International Journal of Gynecology and Obstetrics 132 (2016) 1719

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International Journal of Gynecology and Obstetrics

journal homepage: www.elsevier.com/locate/ijgo

CLINICAL ARTICLE

Comparative study of the clinical features of patients with a tubo-ovarian

abscess and patients with severe pelvic inammatory disease
Luis H. Sordia-Hernndez , Laura G. Serrano Castro, Mara O. Sordia-Pieyro, Arturo Morales Martinez,
Mary C. Sepulveda Orozco, Geraldina Guerrero-Gonzalez
University Center for Reproductive Medicine, Universidad Autnoma de Nuevo Len University Hospital, Monterey, Nuevo Len, Mexico

a r t i c l e

i n f o

Article history:
Received 4 February 2015
Received in revised form 26 May 2015
Accepted 7 September 2015
Keywords:
Leukocytosis
Pelvic inammatory disease
Tubo-ovarian abscess

a b s t r a c t
Objective: To determine the clinical characteristics that indicate the presence of tubo-ovarian abscess (TOA)
among patients with severe pelvic inammatory disease (PID). Methods: An observational cohort study was
performed from October 2011 to March 2013. The study included all patients with a diagnosis of TOA and PID
admitted to a university hospital in Mexico. A complete medical history and physical examination were performed, and laboratory studies were reviewed. A logistic regression analysis was performed on variables with
statistical signicance. Results: Overall, 26 patients with PID and TOA (TOA group) and 26 with PID without
TOA (PID group) were included in the study. Signicant differences between patients with TOA and PID were
found with regard to the patients age (39.3 years vs 33.1 years; P = 0.04), educational level (only elementary,
13 [50%] vs 5 [19%]; P = 0.14), presentation with fever (23 [88%] vs 16 [62%]; P = 0.025), white blood cell
count (21.8 109/L vs 14.9 109/L; P b 0.001), number of deliveries (2.2 vs 1.1; P = 0.01), and presence of
diarrhea (16 [62%] vs 5 [19%]; P b 0.001). The triad of fever, leukocytosis, and diarrhea was positively related
to the presence of TOA. Conclusion: The triad of fever, leukocytosis, and diarrhea should alert clinicians to the
possibility of TOA formation in patients with PID.
2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

1. Introduction

2. Materials and methods

A tubo-ovarian abscess (TOA) represents the most severe form of

pelvic inammatory disease (PID). Approximately 30% of patients
with PID develop this complication [1], which usually occurs in sexually
active women aged between 15 and 40 years, with variable clinical
manifestations. It can begin insidiously, progressing to fever and not
uncommonly to an acute abdomen [2].
An important consequence of TOA is the need for surgery. In general,
a hysterectomy is performed as an urgent procedure, and many women
also require bilateral oophorectomy. The consequences of the induced
menopause on a young womans lifestyle and health are huge.
Even if a TOA is treated conservatively, long-term complications can
ensue. These potential complications include infertility, ectopic pregnancy, and chronic pelvic pain [3]. Therefore, timely diagnosis and treatment of a TOA are crucial for a patients reproductive function and her
health in general.
The aim of the present study was to determine whether there
are clinical manifestations that indicate a diagnosis of TOA in patients
with severe PID.

The present observational cohort study was performed from October

3, 2011, to March 29, 2013, in the Gynecology and Obstetrics Department of the University Hospital Dr. Jos E. Gonzalez in Monterrey,
Mexico with approval from the hospitals Ethics Committee.
The study included all patients with a diagnosis of TOA and severe PID
admitted to the gynecology service during the period mentioned. All patients with severe PID with TOA were consecutively included (TOA
group). Patients admitted with PID without TOA were then consecutively
included (PID group) until the number of patients admitted in the TOA
group was reached. All participants provided written informed consent.
The diagnosis of TOA was made by direct visualization of a pelvic
abscess during exploratory laparotomy. Severe PID was diagnosed if
the patient presented with the clinical signs of acute salpingitis stage II
(salpingitis with pelvic peritonitis) as proposed by Monif in 1982 [4],
together with one or more of the following criteria for hospital admission: body temperature of 38 C or more, an uncertain diagnosis, oral
antibiotic treatment for 48 hours with no response, clinical signs of peritoneal irritation, and nausea and vomiting that impede oral intake.
A complete medical history and a detailed physical examination
were performed on admission. The following data were obtained: age;
marital status; level of education; smoking; alcohol use; age at the
start of sexual activity; number of sex partners; number of pregnancies;
number of deliveries, cesarean deliveries, abortions, ectopic pregnancies,

Corresponding author at: Centro Universitario de Medicina Reproductiva, Hospital

Universitario Dr. Jos Eleuterio Gonzalez, Av. Madero y Gonzalitos, Colonia Mitras
Centro, Monterrrey Nuevo Len, 64460, Mexico. Tel./fax: +52 81 83 48 30 54.
E-mail address: luissordia@telmexmail.com (L.H. Sordia-Hernndez).

http://dx.doi.org/10.1016/j.ijgo.2015.06.038
0020-7292/ 2015 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.

18

L.H. Sordia-Hernndez et al. / International Journal of Gynecology and Obstetrics 132 (2016) 1719

and molar pregnancies; history of sexually transmitted diseases; family

planning methods used, including current and previous use of an intrauterine device; and presence of fever, diarrhea, or pelvic pain.
Findings on physical examination such as the presence of vaginal
discharge, pain on movement of the cervix, pelvic pain, abdominal
pain, and presence of peritoneal irritation such as rebound tenderness
were documented. The number of leukocytes was evaluated with a
complete blood count.
The statistical analysis was performed using SPSS version 21 (IBM,
Amonk, NY, USA) for Mac. The results in the two groups were compared using the 2 or t test as appropriate. P b 0.05 was considered statistically signicant. A logistic regression model was applied, in which
variables with a statistically signicant difference were analyzed using
the Nagelkerke R2 statistic.
3. Results
The mean age of the 52 participants was 36.3 years, with patients in
the TOA group being signicantly older (P = 0.04) (Table 1). The marital
status, highest educational level, age at the start of sexual activity, and
other patient characteristics are shown in Table 1.
The number of sex partners in the TOA group was one for 13 (50%)
patients and two for 12 (46%) patients; one patient reported ve sex
partners (4%). In the PID group, 12 (46%) patients reported one sex
partner, seven (27%) reported two, four (15%) reported three, two
(8%) reported four, and one (4%) reported 15. The difference between
the groups was not signicant (Table 1).
A history of sexually transmitted diseases was found in two (8%)
patients from each group. No differences were found regarding the
use of family planning methods, including use of an intrauterine
device (Table 1).
The number of pregnancies did not differ signicantly between the
groups (Table 1). The mean number of deliveries in the TOA group
was 2.2 1.7. In this group, ve (19%) patients had never delivered,
four (15%) reported a history of one delivery, six (23%) of two deliveries,
six (23%) of three deliveries, two (8%) of four deliveries, two (8%) of ve
deliveries, and one (4%) of six deliveries. In the PID group, the mean
number of deliveries was 1.1 1.4. Twelve (46%) patients had never
had a delivery, six (23%) had had one, four (15%) had had two, two

(8%) had had three, one (4%) had had four, and one (4%) had had ve.
The difference in the number of deliveries between the groups was statistically signicant (P = 0.01) (Table 1).
No differences were found in the number of cesarean deliveries
(Table 1), spontaneous abortions (data not shown), and ectopic pregnancies (data not shown). No patient reported a history of a molar pregnancy.
At the time of diagnosis, 23 (88%) patients from the TOA group had
fever (body temperature 38 C), compared with 16 (62%) patients
from the PID group (P = 0.025).
The number of patients with yellow leukorrhea was similar in both
groups (11 in TOA group vs 10 in PID group), as was the number of patients with green leukorrhea (5 vs 6).
A total of 16 (62%) patients from the TOA group reported diarrhea
on admission; in the PID group, only ve (19%) patients had diarrhea
(P b 0.001).
The mean white blood cell (WBC) count in the TOA group was
21.8 5.3 109/L (range, 10.129.8 109/L), compared with 14.9
5.4 109/L (range, 4.024.4 109/L) in the PID group. The difference
was statistically signicant (P b 0.001). The number of patients with
leukocytosis of more than 15.0 109/L was also signicantly different
between the groups (TOA group, n = 23 [88%]; PID group, n = 15
[58%]; P b 0.01). All patients in the TOA group had a WBC count of
more than 10.0 109/L.
The logistic regression model showed a positive association of TOA
with fever, diarrhea, and leukocytosis of more than 10.0 109/L, with
a Nagelkerke R2 of 0.503.
All patients from the TOA group underwent surgery (abdominal hysterectomy plus bilateral salpingo-oophorectomy). Of the patients from
the PID group, only one required this surgical procedure.
4. Discussion
The present study shows an overall picture of patients with a TOA.
They were typically in their fourth decade of life, married, with a limited
level of education, and with two or three children usually born vaginally. These characteristics vaguely dene the population at greatest
risk for developing this form of PID. More specically, the triad of
fever (body temperature 38 C), diarrhea, and elevated WBC count
(N10.0 109/L) was signicantly associated with the presence of

Table 1
Patient characteristics.a
Characteristic

Total (n = 52)

TOA group (n = 26)

PID group (n = 26)

P value

Age, y
Marital status
Single
Married
Widow
Common law marriage
Divorced
Highest educational level
None
Elementary
Secondary
Preparatory
Bachelor degree
Master degree
Alcohol consumption
Smoking
Age at start of sexual activity, y
Number of sex partners
1
2
IUD use
Number of pregnancies
Number of deliveries
Number of cesarean deliveries

36.3 10.6 (1564)

39.3 10.8 (1564)

33.1 9.7 (1549)

0.04

7 (13)
27 (52)
3 (6)
14 (27)
0

2 (8)
14 (54)
2 (8)
8 (31)
0

5 (19)
13 (50)
1 (4)
6 (23)
1 (4)

0.22
0.78
0.55
0.53
0.31

1 (2)
18 (35)
20 (38)
10 (19)
2 (4)
1 (2)
2 (4)
7 (13)
17.9 4.1 (1232)

0
13 (50)
8 (31)
5 (19)
0
0
1 (4)
2 (8)
18.2 3.7 (1327)

1 (4)
5 (19)
12 (46)
5 (19)
2 (8)
1 (4)
1 (4)
5 (19)
17.5 4.5 (1232)

0.31
0.01
0.25
0.99
0.14
0.31
0.99
0.22
0.70

25 (48)
27 (52)
26 (50)
2.7 1.6 (07)
1.6 1.6 (06)
0.6 1.1 (03)

13 (50)
13 (50)
14 (54)
2.9 1.7 (07)
2.2 1.7 (06)
0.6 0.8 (02)

12 (46)
14 (54)
12 (46)
2.5 1.6 (06)
1.1 1.4 (05)
1.0 1.3 (03)

0.78
0.78
0.57
0.41
0.01
0.13

Abbreviations: TOA, tubo-ovarian abscess; PID, pelvic inammatory disease; IUD, intrauterine device.
a
Values are given as mean SD (range) or number (percentage), unless indicated otherwise.

L.H. Sordia-Hernndez et al. / International Journal of Gynecology and Obstetrics 132 (2016) 1719

TOA. This novel nding will facilitate the prediction of TOA in patients
with PID.
A TOA represents a failure in stopping the progression of severe PID.
This can be the result of the patient not seeking medical care in a timely
manner or of inadequate management of milder forms of the disease by
the medical team.
Early diagnosis and especially early effective treatment are the best
strategies for ensuring that PID does not progress to TOA formation.
A TOA develops in up to 34% of hospitalized patients with PID [5]. The
consequences of this disease can be fatal, with the majority of deaths
resulting from rupture of the abscess. The mortality rate can be as
high as 510%, despite advances in treatment including surgical therapy
[6]. It is therefore essential to identify elements of the clinical picture of
TOA, to guide the early identication of patients who are most likely to
develop this complication.
Leukocytosis is considered to be a minor criterion for the diagnosis of
PID [7]. In the present study, all patients with a TOA had a WBC count of
more than 10.0 109/L; the mean number of leukocytes was signicantly increased in patients with a TOA, and approximately 90% of patients with a TOA had a WBC in excess of 15 109/L. The WBC count
was positively associated with the severity of the infection; given that
a TOA is the most serious form of PID, the presence of a high WBC
count in these patients is understandable.
Fever is also considered to be a minor criterion for the diagnosis of
PID [8]. In previous reports, fever was documented in approximately
50% of patients with PID. [9]. In the present study, the percentage of patients with fever at diagnosis was signicantly higher in the group with
TOAalmost 90% were admitted with fever. As with leukocytosis, fever
is related to the severity of the infection.
Approximately 60% of the patients with a TOA in the present study
reported diarrhea at the time of admission. Diarrhea was three times
more frequent in these patients than in those with a diagnosis of PID.
These ndings contrast with previous reports [2] that the presence of
diarrhea is only associated with atypical PID. Diarrhea that occurs with
PID is considered to be a type of noninfectious diarrhea. This type of
diarrhea has previously been found in abdominal pathologies that can
require surgical treatment, such as intussusception, gastrointestinal
bleeding, acute appendicitis, and ectopic pregnancy [10]. In the present
study, diarrhea was signicantly more common among women with a
TOAprecisely those who required surgical intervention.
Because leukocytosis, fever, and diarrhea were more common
among patients with a TOA, their combined presence represents a
triad that is positively associated with a diagnosis of TOA. This is important because it enables clinicians to suspect the possible progression of
PID to a more severe form with potentially deleterious consequences,
including an increased mortality.
The age of patients with PID and TOA varied widely in previous reports [2,4,8]. In the present study, the mean age was higher in the
group with TOA.
A parameter that has received little attention in the literature is the
marital status. In the present study, more than 50% of the patients were
married, which differs from previous observations that single or divorced patients have a greater risk of more severe forms of PID [8].
There are also reports [5] that relate the highest educational level
inversely with the most severe forms of PID. In agreement with these reports, more than twice as many patients in the TOA group had a maximum educational level that included only basic or primary education.

19

Tobacco consumption has also been linked with PID [5]. However,
the frequency of tobacco consumption in the present study was lower
in the group with TOA, and like alcohol it was not related to the severity
of PID. However, the total number of women who consumed alcohol
and/or tobacco was very small; therefore, it is not possible to make
denite conclusions.
Age at the start of sexual activity [11], the number of sex partners [2],
a history of sexually transmitted diseases [12], and the use of an intrauterine device [13] have been reported as predisposing factors for PID.
In the present study, no relationship was established between these
factors and the severity of PID, specically with the presence of TOA.
Regarding the obstetric history, the number of births, but not the
number of pregnancies, cesarean deliveries, abortions, ectopic pregnancies, or molar pregnancies, was positively associated with the diagnosis
of TOA in the present study. The reason for this association is not known,
but it might be attributable to cervical injury and subsequent colonization with bacteria causing a severe infection.
The limitations of the present study include its observational design,
the small sample size, and the lack of cultures from pelvic secretions.
In conclusion, the triad of fever, leukocytosis, and diarrhea in a patient with PID should alert clinicians to the possibility that the disease
could evolve unfavorably toward the formation of a TOA, an entity
that puts the patients life at risk. Strategies should be taken to address
this risk, including the prescription of a more aggressive antibiotic
regimen and early percutaneous drainage of the abscess. If the center
is not an appropriate setting for dealing with this presentation, prompt
transport to a better equipped center should be ensured.

Conict of interest
The authors have no conicts of interest.

References
[1] Wiesenfeld HC, Sweet RL. Progress in the management of tuboovarian abscesses.
Clin Obstet Gynecol 1993;36(2):43344.
[2] Lareau SM, Beigi RH. Pelvic inammatory disease and tubo-ovarian abscess. Infect
Dis Clin North Am 2008;22(4):693708 vii.
[3] Rein DB, Kassler WJ, Irwin KL, Rabiee L. Direct medical cost of pelvic inammatory
disease and its sequelae: decreasing, but still substantial. Obstet Gynecol 2000;
95(3):397402.
[4] Monif GR. Clinical staging of acute bacterial salpingitis and its therapeutic ramications. Am J Obstet Gynecol 1982;143(5):48995.
[5] Benito V, Seara S, Prieto M, Luelmo E, Garca-Hernndez JA. Tubo-ovarian abscesses:
A retrospective study. [article in Spanish] Prog Obstet Ginecol 2005;48(1):1422.
[6] McWilliams GD, Hill MJ, Dietrich 3rd CS. Gynecologic emergencies. Surg Clin North
Am 2008;88(2):26583 vi.
[7] Workowski KA, Berman SM. CDC sexually transmitted diseases treatment guidelines. Clin Infect Dis 2002;35(Suppl. 2):S1357.
[8] Khan ZE, Rizvi JH. Pelvic inammatory disease and pelvic abscesses. Rev Gynaecol
Perinatal Pract 2006;6(34):18591.
[9] Landers DV, Sweet RL. Tubo-ovarian abscess: contemporary approach to management. Rev Infect Dis 1983;5:87684.
[10] Armon K, Stephenson T, MacFaul R, Eccleston P, Werneke U. An evidence and consensus based guideline for acute diarrhoea management. Arch Dis Child 2001;
85(2):13242.
[11] Kruszka PS, Kruszka SJ. Evaluation of acute pelvic pain in women. Am Fam Physician
2010;82(2):1417.
[12] Trigg BG. Sexually transmitted infections and pelvic inammatory disease in
women. Med Clin North Am 2008;92(5):1083113 x.
[13] Grimes DA. Intrauterine device and upper-genital-tract infection. Lancet 2000;
356(9234):10139.