2001. CID. Brucelosis en La Mujer Embarazada

1172 • CID 2001:32 (15 April) • Khan et al.

M A J O R A R T I C L E

Brucellosis in Pregnant Women

M. Yousuf Khan,1a Manuel W. Mah,1,2b and Ziad A. Memish1,2

1Department of Medicine and the 2Department of Infection Prevention & Control, King Fahad National Guard Hospital, Riyadh,Kingdom of Saudi Arabia

Brucella species occasionally cause spontaneous human abortion, but theories regarding whether they do so

more frequently than do other infectious pathogens remain controversial. We reviewed 92 pregnant women

who presented with acute brucellosis at a Saudi Arabian hospital. From 1983 through 1995, the cumulative

incidence of pregnancy and brucellosis was 1.3 cases per 1000 delivered obstetrical discharges. The incidence

of spontaneous abortion in the first and second trimesters was 43%, and the incidence of intrauterine fetal

death in the third trimester was 2%. Antepartum antimicrobial therapy with cotrimoxazole or cotrimoxazole/

rifampin was protective against spontaneous abortion (relative risk, 0.14; 95% confidence interval, 0.06–0.37;

). The beneficial effect of treatment occurred in women with febrile illness; vaginal bleeding atP ! .0001

presentation usually led to spontaneous abortion. This study demonstrated that the incidence of spontaneous

abortion among pregnant women with brucellosis is high and that these women should receive prompt therapy

with antimicrobial agents when they present for medical care.

Brucellosis, a zoonotic disease of global importance [1],

is endemic in Saudi Arabia (national seroprevalence,

15%) [2]. Endemicity in this region results from the

persistence of domestic animal reservoirs for Brucella

species and the human consumption of unpasteurized

dairy products [3, 4].

Various Brucella species are well-known causes of con-

tagious abortion in cattle, sheep, goats, swine, and dogs

[5]. There is also evidence that brucellosis can produce

spontaneous abortion in humans, which has been dem-

onstrated by rare cases in which Brucella species were

isolated from fetal or placental tissues, but it has not

been demonstrated that brucellosis causes abortions

more frequently than do other bacterial infections [6].

Received 10 July 2000; revised 8 September 2000; electronically published 2April 2001.

a Current affiliation: Department of Medicine, Maricopa Medical Center,Phoenix, Arizona.

b Current affiliation: Department of Medicine, University of Calgary, Canada.

Reprints or correspondence: Dr. Ziad Memish, Infection Prevention & Control,Dept. 2134, King Fahad National Guard Hospital, P.O. Box 22490, Riyadh 11426,Kingdom of Saudi Arabia ([email protected]).

Clinical Infectious Diseases 2001; 32:1172–7� 2001 by the Infectious Diseases Society of America. All rights reserved.1058-4838/2001/3208-0007$03.00

It is believed that brucellosis causes fewer spontaneous

abortions in humans than it does in animals because of

the absence of erythritol in the human placenta and fetus

[7]. Erythritol is a constituent of normal ungulate fetal

and placental tissue and, in cases of bovine abortion,

promotes overwhelming infection of the placenta and

fetus. An additional reason for the lesser role of Brucella

infection in human abortion is the presence of anti-

Brucella activity in human amniotic fluid [8].

In the present study, we reviewed the experience with

brucellosis in pregnant women at a tertiary-care hospital

in Saudi Arabia during a 13-year period. We sought to

characterize clinical presentations, the incidence of abor-

tion, and the effect of treatment with antimicrobial agents

on the occurrence of spontaneous abortion.

PATIENTS AND METHODS

The King Fahad National Guard Hospital (Riyadh,

Saudi Arabia) has served the secondary- and tertiary-

level medical needs of Saudi National Guard soldiers and

their extended families since 1983. Guardsmen come

from bedouin tribes that have retained a nomadic pas-

toral lifestyle that includes the consumption of unpas-

teurized milk from goats, camels, and sheep; many of

Brucellosis in Pregnant Women • CID 2001:32 (15 April) • 1173

Table 1. Characteristics of 92 pregnant womenwith acute brucellosis in Saudi Arabia.

CharacteristicNo. (%)

of patients

Age range, y (n p 92)

16–20 14 (15)

21–25 32 (35)

26–30 19 (21)

31–35 15 (16)

36–42 10 (11)

43–47 2 (2)

No. of pregnancies prior to the studyperiod (n p 88)

0 4 (4)

1 6 (7)

2 7 (8)

�3 71 (81)

No. of spontaneous abortions priorto the study period (n p 86)a

0 62 (72)

1 16 (18)

2 4 (5)

�3 4 (5)

Trimester of pregnancy (n p 92)

1 23 (25)

2 44 (48)

3 25 (27)

a Includes patients who had intrauterine deaths.

these animals are known to be infected with Brucella species.

Because of their nomadic lifestyles, not all pregnant women re-

ceive prenatal care, some are lost to follow-up, and some are

treated for brucellosis at our hospital but subsequently deliver

elsewhere.

The medical record database at the hospital was reviewed,

and all patients who had a discharge diagnosis of brucellosis

and pregnancy from 1983 through 1995 were identified. The

diagnosis of acute brucellosis was based on compatible clinical

features and a serum agglutinin titer of �1:320 or a positive

blood culture result. Patient records were reviewed, and the

following information was extracted: patient age, obstetrical

history, gestational age at the time of infection, symptoms,

results of serological testing and blood cultures for Brucella,

antimicrobial therapy, delivery outcome, results of placental

cultures and histological findings, neonatal status, and neonatal

results of serological testing and cultures for Brucella. The first

trimester of pregnancy was defined as a gestational age of �12

weeks; the second trimester of pregnancy, 112 to �24 weeks;

and the third trimester of pregnancy, 124 weeks. Patients with

brucellosis were considered to have been treated if they received

therapy with cotrimoxazole, rifampin, or a tetracycline for at

least 4 weeks. Fetal deaths that occurred at �24 weeks’ gestation

were designated “spontaneous abortions,” while deaths that

occurred at 124 weeks’ gestation were designated “intrauterine

fetal deaths.”

A variety of microbiological methods were used at our hos-

pital during the 13-year period to isolate Brucella species, de-

termine antimicrobial susceptibility, and detect agglutinating

antibodies; these methods have been described in detail else-

where [9–11]. In brief, samples of blood and body fluids were

cultured by use of the automated BACTEC System (Becton

Dickinson). Before 1987, identification of Brucella organisms

to the species level was not done because of technical limitations

in the microbiology laboratory. In subsequent years, Brucella

isolates were identified to the species level by use of standard

biochemical methods. Antimicrobial susceptibility tests were

performed according to a standard disk diffusion method. Ag-

glutination tests for antibody to Brucella were performed by

means of a microtiter serial dilution technique.

Epidemiological associations were expressed as relative risk

with 95% CIs, and statistical significance was assessed by use

of the x2 test or 2-tailed Fisher’s exact test where appropriate.

All statistical measures were generated by use of Epi-Info, ver-

sion 6 (Centers for Disease Control and Prevention).

RESULTS

From 1983 through 1995, there were 545 cases of brucellosis

at the hospital, of which 92 (17%) occurred in pregnant women

(cumulative incidence, 1.3 cases of brucellosis in pregnant

women per 1000 delivered obstetrical discharges [0.3 cases of

brucellosis in pregnant women per 1000 hospital admissions]).

The characteristics of the 92 pregnant women with acute bru-

cellosis are shown in table 1. The mean age of the women was

26.9 years. Seventy-one (81%) of 88 women had 3 or more

pregnancies prior to the study period, 62 (72%) of 86 had

never spontaneously aborted before, and 44 (48%) of 92 pre-

sented during the second trimester of pregnancy.

Overall, 40 (43%) of 92 pregnant women with acute bru-

cellosis had spontaneous abortions during the first or second

trimester, and 2 (2%) had intrauterine fetal deaths in the third

trimester (table 2). The incidence of abortion was significantly

higher during the first and second trimesters than it was during

the third trimester. To put these rates in context, we calculated

the incidence of spontaneous abortion or intrauterine fetal

death for all women for the period from July 1999 through

June 2000. During this 1-year interval, the total rate of spon-

taneous and missed abortions (i.e., early fetal death before com-

pletion of 24 weeks of gestation with retention of dead fetus

or retained products of conception, not following spontaneous


Table 2. Occurrence of spontaneous abortionand intrauterine death, according to trimester ofpregnancy, in 92 women with acute brucellosisin Saudi Arabia.

Trimester of pregnancyNo. of

patients

No. (%) ofspontaneous

abortions

First 23 12 (52)

Second 44 28 (64)

Third 25 2 (8)a

Total 92 42 (46)a

NOTE. Difference in the incidence of abortion wassignificant for first vs. third trimester ( ) and secondP ! .001vs. third trimester ( ), but not for first vs. secondP ! .0001trimester ( ).P p .4

a These were or included intrauterine fetal deaths.

abortion, induced abortion, or delivery) during the first and

second trimesters combined was 2.8% (589 spontaneous abor-

tions and 121 missed abortions among the 25,540 women who

received antenatal care), and the rate of intrauterine fetal death

during the third trimester was 0.3% (66 intrauterine fetal deaths

among the remaining 24,830 pregnant women who did not

abort during the first or second trimesters).

Of the 92 pregnant women with brucellosis, 91 had positive

serum agglutinin titers that ranged from 1:320 to �1:20,480;

the geometric mean titer was 1:2560. Serological testing was

not performed for 1 patient; brucellosis in this patient was

diagnosed by a blood culture result that was positive for Brucella

species. There was no apparent relationship between the mag-

nitude of the titer and the occurrence of bacteremia. Serum

agglutinin titers �1:2560, compared with those !1:2560, were

not significantly associated with the occurrence of spontaneous

abortion ( ).P p .5

Fifty-two of the 92 women had blood cultures performed.

Twenty-two (42%) of these cultures had positive results: 16

yielded Brucella melitensis, 1 yielded Brucella abortus, and 5

yielded Brucella species that were not identified to the species

level. Antimicrobial susceptibility testing for these 22 isolates

revealed that 18 were susceptible to cotrimoxazole and 4 were

resistant. Eight (36%) of 22 women with brucella bacteremia

aborted, and 16 (53%) of the 30 women for whom blood

cultures were negative aborted; this difference in the incidence

of abortion was not statistically significant ( ).P p .2

The incidence of abortion according to pregnancy trimester,

clinical presentation, and treatment is shown in table 3. Overall,

of the 92 pregnant women with brucellosis, 41 (45%) received

treatment. With all pregnancy trimesters represented, 100% of

38 women who presented with preterm febrile illness received

antimicrobial therapy, and there was 1 intrauterine fetal death

(3%). Of the women in the first and second trimesters who

presented with vaginal bleeding and either with or without

fever, 3 (8%) of 40 were treated with antimicrobial agents, and

all aborted. None of 14 women with febrile illness at term or

postpartum were treated, and there was 1 fetal death. Overall,

60 (65%) of the 92 women with brucellosis were febrile.

The details of antepartum antimicrobial treatment are pre-

sented in table 4. Cotrimoxazole was administered as 1 double-

strength tablet (800 mg or sulfamethoxazole and 160 mg of

trimethoprim), given orally b.i.d., and rifampin was adminis-

tered as 600–900 mg, given orally q.d. Antepartum treatment

with antimicrobial agents was significantly more protective

against the occurrence of abortion than was inadequate treat-

ment or no treatment (RR, 0.14; 95% CI, 0.06–0.37; P !

). However, the incidence of abortion among 22 patients.0001

who received treatment with cotrimoxazole was not signifi-

cantly different from that of 17 patients who received treatment

with a combination of cotrimoxazole and rifampin ( ).P p .6

Follow-up data were available for 36 infants of the 41 women

who were treated: 33 (92%) were normal and well at follow-

up, and 3 (8%) delivered prematurely (2 of the premature

infants died).

Serum agglutinin titers were measured for 7 of the infants

born to women with brucellosis, and 4 of them had titers �1:

320. Cultures of blood specimens from 6 newborns (�1 week

of age) were performed, but only 1 had a result that was positive

for Brucella species; culture of blood from the mother of this

infant with bacteremia was not done. The mothers of 4 of the

6 newborns for whom cultures were performed had brucella

bacteremia, and all presented during the second trimester.

Placentas and fetuses were not systematically studied in this

case series. Cultures of 11 placental specimens and 1 fetal spec-

imen did not yield Brucella species. Histological examination

of 28 placental samples revealed nonspecific inflammatory

changes in 22 of them.

DISCUSSION

We found that the incidence of spontaneous abortion and

intrauterine death among a retrospective cohort of 92 pregnant

women with acute brucellosis due primarily to B. melitensis

was 46%. As shown in the Results section, the rates of spon-

taneous abortion and intrauterine death among women with

active brucellosis substantially exceeded the rates of sponta-

neous abortion and intrauterine death among the general pop-

ulation of pregnant women at our institution during the cor-

responding trimesters. The frequency of fetal loss among

patients with brucellosis was comparable in the first and second

trimesters, but intrauterine fetal death during the third tri-

mester was uncommon. Most of these women were older than

20 years of age, were not primigravid, and most had not had

a spontaneous abortion prior to the study period. Our rate of

incidence exceeds the 10% rate reported by Criscuolo and di


Table 3. Incidence of spontaneous abortion and intrauterine death, according topregnancy trimester and clinical presentation, among 92 pregnant women with acutebrucellosis in Saudi Arabia.

Trimester of pregnancy, presentation

No. of patients

Total TreatedHad spontaneous

abortion

First

Vaginal bleeding with or without febrile illness 12a 1 12

Predominantly febrile illness 11b 11 0

Second

Vaginal bleeding with or without febrile illness 28c 2 28

Predominantly febrile illness 16d 16 0

Third

Febrile illness at term or postpartum 14e 0 1f

Preterm febrile illness 11g 11 1f

Total 92 41 42

a Brucella bacteremia in 1 patient.b Brucella bacteremia in 2 patients, 9 normal deliveries, and 2 premature newborns.c Brucella bacteremia in 7 patients.d Brucella bacteremia in 6 patients, 15 normal deliveries, and 1 premature newborn.e Brucella bacteremia in 6 patients and 1 fetal death. All patients were treated postpartum.f Intrauterine death.g No patients had bacteremia, and all were treated before delivery.

Table 4. Antepartum antimicrobial treatment andpregnancy outcomes for pregnant women with acutebrucellosis in Saudi Arabia.

Treatment

No. of patients

TreatedHad normaldeliveries

Had spontaneousabortion orfetal death

CMZ 23 19 3

CMZ � Rif 17 16a 1

Rif 1 1 0

Total 41 36 4

NOTE. Standard antimicrobial therapy was given to 51 patientsafter abortion or delivery. CMZ, cotrimoxazole; Rif, rifampin.

a Three deliveries were premature.

Carlo [12] in 200 cases of B. melitensis infection in pregnant

women; however, it is similar to the rate of abortion of 31%

among 35 women who were in the first trimester of pregnancy

and who had brucellosis, which was reported by Lulu et al.

[13], and a 40% rate among 30 pregnant women with bru-

cellosis, which was reported by Madkour [14]. Conversely, Sar-

ram et al. [15] observed that, among 51 women who had spon-

taneous abortions during their second trimester, 11.6% had B.

melitensis infection, while Makhseed et al. [16] diagnosed acute

or chronic brucellosis in 7% of 29 women who had spontaneous

abortions and 10% of 51 women who had intrauterine fetal

deaths.

In his classic monograph, Spink [17] stated that “. . . the

passage of time has produced no definitive evidence that the

Brucellae produce abortions any more frequently than do other

species of bacteria.” This statement is difficult to verify because

data on the incidence of abortion caused by other micro-

organisms are lacking or are not directly comparable. For ex-

ample, Campylobacter species, like Brucella species, are well-

described causes of abortion in animals; however, in a series

of 10 pregnant women with Campylobacter jejuni infection who

were at a single hospital, only 1 (10%) had premature labor at

28 weeks’ gestation that resulted in a neonatal death [18]. Other

reports of Campylobacter infection in pregnant women include

a report of a series of cases that were selected on the basis of

the occurrence of abortion [19] and single case reports of fetal

loss in association with septic shock, bacteremia, and diarrheal

illness [20–22].

A MEDLINE search of the literature published from 1966

through 2000 that used the terms “E. coli” and “abortion” did

not yield any reports of studies of patients with Escherichia coli

bacteremia or sepsis who experienced spontaneous abortion.

A similar search for an association between Salmonella species

and spontaneous abortion yielded 1 report of a study of 30

pregnancies that were complicated by typhoid fever and that

resulted in 3 spontaneous abortions (10%) [23].

Although comparative data are limited, an incidence of abor-

tion from 10% to 42% in patients with active brucellosis ex-

ceeds that observed in patients infected with other organisms,

such as Campylobacter species and Salmonella species, and sug-

gests that Brucella species may indeed produce human abor-


tions more frequently than do other bacterial pathogens.

Clearly, there is a need for better evidence to verify this sug-

gestion, which would come from case-control studies; however,

the selection of an appropriate control group is problematic,

because our understanding of the pathogenesis of spontaneous

abortion in women with brucellosis is poor.

Bacteremia is mentioned as a risk factor for spontaneous

abortion in the literature, but our study found no association

between maternal bacteremic status and spontaneous abortion.

Furthermore, although it was not systematically studied, 22 of

28 placental samples that we examined had only nonspecific

inflammation. The lack of evidence of uteroplacental involve-

ment in some cases of abortion has been noted by other in-

vestigators [7, 14]. Collectively, these data reveal that women

with active brucellosis may abort despite the absence of ery-

thritol in the human placenta and fetus, the absence of bac-

teremia, and the absence of specific histological abnormalities

in the placenta. Endotoxin has been implicated in the patho-

genesis of brucellosis [24], and it is possible that its promotility

effect on uterine smooth muscle plays a role in abortion [25].

An important observation from the present study is that the

natural history of brucellosis in pregnant women may be altered

by early institution of antimicrobial therapy. When pregnant

women with febrile brucellosis are treated with antimicrobial

agents before vaginal bleeding occurs, most deliver normally.

However, vaginal bleeding at presentation is an ominous sign: it

rarely happens in women who receive treatment with antimi-

crobial agents, and it is associated with a high rate of spontaneous

abortion. Whether the low rate of treatment in cases of vaginal

bleeding is a marker for failure to diagnose brucellosis and

whether it plays a “permissive” role in subsequent abortion or

intrauterine fetal death is difficult to determine from our data.

The most important reservation against treating brucellosis

in pregnant women is the possibility that the patient would

experience adverse effects of the antimicrobial agents [26]. Al-

though the number of patients in this study was not large, we

were still able to extract from our findings that cotrimoxazole

and rifampin appear to be safe agents for treating brucellosis

in pregnant women, because there were no specific drug-related

adverse effects in the 36 newborns for whom there were follow-

up data. Other researchers have argued that the potential ad-

verse effects of cotrimoxazole in pregnant women may be over-

stated [27], and that the duration of treatment with rifampin

is longer for pregnant women with tuberculosis than it is for

pregnant women with brucellosis [28, 29].

In conclusion, this study demonstrated a remarkably high

incidence of first and second trimester spontaneous abortions

among pregnant women with active brucellosis. Occurrence of

abortion was not associated with either the magnitude of the

serum agglutinin titer or the presence of brucella bacteremia.

However, antimicrobial therapy with either cotrimoxazole or

cotrimoxazole plus rifampin had a strong protective effect

against abortion. Future controlled studies are required before

one can establish the pathogenetic role of brucellosis in causing

human spontaneous abortion and whether Brucella species are

more likely to cause abortion than are other infectious path-

ogens. However, even in the absence of such studies, the ne-

cessity of treating pregnant patients who have brucellosis im-

mediately is clear, because brucellosis “can cause fetal death at

any stage of pregnancy, whether maternal infection is mild or

severe. Therefore, treatment must not be withheld” [30].

Acknowledgments

We thank Dr. Frank Kiel for his valued collaboration in the

brucellosis research conducted at King Fahad National Guard

Hospital (Riyadh, Saudi Arabia).

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2001. CID. Brucelosis en La Mujer Embarazada

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