Staphylococcus Sciuri: an Unusual Cause of Pelvic Inflammatory Disease
Summary: We present the case of polymicrobial pelvic inflammatory disease (PID) that involved Staphylococcus sciuri, S. epidermidis, and Streptococcus agalactiae. In order to determine the frequency of S. sciuri isolation from the female lower genital tract, 3415 vaginal samples were analysed during the one-year study period. S. sciuri was isolated from three (0.09%) samples. In all the three cases, S. sciuri was obtained in mixed culture from outpatients without symptoms of infection. While the origin of S. sciuri in the female genital tract remains to be elucidated, the present study showed that this bacterium may colonize vagina and, moreover, may be involved in the pathogenesis of an infection as serious as PID. The low rate of isolation we established, however, indicates infrequent and, most probably, transient colonization of the female genital tract by S. sciuri.
Keywords: pelvic inflammatory disease, Staphylococcus sciuri, vagina, incidence
Pelvic inflammatory disease (PID) is an inflammatory disorder most commonly caused by the ascent of microorganisms from the female lower genital tract.1 The most important causative pathogens of PID are Chlamydia trachomatis and Neisseria gonorrhoeae.1 However, micro- organisms that can be part of the vaginal flora may also cause PID, especially of polymicrobial aetiology.1 The present study describes for the first time the case of polymicrobial PID that involved Staphylococcus sciuri, and further explores the frequency of isolation of this bacterium from the female lower genital tract.
In September 2000, a 28-year-old-woman consulted her gynaecologist at the outpatient department because of acute pelvic pain, nausea and vomiting. The gynaecological examination demonstrated bilateral adnexitis, and the patient was directed to the Department of Gynecology and Obstetrics, Regional Hospital Prbram.
Detailed examination in the hospital revealed the presence of pelvic pain, adnexal tenderness, cervical motion tenderness, palpable mass, but not abnormal cervical or vaginal discharge, nor the presence of menstrual abnormalities, urinary or proctitis symptoms.
On admission, her blood pressure was 125/80mmHg, temperature was 37.0C, and pulse 76 beats/min. Her white blood cells count was 8.4 10^sup 9^/L, erythrocyte sedimentation rate 35mm/h, C-reactive protein 15mg/L. Renal function and hepatic enzyme levels were normal.
Final diagnosis of PID was made after laparoscopic examination. Purulent material from peritoneal cavity was obtained by peritoneal lavage. The treatment with metronidazole (500 mg every 8h) and doxycycline (100 mg every 12 h) was introduced. Microbiological examination of vaginal sample revealed the pure culture of Candida albicans only. Results of tests for N. gonorrhoeas, C. trachomatis, Ureaplasma urealyticum, Mycoplasma hominis, and bacterial vaginosis were negative.
After incubation of 24 h at 37C, primary agar media inoculated with material obtained by peritoneal lavage remained sterile, but subcultivation of primary broth cultures revealed S. sciuri, S. epidermidis and Streptococcus agalactiae. Susceptibility of the isolates to various antibiotics was tested by the disc diffusion method and it was established that two staphylococcal isolates were susceptible to doxycycline, while the S. agalactiae was resistant to this antibiotic. Anaerobic cultures of the same material remained sterile, as did the cultures for U. urealyticum and M. hominis.
Irrespective of resistance of S. agalactiae to doxycycline, the patient showed improvement after 48 h of treatment, and, therefore, the treatment with metronidazole/doxycycline combination was continued. After 14 days, the patient left the hospital in a good condition.
S. sciuri belongs to the group of coagulase-negative, oxidase- positive, novobiocin-resistant staphylococci. This bacterium is widespread in nature and it could be isolated from a variety of animals2,3 as well as from various food products of animal origin.4,5 It has been shown that this organism may cause serious human infections such as endocarditis,6 peritonitis,7 wound8 and urinary tract infections. However, the incidence of S. sciuri in humans was reported for urinary tract only.9
Although coagulase-negative staphylococci have been recovered from women with PID,10 the present study is the first report describing S. sciuri as the cause of this condition. We presumed that S. sciuri found in the material obtained by peritoneal lavage was clinically significant and not a contaminating organism for three reasons. First, the patient had clear presentation of PID according to both clinical and laboratory parameters. Second, the results of the extensive bacteriological examination excluded all other possible causative agents of PID. Third, S. sciuri, along with S. epidermidis and S. agalactiae, were isolated from the actual infection site which is an otherwise sterile region. Moreover, the material was obtained by peritoneal lavage and not transvaginally, which reduced the possibility for contamination. Therefore, we considered the isolated strain of S. sciuri as one of the causative agents of PID of polymicrobial aetiology.
Since the majority of the cases of PID result from ascending infection from the lower genital tract,1 we evaluated the frequency of isolation of S. sciuri from the vagina. In total, 3415 vaginal swabs were examined for the presence of S. sciuri during 2001. The study population included all patients (2715) attending the outpatient department at the Institute of Microbiology and Immunology, Belgrade, for microbiological examination of the lower genital tract during 2001. The remaining 700 specimens originated from 700 patients attending the Department of Gynecology and Obstetrics at the Regional Hospital in Prbram. Screening for S. sciuri and subsequent identification of the isolates were performed as previously described.9 Of the 3415 vaginal samples examined for the presence of S. sciuri, this bacterium was isolated from three (0.09%) samples. Two isolates originated from patients in Belgrade (0.07%), and one isolate (0.14%) was obtained from patients in Prbram. S, sciuri was isolated from 36-, 39- and 67-year-old women. All women were outpatients and without symptoms of infection. In all three cases, S. sciuri was obtained in mixed culture.
As far as the origin of S. sciuri in the female lower genital tract is concerned, one possible explanation could be sexual transmission. Although we cannot exclude this mode of transmission, it is noteworthy that no S. sciuri isolates were obtained from the urethra of male patients during the period of our study. Since S. sciuri is frequently isolated from animals,2,3 it is reasonable to assume that contact with animals also may have an important role in the colonization of humans. However, the patient with PID as well as three asymptomatic patients with S. sciuri isolates denied the contact with animals. Another possible source for colonization of humans with S. sciuri is food, since S. sciuri has been isolated from dairy and meat products.4,5 It has also been isolated from the digestive tract of animals,11 but its occurrence in human faecal specimens has never been analysed.
While the origin of this principally animal bacterial species in the female genital tract remains mainly speculative, the present study clearly showed that S. sciuri may colonize vagina and, moreover, may be involved in the pathogenesis of an infection as serious as PID. The low rates of isolation we established, however, strongly suggest that colonization of the female genital tract by S. sciuri is only sporadic and, most probably, transient.
1 Mann SN, Smith JR, Barton SE. Pelvic inflammatory disease. Int J STD AIDS 1996;7:315-21
2 Stepanovic S, Dimitrijevic V, Vukovic D, Dakic I, Savic B, Svabic-Vlahovic M. Staphylococcus sciuri as a part of skin, nasal and oral flora in healthy dogs. Vet Microbiol 2001;82:177-85
3 Hauschild T, Schwarz S. Differentiation of Staphylococcus sciuri strains isolated from free-living rodents and insectivores. J Vet Med B 2003;50:241-6
4 Bockelmann W, Hoppe-Seyler T. The surface flora of bacterial smear-ripened cheeses from cow’s and goat’s milk. Int Dairy J 2001;11:307-14
5 Papamanoli E, Kotzekidou P, Tzanetakis N, Litopoulou-Tzanetaki E. Characterization of Micrococcaceac isolated from dry fermented sausage. Food Microbiol 2002;19:441-9
6 Hedin G, Widerstrm M. Endocarditis due to Staphylococcus sciuri. Eur J Clin Microbiol Infect Dis 1998;17:673-5
7 Wallet F, Stuit L, Boulanger E, Roussel-Delvallez M, Dequiedt P, Courcol RJ. Peritonitis due to Staphylococcus sciuri in a patient on continuous ambulatory peritoneal dialysis. Scand J Infect Dis 2000;32:697-8
8 Stepanovic S, Dakic I, Djukic S, Lozuk B, Svabic-Vlahovic M. Surgical wound infection associated with Staphylococcus sciuri. Scand J Infect Dis 2002;34:685-6
9 Stepanovic S, Jezek P, Vukovic D, Dakic I, Petras P. Isolation of members of the Staphylococcus sciuri group from urine and their relationship to urinary tract infections. J Clin Microbiol 2003;41:5262-4
10 Walker CK, Workowski KA, Washington AE, Soper D, Sweet RL. Anaerobes in pelvic inflammatory disease: implications for the Centers for Disease Control and Prevention’s guidelines for treatm\ent of sexually transmitted diseases. Clin Infect Dis 1999;28(Suppl 1):S29-36
11 Goyache J, Vela AI, Collins MD, et al. Corynebacterium spheniscorum sp. nov., isolated from the cloacae of wild penguins. Int J Syst Evol Microbiol 2003;53:43-6
(Accepted 26 April 2004)
S Stepanovic MD PhD1, P Jezek MVD2, I Dakic MD MSc1, D Vukovic MD PhD1 and L Seifert MD3
1 Department of Bacteriology, Institute of Microbiology and Immunology, School of Medicine, Dr Subotica 1, 11000 Belgrade, Serbia; Departments of 2 Clinical Microbiology; 3 Gynecology and Obstetrics, Regional Hospital Prbram, U Nemocnice 84, CZ-26126 Prbram, Czech Republic
Correspondence to: Dr S Stepanovic
Copyright Royal Society of Medicine Press Ltd. Jun 2005