Pediatric Dorothy I. Bulas, Anna R. Nussbaum
MD
Promise MD
A. Ahlstrom, MD #{149}Carlos Regina M. O’Donnell, BA
#{149}
Blask,
Transabdominal (TA) and transvaginat (TV) sonograms (n 116) were obtained in 84 patients aged 12-21 years (mean, 16.2 years) with the dinical diagnosis of acute pelvic inflammatory disease (PID). The studies were compared for image quality and unique diagnostic information. TV sonography demonstrated superior resolution of 25 dilated fallopian tubes. Heterogeneous pelvic masses, described as tubo-ovanian abscesses on TA sonograms, could be separated on TV sonograms into various stages of PID including pyosalpinx, hydrosalpinx, tubo-ovarian complex, and tubo-ovarian abscess. Thirty-one TA and TV studies were normal despite patients fulfilling strict clinical critena for PID. The level of severity of PID, as determined at TA sonography, was altered in 28 cases, with medical therapy changed in 23 cases because of additional TV sonographic findings. TV sonography provided superior anatomic detail in the evaluation of patients with PID, demonstrating abnormalities that were not seen at TA sonography in 71% of patients. terms:
Fallopian #{149} Ovary, abscess,
853.217 gans,
abscess,
85.1298,
85.217
tubes, abscess, 852.217 #{149}Pelvic #{149}Pelvic organs, US,
or-
85.12989
Radiology
1992;
183:435-439
From the Departments of Diagnostic Imaging and Radiology (D.I.B., C.J.S., A.R.N.B.) and Pediatrics (D.l.B., P.A.A., C.J.S., A.R.N.B.), and the Office of the Research Director (R.M.O.), Children’s National Medical Center, 111 Michigan Ave NW, Washington, DC 20010; and the George Washington University School of Mcdicine and Health Sciences, Washington, DC I
(D.I.B., P.A.A., C.J.S., A.R.N.B.,
R.M.O.).
From
1991 RSNA scientific assembly. Received Dccember 2, 1991; revision requested January 3, 1992;
revision
January RSNA,
received
27. Address 1992
January
reprint
22;
requests
Sivit,
MD
#{149}
Pelvic Inflammatory Disease Comparison ofTransabdominal Transvaginal Sonographic
Index
J.
Radiology
accepted
to D.I.B.
the
P ally ally risk
ELVIC
in the Adolescent: and Evaluation’
inflammatory
is a serious transmitted active female (1). Although,
disease
complication infections, teenagers to our
(PID)
of sexuwith sexuat highest knowledge,
optimal therapy has not yet been established, it has been noted that patients with severe disease require prolonged administration of broad spectrum
antibiotics
intravenously
and possible surgical intervention 6). The severity of PID is difficult assess
clinically
Thus, the use of TV sonography in this population merits special attention. The purpose of this study was to determine prospectively if TV sonography was well tolerated in the adolescent population and whether it provided additional information in the diagnosis and management of acute PID.
(7).
The
finding
(2to of a
pelvic mass at transabdominal (TA) sonography has been used as evidence of severe tubo-ovarian inflammation (7,8). Findings from previous series have suggested the need for more individualized therapy, depending on the stage of acute salpingitis (2,3). The use of TA sonography to differentiate among various stages of PID, howeven, is limited (9,10). Swayne et al (11) attempted to correlate TA sonographic findings with laparoscopic findings, but only three sonographic patterns emerged: endometritis, focal
MATERIALS
AND
Over a 14-month period, 106 consecutive female patients aged 12-21 years (mean, 16.3 years) underwent 137 pelvic sonographic
examinations
pected PID. the adolescent cal
and
All
were
pelvic
examinations.
in urine,
blood
admission Twenty-two
when
studies
that
used
transvaginal (TV) sonography, however, have been promising. Its use in identifying dilated fallopian tubes has been established (12). Pyosalpinx, ovarian thickening, and small fluid collections have been identified with TV sonography in patients with PID (13). The role of TV sonography in the evaluation of pelvic infections, however, has yet to be established. Adolescents represent an especially high-risk group because of the high incidence of multiple sexual partners and the prevalence of Neisseria gonorrhoeae and Chlamydia trachomatis. Whether TV sonography is an acceptable examination to perform on adolescents
has
yet
to be established.
were
obtained
at
excluded
from the study because they did not fulfill clinical criteria for the diagnosis of acute ND. Clinical criteria included the presence
20 mm/h,
of preliminary
enythro-
were
possible. patients
sults
Pyo-
and
rates
of the following:
distortion.
A sample
cell counts,
cyte sedimentation
or more
pelvic
to
physi-
from the endocervix was cultured for N gonorrhoeae and C trachomatis. Measurements of human chonionic gonadotropin
salpmnx, hydmosalpinx, acute or chronic salpingitis, tubo-ovarian complex, and tubo-ovarian abscess could not be differentiated on a TA sonogram. Re-
total
of sus-
admitted
unit and underwent
abdominal adnexal
and
because
patients
of lower tenderness,
mass,
METHODS
pain, cervical tenderness,
motion plus one
temperature
of
38#{176}C or greater, white blood cell count 10,500/mm3 (10.5 x 109/L) or greaten,
vated
sedimentation
rate of greaten gonorrhoeae
of N
evidence
of ele-
than and/
or C trachomatis in the endocervix, or pelvic abscess on inflammatory complex at bimanual
examination
or sonography
(14-
17). The remaining
84 patients underwent TA and TV sonography (116 sonograms were obtained) for the initial evaluation and follow-up of acute PID. Within sonogram
72 hours was
of admission,
obtained
with
a pelvic both
TA
and
TV transducers. The purpose of the TV approach was explained to each patient. A consent
form
was
not
used,
since
most
patients were minors and it was difficult to locate legal guardians. Thus, with approval from the Institutional Review
Abbreviations: disease, TA
=
PID = pelvic transabdominal,
inflammatory TV = transvagi-
nal.
435
Board,
only
dune
was
verbal
consent
obtained.
of the
One
proce-
Comparison
sonographer
of TA and TV Sonographic
would perform both TA and TV portions of the examination. A 3-MHz sector transducer and, when possible, a 5-MHz linear transducer
(Acuson,
were
if)
used
Mountain
View,
for the TA portion
amination,
with
for optimal the patient
evaluation voided,
the
patient’s
performed
with
Finding
full
Normal study Uterus Enlarged
After
Endometnial
of the cxbladder
and
both
adnexa.
At the
and
technique
more
All
studies
dently
she
than
the other.
were
At least
unaware
course
and
grams
were
preferred
compared
(D.I.B.,
one
of the
of the TA
compared
34
33
7
0
8
14
5
24
tube/normal
I
5
49
20
0
14
0
15
17
32
(tubo-ovarovary
Pelvic fluid Cul-de-sac Periovarian Abdominal
C.J.S., on
TV
0 2
7 1
radiologists
patient’s
outcome.
one
indepen-
by two radiologists
A.R.N.B.). was
whether
TA
(tubo-
ian complex)
Inflamed
of Findings
tube
No recognizable structures ovarian abscess) Inflamed tube and ovary
conclusion
of both examinations, the patient was asked whether she had experienced any discomfort
fluid
Inflamed fallopian Pyosalpinx Hydrosalpinx Adnexal mass
TV sonography was a 5-MHz, 19-mm-diame-
ten, end-view transducer with a sector angle of 30#{176} (Acuson). Standard views included sagittal and coronal images of the uterus
of PID (116 Sonograms) No.
Cal-
of the organs.
Findings
clinical
and
for
TV
sono-
uterine
mor-
phologic characteristics; ovarian size, contour, and internal architecture; fallopian tube appearance; presence on absence of pelvic
masses;
and
presence
and
contents
of pelvic fluid collections. Ovaries were considered enlarged if ovarian volume was greaten than 14 cm3 (18,19). Fallopian tubes
were
considered
dilated
when
a tu-
bular structure with echogenic walls and folded configuration was identified (12). Doppler was used when necessary to distinguish
between
pelvic
lated fallopian The readers severity
of PID,
studies tem was
grading
separately
rated
such
moderate
were
sys-
PID
or
identified.
but
was
a.
PID
PID
findings
margins
noted
present.
TV
a scoring
ovarian
were
was
the
and
if additional
as ill-defined
mass
TA
and severe. no abnormalities
ovaries
al thickening
a di-
to evaluate
by using
only enlarged
and
the
of mild, moderate, rated mild when
was
veins
tube. were asked
or tub-
no
adnexal
rated
severe
b.
Figure fined
1. with
bladder sonogram
Dilated fallopian tube is clearly delineated with TV sonography and poorly conventional TA sonography. (a) Transverse TA sonogram obtained through (B) demonstrates the uterus (Li) and an amorphous left adnexal mass (arrows). demonstrates a fluid-filled tube (T) containing septations.
Percentage of agreement between readers’ grading of PID severity was
tubo-ovarian
ported metny
and/or
tubo-ovar-
ian abscess was identified within an adnexal mass at TV examination (Table). Once the patient was admitted, cefoxitin, doxycycline, intravenously rated
for
severe, 14 days
obtained
and clindamycin were administered. If PID was
antibiotics were with 26 follow-up
before
completion
PID was rated damycin
mild or
was
discontinued
and doxycycline venously
for
were 7-10
oral doxycycline ditional
7-10
continued sonograms
administered After
Clinical
for an ad-
follow-up
was
evaluated through the analysis of medical records and follow-up studies including one laparoscopy and two laparotomies. Descriptive
summaries
sonographic frequency
findings counts
and
of TV
were
tinuous variables such and patient age were reported plus
or minus
range. 436
#{149} Radiology
I standard
and
reported
percentages. as ovarian deviation
using
the
TA
as Convolume
as means and/or
test
Paired
were
measured
phy. were
Both left and right ovarian included in this analysis. tests
used
McNemar
pairs.
ume
were
to compare
two-sided,
and
were considered significant levels of less than .05.
the reof sym-
Student
ovarian
at TV versus
vol-
TA sonogrameasures All statistifindings
at probability
RESULTS
intra-
discharge,
was continued days.
If
by
for matched
tests
cal
of therapy. moderate, dinand cefoxitin
days.
(b) TV
if
a heterogeneous adnexal mass was identifled at TA examination on a pyosalpinx, complex,
dethe
Patient
Comfort
Fifty-seven believed that as
comfortable
percent of the TV sonography as TA
patients was
sonography.
Twenty-eight percent of patients found the distended bladder required for TA sonogmaphy uncomfortable and thus actually preferred the TV examination. The time to perform the additional TV examination averaged 8.6 minutes (range, 4-21 minutes).
Fallopian Nineteen
four
cases
tified
solely
Tubes cases of pyosalpinx of hydnosalpinx were
with
TV sonography
1). Five cases of pyosalpmnx case of hydrosalpinx were
at TA examination, and wall thickness
and iden-
(Fig
and one recognized
but tubal contents were more clearly
delineated on TV sonograms. Echogenic material and septa within dilated fallopian tubes were demonstrated transvaginally in five cases. Mildly thickened fallopian tubes were identified transvaginally in four cases.
In three be useful veins
cases, TV Doppler in differentiating from dilated fallopian
proved pelvic tubes.
to
Ovaries Ovarian
follicles
were
more
cleanly
delineated transvaginally in 80% of cases, and ovarian margins were more sharply defined in 50% of cases. There
May
1992
Uterus
The uterus appeared normal in 85% of the studies. Endometrial fluid was present in 14 cases (12%), eight of which were identified only on TV sonograms sonography
(Fig 3). Additionally, demonstrated one
intrauterine at TA
gestation
that
TV early
was
missed
sonognaphy.
The smaller field of view of the TV transducer made accurate longitudinal measurement of the uterus difficult. Thus, seven enlarged uteri were identified only at TA sonognaa.
phy.
b.
Figure
2.
TV sonographic
onstrates
depiction of a tubo-ovanian pelvic mass (arrowheads)
abscess. (a) Initial with no recognizable
after
3 weeks
therapy
Tube
(T) remains
a heterogeneous
(b) TV sonogram ovarian
obtained
margins
(arrows).
of antibiotic thickened
and
shows filled
TV sonogram dempelvic structures.
the sharply
with
Pelvic
TV sonognaphy fluid collections
fluid.
and the the
pelvis beyond TV transducer.
the
Fluid
delineated
focal
zone
seven
periovarian
tions that sonography.
of
fluid
were
fled
Inflammation
The
a sharply manginated cases, both fallopian Figure
rows) trial
TV sonogram
3.
demonstrates
of the uterus
fluid
within
(ar-
the
endome-
cavity.
could be recognized transvaginally, but the margins between the structures
were
complete
no
ence
statistically
significant
the
between
the measurement volume:
At TV
sonography,
the
in vol-
16.9 cm3 ± 21.7; TA was 17.3 cm3 ± 22.4; paired Student t test resulted in t = .680, P = .4972. However, 18 ovaries that measured oven 14 cm3 at TA examination were within ume
was
normal
limits
ovaries sonography transvaginally. size
transvaginally,
that
24
were measured This
believed
was
whereas
normal size at TA over 14 cm3 discrepancy in
to be secondary
improved definition gins at TV examination. Twelve enlarged
to
of ovarian ovarian
marcysts
that
appeared to contain internal echoes at TA examination were echofree, translucent cysts at TV sonognaphy. These echoes
most
likely
reverberation
were
artifact
caused
that
present at TV sonography. material within ovarian more cleanly demonstrated
amination tion
of three
Volume
cysts
in 12 additional
TA sonography
183
enabled
ovaries Number
#{149}
located 2
by
was
not
Echogenic was at TV cx-
cases. identifica-
high
it difficult structures
examination
differ-
two modalities of mean ovarian
ill defined.
in
(Fig 2). In these
sonography often strated septations
but no ovarian fled. Intemreaden TV sonographic ity was evaluated.
tissue
could
TV
be identiof TA and
grading of PID sevenIntemreader agree-
for TA sonographic
tions
was
significantly
agreed
interpretalow,
with
the
on only
77%
= .0002). There was closer agreement (90%) between readens’ grading of PID severity when evaluating TV sonognams (P = .3916).
more
echoes
easily were
fluid
nec-
identi-
transvagi-
cases.
at TV sonography was better delineated with TA sonognaphy because its extension into the abdomen.
of
Findings
Of the
initial
acute
PID,
for
sonognaphic
90 studies
performed
31 (34%)
evidence
revealed
no
of pelvic
in-
flammation. All these patients met the clinical criteria for PID, including 26 (84%) with positive cervical cultures. Seventy-two percent of patients who
met agreement
ment
level of severity of the time (P
cases,
better demonand debris levels,
collec-
One patient had abdominal fluid in the Morrison pouch, which was identified only at TA sonognaphy. A large loculated pelvic fluid collection noted
of the adnexa to identify any necogeither at TV on TA
were
cul-de-sac
in five
Clinical
In 20 cases,
distortion
made nizable was
ovary. In 14 tube and ovary
fluid
visualized at TA contents within the
internal
within
nally
TA sonography demonstrated 49 heterogeneous adnexal masses. In 15 pelvic masses noted at TA examination, TV sonography could help identify a dilated fallopian tube as well as
not
collections
ognized;
Tubo-ovarian
demonstrated 15 within the cul-de-sac
the TV sonographic
severe tures.
PID
had
positive
TV sonographic
criteria
for
cervical
cul-
findings
were
con-
firmed surgically in two cases. Ovanian tissue with poorly defined margins and a dilated fluid-filled tube was identified on a TV sonogram in
the
first
patient.
ic salpingitis sions and
At lapanotomy,
with fibrosis
chron-
tubo-ovarian was confirmed.
The level of severity of PID, as graded with TA sonograms, was altered in 28 cases (24%) because of additional TV sonographic findings. TV findings suggested more severe tuboovarian inflammation in 11 cases rated mild or moderate at TA examination. In 17 cases, TV sonographic
second
patient
dilated,
echogenic
findings 23 cases, because
tamed 2 weeks later revealed velopment of a hydrosalpinx
the dewith an
adjacent
sharply
manginated
ovary
(Fig 4d).
Because
of persistent
suggested less severe PID. In medical therapy was altered of additional TV sonographic
findings. No treatment failures noted in this group of patients.
were
was
noted
adheThe
tube
to have and
a
peniova-
nan fluid collections (Fig 4a, 4b). Ovarian margins were ill defined on follow-up TV sonograms (Fig 4c). Laparoscopic findings confirmed the presence of periovarian adhesions and
pyosalpmnx.
a lapanotomy
TV
was
sonograms
ob-
performed.
Radiology
pain, The
#{149} 437
ovary appeared cally inflamed brous obliteration was resected.
normal, but a chronifallopian tube with fiof the distal lumen
DISCUSSION PID refers genital tract tubes and/or
to infection involving contiguous
the
in the upper fallopian structures.
Adolescents
represent
a high-risk
group because of the high prevalence of multiple sexual partners and of N gonorrhoeae and C trachomatis in this patient population (1). Sequelae of PID include ectopic pregnancy, infertility, and chronic pelvic pain (10). PID is a syndrome that may include endometnitis, salpingitis, oophonitis, pelvic peritonitis, and tubo-ovanian abscess. The mechanism of tubal infection is not well understood. It likely begins as a cervical infection with N gonorrhoeae and/or C trachomatis altering the cervicovagmnal environment and resulting in an ovengrowth of endogenous flora. As the infection ascends, the fallopian tubes become hyperemic, thickened, and filled with purulent exudate. Peritoneal spillage may occur. Tubal occlusion may develop, resulting in a pyosalpinx. If the infection subsides at this
stage,
a hydrosalpinx
If peritonitis adhesions
may
progresses, may
result
with
tube and complex. may cause
these organs a tubo-ovarian
to break abscess
Clinically,
acute
discharge,
fusion
ing
prove
the
diagnosis
of
salpingitis
includes
fever,
pelvic
sensitivity
a
and
of the
published to im-
clinical
A clinical
inpatient
diagnosis
therapy
PID has been advocated lems with noncompliance lescent
population.
for
due to probin the ado-
Patients
with
se-
vere disease have a substantially greater recovery of aerobes and anaerobes from culdocentesis fluid (3).
Salpingitis
tubo-ovanian ian abscess 438
with
tubal
occlusion,
complex, and tubo-ovarappear to require pro-
Radiology
#{149}
of PID.
(a) TV
sonogram
(b) TV sonogram
material.
shows
demonstrates
dilated,
convoluted
ovarian
tissue
tube
(cursors)
(T) containadjacent to the
A small amount of periovarian fluid is present (arrows). (c) TV sonogram obtained 1 later shows low-level echoes that remain within the dilated tube and the ill-defined margin between the ovary (0) and the tube (T) (arrows). UT = uterus. (d) TV sonogram obtamed during follow-up examination performed 2 weeks later for persistent pelvic pain shows a thin, dilated fluid-filled tube (arrow). Laparotomy enabled the identification of a chronically inflamed hydrosalpinx.
longed
antimicrobial
against
anaerobes
therapy plus
close
effective follow-up
for possible surgical drainage (2,4,6). Knowledge of the severity of PID is useful for optimal management. The clinical presentation of patients with salpingitis versus those with more severe disease, however, is similar. Physical
plus a positive culture allow a correct diagnosis in up to 87% of patients, but the physician may miss up to 33% of patients with PID (16). Aggressive
echogenic
Progression
down, creating (2,5,20,21).
have been modified
(14-16).
4.
tube. week
tenderness. There is a high degree of inaccuracy, however, in the clinical diagnosis of PID (1,16). When exammed laparoscopically, only 60%-70% of adult women with the presumptive diagnosis of acute salpingitis actually had the disease (22). Criteria for the diagnosis of PID and subsequently
d.
Figure
follow.
ovary, called Further inthe walls of
b.
C.
peniovarian
the inflamed tubo-ovanian flammation
vaginal
a.
examination
may
result
in an
overestimate or an underestimate of the presence of a pelvic mass (23). Up to 70% of adnexal masses identified at sonography may be missed at physical examination (7). Thus, TA sonography became the modality of choice to exclude the presence of a tuboovarian mass. Although the finding of a pelvic mass
on
a TA
sonogram
is often
me-
femred to as a tubo-ovarian abscess, laparoscopic findings may range from pyosalpinx, to tubo-ovarian complex, to tubo-ovanian abscess. The theory that patients may benefit from more individualized therapy, depending on the severity of the disease, suggests
a need stages
The
to further differentiate of PID (2,3).
introduction
allows for visualization
Patten
the
of TV transducers
improved resolution of pelvic organs
et al (19) correlated
and (24,25).
TV sono-
graphic and laparoscopic 16 women with PID. TV
findings sonography
in
enabled the identification inflamed fallopian tubes periovanian inflammation.
of 93% of and 90% of Ovaries
that appeared enlarged, were indistinct, and had peniovarian fluid collections corresponded to lapanoscopic findings of peniovanian exudate and adhesions. Poorly defined adnexal masses seen at TV sonography corre-
lated
with
amorphous
abscess pathologically. by Patten et al (19),
ment
and
periutermne
tubo-ovarian In the series uterine enlarge-
inflammatory
changes were identified in only 25% of cases. However, because all of these patients had additional adnexal abnormalities, the low sensitivity in identifying uterine inflammatory
May
1992
changes did not alter the for the diagnosis of PID. A limiting factor of our
sensitivity study
was
the lack of surgical confirmation in all but two cases. Our TV sonographic findings, however, are similar to the observations made by Patten et al (19). Our study confirmed that these findings
are
unique
to the
TV
exami-
nation. The improved visualization tubal and ovarian inflammation vaginally
various copy.
allows
stages The
one
to differentiate
of PID
ability
of trans-
without
laparos-
to distinguish
a pyo-
salpinx from a tubo-ovanan complex or tubo-ovamian abscess may allow for more individualized medical and interventional therapy. TV fine-needle aspiration abscess
or drainage of tubo-ovamian has already been reported to
be a successful
and
safe
procedure
(26).
Theme are two possible explanations for the finding of 31 normal TA and TV sonograms in patients who met the clinical criteria for PID. Because of the lack of lapanoscopic confirmation, these patients may represent cases of a false-positive
clinical
diagnosis.
with
either
TV
or TA
several
abdominal
before
fluid
We thank Linda Catena, Brown-Jones, RDMS, and Debra
Carin,
for their
RDMS,
Number
#{149}
2
12.
Tessler
FN,
Perrella
Endovaginal
1.
2.
3.
13.
Lande
tubes.
IM, Hill
Adnexal
5.
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SN, Mercer
U, Ismail
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MC, Cosco
FE, Kator
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lections, enlarged uteri, and laterally displaced ovaries missed at TV sonography, these findings did not add to the sensitivity in the diagnosis of acute PID. It is tempting to state that TA sonography is needed only as a backup examination. However, our sonographers had the benefit of the
to orient
performing
phy. A study in which TV and TA sonograms are obtained independently is needed to conclude that only TV sonograms are necessary for the evaluation of acute PID. In summary, TV sonography is a well-tolerated method for the evaluation of adolescents with PID. It provides superior anatomic detail of inflamed adnexa by demonstrating various stages of tubo-ovanian inflammation not previously seen at TA sonography. This additional information, obtained previously only with laparoscopy, may allow for more successful individualized therapy. I
sonogra-
phy. Thus, although TV sonography appears sensitive in the evaluation of PID, its specificity has yet to be determined. Although TA sonography helped identify
TA examination
selves
Pre-
vious series, however, found that up to 87% of patients meeting our clinical criteria had PID when they underwent laparoscopic examination (16). A more satisfying explanation may be that these patients have early or mild tubal erythema, in which case TV sonographic findings might be cxpected to be minimal. Correlation with clinical data remains critical. From our original series of 137 sonograms, five hemorrhagic cysts could not be distinguished from ovarian abscess
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