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INT J TUBERC LUNG DIS 14(6):714719

2010 The Union

Risk of tuberculosis in public transport sector workers,Lima, Peru

O. J. Horna-Campos,* A. Bedoya-Lama, N. C. Romero-Sandoval, M. Martn-Mateo*

*Grups de Recerca dAmerica i Africa Llatines (GRAAL), Unidad de Bioestadstica, Facultad de Medicina, UniversidadAutnoma de Barcelona, Barcelona, Spain; P S San Antonio, Direccin de Salud IV Lima Este, Lima, Peru; GrupoGRAAL, Facultad de Medicina, Pontificia Universidad Catlica del Ecuador, Quito, Ecuador

Correspondence to: Olivia Janett Horna Campos, GRAAL, Unidad de Bioestadstica, Facultad de Medicina, Edifcio Mcampus UAB, Cerdanyola del Valles 08193, Barcelona, Spain. Tel: (+34) 935 813 120. Fax: (+34) 935 812 344. e-mail:ohornac@yahoo.es

Article submitted 14 September 2009. Final version accepted 12 January 2010.

S E T T I NG: Delays rom symptom onset to the diagnosis

and treatment o smear-positive pulmonary tuberculo-

sis (TB) produces possible new cases in persons in close

contact with TB cases, especially in confned spaces such

as overcrowded public transport, which puts other users

and transport workers at risk.O B JE C T I VE : To estimate TB incidence rates in patients

o a health micro-network, and the percentage o trans-

port sector workers among TB and multidrug-resistant

TB (MDR-TB) patients.

DE S I GN: Crude and indirect standardised incidence rates

o TB were calculated rom an exhaustive analysis o all

clinical histories o incident patients in a health micro-

network between 1 January 2007 and 30 June 2008. The

percentage o transport sector workers and the associa-

tion between MDR-TB and working in the transport

sector were analysed.

RESULTS: Standardised incidence rates or transport sec-

tor workers are 2.74.5 times higher than those in the

total working-age male and global population o the

micro-network studied. The association between TB andtransport occupation and MDR-TB and transport occu-

pation is high (respectively OR 3.06, 95%CI 2.24.2

and OR 3.14, 95%CI 1.19.1).

C O NC L US I O N: These results indicate that the use o in-

ormal public transport is a risk actor or TB inection

and an occupational risk in countries with characteris-

tics similar to those in Peru.

KE Y WO R DS : pulmonary tuberculosis; public trans-port; occupational risk

PERU has the second highest burden o tuberculosis(TB) in Latin America,1 with a rate o TB o 123 per100 000 population in 2007.1 According to the PeruvianDepartment o Health (Ministerio de Salud) and theWorld Health Organization (WHO), our to six peopleall ill with TB every hour in Peru, leading to between35 000 and 50 000 cases o TB annually.2,3 O these,10% have multidrug-resistant TB (MDR-TB), while5.8% meet the criteria or extensively drug-resistantTB (XDR-TB).4 These data do not show the consider-able variations between dierent geographical areas.

The Lima metropolitan area accounts or one third

o the population o Peru. A third o the inhabitants oLima live in peripheral areas in conditions o extremepoverty and exclusion.5 As these areas constitute out-lying dormitory neighbourhoods, or most peoplecommuting to work involves travelling considerabledistances6 in public transport. As relatively small ve-hicles are used, overcrowding is common during rushhour, with vehicles sometimes carrying as much astwice their normal capacity.

An earlier study conducted in Lima in 20047 anal-ysed the association between using public transport

and the risk o pulmonary tuberculosis (PTB) amonginhabitants o peripheral areas (odds ratio [OR] 4.9,95% confdence interval [CI] 1.0623.09). The studyound that the situation was worsened by long traveltimes, oten o more than 1 hour (OR 2.7, 95%CI1.1210.10).7

Although perhaps a mere statistical association,there is also the possibility o a causal relationshippotentiated by the long travel times that increase ex-posure to a risk actor (in this case the orm o trans-port). Given these fndings, it was proposed to conducta study gathering new data to increase the consis-

tency o the association described.Since the publication o our earlier article,7 to ourknowledge no urther literature on the relation be-tween the use o long-distance public transport andTB transmission has been published.

MATERIALS

Study population

The Santa Clara Health micro-network consists ofve primary health care centres and orms part o the

S U M M A R Y

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Risk of PTB in transport workers in Lima 715

in this micro-network: the crude rate or the micro-network, TB rates in the working-age population ingeneral and by sex, and the rate among the estimatedpopulation o workers in the transport sector. Sec-ond, the standardised incidence rates (SIRs) between

dierent populations were evaluated. Third, the au-thors compared the percentage o transport sectorworkers among patients with the corresponding fg-ure in the global micro-network population usingodds ratios.

Finally, the association between MDR-TB andworking in the transport sector is described.

The study was approved by the ethics committee oHealth Directorate IV, East Lima (Direccion de SaludIV LimaEste), which is responsible or the micro-network included in this study.

Statistical analysis

As this was a conormity study involving comparisono the values obtained with population reerence val-ues, hypothesis contrasting was perormed by meanso the maximum likelihood ratio, based on binomialor Poisson distribution, depending on the nature othe variable.

In all analyses the G2 statistic was considered sig-nifcant when it exceeded the 95th percentile o the2, with one degree o reedom.14

RESULTS

Study populationThe active clinical histories o 506 TB patients werereviewed: 446 (88.1%) were aged 1564 years, 274were men, 172 women; 22 patients (4.9%) hadMDR-TB. Occupation was known or 249 (90.9%)o the 274 male patients, o whom 44 (17.7%)worked in the public transport sector. Only three pa-tients were HIV-positive and two were alcohol and/or drug addicts.

The proportion o MDR-TB cases among the total506 TB patients was 4.5% (n= 23); 22 were oworking age (4.9%); 17 were men, representing 6.2%

o all men in the study; and six (35.3%) o the menwith MDR-TB worked as public transport drivers orcollectors.

O all the TB cases described, 59.7% were smear-positive, with no dierences by sex (Table 1). Thepercentage o smear-positive TB in this group was72.7%; the small sample size (n = 44) meant that nosignifcant dierences could be ound.

Estimation of TB rates

Table 1 presents the specifc incidence rates/100 000or the Santa Clara health micro-network, which per-mits comparisons, by age and sex, with rates pub-lished by the Ministry o Health or 2007. The Tablealso presents the number o TB and PTB cases ob-served among male transport workers by age group.

public health network o the Peruvian Ministry oHealth. It covers a catchment population o 106 508,representing approximately 23% o the populationo the Ate District, a peripheral urban district o Limawith a population o 478 278.8,9 O these, 71 460

were o working age (1564 years), o which 34 743were male and 36 717 emale.

Poverty in this district aects a considerable pro-portion o the population, the determining actorsbeing high unemployment and low income levelsamong the employed.10

The majority o the population consists o immi-grants rom the mountains who have settled in thearea due to invasions, communal associations and thecreation o new villages and settlements. Many o theseneighbourhoods were created during an era o greatviolence in the 1980s, and were ormed by poor am-

ilies rom the capital itsel.6

Due to the geographical isolation o Ate, one othe most essential economic activities is public trans-port. Public transport is provided by a large numbero companies, which must be registered with the Mu-nicipality o Lima to operate.11 The inormation thesecompanies provide about their services is oten un-reliable, and an overestimation o their capacity inorder to obtain new permits is common.

The Municipality o Lima provided data on thenumber o companies and the characteristics o theirofcial eet, rom which it was possible to determinethe number o workers (drivers and collectors) directly

exposed to the risk o inection associated with operat-ing microbus or combi services. Lima authorities ad-mit the existence o problems with the quality o thisinormation, and estimate that the level o inormalemployment among these companies is around 30%.

Taking into account the proportion o inormal em-ployment estimated by the authorities, the popula-tion o bus and microbus drivers and collectors in thestudy area was estimated at 2069, corresponding to6% o the total male workorce. This proportion is inline with the Ministry o Labours estimated percent-age o 10.3%, which also included retail, communi-

cations and ofce workers.12

Existing public health services are organised intohealth directorates, networks, and micro-networks.These are responsible or implementing vertical Min-istry o Health programmes, one o which is the Na-tional TB Programme (NTP).13

Like the previous study, the present study was con-ducted in the health micro-network o Santa Clara, inall fve o its primary health care centres.

Methods

All clinical histories o patients being treated underthe NTP between 1 January 2007 and 30 June 2008were reviewed and ollowed up in the various healthcare centres o the Santa Clara micro-network.

The authors calculated the ollowing rates o TB

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716 The International Journal of Tuberculosis and Lung Disease

Estimation of ratios between observedand expected rates

Table 2 presents the SIR calculated as total observedcases/total expected cases, where the observed casescorrespond to the health micro-network and the ex-pected cases are those obtained by standardisationusing the indirect method.

Table 2 also shows the crude rate observed ortransport workers and the SIR derived rom the casesexpected in this population o workers calculated us-ing the general rate or Peru, the global rate or themicro-network, that or the working age populationo the network, and fnally the rate or working-agemales in the micro-network.

Estimation of risk of being a TB patient and atransport worker

The percentage o TB patients working in the trans-port sector is 16.05% (95%CI 11.520.6), comparedto 6% (95%CI5.76.2) among men belonging to themicro-network (Table 3). This table also presents theassociation between transport workers and MDR-TBamong the detected cases o TB in men.

DISCUSSION

TB rates observed or the micro-network are higherthan those reported or the general population o Peru,particularly in the age group 1535 years, in whichthe rates were 862 or those aged 1520, 933.04 orthose aged 2025 and 592.97 or those aged 2535.

This is perhaps because 37% o the population all inthese age groups; lack o employment, poor workingconditions and poor living conditions in general alsomake these age groups more prone to disease.15

Table 1 Specific rates of TB by sex and age-group

Sex

Agegroup,years

Population*n

TB (PTB)cases

n

Transportsector

TB (PTB)n

Annualmorbidity

rates, Peru

/100 000

Observedannual

TB rates

/100 000

TB casesobserved/expected

ratio

Male

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Risk of PTB in transport workers in Lima 717

The authors observed that among 2069 bus andmicrobus drivers and collectors, the TB rate was1416.1/100 000 (95%CI 12591588); this did nottake into account the presence otwo transport sec-tor workers aged>65 years, who were thereore out-side the limits set or the working-age population.

The high rate observed in this group may seemsurprising. However, in Peru similar rates have beenreported in other sectors. In a teaching hospital inLima, rates o respectively 932 and 6977/100 000were ound or medical services and laboratory per-sonnel, the only risk actor shared by both groups be-ing the use o public places.16

It is noteworthy that 72.7% o these TB patientswere smear-positive, and given the ailure to complywith transport sector regulations and lack o sicknessand unemployment benefts,17 it is probable that many

continue to work despite their illness. This act cor-roborates fndings rom our previous study,7 in whichinormal public transport was identifed as a settingwith elevated risk o TB inection or users, and espe-cially or the workers, who in turn act as propagatorso the disease.18

The SIRs o transport worker patients increase,depending on what rates they are compared with, thelowest being the value calculated with the rate or meno working age (2.7 times), and the highest being cal-culated using the rate or Peru as a whole (11.6 timeshigher).

The results, expressed in terms o rates, SIR and

risk prevalence, suggest that it is unlikely that the pro-portion o TB and MDR-TB patients observed amongpublic transport workers corresponds to the generalpopulation.

These results could be due to a variety o reasons.First, the community studied is an active populationgroup, which in general has no social security cover-age and difcult access to health care, especially inthe early stages o illness. This means that workersonly seek care when the disease makes it impossibleor them to continue working. This aspect confrmsthat the importance o the problem is underestimated.Second, the lack o sickness benefts means that work-ers are unlikely to accept to participate in a diagnos-tic study. Moreover, even participation in such a studymay lead to rejection by co-workers.

This analysis confrms that public transport work-ers in Lima should be considered at risk o TB andother aerially transmitted diseases (such as inuenza),a component o variability being attributable to theorm o public transport, as demonstrated in the 2007study.7 This association is logical, as drivers and col-lectors are some o the most highly exposed workers,as they are exposed almost daily and or long periods.Furthermore, alcohol consumption, which is commonin this work sector, cannot be considered a specifcrisk actor.

Although the virulence oM. tuberculosis inectioncannot be compared to that o inuenza,19 individualsinected by mycobacteria who subsequently developTB suer more serious consequences, due to the longtreatment and recovery times and subsequent occupa-tional and health-related repercussions, circumstances

that are even more serious in the case o MDR-TBpatients.As this aspect has not previously been documented,

and much less quantifed on a scientifc basis, the au-thors believe that the present study may open a nec-essary line o research and serve to address the prob-lem o ignorance about the risk o inection by anyaerially transmitted disease that these services repre-sent or both passengers and workers, and especiallythe latter.

The only way to confrm these fndings would beto conduct a study specifcally among workers o thissector. However, there are many difculties involved,

and these obliged the authors to tackle this study in aspecifc manner.

The authors recognise the existence o a bias in theestimation o the denominator used in calculatingthe rate o TB among transport sector workers, giventhe existence o 30% inormality in the sector, whichwe assumed to be uniormly distributed. However, theestimated proportion o six people in every 100 em-ployed in the transport sector is not too dierentrom fgures cited by the Peru Ministry o Labour(10.3% in 2007), i we consider that the ofcial fg-ure includes those working in the retail, communica-tions, ofce and transport sectors.

The results obtained stress the need or specifcallydesigned occupational health programmes targetinggroups o this nature, who are difcult to reach or

Table 3 TB and MDR-TB among male transport sector workers in the Santa Clara healthmicro-network

MenTB cases

nPopulation

n OR (95%CI)

Positiveprevalence ratio

(95%CI)

Non-transport workers 230 32 444Transport workers 44 2 025 3.06 (2.214.24) 3.02 (2.24.1)

MDR-TB Not MDR-TB

Non-transport workers 11 219Transport workers 6 38 3.14 (1.119.01) 2.85 (1.117.31)

TB = tuberculosis; MDR-TB = multidrug-resistant TB; OR = odds ratio; CI = confidence interval.

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718 The International Journal of Tuberculosis and Lung Diseasethe reasons mentioned and who lack social securitycoverage and sickness benefts. Furthermore, given thenegative repercussions or the objectives o a NTP, onthe basis o this study we explicitly recommend pro-moting uture studies to confrm these results.

Acknowledgements

This study was partly unded by the Autnoma Solidaria Founda-tion o the Universitat Autnoma de Barcelona (FAS-UAB) and bythe Spanish Lung and Respiratory Diseases Association (SEPAR-solidaria). The authors are grateul or the collaboration o allhealth personnel o the Santa Clara micro-network, and o theEast Lima Health Directorate. Thanks also to Juan Herrera Noble-cilla, o the Lima Municipality Department o Urban TransportRegulation. They are also grateul to the University o Buenos Ai-res School o Public Health or providing a setting in which to dis-cuss and develop this work, and particularly to E Consiglio orconstructive criticism and comments on the text.

References

1 Direccin General, Direccin General de Salud de las Personas,Ministry o Health, Peru (MINSA). Situacin de la Tuberculo-sis en el Per. Inorme de gestin 2007. Lima, Peru: MINSA,2007. [Spanish]

2 World Health Organization. Global tuberculosis control: sur-veillance, planning, fnancing. WHO report 2008. WHO/HTM/TB/2008.393. Geneva, Switzerland: WHO, 2008.

3 World Health Organization. Anti-tuberculosis drug resistancein the world. 4th global report. WHO/HTM/TB/2008.394. Ge-neva, Switzerland: WHO, 2009.

4 Asencios L, Quispe N, Mendoza-Ticona A.Inorme fnal: vigi-lancia de la resistencia a medicamentos antituberculosos en el

Per. Tercera encuesta nacional 20052006. Rev Peru MedExp Salud Publica 2009; 26: 278287. [Spanish]5 Ministerio Pblico, Peru. Poblacin en situacin de pobreza,

segn mbito geogrfco. Lima, Peru: Ministerio Pblico, 2007.http://www.mpn.gob.pe/CD/compendio_estadistico/cap09/ind09.htm Accessed February 2010. [Spanish]

6 Municipalidad de Ate. Distrito. Historia. Lima, Peru: Munici-palidad de Ate, 2009. http://www.muniate.gob.pe/historia.htmAccessed February 2010. [Spanish]

7 Horna-Campos O J, Snchez-Prez H J, Snchez I, Bedoya A,

Martn M. Public transportation and pulmonary tuberculosis,Lima, Peru. Emerg Inect Dis 2007; 13: 14911493.

8 Municipalidad de Ate. Ate en Ciras. ltimos censos. Poblacin.Lima, Peru: Municipalidad de Ate, 2009. http://www.muniate.gob.pe/estadisticas.htm#censosate Accessed February 2010.[Spanish]

9 Direccin IV Lima Este. Microred Santa Clara. Lima, Peru: Di-reccin IV Lima Este, 2009. http://www.limaeste.gob.pe/ Ac-cessed April 2010. [Spanish]

10 Fay M, ed. Directions in development. The urban poor in LatinAmerica. Washington DC, USA: World Bank Publications, 2005.

11 Municipalidad de Lima. Relacin de unidades de transportepor ruta. Gerencia del transporte urbano. http://www.gtu.munlima.gob.pe/Internet_Web/Transporte_Publico/Empresa_Ruta.aspx Accessed February 2010. Lima, Peru: Municipali-dad de Lima, 2009. [Spanish]

12 Programa de estadsticas y estudios laborales, Lima Metropoli-tana. Distribucin de la PEA ocupada segn rama de actividadeconmica 2006 y 2007. Lima, Peru: Ministerio de Trabajo yPromocin del Empleo, 2007. [Spanish]

13 Ministerio de Salud (MINSA). Norma tcnica de salud para el

control de la tuberculosis en el Per. Estrategia Nacional de Pre-vencion y Control de la Tuberculosis (ESN-PCT). Lima, Peru:MINSA, 2006. http://www.minsa.gob.pe/normaslegales/2006/RM383-2006.pd Accessed March 2010. [Spanish]

14 Navarro Gin A, Snchez Prez I, Martn Mateo M. Anlisisestadstico de encuestas en salud: cursos GRAAL 3. Bellaterra,Spain: Universidad Autnoma de Barcelona, Servei de Publica-cions, 2004. [Spanish]

15 Lnnroth K, Holtz T H, Cobelens F, et al. Inclusion o inorma-tion on risk actors, socio-economic status and health seekingin a tuberculosis prevalence survey. Educational series. Int JTuberc Lung Dis 2009; 13: 171176.

16 Alonso-Echanobe J, Granich R M, Laszlo A, et al. Transmis-sion oM. tuberculosis in healthcare workers at a universityhospital in Lima, Peru. Clin Inect Dis 2001; 33: 589596.

17 Mendoza Ticona A, Gotuzo Herencia E. Tuberculosis extrema-damente resistente (TB-XDR): historia y situacin actual. ActaMdica Peruana 2008; 25: 236246. [Spanish]

18 Riley R L, Mills C C, Nyka W, et al. Aerial dissemination opulmonary tuberculosis. A two-year study o contagion in atuberculosis ward. Am J Epidemiol 1995; 142: 314. Dierentto AUF. SW.

19 Miller M, Viboud C, Balinska M, Simonsen L. The signatureeatures o inuenza pandemicsimplications or policy. N Engl

J Med 2009; 360: 25952598.

R S U M

C O NT E XT E : Les retards entre le dbut des symptmesde la tuberculose (TB) pulmonaire bacilloscopie posi-

tive et le diagnostic et traitement sont susceptibles deproduire de nouveaux cas chez les personnes en contacttroit, particulirement dans les espaces confns, tels queles transports publics surchargs, ce qui impose un risquenon seulement aux autres usagers, mais galement auxtravailleurs du secteur des transports.O B JE C T I F : Estimer les taux dincidence de la TB dansun microrseau de sant ainsi que la charge que repr-sente le secteur des transports parmi les patients tuber-culeux et parmi ceux atteints de TB germes multirsis-tants (TB-MDR).S C H MA : On a calcul les taux dincidence (bruts etindirects standardiss) partir dune analyse exhaustivede lensemble des histoires cliniques des cas incidentsdans le microrseau de sant entre le 1 janvier 2007 et le

30 juin 2008. La charge du secteur des transports parmiles patients et lassociation entre le ait dtre un patient

atteint de TB-MDR et de travailler dans le secteur destransports ont t analyss.RSU LTATS : Les taux dincidence standardise chez cestravailleurs sont de 2,7 4,5 ois plus levs que ceux delensemble des hommes en ge de travail et que ceux dansla population totale du microrseau tudi. Lassocia-tion entre la TB et une proession dans les transports esthautement signifcative (OR 3,06 ; IC95% 2,24,2), toutcomme celle qui lie ce secteur et la TB-MDR (OR 3,14 ;IC95% 1,19,1).C O NC L US I O N : Ces rsultats montrent que le recours autransport public inormel constitue un acteur de risquerel dinection tuberculeuse ainsi quun risque proes-sionnel dans les pays dont les caractristiques sont simi-

laires celles du Prou.

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Risk of PTB in transport workers in Lima 719

I NT R O DUC C I N: El lapso de tiempo entre los sntomas

y el diagnstico e inicio de tratamiento de la tuberculo-

sis (TB) pulmonar baciloscopia positiva, hace que el en-

ermo en ambientes llenos y completos contagie a otras

personas, como ocurre en los medios de transporte haci-

nados, poniendo en riesgo a otros usuarios y traba-

jadores del transporte.

O B JE T I VO S : Estimar las tasas de incidencia de enermos

con TB, en la microred de salud en estudio, as como el

peso del sector transporte entre los enermos con TB y

TB multidrogoresistentes (TB-MDR).

DI S E O : Se revisaron de orma exhaustiva las historias

clnicas de pacientes en tratamiento desde el 1 enero del

2007 al 30 junio del 2008. A partir de ah se estimaron

las tasas crudas de TB y se estandarizaron por mtodo

indirecto segn ciras ofciales del pas. De la misma

orma, se estudi la asociacin entre pertenecer al sector

transporte en los pacientes con TB y con TB-MDR.

RESULTADOS: La razn de tasas de incidencia estan-

darizadas representan para los trabajadores entre 2,7 y

4,5 veces superiores a las del total de hombres en edad

laboral y la poblacin estudiada de la microrred. La

asociacin entre los enermos con TB y tener como ocu-

pacin el transporte pblico representan una OR de 3,06

(IC95% 2,24,2) y entre el grupo de enermoscon TB-MDR una OR de 3,14 (IC95% 1,19,1).

C O NC L US I O NE S : Los resultados encontrados muestran

uerte evidencia del uso del transporte pblico inormal

es un actor de riesgo real de ineccin de la TB y un

riesgo ocupacional en los pases con caractersticas simi-

lares en el Per.

R E S U M E N