Infection (2017) 45:697–702
DOI 10.1007/s15010-017-1003-6
CASE REPORT
Streptococcus pyogenes: an unusual cause of salpingitis. Case
report and review of the literature
Mathieu Blot1,4 · Claire de Curraize2 · Arnaud Salmon‑Rousseau1 · Sophie Gehin3 ·
Julien Bador2 · Pascal Chavanet1 · Catherine Neuwirth2 · Lionel Piroth1 ·
Lucie Amoureux2 
Received: 20 December 2016 / Accepted: 27 February 2017 / Published online: 10 March 2017
© Springer-Verlag Berlin Heidelberg 2017
Abstract  Introduction
Background  Streptococcus pyogenes can colonize genitou-
rinary tract, but it is a rare cause of salpingitis.
Case report   We report a case of bilateral salpingitis due to
Streptococcus pyogenes in a 34-year-old woman using an
intra-uterine device and which occurred following a family
history of recurrent S. pyogenes infections. We review 12
other cases reported in the literature, and discuss the patho-
physiological mechanisms of this potentially life-threatening
disease.
Conclusion It is important to take into account consider
Streptococcus pyogenes as a cause of acute salpingitis in
the context of recent intra-familial Streptococcus pyogenes
infections.
Keywords  Salpingitis · Pelvic inflammatory disease ·
Streptococcus pyogenes · Group A Streptococcus · Carriage
Abbreviations
IUD Intra-uterine device
PID Pelvic inflammatory disease
TSS Toxic shock syndrome
* Mathieu Blot
mathieu.blot@chu‑dijon.fr
1
Service de Maladies Infectieuses et Tropicales, CHU de
Dijon, Dijon, France
2
Laboratoire de Bactériologie, CHU de Dijon, Dijon, France
3
Département de Radiologie, CHU de Dijon, Dijon, France
4
Département d’Infectiologie, CHU, 14 rue Paul Gaffarel,
21079 Dijon Cedex, France
Acute salpingitis is one of the most common acute
gynecologic diseases occurring in adolescent or adult
women and commonly recognized as a complication of
infection with a sexually transmitted agent like Chla-
mydia trachomatis and Neisseria gonorrhoeae. Sev-
eral studies have also reported an association between
salpingitis and bacterial-vaginosis-associated organ-
isms (Mycoplasma, Ureaplasma, Gardnerella vaginalis,
anaerobes) [1].
Lancefield group A β-hemolytic Streptococcus, or
Streptococcus pyogenes commonly causes benign and
self-limiting epithelial infections (pharyngitis and impe-
tigo). However, some virulent strains may be responsible
for severe invasive diseases like bacteremia, toxic shock
syndrome or necrotizing fasciitis, due to the production
of superantigens like streptococcal exotoxins [2, 3]. Con-
cerning the female genital tract, invasive infections occur
mostly in the post-partum period (puerperal sepsis) or after
surgery.
Here, we present a case of salpingitis due to S. pyo-
genes, and searched for other cases involving adult women
and published from 1980 to 2016 in the PubMed database
using the terms “Group A Streptococcus”, “Streptococcus
pyogenes”, “salpingitis”, “tubo-ovarian abscess”, “pelvic
inflammatory disease” (PID), “peritonitis”. We retained
12 cases in which fallopian tube infection was clearly
documented [4–15] (Table 1) and discuss the pathophysi-
ological process, the treatment options and the outcome
of this potentially severe infection. Only one case was not
included in the analysis because the full text was not avail-
able [6].
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Table 1  Features of reported cases of Streptococcus pyogenes salpingitis

Reference Patient no Age Past history Symptoms and Clinical exami- TSSa S. pyogenes Laparotomy Imagery, Treatment Outcome
duration nation isolation (-scopy) intraopera-

13
tive, pathology
finding(s)

Goepel [4] 1 15 NA NA Peritonism No PF+ Yes Bilateral pyosal- Penicillin Recovery

pinx
Fikrig [5] 2 32 Nullipare Fever, vomiting, Hypotension, No BC+ Yes Salpingitis Abx, intensive Recovery
abdominal acute respira- supportive
pain tory distress therapy
Barham [6] 3 36 Scleroderma. Vaginal dis- Hypoten- No CVF+, BC+ No Right TOA PenA/Inh, gen- Recovery
CVF S. pyo- charge (5w), sion, vaginal tamycin, Met
genes positive uterus bleeding discharge, (3d), PenA/Inh
culture (5w) (2w, endome- right adnexal (2w)
trial biopsy). tenderness,
Nausea, fever, diarrhea,
myalgia abdominal
pain
Borgia [7] 4 36 No Vaginitis (3d), Fever, abdomen No BC+, PF+ Yes NA PenG (5d), Recovery
fever, rigors, pain, bilateral PenA (9d)
diarrhea (1d), adnexal ten-
lower abdomi- derness
nal pain,
nausea (12 h)
Manalo [8] 5 26 G2P2, Chla- Fever, hypogas- Fever, hemody- No FTF+, PF+ Yes Right TOA, left PenA, Clind, Recovery
mydia tric pain (3w) namic instabil- fallopian tube bilateral
cervicitis (8y). ity, tachypnea, perforation, salpingo-
Sex partner: rash, arthralgia peritonitis oophorectomy
S. pyogenes
pharyngitis
(1 m)
Gisser [9] 6 45 G3P3. IUD Vomiting, diar- Polypnea, Yes BC+, PF+, Yes Peritonitis, uter- Ceftriaxone, Recovery, arthritis
(1y). Husband: rhea (<1d) abdominal IUD+ ine and ovar- Clind, immu- (1m)
asymptomatic tenderness, ian necrosis, noglobulins,
pharyngeal rash. Then pyosalpinx bilateral
S. pyogenes hypotension, salpingectomy
carrier respiratory and hysterec-
distress, fever tomy
Alnaes-Katjavivi 7 28 G2P2, recent Fever, abdomi- Peritonism, rash, No Uterus Yes Right salpingitis Cefuroxime, Recovery
[10] delivery nal pain (2d tender uterus Met (1d),
post-partum) PenA, Clind,
Met (3d),
PenA (3d)
M. Blot et al.
 Table 1  continued
Reference Patient no Age Past history Symptoms and Clinical exami- TSSa S. pyogenes Laparotomy Imagery, Treatment Outcome
duration nation isolation (-scopy) intraopera-
tive, pathology
finding(s)
Saha [11] 8 23 No Abdominal pain, Fever, hypoten- No BC+ Yes Left TOA Broad-spectrum Recovery
diarrhea, vom- sion, perito- Abx with
iting (4d) nism Clind (2d),
PenA (14d)
Venkataramana- 9 31 Multipare. IUD Fever, abdomi- Fever, hypoten- Yes BC−, CVF+ Yes Severe bilateral Cephazolin, Recovery
setty [12] (2d) nal pain, sion, vomiting, salpingitis, Met, vasopres-
vomiting (4d) abdominal endometritis sors, bilateral
pain, diar- salpingectomy
rhea, vaginal and hysterec-
discharge tomy
Solt 13] 10 24 G3P2, tubal Acute right Peritonism, No BC−, CVF+, Yes Ruptured right Broad-spectrum Recovery
occlusion lower abdomi- apyrexia PF+ TOA Abx, Hys-
(Essure® 3 y), nal pain terectomy,
mitochondrial Essure®
disease removal
Cho [14] 11 49 IUD Abdominal pain, Somnolence, Yes BC+, PF+, No Bilateral Broad spectrum Death (2d)
vomiting, hypotension, IUD+ salpingitis, Abx, vasopres-
diarrhea, fever respiratory right TOA, sors. Then,
(5d) distress, peri- peritonitis Clind
tonism
Paulson [15] 12 55 Recently Lower abdomi- Abdominal pain, Yes BC+, CVF+ Yes Necrotized right Vancomycin, Recovery
exposed to nal and pelvic vomiting, fallopian tube piperacillin/
Streptococcus pyogenes: an unusual cause of salpingitis. Case report and review of the…

children who pain (1d) malaise, head- and ovary, tazobactam.

had sore ache, right right cervix Bilateral
throats adnexal mass. hematoma salpingo-
Then septic oophorectomy,
shock, acute hysterectomy
respiratory
distress
Present case 13 34 IUD. Husband Fever, chills, ab Fever, abdomi- No CVF+, BC−, No Bilateral salpin- PenA (14d), Reconvery
and son: S. dominal pain, nal pain IUD− gitis Clind (2d)
pyogenes nausea (3d)
angina (1w)

Abx antibiotics, BC blood cultures, Clind clindamycine, CVF cervico-vaginal fluid, DIC disseminated intravascular coagulation, FTF fallopian tube fluid, Inh Penicillicillinase inhibitor, Met
metronidazole, NA no available data, PenA penicillin A, PenG penicillin G, PF peritoneal fluid, TOA tubo-ovarian abscess, TSS toxic shock syndrome
a
  TSS was defined according the three CDC criteria (1) an hypotension, (2) two or more criteria among: renal impairment, coagulopathy, liver dysfunction, acute respiratory distress, rash, soft
tissue necrosis, (3) S. pyogenes isolation

13
699
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Case
A 34-year-old married woman, with no medical history
apart a well-controlled asthma, presented with abdomi-
nal pain and fever. The patient had had three pregnan-
cies resulting in four live children (21 months, 5, 5 and 9
years old). She had been carrying an intra-uterine device
(IUD) with progestogen for 19 months as her contracep-
tive. Three weeks and one week before the present case,
her husband and older son, respectively, had suffered
from a S. pyogenes sore throat diagnosed with a rapid
antigen detection test and treated with amoxicillin for
6 days. In addition, the family presented a medical his-
tory with several S. pyogenes infections: each of the four
children had been treated for S. pyogenes purulent acute
otitis media before the age of 2, and the twins had been
treated for scarlet fever at the age of 4 (during a school
outbreak). She reported a sudden left iliac fossa pain that
had appeared three days earlier and was associated with
fever (temperature 39.5 °C), chills, nausea and asthe-
nia. Non-steroid anti-inflammatory medication was pre-
scribed but not taken. She reported neither urinary nor
digestive symptoms, but a slightly more abundant vagi-
nal discharge than usual. Physical examination revealed
a febrile woman, who had a sharp pain in the left iliac
fossa and tenderness in the right upper quadrant without
abdominal guarding on palpation. Urine analysis was
normal (white blood cells <10/mm3 and culture was ster-
ile). Oropharyngeal and skin examinations were normal.
The white blood cell count revealed leukocytosis (11,000/
mm3, 80% neutrophils) and C-reactive protein was
160 mg/L. Assay of β-HCG was negative. No other labo-
ratory abnormalities, especially abnormal hepatic enzyme
levels, were present. Abdominal-pelvic and endovaginal
ultrasound showed visible bilateral Fallopian tubes with
thick walls, hypervascularization, without signs of tubo-
ovarian abscess or other abnormalities. A gynecological
examination revealed a scant white discharge, a normal-
appearing non-tender cervix, and bilateral adnexal ten-
derness and fullness. Endocervical and vaginal swab
samples were collected for standard bacterial culture
and specific screening for Neisseria gonorrhoeae, Myco-
plasma, Ureaplasma and Chlamydia trachomatis. Blood
cultures (2 pairs) were performed. An empirical treatment
with oral metronidazole (500 mg twice/24 h) and ofloxa-
cin (200 mg twice/24 h) was begun. Within 24 h, culture
of the vaginal discharge was positive for S. pyogenes.
The strain was fully susceptible to beta-lactams, eryth-
romycin, and clindamycin. Treatment was then switched
to oral amoxicillin 2 g 3 times/24 h and clindamycin
600 mg 3 times/24 h. The IUD was removed 2 days
after the beginning of antibiotic therapy and analyzed
13
M. Blot et al.
but culture remained sterile. Oral amoxicillin and clin-
damycin were maintained for a total of 14 and 2 days,
respectively. Within 48 h, fever and the right upper quad-
rant abdominal pain disappeared but the pain in left iliac
fossa persisted beyond 10 days. The isolate was sent to
the National Reference Center (Centre National de Réfé-
rence des Streptocoques, Paris). The strain belonged to
genotype emm1 and harbored the genes speA, speB, sic,
and smeZ encoding, respectively, streptococcal pyrogenic
exotoxins A and B, streptococcal inhibitor of comple-
ment-mediated lysis, and streptococcal mitogenic exo-
toxin Z. All members of the family were treated with cef-
podoxime proxetil for 8 days as prophylaxis and in order
to break the chain of transmission. Three months there-
after, the patient was symptom free; a new endovaginal
ultrasound showed no abnormalities and cervical bacte-
rial culture was negative. Bacterial cultures of all family
members were performed and free of S. pyogenes (throat,
nose, skin, rectal swabs).
Discussion
Here, we present a case of bilateral salpingitis due to S.
pyogenes, a bacterial cause rarely reported in the literature.
We analyzed 13 cases of S. pyogenes involving post-puber-
tal women: 12 cases found in the literature since 1980, and
our case. S. pyogenes salpingitis appears to be a severe
disease, although publication bias cannot be excluded. We
noted seven out of 13 cases (62%) with signs of severity
(four fulfilling the definition of the US Working Group on
Severe Streptococcal Infections [2]), ten (77%) with local
complications (pyosalpinx, tubo-ovarian abscess, peritoni-
tis) and one death. Our patient presented no such signs of
complication but the infection was quickly diagnosed and
empirical treatment was switched within 4 days. In addi-
tion, the prescribed nonsteroidal anti-inflammatory drugs
were not taken, and this treatment is strongly suspected
to worsen S. pyogenes infection. Interestingly, the clinical
presentation suggested a Fitz-Hugh Curtis syndrome that
has never been reported with S. pyogenes PID.
Upper genital tract infections occur with pathogenic
microorganisms which ascend from the cervix and invade
the endometrium and the fallopian tubes, causing an inflam-
matory reaction (which may lead to functional damage
and tubal factor infertility). The most frequently incrimi-
nated microorganisms are sexually transmitted bacteria
like Chlamydia trachomatis and Neisseria gonorrhoeae.
Recent molecular methods also suggest the role of fastidi-
ous bacteria involved in vaginosis, but only occasionally
S. pyogenes (1 out of 45 cases of salpingitis in the study
of Hebb [1]). Among 9557 cases of invasive S. pyogenes
Streptococcus pyogenes: an unusual cause of salpingitis. Case report and review of the…
infections in the United States between 2005 and 2012, 134
cases (1.4%) of gyneco-obstetrical infections were reported
(endometritis (n  = 82), septic abortion (n  = 11), chorio-
amnionitis (n = 8), puerperal sepsis (n = 33), but no cases
of salpingitis were identified [3]. In one French series, 136
out of 1542 (8.9%) cases of gyneco-obstetrical sepsis were
reported, with no cases of salpingitis [2]. One reason that
might explain the low incidence of S. pyogenes salpingitis
is that this bacterium is not frequently encountered in the
normal flora of the post-pubertal female vaginal mucosa.
In two studies, the vaginal–rectal colonization rate of S.
pyogenes in late pregnancy accounted for 0.03 and 0.27%
of 3472 and 1083 pregnant women, respectively [16, 17].
S. pyogenes probably resides in the vagina for only a short
time, as a result of self-contamination from the pharynx, a
close contact source, or even from gastrointestinal carriage,
which has been reported in some rare cases [18]. Carriage
or exposure to a carrier is an important pathogenic factor in
recurrent S. pyogenes infection, although it is often ignored.
Although mostly found in the nasopharynx, S. pyogenes
can colonize the perineum, anus, vagina, and normal skin.
Patients with S. pyogenes pharyngitis spread the bacteria
through droplets and physical contact. Interestingly, in our
case, the family presented a medical history with several S.
pyogenes infections. Cases of invasive S. pyogenes infec-
tion have been described in patients with their close circle
suffering from sore throat, as in reports 5, 6 and 12 [8, 9,
15] or in cases of recurrent vulvovaginitis [18]. In our case,
the husband and son had been treated with Penicillin A for
6 days but it should be noted that up to 25% of acute phar-
yngitis cases treated with penicillin will have continued
asymptomatic, bacterial carriage within the nasopharynx
[19]. Pharyngeal colonization with beta-lactamase produc-
ing co-pathogens with in vivo inactivation of the penicillin
is one of the arguments proposed to explain this failure to
eradicate carriage [19].
After genital colonization with S. pyogenes, the patho-
genesis was likely due to an ascending genitourinary infec-
tion of a virulent strain of S. pyogenes. Indeed, the strain
that was isolated harbored genes encoding several toxins
and belonged to the emm1 genotype, which is the most
prevalent emm type accounting for invasive infections in
Europe [2].
The gynecologic literature suggests that one of the pre-
requisites for S. pyogenes PID is the mechanical disruption
of the mucosal epithelial barrier, such as during placement
of an intrauterine device (like case 9), a surgical procedure
(like case 3), and the birth process (like case 7). There was
no history of mucosal disruption in our patient. However,
our patient and three others (cases no. 6, 9 and 11) had an
IUD, which could constitute a risk factor in the develop-
ment of salpingitis. To date the studies are controversial. If
IUD insertion is generally considered safe, some authors
701
have hypothesized that the vaginal string appendage of the
IUD may break the mucosal barrier, thereby serving as a
portal of entry for bacteria [9, 14]. Moreover, this foreign
body may serve as a nidus for colonization with biofilm
formation that can lead to infection. In our case, with the
familial history of S. pyogenes, the colonization could have
happened weeks before the onset of clinical symptoms. For
this reason, IUD removal should be performed rapidly after
detection of the infection.
Concerning antimicrobial therapy, the French recom-
mendations and the Center for Disease Control and Preven-
tion guidelines for pelvic inflammatory diseases include
the use of ceftriaxone plus metronidazole plus doxycy-
cline. This association is perfectly adapted in the situation
of S. pyogenes etiology unlike the use of ofloxacin and
metronidazole which is also proposed by our local guide-
lines because of the advantage of an oral administration.
Fortunately, in our case this last association was quickly
switched to amoxicillin, which remains the cornerstone of
therapy since S. pyogenes remains exquisitely sensitive to
penicillin. In addition, the administration of clindamycin in
invasive diseases was probably useful against this virulent
strain of S. pyogenes by inhibiting the synthesis of the tox-
ins. Only six of the 13 cases reviewed and two of the four
TSS reported the use of clindamycin.
In conclusion, it is important to take into account S. pyo-
genes as a cause of acute salpingitis in the empirical treat-
ment, when there are risk factors like a recent intrafamilial
context of S. pyogenes infections. Unlike the use of ofloxa-
cin and metronidazole, which does not cover S. pyogenes,
the association of Ceftriaxone, Metronidazole and Doxycy-
cline, which is recommended when dealing with salpingi-
tis, is perfectly suited in this situation.
Acknowledgements  We thank Philip Bastable for help in reviewing
the manuscript and the Centre National de Reference des Strepto-
coques for typing the strain.
Compliance with ethical standards 
Conflict of interest  There are no potential conflicts of interest for any
authors.
Informed consent  The patient had given her informed consent prior
to this report.
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