied, we compared our findings with those of Han and Kerschne (5) (the Milwaukee group) and Hirai et al (6) (the Hiroshima group), keeping in mind that our study included only abscesses, while the other two studies included both S milleri infections and abscesses.

Results

Our findings are summarized in table 1, and a comparison of our findings with those of the Milwaukee group and the Hiroshima group is shown in table 2.

Sex and age. The male preponderance in our population (86%) was similar to the proportions of both the Milwaukee group and the Hiroshima group--81 and 71%, respectively. Incidentally, in a review of 28 cases of S milleri infection throughout the body, Shlaes et al also found a striking predisposition for males (6:1). (7)

With respect to age, our group was obviously older than the pediatric cohort in the Milwaukee group, and it was generally similar to the Hiroshima group.

Site of abscess. The most common site of abscess in our series was the submandibular space, wherein 5 of 7 cases (71%) were located. This is in contrast to both the Milwaukee and Hiroshima groups, where sinus involvement was most common (the paranasal and maxillary sinuses, respectively.) On the other hand, our finding is compatible with that of an Italian review of 24 deep neck space infections, which found that 67% of the abscesses studied occurred in the submandibular space. (8) It is interesting that in the Italian study, the most common organism isolated from those abscesses was S milleri, which accounted for half of the total.

Comorbidities. Three of the 7 patients in our study (43%) had at least one major comorbidity, the most common being diabetes mellitus. In the Milwaukee group, only 1 of the 26 patients (4%) had a major comorbidity (cystic fibrosis), but this is not surprising considering that this group represented a purely pediatric population. In the Hiroshima group, a major comorbidity was documented in 3 of the 17 patients (18%); there was 1 case each of diabetes mellitus, human immunodeficiency virus infection, and heart failure.

Treatment. All of our patients required surgical intervention and treatment with at least one intravenous antibiotic. Overall, our patients were treated successfully and relatively easily, even though nearly all of them exhibited signs of systemic sepsis on presentation. The exception was patient 5, who died as a direct result of overwhelming S milleri sepsis from his head and neck abscess. A similar death from sepsis in a patient with S milleri head and neck infection was reported in Wales by Flanagan and Mills in 1994. (9) In their case, the deceased patient was a previously healthy adult, whereas our patient had coexisting diabetes mellitus. Jacobs et al reported a series of predominately intra-abdominal S milleri infections in which the mortality rate reached 22%. (10)

Outcomes. Only 1 of the 6 survivors (patient 7) had a difficult course once treatment was initiated. The others were hospitalized for less than 1 week.

Length of stay. The mean length of hospital stay in our series was 8 days. This excluded 1 case in which the patient self-discharged against medical advice on day 3, and the 1 death, which occurred on day 22.

Sensitivity patterns. The S milleri cultured from our patients exhibited universally identical sensitivity patterns, as all the isolates were sensitive to penicillin G, cephalexin, and erythromycin. By contrast, the Milwaukee study found a slight decline in the sensitivity of S milleri to penicillin over the 3-year period from 1996 to 1999, and a much greater decline in sensitivity to erythromycin (from 97 to 84%) over the same 3 years. In the Hiroshima group, only 71% of cases were sensitive to ampicillin, but 100% were sensitive to second-, third-, and fourth-generation cephalosporins. These differences illustrate the regional variations in antibiotic sensitivities in S milleri. In our series, cultures of 4 of the 7 patients (57%) grew organisms other than S milleri; corresponding figures in the Milwaukee and Hiroshima groups were 31 and 53%. In the pediatric (Milwaukee) group, these concomitantly cultured organisms included Aspergillus fumigatus, Eikenella corrodens, Haemophilus influenzae, Peptostreptococcus spp, Proteus mirabilis, Pseudomonas aeruginosa, Staphylococcus aureus, Staphylococcus epidermidis, and Streptococcus pneumoniae. In the adult (Hiroshima) group, they included anaerobes, Fusobacterium spp, Haemophilus spp, methicillin-susceptible S aureus, Peptostreptococcus spp, and Prevotella spp. Our series shows a similar incidence of concomitantly cultured organisms in an adult population.

Discussion

In many ways, our findings were similar to those of the Milwaukee (5) and Hiroshima studies. (6) A notable exception was the difference in antibiotic sensitivity patterns, which are presumably influenced by local antibiotic prescribing practices and environmental factors.

S milleri has several properties that make it so pathogenic. It appears to induce less chemotaxis of polymorphonuclear leukocytes than does S aureus, a common abscess-forming pathogen, (11) and this allows S milleri more time to proliferate prior to phagocytosis. It also appears that it takes leukocytes more time to kill S milleri once they have been phagocytosed, the rate of killing by leukocytes being substantially slower than the rate of killing of S aureus. (11)

S milleri possesses several other cell-surface characteristics that may promote the formation of abscesses, including the production of hyaluronidase. Hyaluronic acid is a major component of the interstitial barrier, and its hydrolysis by hyaluronidase increases the permeability of tissues. (12)

One of the three S milleri subtypes, S intermedius, has been shown to produce a human-specific cytolysin called intermedilysin. Intermedilysin is known to lyse cells of the human immune system, including neutrophils. The presence ors intermedius in sites of deep infection correlates with an increase in the production of this cytolysin. Moreover, S intermedius cultured from dental plaque has also exhibited this increased production. (13)

In vitro studies of S milleri have found a gliding type of motility across surfaces with the production of an extracellular material. This is thought to aid movement in the apparent absence of traditional organs of motility such as flagella. (14) It has been proposed that this may aid in the spread of infective organisms in vivo.

The pathogenicity of S milleri is enhanced by its ability to spread hematogenously. (15) In our series, patient 5 developed infective endocarditis several days after his admission. The ability of S milleri to spread hematogenously, to bind fibronectin, and to cause aggregation of platelets and then be incorporated into clots has been widely implicated in the development of endocarditis. In some studies, 9 to 15% of cases of community-acquired endocarditis have been reported to be caused by S milleri. (16)

In view of the potential for hematogenous spread of S milleri in the head and neck region, prompt and definitive treatment is vital in order to prevent intracranial sepsis. S milleri is the most common organism isolated from sinus-disease-related intracranial sepsis. (12) Another reason for prompt treatment is the space-occupying nature of some head and neck abscesses, which can rapidly lead to airway compromise, as occurred in patient 5 and patient 7 (figure) in our series.

In conclusion, S milleri should be considered as a causative organism in a patient who presents with a head/neck abscess, especially in the presence of poor dental hygiene. The possibility of rapid deterioration, airway compromise, and involvement of anatomically distant organs must be kept in mind. Individual antibiotic sensitivities should be sought as soon as possible, but empiric antibiotic therapy with penicillin or a cephalosporin appears to be very appropriate, at least in Australia. The presence of a co-organism should also be borne in mind.

Acknowledgments

We thank Dr. Rosemary Stratford of the Emergency Department at Gosford Hospital and Mr. Julian Savage of the ENT Department at Southmead Hospital in Bristol, U.K.

[FIGURE OMITTED]

References

(1.) Ruoff KL. Streptococcus anginosus ("Streptococcus milleri"): The unrecognized pathogen. Clin Microbiol Rev 1988;1(1): 102-8.

(2.) GuthofO. Pathogenic strains of Streptococcus viridans; streptococci found in dental abscesses and infiltrates in the region of the oral cavity [in German]. Zentralbl Bakteriol Orig 1956; 166(7-8):553-64.

(3.) Mirzanejad Y, Stratton CW. Streptococcus anginosus group. In:

Mandell GL, Bennett JE, Dolin R, eds. Principles and Practice of Infectious Diseases. Philadelphia: Elsevier Churchill Livingstone; 2005.

(4.) Bert F, Bariou-Lancelin M, Lambert-Zechovsky N. Clinical significance of bacteremia involving the "Streptococcus milleri" group: 51 cases and review. Clin Infect Dis 1998;27(2):385-7.

(5.) Han JK, Kerschner JE. Streptococcus milleri: An organism for head and neck infections and abscess. Arch Otolaryngol Head Neck Surg 2001;127(6):650-4.

(6.) Hirai T, Kimura S, Mori N. Head and neck infections caused by Streptococcus milleri group: An analysis of 17 cases. Auris Nasus Larynx 2005;32(1):55-8.

(7.) Shlaes DM, Lerner PI, Wolinsky E, Gopalakrishna KV. Infections due to Lancefield group F and related streptococci (S. milleri, S. anginosus). Medicine (Baltimore) 1981;60(3):197-207.

(8.) Jankowska B, Salami A, Cordone G, et al. Deep neck space infections. Int Congr Ser 2003;1240:1497-1500.

(9.) Flanagan PG, Mills RG. Fulminant septicaemia due to Streptococcus milleri infection in a previously healthy adult. Eur J Clin Microbiol Infect Dis 1994;13(3):247-8.

(10.) Jacobs JA, Tjhie JH, Smeets MG, et al. Genotyping by amplified fragment length polymorphism analysis reveals persistence and recurrence of infection with Streptococcus anginosus group organisms.

J Clin Microbiol 2003;41(7):2862-6.

(11.) Wanahita A, Goldsmith EA, Musher DM, et al. Interaction between human polymorphonuclear leukocytes and Streptococcus milleri group bacteria. J Infect Dis 2002; 185(1):85-90.

(12.) Willcox MD, Knox KW. Surface-associated properties of Streptococcus milleri group strains and their potential relation to pathogenesis.

J Med Microbiol 1990;31(4):259-70.

(13.) Nagamune H, Whiley RA, Goto T, et al. Distribution of the intermedilysin gene among the anginosus group streptococci and correlation between intermedilysin production and deep-seated infection with Streptococcus intermedius. J Clin Microbiol 2000;38(1):220-6.

(14.) Bergman S, Selig M, Collins MD, et al. "Streptococcus milleri" strains displaying a gliding type of motility. Int J Syst Bacteriol 1995;45(2):235-9.

(15.) Claridge JE III, Attorri S, Musher DM, et al. Streptococcus intermedius, Streptococcus constellatus, and Streptococcus anginosus ("Streptococcus milleri group") are of different clinical importance and are not equally associated with abscess. Clin Infect Dis 2001;32 (10):1511-15.

(16.) Willcox MD. Potential pathogenic properties of members of the "Streptococcus milleri" group in relation to the production of endocarditis and abscesses. J Med Microbiol 1995;43(6):405-10.

Christopher Robert Foxton, MA(Oxon); Smariti Kapila, MBBS; Justin Kong, MBBS; Neil John Thomson, FRACS

From the Department of ENT, Bristol Royal Infirmary, Bristol, U.K. (Dr. Foxton); the Department of ENT, Royal Prince Albert Hospital, Sydney, Australia (Dr. Kapila); the Department of ENT, Sydney Medical School, University of Sydney (Dr. Kong); and the Department of ENT, Gosford Hospital, Gosford, Australia (Dr. Thomson). The work described in this article was performed at Gosford Hospital.

Corresponding author: Dr. Christopher Robert Foxton, 43 St. John's Rd., Clifton, Bristol BS8 2HD, UK. Email: crfoxton@doctors.org.uk
Table 1. Selected characteristics of the 7 patients

                       Patient 1              Patient 2

Age (yr)/sex           39/M                   37/M

Site of abscess        Left submandibular     Left maxillary space
                       space

Comorbidities          Poor dentition         Diabetes mellitus

Clinical               Patient 1 presented    Patient 2 presented
presentation and       febrile and            with rigors and
treatment              tachycardic with       bilateral facial
                       fluctuant              pain and swelling;
                       submandibular          the swelling was
                       swelling; incision     most pronounced over
                       and drainage was       the left zygomatic
                       performed in the       arch; pus was being
                       operating room; in     discharged from a
                       addition, a decayed    decayed left upper
                       molar with free pus    molar, which was
                       from the socket was    extracted in the
                       extracted; the         operating room
                       cavity was packed
                       with a wick and
                       progressively
                       shortened over 5
                       days

Outcome                Discharged home well   Discharged home well
                       on day 6               on day 4

Inpatient              Penicillin G for 6     Penicillin G and
intravenous            days                   metronidazole for 4
antibiotic regimen                            days

Outpatient oral        Amoxicillin and        Amoxicillin/
antibiotic regimen     metronidazole for 14   clavulanate for 14
                       days                   days

                       Patient 3              Patient 4

Age (yr)/sex           73/F                   28/M

Site of abscess        Left submandibular     Left submandibular
                       space                  space

Comorbidities          Ischemic heart         Poor dentition
                       disease, peripheral
                       vascular disease,
                       diabetes mellitus

Clinical               Patient 3 presented    Patient 4 presented
presentation and       afebrile and           afebrile, but with
treatment              systemically well,     left dental pain and
                       but with an            increasing facial
                       increasing swelling    and submandibular
                       under the left angle   swelling; the
                       of the mandible;       presence of an
                       formal incision and    abscess was
                       drainage in the        confirmed on CT;
                       operating room was     local anesthesia was
                       performed, and a       administered, and
                       Penrose drain was      the abscess was
                       placed                 drained; a wick
                                              dressing was placed
                                              and progressively
                                              shortened

Outcome                Discharged home well   Self-discharged
                       on day 4               against advice on
                                              day 3

Inpatient              Penicillin G,          Penicillin G and
intravenous            metronidazole, and     metronidazole for 3
antibiotic regimen     flucloxacillin         days
                       (floxacillin) for 4
                       days

Outpatient oral        Amoxicillin and        Amoxicillin/
antibiotic regimen     metronidazole for 14   clavulanate for 14
                       days                   days

                       Patient 5              Patient 6

Age (yr)/sex           46/M                   37/M

Site of abscess        Bilateral              Right submandibular
                       parapharyngeal         space
                       spaces

Comorbidities          Diabetes mellitus,     Poor dentition
                       developmental delay,
                       and a ventricular
                       septal defect that
                       closed during
                       childhood

Clinical               Patient 5 presented    Patient 6 presented
presentation and       with fever, rigors,    systemically unwell;
treatment              and low blood          a discharging
                       pressure; increasing   abscess was present
                       swelling was present   under the angle of
                       in the submandibular   the mandible; CT
                       spaces, and            confirmed the
                       laryngeal structures   presence of a
                       were not easily        multiloculated
                       palpable; an awake     abscess cavity; 2
                       fiberoptic             decaying mandibular
                       intubation by          teeth were removed
                       incision and           in the operating
                       drainage was           room, and pus was
                       performed in the       evacuated from both
                       operating room         sockets

Outcome                Required high-dose     Discharged home well
                       inotropes in the       on day 5
                       ICU; developed
                       infective
                       endocarditis
                       followed by bowel
                       ischemia that
                       required resection;
                       died from
                       overwhelming sepsis
                       on day 22

Inpatient              Penicillin G and       Penicillin G and
intravenous            metronidazole          metronidazole for 5
antibiotic regimen     followed by            days
                       meropenem; 22 days
                       in all

Outpatient oral        N/A                    Amoxicillin/
antibiotic regimen                            clavulanate for 14
                                              days

                       Patient 7

Age (yr)/sex           39/M

Site of abscess        Right submandibular
                       space

Comorbidities          Poor dentition

Clinical               Patient 7 presented
presentation and       systemically unwell;
treatment              an increasing
                       submandibular
                       swelling had arisen
                       following the recent
                       extraction of a 4.8
                       molar; an awake
                       fiberoptic
                       intubation was
                       performed, followed
                       by incision and
                       drainage in the
                       operating room a
                       total of 3 times
                       over 6 days; the
                       abscess extended to
                       within 1.5 cm of the
                       skull base on the
                       opposite side
                       (figure)

Outcome                Discharged home well
                       on day 21, following
                       prolonged ICU
                       support

Inpatient              Cefazolin,
Inpatient              metronidazole, and
Inpatient              gentamicin, followed
                       by ceftriaxone; 21
                       days in all

Outpatient oral        Amoxicillin/
antibiotic regimen     clavulanate for 14
                       days

Table 2. Comparison of reported head and neck S milleri cases

                                          Milwaukee     Hiroshima
                        Present series      groups       groups
                           (n = 7)         (n = 26)     (n = 17)

Males, n (%)                6(86)          21 (81)       12(71)

Mean age, yr                 42.7           10.7"          62

Most common site        Submandibular     Paranasal     Maxillary
of abscess                  space          sinuses       sinuses

Patients with a          3 (43) (most       1 (4)         3(18)
major comorbidity,         common:
n (%)                      diabetes
                          mellitus)

Most common              Penicillin G    Ampicillin/     Unknown
intravenous (IV)                          sulbactam
antibiotic

Mean duration of IV          9.3             9.9         Unknown
antibiotic use, days

Most common oral         Amoxicillin/    Amoxicillin/    Unknown
antibiotic               clavulanate     clavulanate

Mean duration of              14             12.3        Unknown
oral antibiotic use,
days

* Pediatric cohort.
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Title Annotation:ORIGINAL ARTICLE
Author:Foxton, Christopher Robert; Kapila, Smariti; Kong, Justin; Thomson, Neil John
Publication:Ear, Nose and Throat Journal
Article Type:Case study
Date:Jun 1, 2012
Words:3185
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