Journal of Epidemiology and Global Health

Volume 5, Issue 2, June 2015, Pages 205 - 210

Tuberculosis screening among Bolivian sex workers and their children

Silvia S. Chianga, b, *,, Jessica K. Paulusc, Chi-Cheng Huangd, P.K. Newbya, Dora Castellón Quirogae, Renée Boynton-Jarretta, 1, Lara Antkowiaka, b, 1
aBoston University School of Medicine, Division of General Pediatrics, 850 Harrison Avenue, 5th Floor, Boston, MA 02118, USA
bBoston Children’s Hospital, Department of Medicine, 300 Longwood Avenue, Boston, MA 02115, USA
cTufts Clinical and Translational Science Institute, Tufts Medical Center, 35 Kneeland Street, 8th–11th Floors, Boston, MA 02111, USA
dDepartment of Medicine, Lahey Clinic, 41 Burlington Mall Road, Burlington, MA 01805, USA
eIndependent Consultant, La Paz, Bolivia

RBJ and LA are joint senior authors.

*Corresponding author at: Baylor College of Medicine, Department of Pediatrics, Section of Infectious Diseases, 1102 Bates Street, Suite 1120, Houston, TX 77030, USA. Tel.: +1 (832) 824 4330; fax: +1 (832) 825 4347.
Corresponding Author
Received 20 April 2014, Revised 11 June 2014, Accepted 12 June 2014, Available Online 19 July 2014.
10.1016/j.jegh.2014.06.002How to use a DOI?
Maternal child health; Prostitution; Sex work regulation; HIV screening; Household contact investigation

Bolivian sex workers were more likely than other employed women to report tuberculosis screening only if they reported HIV screening. Of all women with household tuberculosis exposure, <40% reported screening for themselves or their children. Coupling tuberculosis screening with sex workers’ mandatory HIV screenings may be a cost-efficient disease-control strategy.

© 2014 Ministry of Health, Saudi Arabia. Published by Elsevier Ltd.
Open Access
This is an open access article under the CC BY-NC-ND license (

1. Introduction

Bolivia has the Western Hemisphere’s second highest tuberculosis (TB) incidence and prevalence [1]. The city of El Alto (population 843,934 [2]) has been recognized as a TB epicenter [3] with poor indices of disease control and detection [4]. Commercial sex workers (CSWs) have multiple TB risk factors-socioeconomic marginalization, crowded workplaces, limited healthcare access, and high HIV infection risk [57]-but their TB screening practices have been described in only one study, which demonstrated under-screening among Mexican CSWs [8]. TB screening, household exposure, and disease were assessed among El Alto’s CSWs and their children by comparing them with a group of women in other professions (controls) and their children.

2. Methods

2.1. Sample

From July to September 2010, a cross-sectional study was conducted to evaluate TB and other health issues faced by El Alto’s CSWs and their children. One hundred twenty-five CSWs and 125 controls were recruited; eligible participants were 18–45 years old, lived in El Alto, worked outside the home at least two days or nights per week, and had at least one child under the age of ten. Sampling was stratified into five age brackets: 18–25, 26–30, 31–35, 36–40, and 41–45. Enrollment into each group was capped at 80 women (40 CSWs, 40 controls). A similar number of participants in each bracket was achieved except the oldest. Only five 41–45-year-old CSWs with a child under age ten were recruited, so the recruitment of CSWs from the other brackets was expanded to meet enrollment goals.

2.2. Participant recruitment and interviews

Four female Bolivian interviewers recruited eligible participants in three locations adjacent to El Alto’s red-light district: a government-run clinic; House of Hope, a drop-in center for CSWs operated by a faith-based organization; and a church. Interviewers administered one-on-one surveys in closed rooms at the House of Hope and the church. No surveys were administered in the clinic to avoid biased answers to healthcare-related questions. Participants received an incentive of powdered milk purchased for 35 bolivianos (approximately 5 U.S. dollars).

Interviewers obtained informed consent, read survey questions to participants, and recorded answers. To limit bias, interviewers provided standard, minimal clarification to questions. The survey consisted of 39 multiple-choice and 12 open-ended questions. The TB section asked about prior maternal and child TB screening (by skin test, chest radiograph, and/or sputum microscopy), household exposure, and disease. HIV screening history was also assessed. Additionally, participants were asked to provide demographic information and to use three-point Likert scales to rate their perceived quality of and comfort level with healthcare services (detailed in Table 1).

Variable All women (n = 250) CSWs (n = 125) Controls (n = 125) p-Value
Maternal age, mean (SD) 30.62 (6.91) 30.02 (6.39) 31.22 (7.36) 0.17
Wage per day, mean (SD)a 85.19 (72.00) 123.68 (72.81) 46.70 (46.07) <0.0001
Days or nights worked per week, n (%) 0.01
  2–3 88 (35) 45 (36) 43 (34)
  4–5 88 (35) 53 (42) 35 (28)
  6–7 74 (30) 27 (22) 47 (38)
Meals per day eaten by children, n (%) 0.01
  ⩽2 44 (18) 17 (13) 27 (22)
  3 118 (47) 53 (42) 65 (52)
  ⩾4 88 (35) 55 (45) 33 (26)
Highest education level, n (%) 0.24
  Some primary school or less 85 (34) 45 (36) 40 (32)
  Graduated primary school or some high school 93 (37) 50 (40) 43 (34)
  Graduated high school or more 72 (29) 30 (24) 42 (34)
Number of children, n (%) 0.07
  1 52 (21) 24 (19) 28 (22)
  2 80 (32) 48 (38) 32 (26)
  3 51 (20) 27 (22) 24 (19)
  ⩾4 67 (27) 26 (21) 41 (33)
Comfort level with healthcare providers, n (%) 0.44
  Uncomfortable or very uncomfortable 108 (43) 58 (46) 50 (40)
  Neutral 16 (6) 9 (7) 7 (6)
  Comfortable or very comfortable 126 (51) 48 (47) 68 (54)
Perceived quality of healthcare, n (%) 0.72
  Not very good or poor 136 (54) 70 (56) 66 (53)
  Good 97 (39) 48 (38) 49 (39)
  Excellent or very good 17 (7) 7 (6) 10 (8)
Concern about HIV infection, n (%) <0.0001
  Yes 169 (68) 104 (83) 65 (52)
  No 81 (32) 21 (17) 60 (48)
Previous HIV screening, n (%) <0.0001
  Yes 141 (56) 111 (88) 30 (24)
  No 109 (44) 14 (12) 95 (76)
Household TB exposure, n (%)
  Yes 28 (11) 11 (9) 17 (14) 0.23
  No 222 (89) 114 (91) 108 (86)
Prior maternal TB disease, n (%)
  Yes 4 (2) 3 (2) 1 (1) 0.62b
  No 246 (98) 122 (98) 124 (99)
Prior child TB disease, n (%)
  Yes 2 (1) 2 (2) 0 (0) 0.50b
  No 248 (99) 123 (98) 125 (100)

In January 2010, approximately 7.02 bolivianos equaled 1 USD.


Calculated using two-tailed Fisher’s exact probability test because some cell values were < 5.

Table 1

Characteristics of CSWs and controls in El Alto, Bolivia.

Because there was no local institutional review board (IRB) in 2010, this study was approved by a group of local professionals from within and outside the medical field and Boston University School of Medicine’s IRB.

2.3. Statistical analysis

Descriptive characteristics between cases and controls were compared using two-tailed Student’s t and Pearson χ2 tests. Differences in maternal and child TB screening were characterized by odds ratios (ORs) with 95% confidence intervals (CIs). Three multivariable models evaluated the role of potential confounders. Model 1 included maternal age at the time of the interview. Model 2 included maternal age, highest maternal education level, economic variables (daily wage, number of days or nights worked per week, number of children’s meals per day), and healthcare variables (perceived quality of and comfort level with healthcare services). Model 3 included all Model 2 variables and prior HIV screening. Analyses were conducted with SAS version 9.2 (SAS Institute, Cary, NC).

3. Results

Table 1 compares demographic and socioeconomic characteristics between CSWs and controls. Among all participants, 22% and 17% reported previous TB screening for themselves and their children, respectively. Multivariable analysis using Model 2 demonstrated a greater likelihood of TB screening among CSWs (OR = 2.48, CI: 1.12–5.52). However, after further adjustment for HIV screening, the association disappeared (OR = 0.99, CI: 0.37–2.62) (Table 2). The difference in the likelihood of child TB screening between the groups did not reach statistical significance (Table 2).

Screened, n (%) Not screened, n (%) Crude OR (95% CI)
Age-adjusted ORa (95% CI)
Age, socioeconomic, and health care variable-adjusted ORb (95% CI)
Age, socioeconomic, health care variables, and HIV screening-adjusted ORc (95% CI) p-value
Controlsd 21 (17) 103 (83) 1.00 (reference)
CSWs 33 (26) 92 (74) 1.76 (0.95, 3.25)
1.87 (0.99, 3.42)
2.48 (1.12, 5.52)
0.99 (0.37, 2.62)
Children of controls 17 (14) 108 (86) 1.00 (reference)
Children of CSWs 26 (21) 99 (79) 1.67 (0.85, 3.26)
1.72 (0.88, 3.38)
1.59 (0.69, 3.66)
0.79 (0.29, 2.16)

Model 1: adjusted for maternal age (years).


Model 2: adjusted for maternal age (years), maternal education (some primary school, primary graduation/some high school, graduated high school), wages per day ($), days or nights worked per week (2–3, 4–5, 6–7), children’s meals per day (⩽2, 3, ⩾4), perceived quality of medical care (not very good/poor, good, excellent/very good), comfort level of medical care (uncomfortable/very uncomfortable, neutral, comfortable/very comfortable).


Model 3: adjusted for maternal age (years), maternal education (some primary school, primary graduation/some high school, graduated high school), wages per day ($), days or nights worked per week (2–3, 4–5, 6–7), children’s meals per day (⩽2, 3,⩾4), perceived quality of medical care (not very good/poor, good, excellent/very good), comfort level of medical care (uncomfortable/very uncomfortable, neutral, comfortable/very comfortable), HIV testing (yes/no).


One respondent with unknown maternal TB screening history was excluded.

Table 2

Likelihood of maternal and child TB screening by maternal occupation.

Of the 11% of all women who reported household TB exposure, 36% and 39% reported previous maternal and child TB screening, respectively. Table 1 demonstrates the lack of statistically significant differences in rates of household exposure, maternal TB disease, and child TB disease between CSWs and controls. However, this study may not have been adequately powered to detect differences.

4. Discussion

This study yielded two important findings. First, <40% of all women with household TB exposure-the most important epidemiologic risk factor for infection-reported prior TB screening for themselves and their children. The World Health Organization recommends household contact investigation, as well as isoniazid preventive therapy (IPT) for contacts under age five in whom active disease has been ruled out [9]. However, the Bolivian National Tuberculosis Program does not count contact investigation or IPT among its priorities [10]. The <40% screening rate for household contacts of TB patients and Bolivia’s lack of emphasis on prevention are not surprising since low-income countries typically focus resources on symptomatic patients [11]. Nevertheless, recent analyses have demonstrated the cost-effectiveness of IPT in a resource-limited area [12], and household contact investigation in Lima, Peru, has led to a fivefold increase in TB disease detection [13].

The second important finding was an association between HIV screening and TB screening among CSWs. In 2001, Bolivia’s Ministry of Health mandated regular HIV screening for CSWs [14]. Further investigation is needed: to clarify whether required HIV screening led to increased TB screening; to document screening locations for CSWs; and to assess the impact of TB screening for CSWs on disease detection and prevention. Nonetheless, these findings have two potential public health implications. First, incorporating TB screening into medical encounters for which the government has already committed resources may be a cost-efficient strategy to increase detection of a prevalent disease. Second, mandatory regular HIV screening, which increases exposure to healthcare, may translate into other health benefits for CSWs; this possibility also merits further investigation.

This study had limitations. It could not determine causation between HIV screening and TB screening because both were retrospectively reported without information on relative timing. Since this study did not ask participants about HIV status, it is possible that some TB screening was prompted by HIV infection, though the 0.39% HIV prevalence among Bolivian CSWs renders this possibility less likely [15]. This study relied on self-reported data, which may be inaccurate, especially in an undereducated sample. To address this limitation, standard explanations (using simple lay vocabulary) of HIV, TB, differences between latent and active TB, and common diagnostic tests were provided. Interviewer-administered surveys carry a risk of social desirability bias, but given the participants’ low average education level, interviewer-administration was preferred over self-administration. By recruiting participants at a health center, the study may have oversampled women who regularly access medical care, resulting in an overestimation of TB screening. Finally, there was difficulty recruiting eligible 41–45 year-old CSWs, but exclusion of 41–45 year-old CSWs and controls from regression models affected neither the clinical nor the statistical significance.

In conclusion, low rates of TB screening, even among families with household exposure, represent lost opportunities for disease detection and prevention. In addition, further research into the association between HIV screening and TB screening among CSWs could translate into cost-effective TB control strategies in this high-prevalence area.

Conflict of interest


Author contributions

SSC, CCH, LA, and RBJ designed the study. DCQ supervised data collection. JKP and PKN performed analyses. SSC and JKP wrote the manuscript. All authors approved the final version of the manuscript.


This work was funded by Boston Children’s Hospital (Frederick Lovejoy Housestaff Research Award), Boston Medical Center (Joel Alpert Grant), the National Center for Research Resources (UL1 RR025752), and the National Center for Advancing Translational Sciences, National Institutes of Health (UL1 TR000073). The sponsors played no role in study design, implementation, or reporting.

We thank Andy Baker, Andrea Baker, Nancy Cruz, Karem Alipaz, Teresa Barco, Nora Huanca, Lucero Huaricano, Peter Gilbert, Andrea Cruz, Debra Palazzi, Oluwatoyin Ajayi, and the women of El Alto who shared their experiences with us.


[1]World Health Organization, Global Tuberculosis Control 2013, World Health Organization, Geneva, Switzerland. Available from:; 2013 [accessed 01.06.14].
[2] Instituto Nacional de Estadística. Censos: Estado Plurinacional de Bolivia. Available from:; 2012 [accessed 10.06.14].
[3] El Alto concentra mayor número de enfermos por tuberculosis. El Diario [Internet]. Available from:; 2011 [accessed 01.06.14].
[4]J Hermida and L Mendizabal, Demonstration collaborative for tuberculosis management in El Alto, Bolivia. Available from:; 2012 [accessed 10.06.14].
[6]D Palmero, V Ritacco, S Ruano, M Ambroggi, L Cusmano, M Romano, et al., Multidrug-resistant tuberculosis outbreak among transvestite sex workers in Buenos Aires, Argentina, Int J Tuberc Lung Dis, Vol. 9, No. 10, 2005, pp. 1168-70.
[8]MG Velasquez, R Laniado-Laborin, TC Rodwell, P Cerecer, R Lozada, J Cuevas-Mota, et al., Tuberculosis testing among populations with high HIV risk in Tijuana, Baja California, Mexico, Rev Panam Salud Pub, Vol. 32, No. 1, 2012, pp. 30-5.
[9]Stop TB partnership childhood TB subgroup, Chapter 4: childhood contact screening and management, Int J Tuberc Lung Dis, Vol. 11, 2007, pp. 12-5.
[10]Estado Plurinacional de Bolivia, Ministerio de Salud y Deportes, Manual de Normas Técnicas en Tuberculosis. Segunda edición, Ministerio de Salud y Deportes, La Paz, Bolivia. Available from:; 2009 [accessed 17.04.14].
[14]J Friedman-Rudovsky, Prostitutes strike in Bolivia. Time [Internet]. Available from:,8599,1675348,00.html; 2007 [accessed 06.08.13].
[15]Ministerio de Salud y Deportes, Informe nacional sobre los progresos realizados en la aplicacion de UNGASS, Ministerio de Salud y Deportes, La Paz, Bolivia, 2010.
Journal of Epidemiology and Global Health
5 - 2
205 - 210
Publication Date
ISSN (Online)
ISSN (Print)
10.1016/j.jegh.2014.06.002How to use a DOI?
© 2014 Ministry of Health, Saudi Arabia. Published by Elsevier Ltd.
Open Access
This is an open access article under the CC BY-NC-ND license (

Cite this article

AU  - Silvia S. Chiang
AU  - Jessica K. Paulus
AU  - Chi-Cheng Huang
AU  - P.K. Newby
AU  - Dora Castellón Quiroga
AU  - Renée Boynton-Jarrett
AU  - Lara Antkowiak
PY  - 2014
DA  - 2014/07/19
TI  - Tuberculosis screening among Bolivian sex workers and their children
JO  - Journal of Epidemiology and Global Health
SP  - 205
EP  - 210
VL  - 5
IS  - 2
SN  - 2210-6014
UR  -
DO  - 10.1016/j.jegh.2014.06.002
ID  - Chiang2014
ER  -