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O RIGINAL S TUDY

Chlamydia trachomatis Prevalence and Risk Behaviors in Parturient Women Aged 15 to 24 in Brazil

Valdir Monteiro Pinto, MD, MSc,*† Ce´lia Landmann Szwarcwald, PhD,‡ Carla Baroni, BSc,† Lorenzo Lyrio Stringari, BSc,† Lilian Amaral Inoceˆncio, BSc,* and Ange´lica Espinosa Miranda, MD, PhD†

Background: Chlamydia trachomatis (CT) is a sexually transmitted infection having repercussions on reproductive health and impact on the fotus. Our goal was to estimate the prevalence of and risk factors for CT in young parturient women in Brazil. Methods: A national cross-sectional study of parturient women, aged 15 to 24 years, attending Brazilian public hospitals was performed in 2009. Participants answered a questionnaire including demographic, behavioral, and clinical data. A sample of urine was collected and screened for CT and Neisseria gonorrhoeae (NG), using polymerase chain reaction COBAS Amplicor CT/NG (Roche Molecular Systems, Branchburg, NJ). Results: A total of 2400 women were selected and 2071 (86.3%) participated in the study. Mean age was 20.2 years (standard deviation 2.7). Prevalence rates of CT and NG were 9.8% (95% confidence interval [CI]: 8.5–11.1) and 1.0% (95% CI: 0.6%–1.4%), respectively. Four per- cent of women infected with CT also had NG infection. CT associated factors were: being younger (15–19 years old) (odds ratio [OR] 1.6 [95% CI: 1.15–2.17]); first sexual intercourse before 15 years of age (OR 1.4 [95% CI: 1.04–6.24]); having more than 1 sexual partner in lifetime (OR 1.6 [95% CI: 1.13–2.26]); Pap smear screening more than 1 year (OR 1.5 [95% CI: 1.08–2.05]); and NG infection (OR 7.6 [95% CI: 3.05–19.08]). Conclusions: This study shows a high prevalence of CT infection among young pregnant women in Brazil. We suggest that CT screening should be included as part of antenatal care routine in this group in Brazil.

C hlamydia trachomatis (CT) is one of the sexually transmit- ted infections (STI), and has great effect on sexual and

reproductive health. 1,2 CT and Neisseria gonorrhoeae (NG) are responsible for genitourinary infections, pelvic inflammatory

From the *Departamento de DST/AIDS e hepatites virais, Ministe´rio da Sau´de, Brasília, Brazil; †Nu´cleo de Doenc¸as Infecciosas, Universidade Federal do Espírito Santo, Vitoria, Brazil; and ‡Instituto de Comuni- cac¸a˜o e Informac¸a˜o Científica e Tecnolo´gica em Sau´de, Fiocruz, Brazil

The authors thank regional health professionals that were very important to the conclusion of this study: Adelaide Setubal, Alvaro Koenig, Ana Cristina Alcantara, Ana Katherine Gonc¸alves, Ana Paula Guimara˜es, Ernesto Figueiro´ Filho, Helaine Milanez, Ivete Cristina Canti, Jorge Oliveira Vaz, Juan Jose´ Rivas, Kenia Zimmerer Vieira, Marcelino Santos Neto, Marcus Takimura, Maria Alix Leite Arau´jo, Patricia Leite Rodrigues, Renylena Schmidt, Silvana Maria Quintana, Terez- inha Teno´rio da Silva, Vale´ria Aparecida da Silva, Weslane Almeida Magalhaes. They also thank Andressa Bolzan from Ministry of Health who helped with logistics. MCT/CNPq/MS-SCTIE-DECIT/CT-Sau´de number 550580/2007-7 and UNODC-Ministe´rio da Sau´de, Termo de Cooperac¸a˜o number 133/08. Correspondence: Ange´lica Espinosa Miranda, MD, Av. Marechal Campos, 1468–Vitoria–ES–29100-240, Brazil. E-mail: espinosa@ndi.ufes.br. Received for publication February 18, 2011, and accepted April 18,

2011.

DOI: 10.1097/OLQ.0b013e31822037fc Copyright © 2011 American Sexually Transmitted Diseases Association All rights reserved.

disease, chronic pelvic pain, fallopian tube infertility, ectopic pregnancy, and are also associated with cervical cancer. 3,4 CT most frequently affects people 20 years of age. 1 Infection during pregnancy-childbirth cycle can result in premature la- bor, premature rupture of the membranes, and low birth weight. 57 CT also have repercussions for the fotus, which may be infected through the vaginal tract and suffer conjunctivitis and pneumonia. 8

In women, diagnosis of CT infection is difficult in devel-

oping countries because of inadequate infrastructure laboratories to perform diagnostic tests. CT is asymptomatic in approximately 70% to 80% of cases, and remains undetected and thus untreated. This represents one of the principal difficulties for its control. 9 One

of the most important risk factors identified in previous studies is being young, that is, less than 25 years of age. 917

In Brazil, the national prevalence of CT infection has not

been estimated before. Previous local studies in Brazil have shown high frequency of CT in young women. 16,17 The scarcity of data is due to several factors: the lack of clinical symptoms that influences the identification of infected individuals and the problems of access to laboratory tests. These tests are expen- sive and rarely performed in Brazilian public health services. In private healthcare services, CT investigation is only undertaken in symptomatic cases or when a sexual partner reports the diagnosed infection. Prenatal care coverage in the country is about 96.5% and screening for STI is performed routinely only to diagnose HIV and syphilis. 18

The purpose of this study was to estimate the national prevalence of CT infection and its association with NG in parturient women aged 15 to 24 years attending Brazilian public maternity units. This study provides useful information for the elaboration of public health policies on CT screening and the building of indicators for monitoring the strategies to prevent this infection in young women.

METHODOLOGY

A cross-sectional study was conducted in 2009 among

parturient women attending Brazilian public hospitals. Parturi-

ent women attending selected maternity units in 5 geographic macro-regions of Brazil from March to November 2009 were invited to take part in the study.

Data Collection

Each participant was interviewed face-to-face by a trained health professional A face-to-face questionnaire was used for collection of sociodemographic data (age, race/color, schooling, marital status, and family income); clinical data (gestational age, number of pregnancies, number of childbirths, number of miscarriages/abortions, antenatal examinations per- formed); sexual data (age at first sexual intercourse, prior history of STI, gynecological complaints, number of sex part-

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Pinto et al.

ners in the last year and since their first sexual intercourse); and STI/HIV risk behavior (drug use, sex in exchange for money/ goods, and information about sex partners regarding a history of blood transfusions, injecting drug use, bisexual practices, and history of imprisonment). Family income was measured in minimum Brazilian wages (MBW); 1 MBW in 2009 was approximately US$250.

Laboratory Tests

A 20-mL urine sample was obtained from the first amount of urine passed, with the recommendations of no prior genital cleansing and a minimum period of two hours without urinating before sample collection. Samples were analyzed in a semiautomated system called COBAS Amplicor CT/NG (Roche Molecular Systems, Branchburg, NJ) for qualitative in vitro detection of CT and NG, as per the manufacturer’s in- structions at the Molecular Biology Laboratory of the Infec- tious Diseases Unit of the Federal University of Espírito Santo.

Calculation of the Sample Size

The sample size was calculated to estimate the national and regional prevalence rate in parturient women aged 15 to 24 years, with a 95% confidence interval (CI) for 1.5% bilateral size. A 10% prevalence rate was taken as the basis for calcu- lating the sample size. 17 The calculated sample size was 1536 and, considering a 20% loss and a sampling design effect of 1.3, a final sample size of 2400 parturient women was obtained.

Sampling

Sampling was performed in 2 stages. In the first stage, 24 public health system maternity units were randomly chosen, with probability proportional to size, established by the number of

childbirths in the year before the study. The choice of the mater- nity units was stratified by geographic macroregion (North, North- east, Midwest, Southeast, and South) with proportional allocation

to

the number of childbirths in the year before the commencement

of

the study of the year 2009. A total of 100 women were selected

in

each health establishment. At the time of their admission for

childbirth, an interview was performed with regard to filling a designed questionnaire and providing urine samples.

Statistical Analysis

Data were analyzed using the SPSS— data entry statis-

tical program (Statistical Package for the Social Sciences) version 17.0. The data collected were weighted using the num- ber of live births in each geographical region in the year 2008.

A preliminary analysis was performed using exploratory tech-

niques on the data, to check the distribution patterns and trends of the principal variables. Bivariate analysis was then per- formed to check for the presence of association between the variables. 2 tests were used for proportion differences and Student t tests and variance analysis were used for testing differ- ences between mean values. To estimate associations with the presence of CT infection, the odds ratio (OR) was used as a measure of association, estimated with a 95% CI. Multivariate analysis was performed to estimate joint effects of independent variables, through the use of logistic regression models.

Ethical Aspects

This project was submitted to the Research Ethics Com-

mittee of the Health Sciences Centre of the Federal University

of Espírito Santo (Committee approval number 112/07) and to

the ethical committee of each maternity unit taking part in the study. All selected women were invited to take part voluntarily

TABLE 1. Prevalence of Chlamydia trachomatis Infection in Brazilian Parturient Women, by Geographical Region (N 2071)

Region

Sample Size

CT

%

95% CI

North

269

38

14.1

9.9–18.3

Northeast

696

60

8.6

6.5–10.7

Midwest

159

18

11.3

6.3–16.3

Southeast

714

70

9.8

7.6–12.0

South

233

16

6.9

3.6–10.2

Brazil

2071

202

9.8

8.5–11.1

in the study and those who accepted signed a written consent form. Those who were diagnosed as being infected received treatment in accordance with the Brazilian guidelines for Sex- ually Transmitted Diseases Control. 18

RESULTS

Of the sample of 2400 parturient women, a total of 2071 (86.3%) were included in the study. No specific information was gathered about nonrespondents. Some of them presented with bleeding during sample collection and were excluded (3.7%), some declined to participate because they were in pain (2.0%), and some accepted to participate but samples were lost during transportation (unfrozen, shed, and/or mixed) (8.0%). The mean age was 20.2 years (standard deviation [SD] 2.69) and mean of formal education was 8 years (SD 2.4). The prevalence rate of CT infection was 9.8% (95% CI:

8.5%–11.1%) and NG was 1.0% (95% CI: 0.6%–1.4%). Four percent of women with CT had a positive test results for NG. Table 1 shows the distribution of CT prevalence rates in the macroregions of Brazil. The highest rate was found in the Northern region (14.1%) and the lowest rate in the Southern

region (6.9%). Table 2 shows CT results by sociodemographic charac- teristics. Women with positive test results were younger (15–19 years) (54.0% vs. 38.1%, P 0.046); reported not living maritally with their partners (38.6% vs. 26.6%, P 0.000), and were poorer (had income less than 4 MBW) (97.0% vs. 92.9%,

P 0.025).

The age of onset of sexual activity ranged from 9 to 24 years, with the mean of 15.6 years (SD 2.7). As shown in Table 3, women with Chlamydia diagnosis reported to be sexually active earlier— before 15 years of age (41.6% vs. 31.9%, P 0.007), have more than 1 sexual partner in the last year (8.9% vs. 4.7%, P 0.016), and more than 1 sexual partner in their lifetime (72.8% vs. 63.1%, P 0.007). They

also reported illicit drug use more frequently (10.4% vs. 5.6%,

P 0.012), including injecting drug use (2.0% vs. 0.5%, P

0.040). No differences were found in terms of prior history of STI (P 0.393) or prostitution (P 0.665). Table 4 describes CT prevalence rate by clinical char- acteristics. Parturient women with a positive CT test result gave birth prematurely more frequently (21.8% vs. 16.1%, P 0.046) and had a higher number of positive NG tests (4.0% vs. 0.6%, P 0.001) when compared to the women without CT. Attending to 6 or more antenatal care appointments were signifi- cantly less among women with CT (3.7% vs. 54.6%, P 0.016). Pap smear screening during the preceding year was also signifi- cantly less in women with CT (37.1% vs. 47.8%, P 0.004). The factors associated with CT in the multivariate logis- tic regression analysis were as follows: age ranging from 15 to

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Chlamydia trachomatis in Brazil

TABLE 2. Sociodemographic Characteristics of Parturient Women Attending Brazilian Public Maternity Units and Association With C. trachomatis (N 2071)

Variables

 

Sample Size

CT

CT

OR (95% CI)

Age (yr)

 

15–19

 

822 (39.7)

109 (54.0)

713 (38.1)

1.9 (1.42–2.46)

20–24

1249 (60.3)

93 (46.0)

1156 (61.9)

1

Schooling (yr) Up to 8 9 and over

1224 (59.1)

124 (61.4)

1100 (58.9)

1.1 (0.83–1.50)

847 (40.9)

78 (38.6)

769 (41.1)

1

Marital status Does not live with partner

575 (27.8)

78 (38.6)

497 (26.6)

1.7 (1.29–2.35)

Married

or living together

1496 (72.2)

124 (61.4)

1372 (73.4)

1

Income

 

Up

to 4

minimum wages

1933 (93.3)

196 (97.0)

1737 (92.9)

2.5 (1.08–5.70)

4

minimum wages

138 (6.7)

6 (3.0)

132 (7.1)

1

Geographical region

 

North

 

269 (13.0)

38 (18.8)

231 (12.4)

2.2 (1.21–4.130)

Northeast

696 (33.6)

60 (29.7)

636 (34.0)

1.3 (0.73–2.31)

Midwest

159 (7.7)

18 (8.9)

141 (7.5)

1.8 (0.88–3.61)

Southeast

714 (34.5)

70 (34.7)

644 (34.5)

1.5 (0.85–2.64)

South

233 (11.3)

16 (7.9)

217 (11.6)

1

19 years (OR 1.6 [95% CI: 1.15–2.17]); onset of sexual activity before 15 years old (OR 1.4 [95% CI: 1.04 – 6.24]); more than 1 sexual partner in their lifetime (OR 1.6 [95% CI:

1.13–2.26]); Pap smear screening more than 1 year ago (OR 1.5 [95% CI: 1.08 –2.05]); and NG coinfection (OR 7.6 [95% CI: 3.05–19.08]) (Table 5).

DISCUSSION

This is the first population-based study at the national level in Brazil to determine the prevalence of CT in young pregnant women. We identified a prevalence rate of 9.8%. Previous local studies in Brazil have shown similar results regarding the prevalence of CT in pregnant and adoles-

cent women. A study performed in the city of Vito´ ria, Espírito Santo, identified CT in 12.2% of sexually active female ado- lescents. 19 Menezes et al. 20 found 7.8% of CT in pregnant women in Recife, Pernambuco, and a study of female adoles- cents in Goiaˆnia, Goia´s, reported a 19.6% of CT. 16 A study performed in 6 cities using a convenience sample reported a 9.4% of CT among pregnant women. 17 Our findings are also in agreement with other studies performed among asymptomatic young women in other coun- tries. Rates from 1.7% to 17% were described in different Euro- pean countries 12,13 and from 4.4% to 15.5% in United States. 9,21 Other studies reported 10.1% of CT in pregnant women in China, 22 8% in Botswana, 14 and 7.7% in Venezuela. 15

TABLE 3. Behavioral Characteristics of Parturient Women Attending Brazilian Public Maternity Units and Association With C. trachomatis (N 2071)

Variables

Sample Size

CT

CT

OR (95% CI)

Age at first sexual intercourse Under 15 yr 15 yr or over No. partners/life

680 (32.8)

84 (41.6)

596 (31.9)

1.5 (1.13–2.05)

1391 (67.2)

118 (58.4)

1273 (68.1)

1

1

744 (35.9)

55 (27.2)

689 (36.9)

1

1

1327 (64.1)

147 (72.8)

1180 (63.1)

1.6 (1.13–2.16)

No. partners/yr

1

1966 (94.9)

184 (91.1)

1782 (95.3)

1

1 Prior STI Yes No Sex worker Yes No Illicit drug use Yes No Injecting drug use Yes No

105 (5.1)

18 (8.9)

87 (4.7)

2.0 (1.18–3.40)

103 (5.0)

7 (3.5)

96 (5.1)

0.7 (0.30–1.45)

1968 (95.0)

195 (96.5)

1773 (94.9)

1

16 (0.8)

2 (1.0)

14 (0.7)

1.3 (0.30–5.88)

2055 (99.2)

200 (99.0)

1855 (99.3)

1

125 (6.0)

21 (10.4)

104 (5.6)

2.0 (1.20–3.22)

1946 (94.0)

181 (89.6)

1765 (94.4)

1

14 (0.7)

4 (2.0)

10 (0.5)

3.8 (1.17–12.05)

2057 (99.3)

198 (98.0)

1859 (99.5)

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2057 (99.3) 198 (98.0) 1859 (99.5) 1 Sexually Transmitted Diseases ● Volume 38, Number 10, October

Pinto et al.

TABLE 4. Clinical Characteristics of Parturient Women Attending Brazilian Public Maternity Units and Association With C. trachomatis (N 2071)

Variables

Sample Size

CT

CT

OR (95% CI)

Gestational age Under 36 wk 36 wk Antenatal care Yes No Antenatal sessions* Up to 5 6 or more Gynecological complaints Yes No Last cytology Last year More than 1 yr ago Gonorrhoea test Positive Negative

344 (16.6)

44 (21.8)

300 (16.1)

1.5 (1.02–2.08)

1727 (83.4)

158 (78.2)

1569 (83.9)

1

1974 (95.3)

185 (91.6)

1789 (95.7)

1

97 (4.7)

17 (8.4)

80 (4.3)

2.1 (1.19–3.54)

733 (37.1)

84 (45.4)

649 (36.3)

1.5 (1.08–1.98)

1241 (62.9)

101 (54.6)

1140 (63.7)

1

511 (24.7)

58 (28.7)

453 (24.2)

1.3 (0.91–1.74)

1560 (75.3)

144 (71.3)

1416 (75.8)

1

969 (46.8)

75 (37.1)

894 (47.8)

1

1102 (53.2)

127 (62.9)

975 (52.2)

1.6 (1.15–2.10)

20 (1.0)

8 (4.0)

12 (0.6)

6.4 (2.58–15.80)

2051 (99.0)

194 (96.0)

1857 (90.4)

1

*Total number of women attending antenatal sessions (1974 cases).

In agreement with other authors, our results also showed an association between CT and age, with higher frequency among the youngest group of women, 9,10,1317,2325 as well as among women who reported having had more than 1 sex partner in their lifetimes, 10,16,17 and in those with NG coinfec- tion. 9,24 These observations highlight that a systematic evaluation needs to be performed concerning risk factors related to sexual behavior in this group. Clinical studies of behavioral interventions, services for sex partners, and treatment services have shown promising results in reducing the risk of bacterial infection, dura- tion of infection, and number of sexual partners. 25 We found that Chlamydia infection showed an associa- tion with lack of yearly Pap smear screening. This may be explained by the fact that women who take care of their own health have a greater chance of having infections diagnosed and treated earlier, as suggested by Wilson et al., 12 than women who do not seek healthcare. Although a cross-sectional study is not ideal for deter- mining risk factors, its application is justified. CT prevalence and risk factors in young women at child-bearing age is im- portant to demonstrate the susceptibility of this population

TABLE 5. Multivariate Analysis of Factors Associated With C. trachomatis Infection in Parturient Women Attending Brazilian Public Maternity Units, 2009

Variables

OR (95% CI)

P

Age (15–19 vs. 20–24 yr) Age at first sexual intercourse (Under 15 vs. 15 yr or over) No. partners/life (more than 1 vs. 1) Last cytology (more than 1 yr vs.

1.6 (1.15–2.17)

0.005

1.4

(1.04–6.24) 0.029

1.6 (1.13–2.26)

0.008

1.5

(1.08–2.05) 0.015

up to 1 yr ago) Gonorrhoea test (positive vs. negative) 7.6 (3.05–19.08) 0.000

Variables included in the model are as follows: age, marital status, income, geographical region, age at first sexual intercourse, number of sex partners/yr, number of sex partners/life, drug use, gestational age, antenatal sessions, last cytology, and gonorrhoea testing.

group to complications caused by this infection during the pregnancy-childbirth cycle and puerperium. Given the low prevalence of some risk factors in this sample, it is possible that the number of women studied was not sufficient to find statis- tical association between some independent variables and Chlamydia infection. The possibility of biased answers cannot be rule out because of the general tendency to give socially acceptable replies in face-to-face interviews. Also, we only included public hospitals and therefore cannot draw conclu- sions on private ones; however, it is important to say that about 70% of the childbirths take place in public hospitals. Bacterial STI have been neglected in recent times due to an increase of viral STI epidemic, especially HIV, which can lead to the misguided suggestion that these agents are diseases of the past, of less importance, and of limited interest to professionals providing healthcare. On the contrary, as demon- strated recently, these infections are a huge burden for health and the economy accounting for 17% of economic losses, mainly in developing countries, caused by the health-disease binomium. 26 Nevertheless, great progress has been achieved in STI prevention by using, in the majority of cases, multiple ap- proaches such as, for example, adding a screening program to prevention strategies for risk populations, which has been shown to be cost effective. 27 Thus enabling early diagnosis and timely treatment and, therefore, reducing morbidity caused by highly asymptomatic diseases such as Chlamydia infections. Given the well-established association between Chla- mydia infection and pelvic inflammatory disease, fallopian tube damage and scarring, infertility, ectopic pregnancy, as well as conjunctivitis and pneumonia in newborn babies, efforts to reduce this infection among teenagers and young adults can produce an important effect on morbidity arising from this disease. A recent US Preventive Services Task Force publica- tion on measures to prevent STIs emphasized the importance of introducing the investigation of Chlamydia infection in all pregnant women aged 24 years. 28 Our results show high CT prevalence in young parturient women in Brazil. This suggests that diagnostic tests for this

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Chlamydia trachomatis in Brazil

infection should be included in screening programs for young pregnant women. Timely diagnosis and treatment could pro- vide peace of mind to women worried about the outcome of their current pregnancy and the future of their sexual and reproductive health. As most cases are asymptomatic, a screen- ing program is one of the important means for identifying undiagnosed infection and to provide earlier treatment to these women and their sexual partners.

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