Social stigma towards neglected tropical diseases: a systematic review Free

Abstract

Background

People affected by neglected tropical diseases (NTDs) are frequently the target of social stigmatization. To date not much attention has been given to stigma in relation to NTDs. The objective of this review is to identify the extent of social stigma and the similarities and differences in the causes, manifestations, impact of stigma and interventions used between the NTDs.

Methods

A systematic review was conducted in Pubmed, ScienceDirect, PsycINFO and Web of Knowledge. The search encompassed 17 NTDs, including podoconiosis, but not leprosy as this NTD has recently been reviewed. However, leprosy was included in the discussion.

Results

The 52 selected articles provided evidence on stigma related to lymphatic filariasis (LF), podoconiosis, Buruli ulcer, onchocerciasis, schistosomiasis, leishmaniasis, Chagas disease, trachoma, soil-transmitted helminthiasis (STH) and human African trypanosomiasis. The similarities predominated in stigma related to the various NTDs; only minimal differences in stigma reasons and measures were found.

Conclusion

These similarities suggest that joint approaches to reduce stigmatization may be feasible. Lessons from leprosy and other stigmatized health conditions can be used to plan such joint approaches. Further research will be necessary to study the efficacy of joint interventions and to investigate stigma related to NTDs for which no evidence is available yet.

Introduction

Neglected tropical diseases

Neglected tropical diseases (NTDs) impair the lives of more than a billion people around the world and threaten the lives of millions more.¹ Although caused by different aetiological agents, NTDs are categorized as a group because of their geographical spread and their neglected status.^1,2 The categorization of the NTDs as a group intends to facilitate their control and care in a coordinated and integrated way.¹ To achieve coordinated care and control, five integrated strategies are recommended by WHO, which aim at fully controlling, preventing and possibly even eliminating several NTDs.¹

According to WHO, the group of NTDs comprises 17 disease entities, caused by either viruses: dengue/chikungunya and rabies; bacteria: Buruli ulcer, leprosy, trachoma and endemic treponematoses (e.g., yaws); protozoa: Chagas disease, human African trypanosomiasis (HAT or sleeping sickness) and leishmaniasis; or helminths: dracunculiasis (guinea-worm disease), echinococcosis, foodborne trematodiases, lymphatic filariasis (LF), onchocerciasis (river blindness), schistosomiasis, soil-transmitted helminthiasis (STH) and taeniasis/cysticercosis.^1,3 In addition to this list of 17 disease entities, podoconiosis is also highlighted by WHO as a neglected tropical condition.⁴

Stigma

People with NTDs are prone to social stigmatization and discrimination, due to the physical impairments and disfigurements that accompany some of the NTDs.⁵ Over the last half century, social stigma has become a topic of growing interest and study, particularly in the fields of public health and social health sciences.^6,7 Stigma may be defined as ‘a social process, experienced or anticipated, characterized by exclusion, rejection, blame or devaluation that results from experience, perception or reasonable anticipation of an adverse social judgment about a person or group’.⁸ As denoted by Weiss, three types of stigma can be distinguished: enacted, anticipated and internalized stigma.⁷ Enacted stigma encompasses discrimination or social exclusion ‘enacted’ by the community or experienced by the person that is affected by the stigmatized disease.^7,9 For the purpose of this review enacted stigma also encompasses the negative attitudes expressed by the community. Anticipated stigma is the perception of the individual that stigmatization is likely to occur. In other words, an anticipation of the actual, enacted stigma.^7,10 In the case of internalized stigma, the affected individual has internalized negative stereotypes or negative attitudes, may feel ashamed or guilty because of their condition and may withdraw themselves from social participation.⁷

When related to diseases, stigma causes an immense social and psychological burden, in terms of social exclusion, reduced quality of life and poor mental health.¹¹ Especially in relation to mental health it has been shown that there is a close relation to stigma in the field of NTDs,^12,13 which causes significant comorbidity and adds to the global burden of NTDs.¹⁴ In addition to these social and psychological consequences, health-related stigma can hamper the care and control of the concerned disease in areas such as health-seeking behavior, treatment uptake and adherence and political commitment to disease control.^6,7 People suffering from stigmatized diseases tend to delay their health seeking to avoid social reprimands, resulting in prolonged transmission in the case of infectious diseases. In addition, social stigma may affect the treatment uptake or adherence of patients. Poor or non-adherence may be the result of a reduced frequency and quality of the patient–provider interactions, because people suffering from a stigmatized disease tend to travel further for or even discontinue their treatment to avoid disclosure.^6,7,15,16 Furthermore, health care personnel themselves may stigmatize patients, which negatively affects health service provision and leads to a reduced access to diagnosis and treatment.¹⁷

Problem statement

Despite the enormous impact of social stigmatization and discrimination, so far only limited attention has been given to stigma in relation to NTDs.^2,17 The only exception is leprosy-related stigma, which has been widely covered.^7,18–20 Moreover, the information that is available about stigmatization and discrimination in relation to NTDs is usually focused on the stigmatization of one single NTD. Insights into the extent of NTD-related stigma in terms of how commonly a given condition is stigmatized (reflected by the quantity of published evidence) and especially the similarities and differences in stigma among the different diseases, could contribute to the reduction of stigma related to NTDs; thus, reducing the psychosocial burden and facilitating NTD control. Understanding the differences and similarities in stigma among the different NTDs will indicate what aspects favor a joint approach to stigma reduction, just as is used in the prevention and treatment of the NTDs, and what aspects require an NTD-specific focus. Hence, the research objective of this study is to elucidate the extent of social stigma related to NTDs, with a specific focus on the common features and the differences in the causes, manifestations, and impact of stigma and interventions used between the various NTDs.

Methods

Literature search

Eligibility criteria

Eligible studies to determine the extent of stigma associated with NTDs had to reflect stigma, whether enacted, anticipated or internalized, related to one or more NTDs. Included were studies published in Dutch or English language of which a full text copy was available. Only studies based on primary data were taken into account. No restrictions in publication year were applied. Studies that were not published in peer-reviewed, scientific journals, and animal studies were excluded.

Information sources

In January 2015, studies were identified by conducting a systematic search in four electronic databases: Pubmed, ScienceDirect, PsycINFO and Web of Knowledge. The search was further supplemented by scanning the reference lists of all included articles, and by an additional search in Google Scholar using the search terms ‘stigma’, ‘discrimination’ and ‘neglected tropical diseases’.

Search strategy

The systematic review was conducted in line with PRISMA guidelines.^21,22 Considering the objective of this review to qualitatively assess the evidence available on stigma related to NTDs, items of the PRISMA guideline which relate to the quantitative assessment of the evidence were not deemed relevant and therefore were not taken into account (also see PRISMA checklist in Supplementary File 1). The applied search syntax was restricted to title, keywords and abstract. Search terms used in all four databases included synonyms for the main search domain, NTDs, combined with synonyms of the main search outcome, stigma. Regarding the search syntax used for the NTD domain, synonyms for each of the 17 individual tropical diseases of the WHO NTD list were addressed, alongside synonyms for the general neglected tropical disease term itself (see Box 1 for the search syntax used in Pubmed). Leprosy was not included, because the stigma related to this NTD had been recently reviewed.^20,23 However, published evidence on leprosy-related stigma will be used for comparison in the discussion.

Study selection

During the article selection, all titles and abstracts retrieved in the electronic search were screened by the reviewer (KH) in order to remove duplicates and to identify eligible studies based on the inclusion and exclusion criteria. Reference Manager (Thomson Reuters, New York, NY, USA) was used to facilitate the removal of duplicates. Subsequently, attempts were made to retrieve the full text of all studies deemed eligible. This was followed by a screening of the available full articles by the reviewer (KH) and an additional screening of the applicability of the inclusion and exclusion criteria by both authors done independently in case of doubtful eligibility. After the independent screening a consensus meeting was held to discuss the final inclusion in the review (see Figure 1 for the flow diagram).

Data extraction and analysis

Data were extracted by the reviewer (KH). The data extraction included several variables reflecting the domain and outcome: the type of NTD reported, the type of stigma, the manifestations and consequences of the stigmatization, the reasons for stigmatization and the measures taken against stigmatization. In addition, data variables reflecting the study characteristics were added: the first author, publication year, study design, type of study, study sample characteristics and study perspective. The data were evaluated for accuracy and completeness before proceeding to the data analysis. The data analysis comprised the comparison of extracted data in order to elucidate the extent of stigma associated with NTDs, along with the cross-cutting features and the differences in stigma between the various NTDs.

Results

Search results

The flow diagram in Figure 1 shows that the systematic search identified 771 studies. Twenty-six additional studies were retrieved through the supplementary search in Google Scholar and via the reference lists. Among the identified studies, 181 duplicates were removed and 521 studies were excluded after scanning the titles and abstracts. The full text of the remaining 95 articles was assessed for eligibility, after which a further 43 studies were excluded. The remaining 52 articles were included in the systematic review.

Description of the included studies

The 52 studies incorporated in the review were published between 1988 and 2015. Several study designs were used, including cross-sectional, grounded theory, ethnographic/anthropological, survey, case study and multidisciplinary study. The majority of the included studies employed qualitative research methods; 16 studies used mixed methods and 13 studies applied quantitative research methods. The continent of Africa was the location of most of the studies (36, of which one was cross continental), while 10 studies were conducted in Asia, 6 in North/South America and 1 in Europe. The perspective chosen by the incorporated studies was mostly a combination of an individual and a community perspective. Fourteen studies reflected solely an individual view and eight studies described their results exclusively from the community perspective. Eight studies adopted a gender-specific approach in their study. In total 10 different NTDs are outlined in the reviewed articles. For a further description of the included studies see Table 1.

Stigma related to neglected tropical diseases

Lymphatic filariasis

Medium to high levels of stigma were found by the 18 studies that cover stigma related to LF (see Table 2). However, four studies concluded that, despite a certain degree of stigmatization towards LF patients, in general there is community support and acceptance of patients without severe ostracism.^24–27 Several factors are reported that either positively or negatively affect the level of stigma related to LF. For instance, Kumari et al. found that the more advanced the stage of the disease, the higher the stigma related to it,²⁸ whereas Lu et al. remarked that the localization of the disease influences the level of stigma, with affected genitals causing higher levels of stigma than affected extremities.²⁷ Also, patients with a low level of income,²⁹ female gender and young age³⁰ are reported to be more susceptible to stigmatization. Manifestations of enacted, anticipated and internalized stigma were all found in relation to LF. In terms of social consequences, reduced work and education opportunities, impediments in sexuality and relationships, and social isolation were highlighted.^13,24–40 Reported health consequences included restricted treatment-seeking behavior as a result of embarrassment and fear of exposure,^{27,29,31,33,38} reduced access to diagnosis and treatment due to disinterest of health personnel in LF,^35,37 and poor health outcomes in terms of lymphedema progression, infection and disability.^37,38 In addition, psychological consequences consist of low self-esteem, feelings of shame and embarrassment, fear and anxiety, and mental distress, including depression, decreased quality of life, engaging in victim behaviour and suicidal tendencies.^{13,24,25,27–31,33–40}

Frequently extracted reasons for stigmatization in relation to LF comprised physical appearance,^{13,24,25,27–31,33,35–39} fear of contagion,^{13,27,29,30,33,37–40} the inability to fulfil a certain gender role,^{13,24–27,31,32,34–40} and being a burden on either the family or society.^{26,27,29,33,34,36–38,40} The inability to fulfil a certain gender role is defined here as the inability to reproduce, have sexual relations and perform household chores, whereas the (financial) burden on the family and society encompasses the involved treatment costs and the missed earnings from the inability to work. Health education for patients and the community was highlighted as a way to overcome stigmatization,^{13,24,27,28,30,31,33,36,38–40} with a focus on the curability³³ and prevention,²⁷ alongside the necessity to adapt to the local cultural and educational standards²⁷ and the involvement of influential community agents.³⁰ Disease management is adopted as another method, in the shape of prevention^28,36,38 improved access to health care^{27,30–32,34} or health care with a focus on gender,³³ on faith¹³ or on the social and economic context.^29,39,40 Also personal support, by means of support groups, counseling, rehabilitation and social welfare, are mentioned as methods to overcome the consequences of stigmatization.^{13,25,28,29,33,36–40} Person et al. furthermore proposes a multi-faceted behavioral intervention targeting patients experiencing stigma, those who stigmatize and social systems that promote or fail to inhibit stigmatization.³⁷

Podoconiosis

Twelve studies reflect the stigma related to podoconiosis (see Table 3). A low level of knowledge with regard to podoconiosis,^41,42 a more advanced disease stage,^43,44 a higher than median income and longer duration of stay within an area⁴³ were reported to result in a higher level of stigma. Factors such as age, gender and level of education did not have an impact on the level of stigma.⁴⁴ Manifestations in terms of enacted stigma include spitting on patients, exclusion, avoidance, derogatory name calling and looking down on podoconiosis patients and their family.^44–49 Also anticipated stigma is reported,^43–51 with fear of insults or mistreatment and fear of disclosure, manifesting in the tendency of patients to hide themselves and their condition.^44–49 Internalized stigma manifested in feelings of shame or guilt, living in fear, suicide attempts and the perception of patients that stigmatization is normal.^44,47,48,52 Consequences related to the stigmatization of podoconiosis were social, psychological and health related in nature. The underlying reason for the stigmatization is often the belief that the disease is either genetically susceptible^{44–48,50,52} or infectious, the latter resulting in a fear of contagion.^{41,42,44,45,48,52} However, appearance,^{41–44,46,48–51} the inability to fulfil a certain societal or gender role,^{41,42,44,48,52} being a burden to the family,^44,48,52 and witchcraft or a curse from God⁵² were also identified as reasons for stigmatization. Health education,^{41,42,44–48,50,52} disease management,^{41,44–50,52} and personal support^43,44,51,52 are reported as measures to overcome the stigmatization related to podoconiosis. Health education for patients, health care providers and/or the community should focus on the etiology, the preventability and treatability of the disease^45,46,50,52 and should engage (former) patients as educators.^42,48 Moreover, the personal support should be shaped by personal counselling, psychosocial care and support in generating alternative income measures.^43,51,52 Additionally, Tora et al. suggest a multi-agency, multi-level and multi-strategy approach,^44,49 and advise to draw lessons from measures taken in relation to other stigmatized diseases.⁴⁴

Buruli ulcer

Avoidance, insulting, exclusion, pitying and thinking less of the patient and their families are manifestations of the enacted stigma reported, whereas, from the patients point of view, social isolation, keeping others from knowing about the condition, shame attached to the disease, fear to interact in the community and thinking less of themselves are manifestations of anticipated and internalized stigma.^53–59 Adamba and Owus reported that 62% of the patients with Buruli ulcer suffer from either real or perceived stigma towards them.⁵³ In contrast, the research of Renzaho et al.⁵⁸ and Amoakoh and Aikins⁵⁴ indicated that, in general, despite some stigma surrounding Buruli ulcer, there is community acceptance and sympathy towards Buruli ulcer patients. Social consequences comprise social isolation, reduced employment and education opportunities as well as various problems in the area of relationships.^53,55–59 Delayed treatment seeking is reported by four studies as a health-related consequence,^53–55,58 which is contradicted by the results of two other studies that indicate that Buruli ulcer stigma has no effect on treatment seeking behavior.^57,59 Furthermore, the shame^53,56,58 as well as the low self-esteem⁵⁸ indicate the psychological impact of the stigma related to Buruli ulcer. Appearance^{53,55–57,59} and fear of contagion^53,55,58,59 are most frequently reported as reasons for stigmatization. In relation to health education as measure against stigmatization, Aujoulat et al.⁵⁵ and Renzaho et al.⁵⁸ proposed the engagement of Buruli ulcer patients, whereas Amoakoh and Aikins,⁵⁴ and Renzaho et al.⁵⁸ recommend including Buruli ulcer awareness activities in the school curriculum. Also, modification of the existing disease management is suggested as another possibility to overcome stigma.^56,58,59 Furthermore, personal support by means of enrolment of Buruli ulcer affected households in a social protection program,⁵³ or by including stigma reduction strategies and social rehabilitation in disability prevention programs⁵⁶ are brought forward as measures against stigmatization (see Table 4).

Onchocerciasis

The five studies on onchocerciasis, mostly relating to onchocercal skin disease, detected enacted, anticipated and internalized stigma (see Table 5). Manifestations of enacted stigma included avoidance, disrespect, name calling, ridiculing, abuse, exclusion, and thinking less of and pitying the patient and family.^60–64 Anticipated stigma is characterized by the patient's fear of disclosure and subsequent fear of enacted stigma, causing them to conceal their condition and avoid people and social participation,^60–62,64 whereas manifestations of internalized stigma comprise feelings of embarrassment, shame and inferiority, and reduced dignity.^60–64 Certain socio-demographic and health-related factors were reported to influence the levels of stigma related to onchocerciasis; namely, the level of education, employment status, age, gender, health status, and type and stage of onchocerciasis.^62–64 The multi-country study of Vlassoff et al. detected no difference in stigma expressed amongst the various African countries they studied.⁶⁴ Problems in the relational and sexual sphere, limited occupational (e.g., leadership) and educational opportunities as well, as social isolation were reported as social consequences related to onchocerciasis.^60–64 The delay in seeking healthcare can be seen as a health consequence,⁶² whereas low self-esteem, anxiety and fear, depression, suicidal tendencies and compromised dignity are reported as psychological consequences.^60–63 Similar reasons for stigmatization^61–64 as in the above NTDs were mentioned in relation to onchocerciasis. Health education^60,63,64 and disease management^60,62–64 are suggested as methods to reduce stigma. However, the study from Brieger and colleagues found that disease management via treatment with ivermectin had no effect on the level of stigma related to onchocerciasis.⁶¹

Schistosomiasis

Enacted,^65–68 anticipated^65–67 and internalized^65–68 stigma related to schistosomiasis is reflected in the reviewed articles (see Table 5). Enacted stigma manifested as avoidance, negative attitudes, labelling and making fun of schistosomiasis patients,^65–68 and as shame and embarrassment related to schistosomiasis in the case of the internalized stigma.^65–68 Anticipated stigma is apparent from the fear of disclosure and the subsequent fear of enacted stigma by the community.^65–67 Limited employment and education opportunities, social isolation and blemished reputation, alongside problems in the relational sphere were reported as social consequences of schistosomiasis.^65–68 Delay in health seeking^65–68 and reduced capabilities to obtain treatment due to discrimination by health care workers⁶⁶ reflect the health-related consequences. Shame, embarrassment and fear contemplate the psychological consequences for schistosomiasis patients.^65–67 Reasons for stigmatization include fear of contagion,^65–68 witchcraft,⁶⁶ being a financial burden on the family⁶⁶ and promiscuity, because of the wrong assumption that schistosomiasis is sexually transferrable.^65–67 The measures to overcome stigmatization comprise health education with a focus on perceptions and attitudes of the community and the patients,^65–68 alongside disease management which will, either directly⁶⁸ or indirectly due to the disappearance of the disease,^66,67 lead to a reduction of the stigmatization.

Leishmaniasis

The studies of Reithinger et al.⁶⁹ and Yanik et al.⁷⁰ provide insights into the relation between stigma and leishmaniasis (Table 5). Enacted and internalized stigma manifested in either exclusion from communal life and social groups, or feeling disfigured, having a low self-esteem and a decreased body satisfaction.^69,70 The study of Reithinger et al. concluded that a high level of stigma is associated with leishmaniasis and that the intensity of stigma depends on the severity and visibility of the leishmaniasis lesions.⁶⁹ Social, physical and emotional isolation due to exclusion from social groups, and decreased marriage opportunities were reported as social consequences of leishmaniasis-related stigma, whereas depression and anxiety represent the psychological consequences.^69,70 A blemished appearance, the fear of contagion and the inability to fulfil certain gender roles are described as the underlying reasons for the stigmatization.^69,70 Reithinger et al. proposed disease management and health education with a focus on reduction of the social impact of leishmaniasis, on disease transmission and on prevention as measures to reduce stigma.⁶⁹

Chagas disease

The article of Guariento et al. covers enacted stigma related to Chagas disease in the labor market (Table 5).⁷¹ Manifestations of enacted stigma include having Chagas disease as the reason for being fired from work (8.9%) and as the cause of not passing the pre-hiring assessment (92.3% of the 9.1% undergoing pre-hiring physical examinations). The social consequences described are diminished work opportunities.⁷¹ Performance impediments as the result of cardiac involvement of Chagas disease are emphasized as the reason for stigmatization.⁷¹ The article of Guariento et al. only detected the stigmatization with their survey, no measures against it are offered.⁷¹

Human African trypanosomiasis

The study of Robays et al. describes stigma related to the neurological impairments that accompany HAT (see Table 5).⁷² Manifestations of the enacted and internalized stigma are ‘not being taken seriously as a patient’ and feelings of shame, respectively.⁷² However, the authors conclude that there is only minimal stigma related to HAT, because the disease does not result in exclusion from society. This limited stigma is explained by the fact that HAT is highly endemic in the study area and thus everybody has been confronted with the disease.⁷² The social consequence that is reported is the assumed inability to produce offspring, whereas reluctance to seek health care and the subsequent delay of treatment are highlighted as health consequences related to HAT.⁷² The performance impediments that are caused by HAT, especially due to the neurological impairments, are seen as the reason for the stigmatization.⁷² The authors claim that no drastic measures are needed, since there is only a minimal amount of stigma related to HAT. They suggest, however, that the confidentiality of the HAT screening should be improved in order to reduce the limited stigmatization attached to public disclosure.⁷²

Soil-transmitted helminthiasis

The only account of stigma-related STH concerns hookworm-related cutaneous larva migrans (Table 5).⁷³ Expressions of enacted stigma include teasing and bullying of patients due to their skin impairments, as well as social exclusion. Conversely, patients feeling ashamed (64.8%), covering up their lesion (34%) and withdrawal from social networks due to fear of stigmatization are signs of internalized and anticipated stigma.⁷³ Social consequences include social exclusion and problems at work or school, whereas psychological consequences include a reduction of self-esteem.⁷³ Reasons for this stigmatization include misconceptions about the etiology, either being infectious or related to poor personal hygiene, and the mutilated appearance.⁷³ Schuster et al. indicated that disease management by means of ivermectin treatment improves the quality of life of patients with hookworm-related cutaneous larva migrans, inter alia due to reduction of stigma.⁷³

Trachoma

Palmer et al.'s paper covers the stigma related to trachoma, in particular related to the effect of trichiasis on the quality of life of women (Table 5).⁷⁴ The enacted stigma related to trichiasis is characterized by social exclusion, labelling, cursing and an unwillingness of community members to have dinner with or marry patients with trichiasis.⁷⁴ The anticipated stigma is manifested by social withdrawal of women with trichiasis, while embarrassment of others seeing their purulent eyes constitutes the internalized stigma component.⁷⁴ Reduced working opportunities, social isolation, decreased social status, the inability to fulfil religious and social obligations, and problems in relationships comprise the social consequences reported. In addition to social consequences, Palmer and colleagues found evidence of psychological consequences in terms of embarrassment and shame.⁷⁴ The purulent appearance of the eyes and the feared contagiousness, alongside the inability to fulfil a certain gender role and being a social and financial burden on the family are highlighted as the underlying reasons for the stigmatization related to trachoma.⁷⁴ Disease management and health education in terms of tailor-made messages to the community are assumed to help improve the quality of life of the trichiasis patients due to the reduction of the stigma related to trachoma.⁷⁴

Discussion

Extent of stigma related to neglected tropical diseases

The purpose of this systematic review was to elucidate the extent to which people affected by NTDs are stigmatized. The results from the 52 studies included in this review revealed evidence of stigma affecting the people suffering from no less than 10 NTDs. There was evidence of widespread stigma related to LF, podoconiosis, Buruli ulcer, onchocerciasis and leishmaniasis. The widespread and severe stigmatization of persons affected by leprosy is already well known.^{12,15,75–83} The evidence is less firm for Chagas disease, schistosomiasis, trachoma and STH (hookworm-related cutaneous larva migrans), since they were only covered by one article each. The findings in the case of HAT, also covered by only one article, revealed only minimal stigmatization of affected persons. Furthermore, it needs to be stressed that four LF articles,^24–27 two podoconiosis articles^41,42 and one Buruli ulcer article⁵⁸ indicated that, in general, there was community support and acceptance of the patients. A difference in geographical distribution and cultural differences would be a logical explanation for this difference, but this does not clearly emerge in this review. Considering the impact of LF, podoconiosis, Buruli ulcer, leishmaniasis, trachoma, hookworm-related cutaneous larva migrans, onchocerciasis and also leprosy on the physical appearance of the person affected, stigmatization was to be expected. However, for Chagas disease, HAT and schistosomiasis, with limited or no visible characteristics, stigmatization was less anticipated. For the remaining seven disease entities, dengue/chikungunya, dracunculiasis, echinococcosis, foodborne trematodes, rabies, taeniasis/cysticercosis and endemic treponematoses, no evidence of stigma was found in our review. This might mean that they are not stigmatized or that no research has been conducted regarding the psychosocial consequences of these NTDs.

Similarities in neglected tropical disease related stigma

The review identifies many cross-cutting features of stigma across the NTDs (see Table 6). Foremost, similarities in the types of stigma and their manifestations are highlighted by this study and can also be found related to leprosy.^{15,75–78,84} Despite the different approaches within the review articles, all information fitted within the framework of stigma types that was outlined by Weiss⁷ and no adaptations needed to be made. It is important to underline that the term ‘enacted stigma’ used in this review included discrimination as well as negative attitudes from the individual and the community perspective. With the exception of Chagas disease, studies on all other NTDs included in Table 6 provided evidence of both experienced and community stigma, as well as of anticipated or internalized stigma. The probable reason for this not being the case for Chagas disease is that there was only one study focusing on stigma related to Chagas disease, which only looked at its effect on the labour market. Also the manifestations of enacted, anticipated or internalized stigma were equivalent amongst all 11 NTDs. A clear overlap in consequences related to NTD stigma was also seen. Equivalent social, health-related and psychological consequences were described regarding the 10 stigmatized NTDs in this study as well as in leprosy.^{15,75–78,84,85} The social consequences that were found in this study are corroborated by several other non-primary data studies on NTDs.^{5,7,11,17,84,86,87} The health-related consequences^{5–7,11,17,84,87–89} and the psychological consequences^{11,17,84,86,87} found in this study are endorsed. In addition, it seems that the social and health consequences of stigma related to NTDs can contribute to the development of psychological consequences, such as anxiety and depression.^11,14

Appearance, fear of contagion, being a burden to the family and the inability to fulfil particular gender roles were found to be cross-cutting motives for stigmatization of people with NTDs, including leprosy.^{15,76,78,84,85} Several other studies looking at the stigma related to NTDs reported corresponding reasons for stigmatization.^{6,7,11,17,20,86,87,89}

Finally, the suggested measures against stigmatization, health education and disease management were also similar across the field of NTDs. Research of Alonso and Alvar,⁷ Kassi et al.,¹⁷ Weiss,⁸⁶ and Zeldenryk et al.⁸⁷ confirms the use of health education for patients and for the community as a method to overcome NTD-related stigma, whereas the need to focus disease management on the psychosocial impact of NTDs is also corroborated by several studies.^{6,7,11,17,86,87,89} Compared to the other NTDs, much more work has been done to reduce leprosy-related stigma, whereby reported measures also include elements of disease management⁷⁶ and health education.^12,75 It should be noted that the effectiveness of these measures has often not been demonstrated. Also in the majority of the articles reviewed no attempt was made to examine the efficacy of the interventions suggested. To be effective, health education needs to address specific cultural and religious beliefs, and the specific questions and fears that people have in a given community,^90–92 and it needs to be combined with other interventions.^18,92,93 Available evidence from studies in leprosy show that concerted multi-level interventions are needed to achieve lasting effects.^18,92–94 Disease management is an important but indirect intervention with regard to stigma. Since the visible impact of NTDs has been shown to be an important determinant of stigma, lessening this through appropriate disease management should have a positive effect on stigma, as has been demonstrated by wound management in leprosy.^18,78,95 The choice of interventions will depend on the types of stigma one seeks to address. Interventions such as health education and contact with the community are used to reduce community stigma, whereas disease management, personal support and counselling are used to mitigate (the effects of) internalized, anticipated and experienced stigma.

Differences in stigma between neglected tropical diseases

A few remarkable differences were found in the reasons for stigmatization and the measures against it (Table 6). In terms of reasons for stigmatization, perceived hereditary etiology, performance impediments and perceived link with promiscuity were only found for particular NTDs. The perception that the disease has a genetic component as a motive for stigmatization was predominantly related to podoconiosis, whereas less frequently this was also found related to LF, onchocerciasis and leprosy. This difference can be explained by the fact that podoconiosis, contrary to the other NTDs, has a genetic etiology in addition to an exposure to environmental chemicals in volcanic soils.⁹⁶ Performance impediments as a cause for stigmatization were described specifically for Chagas disease and HAT. The lack of physical attributes of Chagas disease and HAT could account for this divergent reason for stigmatization. Promiscuity is perceived to be the underlying reason for stigmatization in persons with schistosomiasis and to a lesser degree to persons with LF and leprosy. In the case of schistosomiasis, the localization of the signs and symptoms in the urinary tract may feed the perception of an association with sexual intercourse.

Alongside the many parallels in suggested measures against stigmatization, personal support in terms of rehabilitation, counselling and support groups was only identified in relation to leprosy, LF, podoconiosis and Buruli ulcer, probably due to the more elaborate work done and information available on these four NTDs. Especially in relation to leprosy, personal support has often been used as a measure to diminish the consequences of stigma.^15,18,78 Improved self-esteem, increased participation and community support/acceptance are results of the personal support offered by self-care groups,^15,18,95 socio-economic rehabilitation,⁷⁸ and counseling.¹⁵ Various other studies proposed personal support to mitigate the effects of stigma, with Litt et al. suggesting disease rehabilitation,¹¹ Kassi et al. advising empowerment of the patients,⁸⁶ and Weiss proposing advocacy groups and counseling.⁷ Leprosy literature^{19,84,93,94,97} and one article related to podoconiosis⁴⁴ stress the importance of learning from other stigmatized health conditions, in particular mental health and HIV/AIDS, in the approach of reducing stigmatization and the possibility to implement joint interventions due to the similarities found in stigmata related to health conditions. This opportunity should also be noted by those working with the other NTDs, since it is likely to be very relevant in their battle against stigma.

Limitations

A few limitations of this review need to be acknowledged. The language restriction of the review can be seen as a limitation, since articles in languages other than English and Dutch were not taken into account. Another potential limitation was the fact that the article selection and data extraction was predominantly conducted by one reviewer. The effect of this bias was limited by consulting the second author in the article selection process and by the fact that the second author extensively reviewed the obtained results.

Conclusions

In conclusion, this systematic review found evidence for stigma attached to LF, podoconiosis, Buruli ulcer, onchocerciasis, schistosomiasis, leishmaniasis, Chagas disease, trachoma and STH (hookworm-related cutaneous larva migrans) and to a lesser extent to HAT. This is added to the extensive body of evidence of stigma against leprosy. The obvious and extensive similarities in stigma types, manifestations and effects among the different NTDs, including leprosy, suggest opportunities for joint approaches to reduce of stigma in NTDs. Such joint approaches should incorporate multiple strategies at different levels to address stigma in society. Interventions are also needed aimed at persons affected by NTDs and their families, paying specific attention to the mental health consequences of stigma. To optimize the stigma reduction approaches, lessons should be drawn from other stigmatized health conditions. Future research should focus on design and implementation of joint strategies and interventions to overcome stigma and on demonstrating the impact of these measures. Moreover, further research is necessary to investigate stigma related to the seven NTDs for which no evidence was found by this systematic review. Additional research is also needed on the differences in stigma and its consequences among countries and cultures in case of the NTDs already included in this study, on the extent and severity of NTD-related stigma and on the mental health consequences of stigma related to the various conditions.

Supplementary data

Supplementary data are available at International Health online (http://inthealth.oxfordjournals.org/).

Authors' contributions: WvB conceived the study; KH carried out the systematic review and drafted the manuscript; WvB revised the manuscript. All authors read and approved the final manuscript. WvB is the guarantor of the paper.

Funding: None.

Competing interests: None declared.

Ethical approval: Not required.

References