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Page 1: Tuberculosis - WHO · 2. Tools for the study of gender and TB 8 –Ethnography and cultural epidemiology 8 –A framework for the study of gender and TB 9 3. Occurrence and basic

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Page 2: Tuberculosis - WHO · 2. Tools for the study of gender and TB 8 –Ethnography and cultural epidemiology 8 –A framework for the study of gender and TB 9 3. Occurrence and basic

G e n d e rin Tuberculosis

R e s e a r c h

Department of Gender, Women and HealthFamily and Community Health

Page 3: Tuberculosis - WHO · 2. Tools for the study of gender and TB 8 –Ethnography and cultural epidemiology 8 –A framework for the study of gender and TB 9 3. Occurrence and basic

© World Health Organization 2005

All rights reserved. Publications of the World Health Organization can be obtained fromWHO Press, World Health Organization, 20 Avenue Appia, 1211 Geneva 27, Switzerland(tel: +41 22 791 2476; fax: +41 22 791 4857; email: [email protected]). Requestsfor permission to reproduce or translate WHO publications - whether for sale or for non-commercial distribution - should be addressed to WHO Press, at the above address(fax: +41 22 791 4806; email: [email protected]).

The designations employed and the presentation of the material in this publication donot imply the expression of any opinion whatsoever on the part of the World HealthOrganization concerning the legal status of any country, territory, city or area or of itsauthorities, or concerning the delimitation of its frontiers or boundaries. Dotted lineson maps represent approximate border lines for which there may not yet be fullagreement.

The mention of specific companies or of certain manufacturers' products does notimply that they are endorsed or recommended by the World Health Organization inpreference to others of a similar nature that are not mentioned. Errors and omissionsexcepted, the names of proprietary products are distinguished by initial capital letters.

All reasonable precautions have been taken by WHO to verify the information con-tained in this publication. However, the published material is being distributed with-out warranty of any kind, either express or implied. The responsibility for the inter-pretation and use of the material lies with the reader. In no event shall the WorldHealth Organization be liable for damages arising from its use.

The named authors alone are responsible for the views expressed in this publication.

Printed in Italy

Gender in tuberculosis research

WHO Library Cataloguing-in-Publication Data

Gender in tuberculosis research / by Daryl Somma ... [et al.].

(Gender and health research series)

1. Tuberculosis, Pulmonary - epidemiology 2. Tuberculosis, Pulmonary - ethnology 3. Treatment outcome 4. Health services accessibility 5. Gender identity 6.Sex factors 7. Research I.Somma, Daryl. II.Series.

ISBN 92 4 159251 6 (NLM classification: W 84.3)ISSN 1813-2812

ii

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Acknowledgements 1Preface 2Abstract 3List of abbreviations 4

1. Introduction 52. Tools for the study of gender and TB 8

–Ethnography and cultural epidemiology 8–A framework for the study of gender and TB 9

3. Occurrence and basic epidemiology of TB 114. Help-seeking and access to health services 165. Diagnosis and initiating treatment 216. Treatment adherence 247. Treatment outcome 278. A multicountry study of gender and TB 289. Gender in health policy for TB control 3110. Conclusion 3511. References 37

Contents

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Acknowledgments

This document was prepared for theWHO Gender and Health ResearchSeries by Daryl Somma, MPH;Christian Auer, PhD; AbdallahAbouihia, MSc; and Mitchell G. Weiss,MD, PhD, Department of Public Healthand Epidemiology, Swiss TropicalInstitute, Basel, Switzerland. Theauthors would like to express theirthanks to the following individualswho provided valuable input to thesection on cultural epidemiology: MRChowdhury and F Karim, BRAC,Dhaka, Bangladesh; S Jawahar andS Ganapathy, Tuberculosis ResearchCentre, Chennai, India; J Kemp,I Makwiza and L Sanudi, The Equi-TBKnowledge Programme, Lilongwe,Malawi; and E Jaramillo and N Arias,Centro Internacional de Entrenamientoe Investigaciones Médicas, Cali,Colombia.

The Gender and Health ResearchSeries was developed by theDepartment of Gender, Women andHealth (GWH), under the supervisionof Dr Claudia García-Moreno and withsupport from Dr Salma Galal.

GWH gratefully acknowledges thevaluable comments received from:Anna Thorson, School of Public Healthin Gothenburg University, Sweden andMukund Uplekar, StopTB Partnership,and would like to thank Ann Morganfor copy-editing this series.

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The WHO Gender and HealthResearch Series has been developedby the Department of Gender, Womenand Health (GWH), with assistancefrom other WHO departments, inorder to address some of the mainissues involved in integrating genderconsiderations into health research.This publication on Gender inTuberculosis Research constitutesone of the booklets in this series.

Sex and gender are both importantdeterminants of health. Biological sexand socially-constructed gender inter-act to produce differential risks andvulnerability to ill health, and differ-ences in health-seeking behaviour andhealth outcomes for women and men.Despite widespread recognition ofthese differences, health research hashitherto, more often than not, failedto address both sex and gender ade-quately.

In applied health research, includ-ing the social sciences, the problemhas traditionally been viewed as oneof rendering and interpreting sex dif-ferentials in data analysis and explor-ing the implications for policies andprogrammes. However, examining thegender dimensions of a health issueinvolves much more than this; itrequires unravelling how gender rolesand norms, differences in access toresources and power, and gender-based discrimination influence maleand female health and well-being.

Integrating gender considerationsin health research contributes to bet-ter science and more focused

research, and, consequently, to moreeffective and efficient health policiesand programmes. With these ambi-tions in mind, the objectives of thegender and research series are to:

raise awareness of the need to integrate gender in healthresearch;provide practical guidance onhow to do this; andidentify policies and mechanismsthat can contribute to engenderinghealth research.

The series is aimed at researchers,research coordinators, managers ofresearch institutions, and researchfunding agencies. It comprises book-lets covering both a general introduc-tion to “engendering” the researchprocess as well as topic-specificissues such as lung cancer, tuberculo-sis and mental health. The researchseries will be extended to other healthtopics in time.

Each booklet will review the partic-ular health issue from a gender per-spective, identify best practices inaddressing gender in research and thegaps in gendered research, and makerecommendations to address thosegaps.

Preface

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Research clarifying the role of genderin tuberculosis control is concernedwith specific sociocultural, socioeco-nomic, and structural barriers affect-ing men and women, as distinct fromsex-based differences in the biologicalvulnerability affecting epidemiologyand pathophysiology of pulmonaryTB. This review examines variousstudies in the literature of health andsocial science research and recentinnovative studies undertaken byWHO/TDR.

The findings indicate that womenprogress from infection to active TBfaster than men do, but the reportedincidence of pulmonary TB amongwomen is nearly always lower thanfor men. It remains unclear whether

and to what extent these differencesare a true reflection of disease inci-dence or an indication of health sys-tem failures to detect and reportfemale cases. We also know that forunexplained reasons, women aremore likely than men to adhere totreatment and to complete a fullcourse. Research on gender and TBnow needs to focus on ways ofenhancing the effectiveness of casefinding for women, preventing treat-ment default, and identifying opera-tionally precise reasons for defaultamong men and women. The step-wise gender-specific barrier frame-work guiding this review helps toensure a practical focus for suchresearch.

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Abstract

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BRAC Bangladesh Rural Advancement Committee

CIDEIM Centro Internacional de Entrenamiento e InvestigacionesMédicas

DANTB Danida Assisted Revised National Tuberculosis ControlProgramme

DOTS Directly observed treatment, short course*

HIV/AIDS Human immunodeficiency virus/acquired immunodeficiencysyndrome

IEC Information, education and communication

ILO International Labour Organization

NGO Nongovernmental organization

NTPs National tuberculosis programmes

PHC Primary Health Care

TB Tuberculosis

TDR WHO Special Programme for Research and Training inTropical Diseases

UNDP United Nations Development Programme

List of abreviations

* DOTS is the internationally-recommended TB control strategy which combines five elements:political commitment, microscopy services, drug supplies, surveillance and monitoring systems,and use of highly efficacious regimes with direct observation of treatment.

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Tuberculosis (TB) remains a majorcause of infectious disease mortalityworldwide, responsible for an estimat-ed 1.6 million deaths annually or2.8% of global mortality. In 2002,nearly twice as many men died fromtuberculosis as women (1 055 000deaths or 3.5% of all deaths in menand 550 000 deaths or 2.0% of alldeaths in women). Even so, morewomen died of TB than from allmaternal conditions (1.9% of allfemale deaths) and breast cancer(1.8% of all female deaths) (WHO,2003a). Both women and men withTB are likely to be in their most pro-ductive years, that is, in the age range15-44 years old (Stop TB, 2003). Atthis age men are typically responsiblefor earning and supporting their fami-lies, whereas women as workers,mothers and caregivers usually havefamilies and children who suffer addi-tionally from their illness and death.

Notification rates of pulmonary TBfor males are nearly always higherthan that for females (Borgdorff et al.,2000). However, the true magnitudeof male excess for pulmonary TB isdifficult to quantify, partly becausecase detection in most prevalencesurveys is by sputum microscopy,which appears to be less sensitive indetecting TB in women than it is inmen. Questions and debate persistabout whether the male preponder-ance for TB stems more from sex (i.e.biological) differences or more fromsociocultural or gender-based differ-ences (Thorson et al., 2000;Borgdorff & Maher, 2001; Thorson &Long, 2001). The distinction between

"sex" and "gender" as terms fordescribing differences between menand women, and role of gender as adeterminant of health status, areexplained in more detail in Box 1 (nextpage).

Rates of TB are generally highacross the countries of south-eastAsia, where TB accounts for between4.3% and 7.2% of total deaths(WHO, 2003a). Demographic ques-tions here are especially concernedwith a disproportionately high femalemortality from TB relative to otherworld regions (Sen, 2003). Persistingpatterns of social discriminationagainst women and unfulfilled socialresponsibilities of men underscorediverse and complex relationshipsbetween cultural values, social prac-tices, and gender-related health andsocial policy. Widespread stigma tar-geting people with TB, especiallywomen, further complicates the inter-actions between this disease and nor-mative gender roles in this part of theworld (Hudelson, 1996; Balasubramanianet al., 2004). Almost everywhere,however, interactions between socie-ty, culture and TB control raise impor-tant questions about the role of gen-der and discrimination in all aspects ofthe disease, from case finding to diag-nosis, treatment and eventual out-come. Public health professionals con-cerned with TB have long emphasizedthe role of poverty, living conditionsand non-specific determinants ofhealth. In 1921, Allen Krause, directorof the TB laboratories at JohnsHopkins noted:

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1. Introduction

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Sex and Gender

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Sex is the term used to distinguish men and women on the basis of their bio-logical characteristics. Gender on the other hand refers to those distinguish-ing features that are socially constructed. Gender influences the control menand women have over the determinants of their health, for example, their eco-nomic position and social status, and their access to resources. Gender con-figures both the material and symbolic positions that men and women occu-py in the social hierarchy, and shapes the experiences that condition theirlives. Gender is a powerful social determinant of health that interacts withother variables such as age, family structure, income, education and social sup-port, and with a variety of behavioural factors.

What then do we mean by gender-sensitive research and why is it consid-ered to be so important? Research that fulfils this objective includes consider-ations of gender at all levels of the research process, from commissioning andstudy design through to dissemination of the results. Moreover, sex and gen-der must be identified as key variables, in all measures, reported separatelyand the differences discussed (Doyal, 2002).

Health research that is gender sensitive is necessary because sex and gen-der rank among the key factors, alongside socioeconomic status, ethnicityand age, that determine the health of women and men. Sex and gender affectbiological vulnerability, exposure to health risks, experiences of disease anddisability, and access to medical care and public health services. Researchwhich is gender in-sensitive may result in study design which is unable to dif-ferentiate between women and men in the identification of key findings andtheir policy implications. Gender-sensitive research, on the other hand, is morelikely to lead to improved outcomes in treatment and preventative interven-tions (Doyal, 2002).

The role of gender in public health is now widely acknowledged and is acore component of many health programmes, both international and national.Sex and gender as determinants of health, and as components of a conceptu-al framework for health research, are discussed in more detail in an accompa-nying booklet in this WHO Gender and Health Research Series.

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“The solution of the tuberculosis problemis partly dependant on the removal ofother evils and inequalities which consti-tute, no doubt, a more fundamental prob-lem than does tuberculosis itself.” (quot-ed in Farmer, 1999).

Various extraordinary social stres-sors, such as war, migration, impris-onment and forced labour may alsopotentiate the spread of TB in affect-ed countries and communities, withgender-specific effects on both menand women.

This review is concerned with theinterrelated aspects of gender andcontrol of pulmonary TB, and hasbeen prepared as one of a series ofdisease-specific studies of health andgender. Following a brief overview ofthe broad categories of scientificinquiry that can be used to study gen-der and TB, the main part of the doc-ument reviews what is currentlyknown about gender influences on theoccurrence of TB, help-seeking behav-

iour, diagnosis and treatment initia-tion, treatment adherence, and dis-ease outcome (sections 3-7). For eachof these main areas of study, specificrecommendations for future researchare given. Preliminary results from therecently completed four-country studyof gender and TB, conducted underthe auspices of the WHO SpecialProgramme for Research and Trainingin Tropical Diseases (TDR), are pre-sented in a separate section (section8). By integrating the methodologiesof the social sciences, basic epidemi-ology and cultural epidemiology,these studies have provided somevaluable insights into the way thatgender shapes the experience of TB.Finally, a number of representativepolicy documents are analysed with aview to assessing what progress hasbeen achieved to date in terms ofintegrating gender into TB control pro-grammes at both the national andglobal level (section 9).

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Ethnography and cultural epidemiology

Successful TB control requires identi-fication of people with signs andsymptoms of TB, confirmation ofdiagnosis, efficacious treatment regi-mens and sustained case holding.Consequently, WHO has developed itsTB control programme, DOTS (direct-ly observed treatment, short course)well beyond the hallmark of directobservation. DOTS combines five keyelements: political commitment, diag-nosis with sputum microscopy ofsymptomatic clinic patients, standard-ized and supervised short-coursechemotherapy that includes directobservation, regular drug supply, anda standardized recording and reportingsystem for documentation of treat-ment for both individual patients andoverall programme performance.

The determinants of illness behav-iour, which ultimately determines thesuccess of a TB control programme,are, however, rooted in social and cul-tural contexts. Risky and help-seekingbehaviours are influenced not only bythe accessibility of services but alsoby personal experiences and mean-ings of illness, as well as by sociocul-tural responses. The latter may eitherencourage (e.g. by promoting theimportance of health care and treat-ment) or restrict (e.g. by instillingshame, humiliation and fear of disclo-sure among affected persons) theeffective use of health services.Social environments are a strong influ-ence on health-seeking behaviour,

adherence to treatment, and ultimate-ly, illness outcome.

Ethnographic study has proved tobe a valuable tool for identifying thesociocultural features of TB and theirimpact on TB control. Ethnographicstudy techniques provide: a) cate-gories of local experience, meaningand behaviour with reference tosymptoms and the impact of illnesson people's lives; b) ideas about thecause and appropriate ways of dealingwith illness; and c) strategies to dealwith symptoms. Local knowledge ofillness not only helps to explain theimpact of TB on individuals, familiesand communities, but also contributesto the formulation of effective controlstrategies.

Local normative differences affectthe ways that men and women withTB experience and explain their condi-tion, and what they do about it.Ethnographic studies in Vietnam, forexample, have identified several dif-ferent types of TB (Long et al.,1999a). Among women, TB was fre-quently attributed to emotional andsocial causes, such as worrying, anunhappy life, and poverty; men, onthe other hand, identified hard manu-al labour, or questionable social activ-ities (e.g. going out with friends toeat, drink and smoke) as causes ofTB. Individuals' perceptions of riskcan play a decisive role when it comesto seeking help for TB. For instance,women may be more likely to mini-mize or ignore symptoms of TB if they

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2. Tools for the study of genderand TB

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believe that men are more likely tosuffer from TB; furthermore if theyconsider themselves unlikely to be atrisk, this might discourage those withTB from seeking treatment. Similarly,health professionals may also be lessaggressive in considering and diag-nosing TB in women with respiratorysymptoms.

Local sociocultural contexts canalso influence other aspects of TB-related experience and meaning. InKenya and Pakistan, doubts aboutwhether TB can be completely curedwere commonly observed (Liefoogheet al., 1995; 1997). Notions aboutthe futility of treatment may deterpatients from seeking care, or under-mine advocacy for improvedresources and access to TB services.In Pakistani communities, social costsare especially high for individualsidentified with TB; women in particu-lar are fearful of contracting TBbecause it decreases a singlewoman's marriage prospects andincreases the married women's vul-nerability to divorce. Such stressorsdiscourage women from acknowledg-ing symptoms and seeking appropri-ate care.

Anthropological studies generallyfocus on the community as the unit ofstudy, and thus generate useful infor-mation about the practical impact ofculture and gender on TB in affectedcommunities as a whole. Variationamong residents within communitiesis more difficult to study with anthro-pological methods. The strength ofsuch methods lies in their ability tosuggest a causal web of interactionsbetween culture, gender and illness;such hypotheses require furtherresearch to test their validity.Anthropological studies also raise

questions about the relative impact oflocal experience, meaning and behav-iour. Cultural epidemiological researchaddresses the questions raised byanthropological studies and examinesthe relative role of particular ethno-graphic findings (Weiss, 2001).

A framework for the study of genderand TB

To be effective public health modelsfor TB control need to take account ofthe effects of poverty, inequity andother social, educational, political andeconomic factors that together influ-ence health and illness behaviour.Each of these factors, all of which aremediated by gender, affects variousaspects of disease control.

Uplekar and colleagues (2001)have formulated a stepwise attritionmodel for the purpose of analysingthe impact of gender on TB control(see Figure 1). Their model suggests aresearch agenda for addressing ques-tions about the role of gender at vari-ous points in the sequence of eventsfrom initial awareness of symptoms toillness outcome. Seven steps aredefined:

(1) awareness of symptoms,(2) appropriate help seeking, (3) interaction with health

services,(4) diagnosis,(5) initiation of treatment,(6) adherence to treatment,(7) positive outcome.

The model relies on a framework toidentify a series of barriers that maylead to gender disparities at each ofthe above steps and thus compromisethe effectiveness of TB control pro-grammes. In order to identify these

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barriers at each step in the course ofeffective TB control, the frameworkposes questions about "self-image,status in the family and society,access to resources, manifestationand expression of symptoms and stig-ma associated with TB" (Uplekar etal., 2001). The framework recognizesthat gender not only influences thebehaviour of TB-affected persons inthe community, but also influencesprovider bias, the effectiveness ofsputum examination, and the level ofclinical suspicion required to make adiagnosis of TB. Consequently, themodel identifies specific researchneeds to determine whether and howvarious barriers affect the gender bal-ance of TB.

Although other investigators haveanalysed various aspects of gender,none has done so within such a com-prehensive framework that seeks tocover the full range of activitiesrequired for planning TB control. Forexample, Johansson and colleagues(2000), in common with several other

studies, consider gender as a majordeterminant of disease recognition,health-seeking, treatment and out-come, alongside contextual factorssuch as socioeconomic status andcultural values. The gender-specificbarrier framework outlined above,however, is particularly usefulbecause it helps researchers and poli-cy-makers to examine systematicallythe critical features of TB control.This review has been shaped to alarge extent by this framework, butconsolidates some of its elementsthat are not amenable for individualstudy. The modified gender-specificbarrier framework, on which the mainpart of this review is based, thus cov-ers the following topics:

1. Occurrence and basic epi-demiology of TB.

2. Help seeking and access to health services.

3. Diagnosis and initiating treatment.

4. Treatment adherence.5. Treatment outcome.

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(Source: Uplekar et al., 2001)

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Although an estimated one third ofthe world's population is infectedwith TB, only 5-10% of those withoutHIV/AIDS will proceed from infectionto active pulmonary TB (active casesare identified by a positive sputumsmear). A compromised immune sys-tem increases that percentage.Among the major world regions, southand south-east Asia have the largestincidence of infectious cases and themost deaths, although the highest percapita incidence rates and mortalityoccur in sub-Saharan Africa (WHO,2003a).

Sex-specific incidence and preva-lence data are the starting point forthe analysis of sex and gender differ-ences in the occurrence of any dis-ease, and TB is no exception.According to WHO data on case noti-fications of sputum-positive TB, 70%more men than women have activeTB (Diwan & Thorson, 1999; Uplekaret al., 2001). The observed maleexcess in notifications may bebecause there are fewer women in thepopulation with active TB, but it couldbe a consequence of the fact thatfewer women with TB present fortreatment, or that, among thosewomen with TB who come to a clinic,fewer are identified as smear positive.

Recently reported WHO data revealthat the male:female ratio for casenotifications of smear-positive casesin DOTS areas of the WHO regions forall ages range from 1.35:1 in Africa to2.16:1 in Europe (WHO, 2004).

Ratios for specific age groups in eachof the WHO regions are given in Table1 (page 12). Analysis of gender differ-ences is inhibited by the fact that datafor DOTS detection rates and DOTStreatment success are not disaggre-gated by sex in the annual WHOreports on global tuberculosis control.

Research findings uniformly sug-gest that prior to adolescence there islittle difference between men andwomen in terms of their TB infectionrates. From approximately age 15onwards, however, when both biolog-ical and social changes associatedwith adolescence differentiate thesexes more markedly, men begin toovertake women in their rates ofinfection. Moreover, as they growolder, men have a higher likelihood ofprogressing from infection to disease(Long, 2000). Men are typically morewidely exposed to other people withinfectious TB, as a consequence oftheir greater social interaction outsidethe home. Other behavioural differ-ences between men and women thatmay contribute to higher risk for infec-tion among men and progression frominfection to active TB from a weak-ened immune system include smok-ing, alcoholism, migration and in somecases, imprisonment.

Several studies have attributed thelower infection rates in women to lesssocial interaction outside the home,something that is characteristic ofadolescent females in many societies(Fair, Islam & Chowdhury, 1997;

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3. Occurrence and basic epidemiology of TB

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Source: WHO (2004). Global tuberculosis control: surveillance, planning, financing. WHOreport 2004. Geneva, World Health Organization (computed from data presented in Annex 2).

WHORegion

Age group (years) Total

AfricaAmericasSouth-EastAsia

EuropeEasternM e d i t e r r a n e a n

WesternPacific

0.840.840.60

0.780.92

0.78

0.941.221.33

1.341.25

1.40

1.281.391.66

1.811.51

1.78

1.731.652.39

2.971.49

2.27

1.951.842.90

4.271.46

2.54

1.871.873.08

2.971.36

2.51

2.041.583.15

1.221.40

2.48

1.351.492.03

2.161.37

2.09

Total 0.78 1.18 1.50 2.06 2.45 2.48 2.36 1.74

Table 1Male:female ratio of smear-positive TB notifications, by agegroup and WHO region

0-14 15-24 25-34 35-44 45-54 55-64 65+

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Dolin, 1998). Evidence from India, forinstance, shows that working womenwith a wider pattern of social interac-tions, particularly rural women andwomen commuting between rural andurban areas, are more vulnerable toinfection and the disease (Ogden,Rangan & Lewin, 1999). The argu-ment is not entirely satisfactory, how-ever, inasmuch as transmission pat-terns suggest that TB spreads readilyindoors, and the risk of infection ispromoted by prolonged close contact.Caring for old or sick people, tasksthat traditionally are a feature offemale gender roles in many societies,would, for example, possibly increasewomen's risk of infection throughclose contact more than a man's(Diwan & Thorson, 1999).

A number of studies have shownthat the rate of progression frominfection to disease is significantlyhigher for women of reproductive agethan for men of the same age. Thereis also some evidence to suggest thatafter adolescence until age 25-30years, women with TB have a highercase:fatality ratio than men in thesame age group with TB (Connolly &Nunn, 1996; Holmes et al., 1998). Aprospective cohort study inBangladesh, for example, reportedthat women aged 10-44 years of agehad a 130% higher risk of progressingfrom infection to clinical disease thanmen in the same age group (Dolin,1998). Some questions remain aboutthe validity of these findings; morecases during child-bearing years maybe a reflection of better detectionrather than higher rates, as womenattend clinics more frequently for pre-and postnatal care, and for healthcare needs of their young children(Long, 2000).

The reasons for the higher rates ofprogression from infection to diseaseand higher mortality in women remainunclear (Dolin, 1998). Sex differencesand physiological changes occurringin pregnancy are unlikely to be theonly factors. It is possible that genderinequalities governing various risk fac-tors, such as poor nutrition, maymake women at this stage of life morevulnerable to progression from infec-tion to active pulmonary TB.Differences in treatment complianceand sociocultural barriers to help-seeking have also been proposed aspossible explanations (Dolin, 1998).Gendered differences in help-seekingbehaviour mean that women typicallydelay seeking care and hence treat-ment, thereby increasing their risk ofTB mortality (i.e. the so-called gender-specific barrier hypothesis).

Historical evidence from Europeand North America suggests that dur-ing the mid-1900s, when the preva-lence of active TB was high, womenaged between 15 and 35 years hadhigher rates of active TB than men inthe same age cohort (WHO, 2003b).These data support the theory thatthe apparent lower female incidenceof active disease globally is less areflection of biological differences invulnerability but rather a consequenceof gross undercounting of activefemale cases, perhaps because clini-cians are less attentive to diagnosingTB in women. If true, these data alsolend weight to the gender-specificbarrier hypothesis mentioned abovewhich suggests that later help-seek-ing in women means that they havemore advanced TB when they eventu-ally do present for treatment, andthus higher case-fatality rates.Accordingly, a late presentation hasbeen attributed to sociocultural per-

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ceptions of TB that influence aware-ness of the seriousness of, andresponse to, symptoms. If TB is morelikely to present in women in gender-specific patterns that socioculturalperceptions do not associate with TB,then the significance of symptoms aremore likely to be minimized, which inturn further reduces opportunities fordiagnosis (Ogden, Rangan & Lewin,1999).

Research conducted in Kenya byLiefooghe and colleagues (1997)revealed that TB patients only soughttreatment after they had additionalsymptoms beyond persistent cough.Elsewhere, many patients failed toidentify TB or even to consider thepossibility of TB from their symptoms,especially the less well educated, whowere often women (HealthScopeTanzania, 2003). This results in a ten-dency among individuals to minimizethe importance of their health prob-lems and to discount or ignore theneed for treatment. Ogden, Rangan &Lewin (1999) in their study in Indiafound that patients with TB oftenfound it difficult to differentiate symp-toms of a serious condition fromthose of milder problems, such as acommon cold. Consequently, manypatients did not present to a healthcentre or clinic for treatment untilthey experienced haemoptysis. Hoa etal. (2003) found that Vietnamese menwith prolonged cough had betterknowledge of TB symptoms than didwomen, and that recognition of symp-toms they associated with TB corre-lated with seeking hospital care.

Research has demonstrated thatmen and women do in fact experienceand interpret symptoms of TB differ-ently. According to a study carriedout in Vietnam by Long, Diwan &

Winkvist (2002), women with TBreport cough, sputum expectorationand haemoptysis less frequently thando men. If women present to healthcentres without these characteristicsymptoms, clinicians may not consid-er TB as a diagnosis. Health-careproviders need to be aware of thepossibility that some female TBpatients may present with symptomsthat are atypical for men with TB. It isimportant to consider gender-specificillness experience and reportingstyles, and to recognize that such dif-ferences may vary between settingsand cultures.

Pandemic HIV infection and AIDSfurther complicate TB epidemiologyand control. TB is the most significantand life-threatening opportunisticinfection for HIV. In India, Myanmar,Nepal and Thailand between 56% and80% of people with AIDS also haveTB (WHO, 2003b); men have a highercoinfection rate than women. The sit-uation is different, however, in sub-Saharan Africa, where women havehigher rates of TB coinfection withHIV than men (WHO, 2003b).

The social response to TB may beaffected by regional patterns ofHIV/AIDS comorbidity. Several stud-ies have shown that in areas whereHIV prevalence is high, and wherepeople are aware of frequent coinfec-tions and the shared symptoms of HIVand TB (e.g. wasting), the stigma tar-geting people with TB is often greaterbecause they are assumed to haveHIV/AIDS also. Consequently, in aneffort to avoid the stigma of HIVinfection, patients may be deterredfrom seeking health care for their TB(HealthScope Tanzania, 2003). Aswomen tend to be more vulnerable tothe impact of social stigma, this can

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represent an additional gender-relatedbarrier to women's access to healthservices, diagnosis and timely treat-ment.

In some parts of the world, destabil-isation and stress arising from national,social and economic transitions haveimpacted adversely on TB e p i d e m i o l o-gy and control. For instance, in theRussian Federation, the male:femaleratio of smear-positive TB casesu n d e r DOTS is 3.78, which compareswith an average for the whole of theWHO European Region of 2.16 (WHO,

2004). In the former Soviet republics,the resurgence in pulmonary TB duringthe past decade has been largely attrib-uted to the fragmentation of healthservices and to socioeconomicupheavals. Social stressors associatedwith the transition have contributed tohigher levels of unemployment, migra-tion and alcoholism, and a decline in liv-ing standards. Such factors and others(e.g. high rates of incarceration) havefuelled the current TB and multidrug-resistant TB epidemic, particularlyamong Russian men (Coker, 2001;Shilova, 2001).

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Recommendations for future research:epidemiology of TB

Greater programme monitoring and more focussed studies are neededto compare male and female rates of TB, and thereby to clarify themagnitude of differences in relation to both biological and sociocultu-ral determinants. Such research needs to consider sociocultural differences, patterns of other disease morbidity and local TB control programme strategies.

The study of the progression from infection to disease should not belimited to reproductive health issues; both biological factors and thegendered aspects of men's and women's lives that contribute to socialstress and support should also be considered.

Recognizing the importance of TB as an opportunistic infection forHIV/AIDS, research is needed to clarify the distinctive gender-basedvulnerabilities of men and women with reference to particular riskfactors and the social dynamics of coinfection with this disease.

Efforts to destigmatize both HIV/AIDS and TB should identify thedisease-specific, culture-specific and gender-specific basis of socialdisqualification with reference to asymptomatic HIV infection, symptomatic AIDS and pulmonary TB, clarifying the particular waysthat each may lead to correctable misperceptions of risks andunwarranted social exclusion.

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Many of the sociocultural and socioe-conomic factors that influence detec-tion rates of TB also affect help-seek-ing behaviour in both men andwomen. Some studies support thepremise that the relatively lower num-ber of female cases of active TB maybe a consequence of barriers to help-seeking affecting women more thanthey do men. In Nepal, for example,Cassels and colleagues (1982) report-ed that among those who presentedto health centres voluntarily, only28% of TB cases were female.However, this percentage rose to46% among those detected throughactive case finding. Harper, Fryatt &White (1996) also demonstrated thatactive as opposed to passive casefinding in Nepal identified more femaleTB patients. These findings indicatethat Nepalese women with TB areundercounted in clinic-based data.The undercounting is likely to be aresult of a combination of factorsincluding social barriers (e.g. TB-relat-ed stigma), women's immobility, eco-nomic dependence on husbands orfamily, and lack of education andawareness of the significance of TBsymptoms.

In a recent population-based studyfrom Vietnam that screened house-hold residents for TB, Thorson et al.(2004) showed that prevalence ofsmear-positive pulmonary TB wasslightly higher among women thanmen (male:female ratio, 1:1.22). Thisis in contrast to TB programme data,which report a 2:1 ratio of male

cases. On the other hand, in TamilNadu, India, Balasubramanian and col-leagues (2004) reported communityprevalence rates of smear-positive TBthat were higher for men than women(male:female ratio, 6.5:1); the maleexcess was reduced among TB clinicpatients (male:female ratio, 2.7:1).The findings of this study imply thatwomen with TB are more likely toaccess clinical services of primaryhealth-care institutions than are men.

Several studies have identified anumber of reasons for delayed help-seeking that are common to both menand women. These include:

distrust or a lack of confidence ingovernment health facilities combined with the inconvenienceand high cost of accessing such services (owing to distance from,and cost of travel to the clinic,and time lost from work);

social stigma and reluctance todisclose their condition to others;

a failure to attribute symptoms toTB or to acknowledge theseriousness of symptoms andthe need for treatment (Godfrey-Faussett et al., 2002).

Although women in the aboveTamil Nadu study faced greater stig-ma and other barriers to accessinghealth services, they were in factmore likely than men to do so.Balasubramanian and colleagues

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4. Help seeking and access tohealth services

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(2004) attribute this to the fact thatwomen are better able to attend clin-ics during opening hours, and becausethey are more likely to visit healthcentres for immunizations and foradvice regarding health problems oftheir children.

In other parts of the world, womentend to be more likely than men toignore the first signs and symptomsof TB and thus delay seeking treat-ment. In the United Republic ofTanzania, the average delay beforeseeking care at a public TB facility is8 weeks among female patients but 6weeks for male patients (HealthScopeTanzania, 2003). A woman's role asthe primary family caregiver, coupledwith a lack of financial control withinthe household, typically means that awoman places the needs of her chil-dren and other family members aboveher own, thus delaying help seekingfor her own health problems, orreserving scarce resources for thecare of other family members instead.Some women may never seek care.The same is true for men who are theprimary breadwinners in the house-hold; for them seeking timely caremay be difficult or impossible, andadhering to treatment in a DOTS pro-gramme may impose the risk of losingwages or becoming unemployed.

Several lines of evidence indicatethat stigma plays a greater role inshaping women's experience of ill-ness and help-seeking behaviour thanmen's. Being largely dependent ontheir husbands or families, women'sconcerns about the social impact ofTB may include realistic fears of isola-tion, rejection from their family house-holds and even divorce. Various fac-tors are responsible for such con-cerns, in particular, misconceptions

about the risk and spread of TB.Godfrey-Faussett and coworkers(2002) reported that among a sampleof Zambian men and women, 79%declared that they would not like touse the same eating utensils as a TB-positive relative who was currentlyundergoing treatment, 60% wouldnot like to marry someone who previ-ously had TB, and 49% had wouldrefuse to sleep in the same bed as aspouse in treatment for TB. Generallyspeaking, women are more frequentlytargets for such biases than men.According to a study by Johansson etal. (2000), women in Vietnam fearstigma more than men, so much sothat they would often opt to isolatethemselves as protection from stigma-tizing interactions. Men, on the otherhand, were more likely to be con-cerned with the economic burden ofTB and its impact on their ability towork and earning potential. In sum, itappears that both men and womenmay deny TB symptoms for fear ofTB-related stigma, but for differentreasons.

Interestingly, when TB patients doseek care, many do not go directly topublic health clinics. Several studieshave found that women in particularreach clinical treatment servicesthrough a more circuitous route, pre-ferring to seek help first from tradi-tional healers or private practitioners(Johansson et al., 2000, Thorson etal., 2000; Yamasaki-Nakagawa et al.,2001; Rajeswari et al., 2002; Sudhaet al., 2003). In India, initial help-seeking from private practitioners iscommon; Rajeswari and colleagues(2002) found that 54% of patientsfirst sought care from private practi-tioners whereas only 27% went firstto government health facilities forhelp. A study carried out in rural and

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urban districts in Pune, India, revealedthat 60% of patients sought care out-side of government facilities, and thatamong those who did seek care atgovernment facilities, over two thirdsalso consulted non-allopathic healers(Uplekar & Rangan, 1996). Otherstudies have demonstrated similarpatterns of help-seeking behaviour. InNepal, Yamasaki-Nakagawa et al.(2001) reported that approximatelyhalf of all study subjects (men andwomen) first sought care from a pri-vate practitioner, and, furthermore,that more women had consulted suchproviders before they were diagnosedwith TB. Nearly all patients in thisstudy (94%) had ready access to tra-ditional healers, i.e. they were reach-able within 30 minutes. Government-run health facilities were less accessi-ble to most people in that only 50%of those surveyed said that they couldreach such services within 30 min-utes. In a rural Pune district, India, ithas been reported that many patientsmust travel 15 km or more to a healthclinic for treatment (Morankar &Weiss, 2003).

Private health care providers donot necessarily prescribe the optimaltreatment for TB, a problem that iswell documented in Mumbai (Uplekar,1995). They are also less likely todiagnose TB with sputum smears,depending rather more on less reliableX-ray techniques. As indicated above,women are more likely to consultdiverse sources or "shop" for treat-ment, even when they do not delayseeking care longer than men. In addi-tion, not only are women more likelythan men to first consult private doc-tors, but they are also more likely tomedicate themselves (Ogden, Rangan& Lewin, 1999; Thorson et al.,2000). The "shopping" for treatment

often delays diagnosis and the start ofeffective treatment. This is a problemnot only for the patients themselvesbut also for the public at large,because more people are exposed topotentially infectious persons for alonger period of time. Focus groupdiscussions in Vietnam have suggest-ed that although men typically neglecthealth seeking for TB until symptomsbecome severe, they are then morelikely to seek care at a governmenthospital (Thorson & Diwan, 2001).

Somewhat paradoxically, povertymay compel people with TB to seekcare in the private sector instead of atDOTS programme clinics. AlthoughTB medicines in the public sector areprovided without charge, hidden costs(such as the cost of travel) may putthese services beyond the reach ofmany (Johansson et al., 2000). InNepal, women first sought care fromprivate practitioners, even when theywere aware that free treatment wasavailable at the government healthclinics, largely because householdresponsibilities discouraged themfrom travelling the longer distances togovernment clinics (Yamasaki-Nakagawa et al., 2001). Some nation-al guidelines require patients to stay inhospital for the first two months oftreatment, which can impose a seri-ous economic burden on both patientsand their families if they cannot workduring that period (Johansson et al.,2000).

In addition to their proximity, otherfactors may contribute to the appealof private practitioners. Local privatedoctors and traditional healers areoften well known and trusted, andperceived as more responsive topatients' needs. Patient-centred serv-ices, convenient hours and advice

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Recommendations for research: access to treatment

More research is needed on gender-specific barriers to health care, inparticular those relating to symptomatology, lifestyle and social roles.Findings should be used to guide information, education and communication (IEC) interventions that are capable of surmountingpatient-specific and health-system barriers to appropriate help-seeking for TB.

The utility of active case finding should be investigated to complementthe passive case finding that typifies most DOTS programmes, so thatsuch data may quantify more accurately the true magnitude of thetreatment gap.

As poor women tend to prioritize the needs of other family membersover their own, especially their children's, the feasibility and useful-ness of integrating TB diagnostic services with maternal and child health care, Integrated Management of Childhood Illnesses services, and/or Safe Motherhood initiatives should be explored.

The feasibility and possible benefits of restructuring clinic operations (e.g. adjusting the opening hours) should be investigated. The impact of minimizing inconvenience for patients with other ongoing responsibilities should form part of such investigations.

The impact of reducing the emotional burden and of improving clinicattendance of patients by enhancing social support skills and prioritiesfor community advocacy among health-care personnel, in a manner sensitive to identified gender-specific patient needs, should bestudied.

In connection with widely-recognized priorities for improving thequality of TB care, the value of including a gender component in casemanagement training for the distinctive contexts of both public healthservices and private practice should be explored.

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that goes beyond antibiotics (e.g.counselling on lifestyle and diet)offered by private practitioners arelikely to be highly valued by patients(Ogden, Rangan & Lewin, 1999).

Sensitivity to social concerns and theemotional impact of TB on womenmay also determine whether or notparticular providers are acceptable(Uplekar et al., 1999).

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It is useful to distinguish "patientdelay", a term used to refer to thetime from onset of symptoms to firstcontact with a health-care provider,from "provider delay", which refers tothe time from first contact with ahealth-care provider to diagnosis.Several studies have shown that evenin settings where more women thanmen present for care, they experiencelonger provider delays (Long et al.,1999b; Needham et al., 2001). InVietnam, according to a study carriedout by Long and colleagues (1999b)provider delay averaged 3.8 weeksfor men but 5.4 weeks for women. Inan attempt to determine the reasonsfor this, Thorson and Johansson(2004) analysed physicians' percep-tions of the longer provider delay forfemale TB patients. Among the rea-sons given, physician respondentsmentioned the behaviour of femalepatients, explaining that even after aconsultation requesting sputum fordiagnostic testing, female patientsoften returned home for approvalfrom their family and neighboursbefore providing a sputum sample.Men, on the other hand, were morelikely to demand a comprehensivediagnostic evaluation from their doc-tors (Thorson & Johansson, 2004).Delayed diagnosis compromises thehealth of women patients, and it alsopotentiates the spread of infection.

An earlier population-based studyin Vietnam found that sputum testingwas prescribed for men with symp-toms of prolonged cough significantlymore often than it was for women

(Thorson et al., 2000). The WHO nowrecommends that all patients whopresent at health centres with a pro-longed cough (i.e. of more than threeweeks duration) should be tested forpulmonary TB through direct micro-scopic examination of sputum.However, some evidence suggeststhat such screening procedures maybe less sensitive for detecting TB infemale patients than in men (WHO,2002). Low sputum positivity amongwomen with TB may result fromwomen's inability to produce sputumof the required quantity and qualityfor testing. False negative results arethus more common in women than inmen. It is therefore critical thathealth-care providers recognize thatwomen with TB are more likely topresent for treatment without norma-tive symptoms and without positivemicroscopy (WHO, 2002).

Women may still experience longerdiagnostic delays even when theypresent with typical symptoms. InVietnam, Thorson et al. (2000)reported that in settings where theprevalence of prolonged cough is sim-ilar for men and women (1.5% formen, 1.3% for women), women wereless frequently tested by sputumsmear microscopy than men (36% ofmen versus 14% of women in studysample). Observations in Bangladesh(Begum et al., 2001) and India(Uplekar et al., 1999) also indicatethat fewer women undergo sputummicroscopy when they seek treat-ment for comparable respiratorysymptoms. Whereas two out of every

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5. Diagnosis and initiating treatment

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three men with chest symptoms weretested for TB in a clinic in Gujarat,India, only one out of every threewomen with similar symptoms under-went sputum examination (Uplekar etal., 1999).

Several studies have explored thepossible reasons for the observed dif-ferences in speed and probability ofdiagnosis. One possible explanationoffered is that women may be tooembarrassed or ashamed to produce asputum sample at the health centrebecause it is socially discomforting forthem to cough vociferously in public(Uplekar et al., 1999; Begum et al.,2001; DANTB, 2002). Alternatively,some women may be physicallyunable to produce quality sputum(Murthy et al., 2000). In order toovercome such physiological limita-tions, Murthy and colleagues (2000)used a bronchodilator, oral salbuta-mol, to facilitate sputum productionfor clinic patients; patients who haddifficulty producing sputum formicroscopy were given a seconddose. Use of oral salbutamol wasfound to increase the rate of positivediagnostic testing for TB overall (ofthe 636 identified sputum-positivecases, 206 required salbutamol). Inthe sample of 2 099 patients who

presented with chest symptomsroughly equal numbers of men andwomen tested positive for TB. Theenhanced diagnostic sensitivity wasmost notable for women, whose ratesof positivity nearly doubled.Experience elsewhere, reported by theTuberculosis Research Centre (2003)in Chennai, found that use of thebronchodilator failed to improve diag-nostic sensitivity.

There are a range of factors, bothgeneral and gender-specific, that actto delay the start of treatment evenafter a correct diagnosis for TB; theseinclude insufficiently staffed and poor-ly supplied clinics, difficulty in reach-ing a clinic due to high transportcosts, and competing responsibilitiesand social obligations. The latter arelikely to be a particular problem forwomen with TB; in some settings itmay be difficult for them to get to theclinic to receive their medicines. Inaddition, health-care providers maydeny proper treatment to certainpatients (Singh et al., 2002). Datafrom two DOTS clinics in New Delhi,India, revealed that more than half ofthe patients were denied DOTS thera-py, the majority of whom were verypoor and/or socially marginalized(Singh et al., 2002).

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Recommendations for research:diagnosis and treatment

There is a continued need to study clinical presentations of symptoms, patterns of illness experience and the perceived causes of symptoms in order to distinguish gender-specific from atypical presentationsof TB.

Further research is also needed to determine the reasons for provider delay in diagnosis, especially in the case of women, with a view toimproving the diagnosis of TB generally and minimizing the genderdifferentials in diagnosis through training and supervision of health-care personnel.

Further study of the efficacy of bronchodilators, such as oralsalbutamol, for improving the quality of sputum for microscopyis needed. Such innovations for enhancing the sensitivity of diagnosisrequire further consideration and study to ensure the effectiveness ofsputum examination in the context of DOTS programmes. The impactof structural adjustments in the organization of clinic operations and behaviour adjustments in patient provider interactions should alsobe studied.

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Treatment adherence is a criticaldeterminant of successful TB control;poor adherence may result in bothtreatment failure and development ofresistance to TB medicines. Analysisof gender differentials has indicatedthat women who are diagnosed andbegin treatment for TB are more likelyto adhere to treatment for a fullcourse than are men (Chan-Yeung etal., 2002). They are also more likelyto have a positive treatment outcome(Bernatas et al., 2003). Male:femaledifferences in treatment adherenceare thought to be a reflection of thecommitment of the subset of tena-cious women who overcome barriersto seeking health care and receive adiagnosis. Implicitly referring to a bar-rier model, Uplekar et al. (1999) havesuggested that the antagonistic socio-cultural and socioeconomic barrierswomen face prior to treatment act tofilter out those who would potentiallydefault from treatment. However, thehigher utilization of clinics by womenin some settings counters the argumentthat greater motivation arises fromovercoming barriers (Balasubramanianet al., 2004). Alternatively then, onemight ask whether the greater vulner-ability of women to stigma may moti-vate those with confidence in thevalue of treatment to stick with it,and in so doing remove the target oftheir stigma.

Although stigma might sometimesact as a motivator, it often causesproblems for treatment adherence.Women's sensitivity to social stigma,in particular, has given cause for con-cern in DOTS programmes, which

have become the cornerstone of TBcontrol. The policy is based on thepremise that observing patients takingtheir medicines in a health centre or athome improves treatment adherenceand outcome. Direct observation oftreatment, however, can make itmuch harder to conceal one's illnessfrom the community. Morankar andWeiss (2003) reported that for 70%of women in Maharashtra, India, con-suming medicines in the presence of ahealth-care practitioner was unac-ceptable. If they must take their med-icines under direct observation, thesewomen preferred to do so under thesupervision of a female nurse. Thesefindings support those of an earlierstudy, by Balasubramanian et al.(2000), which also indicate thatwomen are less likely to accept DOTthan men because of concerns aboutsocial stigma (61% compared with76%, P = 0.06), and that failure toreceive DOT accounted for most ofthe treatment failures. The authorswent on to suggest that, as an alter-native, other persons, such as trainedmidwives, community volunteers,shopkeepers, members of nongovern-mental organizations (NGOs), religiousleaders, students, cured patients andfamily members, might be able to pro-vide DOT more effectively outsideclinic settings.

Whereas stigma is typically citedby women as one of the primary rea-sons for their treatment dropout, nar-rative accounts of men are more like-ly to emphasize economic concerns asthe cause of treatment dropout (e.g.loss of wages from missed work).

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According to the results of a study inMumbai, India, women who droppedout of treatment did so because ofhousehold responsibilities, andbecause they wished to keep theircondition secret (Nair et al., 1997).Among the primary reasons given fordropping out of treatment in Vietnam,men listed a lack of understanding ofthe importance of sustained treatmentand concern about the adverse eco-nomic impact of TB care and treat-ment on their household finances(Johansson et al., 1999). Perceivedbenefits were outweighed by thesocial and economic costs. Womencited concerns about interactions withhealth-care providers and social stig-ma as the main reasons for theirdefault.

Not all factors that influenceadherence to treatment exhibit suchpronounced gender bias; some factorsaffect both men and women equally.Getahun and Aragaw (2001) identi-fied clinical improvement as the mostcommon reason for treatment discon-tinuation in their community-basedstudy in Ethiopia, followed by the dis-tance of the treatment facility. Herefamily and social supports were foundto be a critical element in promotingtreatment adherence.

Although concern about the eco-nomic impact of absence from work isa factor frequently emphasized formen, experience has shown thatstrategies to overcome this particularbarrier may offer effective options forimproving treatment adherence inboth men and women. An examplefrom South Africa has demonstratedbusinesses, as well as workers, canbenefit from the provision of health-care services in the workplace. Thecompany, Anglo Gold, estimated that

it was losing US$ 410 per year per TBpatient in lost shifts. By introducing acomprehensive TB control and pre-vention programme, it not only savedUS$ 105 per employee, but alsoreduced the occurrence of active TBamong HIV-positive workers(WHO/ILO, 2003). In Bangladesh,Youngone Industries, the largestemployer in the high-prevalenceChittagong Export Processing Zone,developed a comprehensive TB pro-gramme that eliminated the TB treat-ment default among its predominantlyfemale workforce (WHO/ILO, 2003).This programme, which was devel-oped as a component of a broaderDOTS strategy in the national TB pro-gramme, protected employees byensuring they could not be dismissedbecause of a diagnosis of TB, offeredfree treatment and provided a com-mitment that patients could return towork as soon as their sputum testednegative for TB. In addition to on-sitelaboratory facilities, the programmeprovided educational and counsellingservices that addressed a broad rangeof issues, from hygiene to stigma.Given that recent estimates put thecost of TB at around US$ 12 billionannually in terms of lost labour pro-ductivity alone (WHO/ILO, 2003), thebenefits of such policies are potential-ly very great indeed.

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Recommendations for research:treatment adherence

Gender-specific impediments to treatment adherence, which appear to have a greater effect on men, require more in-depth study.Hypotheses based on known gender differences, such as the premisethat enhanced social vulnerability and greater stigma affecting womenmay lead those who come for treatment to pursue it more diligently, should be tested.

Given that patients in some settings avoid clinics for fear of disclosure of their condition, future research should investigate the impact onadherence of directly observed treatment performed outside clinicsettings, using family members, private practitioners, midwives, curedpatients or other community members. Setting-specific comparisons of clinic-based and community-based DOTS are also required.

To respond to the problems for men of clinic attendance andtreatment adherence, the value of TB diagnostic and treatmentservices in the workplace should be analysed in greater detail. Thereis a need to consider both case identification and treatment outcomesof patients with reference to added convenience and also employerresponses in terms of the potential economic benefits of lessabsenteeism, greater productivity and reduced travel expenses.

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As women are more likely than mento adhere to treatment, one wouldexpect women to have more positivetreatment outcomes. The gender-spe-cific barrier hypothesis also suggeststhat women should outperform men inadherence and illness outcome.Research in both Africa and Asia con-firms the anticipated links betweenadherence and outcome. For example,among study participants in threeurban and rural districts of Tanzania(Hai, Morogoro and Kinondoni), 5% ofwomen and 6% of men defaultedfrom treatment, and following treat-ment, 67% of women, compared with63% of men, were free of TB(P < 0.05) (HealthScope Tanzania,2003). In Thailand, multivariate analy-sis revealed that, for the same courseof treatment, being male was a strongrisk factor for unsuccessful treatmentoutcome, even after allowing for o t h e r

c onfounding variables (Pungrassamiet al., 2002).

Adherence to treatment over thefirst three months has been shown tobe an especially critical determinant ofcure. The decision of patients to com-plete the full course of treatmentinvolves an accommodation of per-sonal perceptions of health status andrisk, which are in turn influenced bycultural and personal meanings ofsickness and cure. This accommoda-tion is a kind of subjective cost-bene-fit analysis in which the personal,social and financial burdens areweighed against the expectations of acure (Liefooghe et al., 1995). Identifyingthe critical determinants of analysesof this type for women and men willhelp to guide the development ofmore effective programmes for TBcontrol.

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7. Treatment outcome

Recommendations for research: disease outcome

More research is needed to unravel the mix of factors that interact toproduce the more favourable treatment outcomes for women. Research of this nature needs to consider the determinants suggested by gender-specific motivations and the barrier hypothesis.

Gender-specific determinants of poor treatment outcome need to be identified and their mode of action understood in order to developappropriate policies to counter their effects.

The study of gender effects should begin but not end with comparisons of men and women. They should explain gender differences by studying interactions that clarify gender-specific effects of explanatory variables on TB-related stigma, provider and patient delay, and treatment outcome.

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Recently completed field research in a four-country collaborative studyof gender and TB, supported by the United Nations DevelopmentP r o g r a m m e/World Bank/WHO SpecialProgramme for Research and Trainingin Tropical Diseases (TDR), has exam-ined many of the questions posed bythe gender-specific barrier frameworkthat guides the present review.Participating research institutionsinclude the Equi-TB KnowledgeProgramme in Lilongwe, Malawi; theTuberculosis Research Centre inChennai, India; BRAC (formerly theBangladesh Rural AdvancementCommittee) based in Dakha,Bangladesh, and now active through-out the country; and CentroInternacional de Entrenamiento eInvestigaciones Médicas (CIDEIM) inCali, Colombia. The Bangladesh sitesare exclusively rural, the Malawi sitesboth rural and urban, and the remain-ing sites exclusively urban.

As part of the TDR study, the TB-related experience, meaning, andbehaviour and self-perceived stigma inmen and women were compared.Locally appropriate variables for studywere identified from experience ateach of the sites. Indicators of stigmawere analysed individually and collec-tively (i.e. as an index) in order toquantify the magnitude of stigmaaffecting patients and to identify itsmain determinants. The analysis ofthe individual features of stigma con-sidered their frequency and the narra-

tive context that explained the natureof social concerns about TB.Specifying the prominence and distri-bution of variables facilitated genderstudy and comparisons within sitesand across sites, and examination ofthe practical implications of sociocul-tural aspects of TB and the socialresponses to it. It also indicated howto identify sociocultural determinantsof patient delay and provider delay.

Broadly speaking, the resultsobtained from these studies are con-sistent with features of the gender-specific profiles of TB reported in the lit-erature reviewed above. Nevertheless,the study also revealed some interest-ing differences between the studylocations. Blood in sputum wasreported more frequently by men thanwomen in India, and it was identifiedas the most troubling symptom bymen, but not women, in both India(12.1%) and Bangladesh (9.6%). Itwas not, however, a distinctivelymale concern in either Malawi orColombia. Concerns about the impactof TB on earnings and income weremale issues in the two south Asiansites, and also in Malawi. One or moreof a variety of vague, non-specificsomatic symptoms predominated inwomen at all sites, including fever,chest pain, breathlessness, weaknessand other physical symptoms.

Of the perceived causes of TB,abused substances – either smoking,alcohol or other drugs – dominated the

8. A multi-country study of genderand TB

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male responses at most sites.Bangladesh was a notable exception,where only 1 of 100 respondentsidentified alcohol as a cause of theirTB. In Colombia, alcohol, drugs andsmoking were all mentioned frequent-ly by the vast majority of respon-dents, but only smoking was reportedmore frequently by men as a cause(men, 94.0%; women, 81.3%;P < 0.01). Only in Malawi, where TBis most closely linked with HIV/AIDS,did more women emphasize sexualcontact as the cause of their TB thanmen (women, 28.0%; men, 4.0%;P < 0.01). Narrative accounts indi-cated the particular nature ofwomen's concerns in settings whereHIV/AIDS is rampant. "Maybe becausemy husband…he is a driver, maybe wherehe was going he was with other women."A vulnerability to the effects of theirhusbands' behaviour was a pervasiveconcern for many women in Malawi.

The men who identified sexualcontact as the cause of their TB werenot only fewer in number in Malawi,but their accounts were also qualita-tively different, focussing on theiractive, rather than passive, role andpower in the relationship. Men typical-ly focussed on the TB itself, ratherthan on their vulnerability to the

effects of their spouse's behaviour.For example, a man who identifiedsexual contact as a perceived causeexplained, "I suspect that my former girl-friend passed the disease to me. I wantedto marry that lady … but I did not knowthat she had TB. When I knew she had TB,I changed my mind and decided not tomarry her. A few months later, I begancoughing."

The multi-country studies alsosought to examine the effects of gen-der and other cultural epidemiologicalvariables on stigma. Multivariate mod-els were used to identify specificexplanatory variables for each of theoutcomes of interest at each site. Theanalysis also considered interactionsbetween each of these variables and avariable for sex (specified as womenwith reference to men as baseline), toidentify not only the overall effects ofgender, but also gender-specificeffects of each of these variables (seeBox 7, page 30). This approach to thestudy of sociocultural determinants isalso applicable to more specific analy-ses of patient delay and providerdelay (see Box 8, page 32). Furtherdetails from the cross-site analysis ofthe WHO/TDR studies in four coun-tries will be presented in a forthcom-ing TDR report.

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Stigma

Illness-related stigma refers here to social disqualification from full socialacceptance by virtue of the identification of a person with TB,ignoring other aspects of this person's identity that might otherwise motivate compassion and support. Such stigma may be socially enacted, self-perceived, or anticipated by people with a stigmatized condition. EMIC interviews, which are locally adapted instruments for cultural epidemiological study, inquired about respondents' TB-related experience and indicators of self-reported stigma. Examining thesecollectively as an index of stigma, the investigators assessed andcompared the magnitude of stigma and analysed its determinants. Narrativeaccounts in response to questions over the course of these interviews, whichwere maintained as a component of the data set, indicate the nature of stig-ma as reported by the respondent, and clarify the role of disease-specific, gen-der-specific, and site-specific features and determinants.

Findings indicated common cross-site and distinctive site-specific featuresof stigma. Particular concern about loss of social status was related to theoverall index of stigma in Bangladesh, India and Colombia. In India, however,a gender-specific effect of that variable suggested that this was less of anissue for women, compared with men. This suggests that the social exclusionarising from the disease was more likely to be a novel experience for men, asillustrated by men's narratives such as:

“I have been given a separate plate for my use and I am using a separate matto sleep by my family. Really this hurts me a lot.”

For some of these men, such a recalibration of social status reverses the hier-archies of power in the household:

“This illness has affected my relationships within the family. My sister andbrother are very nasty to me. My sister refuses to share her mat with me. Mybrother gets irritated when I cough.”

In addition to this social suffering, male responses also indicated two addition-al concerns about dependency and responsibility. Some worried that their owndependency needs within the household might not be fulfilled:

“If my wife and son know about my disease they may even feel ashamed totalk to me. I may be asked to get out of the home.”

Others burdened by a sense of responsibility spoke of their concerns about reper-cussions of the social response to their condition for the rest of the family.

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A range of TB policy documents arebriefly examined below in order togain some indication of the extent towhich public health programmes cur-rently acknowledge gender-basedissues and concerns. Particular atten-tion has been paid to policies for thecontrol of TB in the low- and middle-income countries.

Gender sensitivity is notably lack-ing in some of the most influentialdocuments of globally active NGOs,which one might expect to be moreattentive to social and cultural con-cerns. The International Union againstTuberculosis and Lung Disease, forexample, has published an importantand useful document, Management oftuberculosis: a guide for low-incomecountries (IUTLD, 2000), which isinattentive to gender. The WHO/ILOGuidelines for workplace TB controlactivities (2003) refers to women andTB in the workplace with only cursoryconsideration of gender. They doacknowledge, however, the impor-tance of extending TB services toentire families and the importance ofequal access to treatment for menand women. The AmsterdamDeclaration on Tuberculosis makes nospecific mention of gender (2000).

WHO's guidelines for nationaltuberculosis programmes (NTPs)make a number of recommendationsand include operational strategies thatacknowledge the importance ofthe social context of TB.Recommendations for national TB pol-

icy, however, have thus far beenmore concerned with the technicalaspects of TB control and less so onthe more sociocultural aspects. Theguidelines emphasize the importanceof each NTP developing a strong cen-tral unit, creating a programme manu-al, implementing a case reporting andrecording system, initiating trainingprogrammes, developing networks ofdecentralized microscopy services,incorporating DOTS treatment servic-es within the existing primary healthcare (PHC) system, assuring reliabledrug and equipment supply systems,and drafting a plan for supervision(WHO, 2003c). They also recommendthe development of IEC and socialmobilization campaigns, the involve-ment of private and voluntary health-care providers, economic analysis andfinancial planning, and ongoing opera-tional research (WHO, 2003c). Many,if not all, of these technically- andsocially-oriented priorities for policywill benefit from the inclusion of agender perspective.

With its focus on social and humanrights issues at the global level,another WHO document, Guidelinesfor social mobilization: a human rightsapproach to tuberculosis (Hannum &Larson, 2001), examines the impactof TB on various vulnerable groups,including women, children, the poor,migrants, refugees and prisoners. Thispolicy document elaborates keyaspects of gender and relevantaspects of the sociocultural contextsof women's health, including stigma,

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9. Gender in health policy for TB control

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Timely help seeking

Multivariate analyses of sociodemographic and sociocultural determinants ofdelay from first awareness of symptoms to diagnosis of TB were completedat three sites. In Bangladesh, cough and increasing age were associated witha longer delay, and social problems collectively were associated with a short-er delay. In India, female sex, a higher level of education, sexual contact as aperceived cause of TB, and prior help seeking in a healing temple were asso-ciated with a longer delay; cough, blood in sputum and concern about thecourse of illness were associated with a shorter delay. In Malawi, loss of joband wages, drug abuse as a perceived cause, and prior help seeking at anNGO clinic were associated with a longer delay.

The multivariate analysis also considered interactions between explanato-ry variables and sex (female compared with male). Findings in Bangladeshshowed that women who had never been married, married women with mar-ital problems, women reporting humoral perceived causes (heat-cold imbal-ance), and women giving prominence to social problems had longer diagnos-tic delays. In India, women who previously sought help from private doctorshad longer delays; women with more prominent physical symptoms and priorhelp from traditional or magico-religious healers had a shorter delay. InMalawi, women with more prominent concerns about the course of illness andwith prominent emotional symptoms had a longer delay; those with moreprominent physical symptoms had a shorter delay.

These findings suggest that in Bangladesh marginalized social status andthe prominence of traditional concepts to explain TB had a gender-specificeffect in prolonging time to diagnosis for women. In India, prior help seekingfrom traditional healers and temples was associated with increased delay forthe overall sample, but this was significantly less of a factor for women, pos-sibly because traditional practices among women are more normative than formen. In Malawi, more prominent physical symptoms reduced delay and promi-nent emotional symptoms increased delay for women; these findings suggestgreater sensitivity among providers to physical symptoms of TB, and they indi-cate a need to examine the role of the psychosocial impact of TB on bothpatient and provider delay.

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discrimination, access to health serv-ices and issues of abandonment.

National programmes are encour-aged to focus on practical indicatorsof programme success, including forexample, high case detection rates,high cure rates and low levels of drugresistance; less attention tends to begiven to questions about how genderand other social contexts might relateto such goals (WHO, 2003c). Someauthors have suggested that insofaras vertical programmes may discour-age intersectoral collaboration, it isdifficult to motivate attention to gen-der-related issues or to implementgender-sensitive policy within them(Ogden et al., 1999). The RevisedNational Tuberculosis ControlProgramme in India, however, illus-trates how vertical programmes inhigh-burden countries aim to movetowards a more decentralized modeland to make themselves more respon-sive to social and cultural contexts(Ministry of Health and FamilyWelfare, Government of India, 2002).

India's National Health Policy 2002focuses throughout on the health ofthe poor, and dedicates a section tothe health of women and relatedsocioeconomic and cultural issues(Ministry of Health and FamilyWelfare, Government of India, 2002).The document acknowledges theimportance of women's health as amajor determinant of the health ofentire communities. The policyendorses the need to expand the pri-mary health care infrastructure toincrease women's access to care. Thepolicy also recognizes a need toreview staffing in the public healthservice, so that it may become moreresponsive to specific needs ofwomen. The priority of high-burden

diseases explicitly refers to TB, andthe document acknowledges the needfor "separate schemes, tailor-made tothe health needs of women, children,geriatrics, tribals, and other socioeco-nomically under-served sections".

Such attention to society, cultureand gender is, however, exceptional.Most national and international TBpolicy documents give these topicsrather more perfunctory considera-tion. This largely reflects inattentionto such questions in prior research,and consequently, a lack of under-standing about how to achieve a gen-der-sensitive health policy. TheManual of the National Tuberculosisand Leprosy Programme in Tanzania(2003) provides a good illustrativeexample of the prevailing status ofgender in NTPs (Ministry of Health,United Republic of Tanzania, 2003).Sections for which consideration ofgender issues would be highly rele-vant, such as patient education,makes no reference to the specificvulnerabilities, problems, needs orstrengths of either men or women.The manual does acknowledge thespecial needs of women with refer-ence to biological sex differences,identified as "treatment in specialcases", considering guidelines totherapy for pregnant or breastfeedingwomen, and for women who take oralcontraceptives. The Manual of proce-dures which is intended to serve as aguide for the national TB programmein the Philippines makes no mentionof gender or other issues specific towomen (Department of Health, 2001).The South African T u b e r c u l o s i sControl Programme practical guide-lines (South African Department ofHealth, 2000) also neglects questionsof both gender and the particularneeds of women.

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Nor is the lack of attention to gen-der issues a matter for the low- andmiddle-income countries alone. In theUnited States of America, the NewYork City Bureau of TuberculosisControl similarly refers extensively toTB in pregnant women, HIV-positivewomen and breastfeeding women intheir clinical policies and protocols(New York City Department of Health,1999). A recommendation for coun-selling services for such women, how-ever, would clearly benefit from moreexplicit consideration of genderissues.

It is difficult to comment on thediverse approaches to gender issuesin local TB policies that exist interna-tionally. One can no doubt findextreme examples of both insensitivi-

ty and sensitivity to gender. One inno-vative approach has been adopted bythe Tuberculosis Research Centre inChennai, India, which has been work-ing with local filmmakers to producedramas and documentaries that high-light the various options for clinic andcommunity-based TB treatment.These depict in a poignant and social-ly-acceptable way the key gender-related problems and solutions. Thefilms are used to stimulate discussion,promote awareness and indicate howfamilies and communities mayrespond to TB. They show the waysin which the disease can affectwomen and men, the problems itimposes on families, and examples ofhow families and communities haveresponded.

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The epidemiology and course oftuberculosis differs for men andwomen. Women progress from infec-tion to active TB faster than men do,but the reported incidence of pul-monary TB among women is nearlyalways lower than for men. It remainsunclear whether and to what extentthese differences are a true reflectionof disease incidence, as recentresearch from India suggests, or anindication of health system failures todetect and report female cases, asgender-based barrier models of limitedaccess to health care and diagnosissuggest. TB case identification inDOTS programmes typically relies onpassive case finding, based on symp-tomatic patients presenting to healthcentres for diagnosis by sputumsmear and treatment. Clinical presen-tations of TB affecting men andwomen also differ.

TB gender research is concernednot only with clarifying differencesbetween men and women in the bio-logical vulnerability and pathophysiol-ogy of pulmonary TB; it also aims toelucidate the particular problems andsignificant sociocultural and socioeco-nomic barriers men and women facewhen seeking TB care and treatment.Although research has begun to clari-fy the point, we do not yet fullyunderstand the gender-specific symp-tomatology of TB, which must takeinto account variation across cultures.If unrecognized in the routine courseof clinical assessment, sex-specificclinical presentations of TB may inter-fere with diagnosis and timely treat-ment of women. In addition, further

research is required to better under-stand men's underutilization and time-ly access of health services for diag-nosis and treatment, and their prob-lems with adherence.

Many of the studies considered inthis review have begun to addressthese questions, and more with apractical focus on programme-specificoperations are needed. We know thatfor unexplained reasons, women aremore likely than men to adhere totreatment and to complete a fullcourse. Consequently, women whoreach treatment are also more likelythan men to be treated successfully.Research on gender and TB nowneeds to focus on ways of enhancingthe effectiveness of case finding forwomen, preventing treatment default,and identifying operationally precisereasons for default among men andwomen. The stepwise gender-specificbarrier framework guiding this reviewhelps to ensure a practical focus forsuch research. We have also indicat-ed how basic epidemiology, healthsocial sciences and cultural epidemiol-ogy have addressed these aims in afour-country collaborative study sup-ported by TDR.

Because most people with TB canbe successfully treated and cured, thechallenge for health policy-makersand health systems is especiallypoignant. Successful control of TBrelies on competent services and theavailability of effective medicines,which are accessible and attractive topeople who need them, and that clin-ical services are well managed and

10. Conclusion

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able to fulfil their obligations.Attention to issues of gender is vitalto achieve such goals generally, butespecially for TB because questions ofgender norms and inequality are cen-tral to the experience, meaning andbehaviour of people with this diseasein the low- and middle-income coun-

tries where this disease takes thegreatest toll. A commitment to thegender-sensitivity of interventions,guided both by needed research andby applying in DOTS programmeswhat we already know, will help toensure that TB control is as effectiveas it can be for everyone.

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