The impact of leishmaniasis on mental health and psychosocial well-being: A systematic review


Autoři: Malini Pires aff001;  Barry Wright aff001;  Paul M. Kaye aff002;  Virgínia da Conceição aff004;  Rachel C. Churchill aff002
Působiště autorů: Mental Health Research Group, Hull York Medical School and Dept. of Health Sciences, University of York, England, United Kingdom aff001;  Centre for Reviews and Dissemination, University of York, England, United Kingdom aff002;  Centre for Immunology and Infection, Hull York Medical School and Dept. of Biology, University of York, England, United Kingdom aff003;  Institute of Public Health, University of Porto, Portugal aff004
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223313

Souhrn

Background

Leishmaniasis is a neglected tropical parasitic disease endemic in South Asia, East Africa, Latin America and the Middle East. It is associated with low socioeconomic status (SES) and responsible for considerable mortality and morbidity. Reports suggest that patients with leishmaniasis may have a higher risk of mental illness (MI), psychosocial morbidity (PM) and reduced quality of life (QoL), but this is not well characterised. The aim of this study was to conduct a systematic review to assess the reported impact of leishmaniasis on mental health and psychosocial wellbeing.

Methods

A systematic review of the literature was carried out. Pre-specified criteria were applied to identify publications including observational quantitative studies or systematic reviews. Two reviewers screened all of the titles, abstracts and full-studies and a third reviewer was consulted for disagreements. Data was extracted from papers meeting the criteria and quality appraisal of the methods was performed using the Newcastle-Ottawa Scale or the Risk of Bias in Systematic Review tool.

Results

A total of 14 studies were identified from 12,517 records. Nine cross-sectional, three case-control, one cohort study and one systematic review were included. Eleven assessed MI outcomes and were measured with tools specifically designed for this; nine measured PM and 12 measured QoL using validated measurement tools. Quality appraisal of the studies showed that six were of good quality. Cutaneous leishmaniasis and post kala-azar dermal leishmaniasis showed evidence of associated MI and PM including depression, anxiety and stigma, while all forms of disease showed decreased QoL. The findings were used to inform a proposed model and conceptual framework to show the possible links between leishmaniasis and mental health outcomes.

Conclusion

There is evidence that leishmaniasis has an impact on MI, PM or QoL of patients and their families and this occurs in all the main subtypes of the disease. There are however large gaps in the evidence. Further research is required to understand the full extent of this problem and its mechanistic basis.

Klíčová slova:

Anxiety – Depression – Leishmaniasis – Lesions – Mental health and psychiatry – Psychological and psychosocial issues – Quality of life – Systematic reviews


Zdroje

1. Desjeux P, Jannin J, Bern C, Boer M den, Alvar J, Herrero M, et al. Leishmaniasis Worldwide and Global Estimates of Its Incidence. PLoS One. 2012;7: e35671. doi: 10.1371/journal.pone.0035671 22693548

2. Bhattacharya SK, Dash AP. Elimination of kala-azar from the Southeast Asia Region. Am J Trop Med Hyg. 2017;96: 802–804. doi: 10.4269/ajtmh.16-0279 28115678

3. WHO- World Health Organization. Fact Sheets- Leishmaniasis [Internet]. 2019 [cited 18 Apr 2019]. Available: https://www.who.int/en/news-room/fact-sheets/detail/leishmaniasis

4. Zijlstra EE, Musa AM, Khalil EAG, El Hassan IM, El-Hassan AM. Post-kala-azar dermal leishmaniasis. Lancet Infect Dis. 2003;3: 87–98. doi: 10.1016/S1473-3099(03)00517-6 12560194

5. Handler MZ, Patel PA, Kapila R, Al-Qubati Y, Schwartz RA. Cutaneous and mucocutaneous leishmaniasis: Clinical perspectives. J Am Acad Dermatol. 2015;73: 897–908. doi: 10.1016/j.jaad.2014.08.051 26568335

6. Kassi M, Kassi M, Afghan AK, Rehman R, Kasi PM. Marring leishmaniasis: The stigmatization and the impact of cutaneous leishmaniasis in Pakistan and Afghanistan. PLoS Negl Trop Dis. 2008;2: 1–3. doi: 10.1371/journal.pntd.0000259 18958168

7. Afghan AK, Kassi M, Kasi PM, Ayub A, Kakar N, Marri SM. Clinical manifestations and distribution of cutaneous leishmaniasis in Pakistan. J Trop Med. 2011;2011: 359145. doi: 10.1155/2011/359145 22174721

8. Al-Kamel MA. Impact of leishmaniasis in women: a practical review with an update on my ISD-supported initiative to combat leishmaniasis in Yemen (ELYP). International Journal of Women’s Dermatology. 2016. doi: 10.1016/j.ijwd.2016.04.003 28492018

9. Reithinger R, Aadil K, Kolaczinski J, Mohsen M, Hami S. Social impact of leishmaniasis Afghanistan. Emerg Infect Dis. 2005;11: 634–636. doi: 10.3201/eid1104.040945 15834984

10. Bennis I, Belaid L, De Brouwere V, Filali H, Sahibi H, Boelaert M. “The mosquitoes that destroy your face”. Social impact of Cutaneous Leishmaniasis in South-eastern Morocco, A qualitative study. PLoS One. 2017;12: e0189906. doi: 10.1371/journal.pone.0189906 29261762

11. Lima VMF, Gonçalves ME, Ikeda FA, Luvizotto MCR, Feitosa MM. Anti-leishmania antibodies in cerebrospinal fluid from dogs with visceral leishmaniasis. Brazilian J Med Biol Res. 2003;36: 485–489. doi: 10.1590/S0100-879X2003000400010 12700826

12. Marangoni NR, Melo GD, Moraes OC, Souza MS, Perri SH V, Machado GF. Levels of matrix metalloproteinase-2 and metalloproteinase-9 in the cerebrospinal fluid of dogs with visceral leishmaniasis. Parasite Immunol. 2011;33: 330–334. doi: 10.1111/j.1365-3024.2011.01285.x 21332759

13. Hashim FA, Ahmed AE, El Hassan M, El Mubarak MH, Yagi H, Ibrahim EN, et al. Neurologic changes in visceral leishmaniasis. Am J Trop Med Hyg. 1995;52: 149–154. doi: 10.4269/ajtmh.1995.52.149 7872442

14. Diniz LMO, Duani H, Freitas CR, Figueiredo RM, Xavier CC. Neurological involvement in visceral leishmaniasis: case report. Rev Soc Bras Med Trop. 2010;43: 743–745. doi: 10.1590/s0037-86822010000600031 21181038

15. Chunge CN, Gachihi G, Muigai R. Is neurological involvement possible in visceral leishmaniasis in kenya? Trans R Soc Trop Med Hyg. 1985;79: 872. doi: 10.1016/0035-9203(85)90143-9

16. Prasad LSN, Sen S. Migration of Leishmania donovani amastigotes in the cerebrospinal fluid. Am J Trop Med Hyg. 1996;55: 652–654. doi: 10.4269/ajtmh.1996.55.652 9025693

17. Fasanaro A, Scoleri G, Pizza V, Gaeta G, Fasanaro A. Guillain-Barré syndrome as presenting manifestation of visceral leishmaniasis. Lancet. 1991;333: 1142.

18. Kumar N, Pandey K, Das VNR, Sinha PK, Topno RK, Lal CS, et al. HIV infection, visceral leishmaniasis and Guillain-Barre syndrome in the same patient: a case report. Ann Trop Med Parasitol. 2008;102: 185–188. doi: 10.1179/136485908X267885 18318942

19. Attarian S, Serratrice J, Mazodier C, Disdier P, Azulay JP, Pouget J. [Guillain-Barre syndrome revealing visceral leishmaniasis in an immunocompetent woman]. Rev Neurol. 2003;159: 1046–1048. doi: MDOI-RN-11-2003-159-11-0035-3787-101019-ART7 [pii] 14710025

20. Melo GD, Silva JES, Grano FG, Souza MS, Machado GF. Leishmania infection and neuroinflammation: Specific chemokine profile and absence of parasites in the brain of naturally-infected dogs. J Neuroimmunol. 2015;289: 21–29. doi: 10.1016/j.jneuroim.2015.10.004 26616868

21. Melo GD, Goyard S, Fiette L, Boissonnas A, Combadiere C, Machado GF, et al. Unveiling Cerebral Leishmaniasis: Parasites and brain inflammation in Leishmania donovani infected mice. Sci Rep. 2017;7: 1–13. doi: 10.1038/s41598-016-0028-x

22. Singhal G, Jaehne EJ, Corrigan F, Toben C, Baune BT. Inflammasomes in neuroinflammation and changes in brain function: A focused review. Front Neurosci. 2014;8: 1–13. doi: 10.3389/fnins.2014.00001

23. Stewart JC, Rand KL, Muldoon MF, Kamarck TW. A prospective evaluation of the directionality of the depression-inflammation relationship. Brain Behav Immun. 2009;23: 936–944. doi: 10.1016/j.bbi.2009.04.011 19416750

24. Taraz M, Khatami MR, Gharekhani A, Abdollahi A, Khalili H, Dashti-Khavidaki S. Relationship between a pro- and anti-inflammatory cytokine imbalance and depression in haemodialysis patients. Eur Cytokine Netw. 2012;23: 179–186. doi: 10.1684/ecn.2013.0326 23360798

25. Oliveira Miranda D, Soares De Lima TA, Ribeiro Azevedo L, Feres O, Ribeiro Da Rocha JJ, Pereira-Da-Silva G. Proinflammatory Cytokines Correlate with Depression and Anxiety in Colorectal Cancer Patients. Biomed Res Int. 2014;2014: 1–5. doi: 10.1155/2014/739650 25309921

26. Ford DE, Erlinger TP. Depression and C-Reactive Protein in US Adults: Data from the Third National Health and Nutrition Examination Survey. Arch Intern Med. 2004;164: 1010–1014. doi: 10.1001/archinte.164.9.1010 15136311

27. Vogelzangs N, de Jonge P, Smit JH, Bahn S, Penninx BW. Cytokine production capacity in depression and anxiety. Transl Psychiatry. 2016;6: e825. doi: 10.1038/tp.2016.92 27244234

28. Furtado M, Katzman MA. Examining the role of neuroinflammation in major depression. Psychiatry Res. 2015;229: 27–36. doi: 10.1016/j.psychres.2015.06.009 26187338

29. Howren MB, Lamkin DM, Suls J. Associations of depression with c-reactive protein, IL-1, and IL-6: A meta-analysis. Psychosom Med. 2009;71: 171–186. doi: 10.1097/PSY.0b013e3181907c1b 19188531

30. Dowlati Y, Herrmann N, Swardfager W, Liu H, Sham L, Reim EK, et al. A Meta-Analysis of Cytokines in Major Depression. Biol Psychiatry. 2010;67: 446–457. doi: 10.1016/j.biopsych.2009.09.033 20015486

31. Alesci S, Martinez PE, Kelkar S, Ilias I, Ronsaville DS, Listwak SJ, et al. Major depression is associated with significant diurnal elevations in plasma interleukin-6 levels, a shift of its circadian rhythm, and loss of physiological complexity in its secretion: Clinical implications. J Clin Endocrinol Metab. 2005;90: 2522–2530. doi: 10.1210/jc.2004-1667 15705924

32. Berk M, Williams LJ, Jacka FN, O’Neil A, Pasco JA, Moylan S, et al. So depression is an inflammatory disease, but where does the inflammation come from? BMC Med. 2013;11. doi: 10.1186/1741-7015-11-200 24228900

33. Bennis I, De Brouwere V, Belrhiti Z, Sahibi H, Boelaert M. Psychosocial burden of localised cutaneous Leishmaniasis: A scoping review. BMC Public Health. 2018;18. doi: 10.1186/s12889-018-5260-9 29544463

34. APA. American Psychiatric Association, 2013. Diagnostic and statistical manual of mental disorders (5th ed.). American Journal of Psychiatry. 2013. doi: 10.1176/appi.books.9780890425596.744053

35. Munley PH. Erik Erikson’s theory of psychosocial development and vocational behavior. J Couns Psychol. 1975; doi: 10.1037/h0076749

36. Erikson EH. Childhood and Society. 1st ed. New York: W. W. Norton & Company Inc.; 1963.

37. Erikson E. Identity: Youth and Crisis. First. New York: W. W Norton & Company, Inc; 1968.

38. Caruso R, Nanni MG, Riba MB, Sabato S, Grassi L. The burden of psychosocial morbidity related to cancer: patient and family issues. Int Rev Psychiatry. 2017;29: 389–402. doi: 10.1080/09540261.2017.1288090 28753076

39. Galway K, Black A, Cantwell M, Cardwell CR, Mills M, Donnelly M. Psychosocial interventions to improve quality of life and emotional wellbeing for recently diagnosed cancer patients. Cochrane Database of Systematic Reviews. 2012. doi: 10.1002/14651858.CD007064.pub2 23152241

40. Zimmerman M, Chelminski I, Young D, Dalrymple K, Martinez J, Morgan TA. Which DSM-IV personality disorders are most strongly associated with indices of psychosocial morbidity in psychiatric outpatients? Compr Psychiatry. 2012; doi: 10.1016/j.comppsych.2012.02.008 22497671

41. Hofstraat K, van Brakel WH. Social stigma towards neglected tropical diseases: a systematic review. Int Health. 2016;8: i53–i70. doi: 10.1093/inthealth/ihv071 26940310

42. World Health Organization. WHOQOL: Measuring Quality of Life. In: WHO [Internet]. 2018 [cited 16 Sep 2018]. Available: http://www.who.int/healthinfo/survey/whoqol-qualityoflife/en/

43. Pires M, Dunn-Roberts A, Churchill R, Wright B, Kaye P. The impact of leishmaniasis on mental health: a systematic review. In: PROSPERO: CRD42018104369 [Internet]. 2018. Available: https://www.crd.york.ac.uk/prospero/display_record.php?RecordID=104369

44. CRD. Centre for Reviews and Dissemination—Systematic Reviews: CRD’s Guidance for Undertaking Systematic Reviews in Health Care. York Cent Rev Dissem. 2009;

45. Moher D, Liberati A, Tetzlaff J, Altman DG, Altman D, Antes G, et al. Preferred reporting items for systematic reviews and meta-analyses: The PRISMA statement (Chinese edition). J Chinese Integr Med. 2009;6: e1000097. doi: 10.3736/jcim20090918

46. Higgins J, Green S. Cochrane handbook for systematic reviews of interventions version 5.1.0 [Internet]. 2011 [cited 1 Nov 2018]. Available: www.cochrane-handbook.org

47. Weiss MG. Stigma and the Social Burden of Neglected Tropical Diseases. PLoS Negl Trop Dis. 2008;2: e237. doi: 10.1371/journal.pntd.0000237 18478049

48. Meheus F, Abuzaid AA, Baltussen R, Younis BM, Balasegaram M, Khalil EAG, et al. The economic burden of visceral leishmaniasis in Sudan: An assessment of provider and household costs. Am J Trop Med Hyg. 2013;89: 1146–1153. doi: 10.4269/ajtmh.12-0585 24189368

49. Wells G, Shea B, O’Connell D, Peterson J, Welch V, Losos M, et al. The Newcastle-Ottawa Scale (NOS) for assessing the quality of nonrandomised studies in meta-analyses [Internet]. 2012 [cited 28 Aug 2018]. Available: http://www.ohri.ca/programs/clinical_epidemiology/oxford.asp

50. Higgins JP, Green S. Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. Cochrane Handbook for Systematic Reviews of Interventions: Cochrane Book Series. 2008. doi: 10.1002/9780470712184

51. Modesti PA, Reboldi G, Cappuccio FP, Agyemang C, Remuzzi G, Rapi S, et al. Panethnic Differences in Blood Pressure in Europe: A Systematic Review and Meta-Analysis. PLoS One. 2016;11: e0147601. doi: 10.1371/journal.pone.0147601 26808317

52. Whiting P, Savovic J, Higgins JP, Caldwell DM, Reeves BC, Shea B, et al. ROBIS: A new tool to assess risk of bias in systematic reviews was developed. J Clin Epidemiol. 2016;69: 225–34. doi: 10.1016/j.jclinepi.2015.06.005 26092286

53. Alemayehu M, Wubshet M, Mesfin N, Tamiru A, Gebayehu A. Health-related quality of life of HIV infected adults with and without Visceral Leishmaniasis in Northwest Ethiopia. Health Qual Life Outcomes. 2017;15. doi: 10.1186/s12955-017-0636-6 28851361

54. Simsek Z, Ak D, Altindag A, Gunes M. Prevalence and predictors of mental disorders among women in Sanliurfa, Southeastern Turkey. J Public Health (Bangkok). 2008;30: 487–493. doi: 10.1093/pubmed/fdn025 18400696

55. Turan E, Kandemir H, Yesilova Y, Ekinci S, Tanrikulu O, Kandemir SB, et al. Assessment of psychiatric morbidity and quality of life in children and adolescents with cutaneous leishmaniasis and their parents. Postep dermatologii i Alergol. 2015;32: 344–348. doi: 10.5114/pdia.2015.54744 26759542

56. Vares B, Mohseni M, Heshmatkhah A, Farjzadeh S, Safizadeh H, Shamsi-Meymandi S, et al. Quality of Life in Patients with Cutaneous Leishmaniasis. Arch Iran Med. 2013;16: 474–477. 23906253

57. Yanik M, Gurel MS, Simsek Z, Kati M. The psychological impact of cutaneous leishmaniasis. Clin Exp Dermatol. 2004;29: 464–467. doi: 10.1111/j.1365-2230.2004.01605.x 15347324

58. Alemayehu M, Wubshet M, Mes N, Gebayehu A. Effect of Health Care on Quality of Life among Human Immunode fi ciency Virus Infected Adults With and Without Visceral Leishmaniasis in northwest Ethiopia : A Longitudinal Follow-Up Study. 2018;98: 747–752. doi: 10.4269/ajtmh.17-0458 29363454

59. Chahed MK, Bellali H, Ben Jemaa S, Bellaj T. Psychological and Psychosocial Consequences of Zoonotic Cutaneous Leishmaniasis among Women in Tunisia: Preliminary Findings from an Exploratory Study. PLoS Negl Trop Dis. 2016;10. doi: 10.1371/journal.pntd.0005090 27788184

60. de Castro Toledo AC, da Silva RE, Carmo RF, Amaral TA, Profeta Luz Z lia M, Rabello A. Assessment of the quality of life of patients with cutaneous leishmaniasis in belo Horizonte, Brazil, 2009–2010. A pilot study. Trans R Soc Trop Med Hyg. 2013;107: 335–336. doi: 10.1093/trstmh/trt021

61. Govil D, Pedgaonkar SP, Chandra Das K, Sahoo H, Lhungdim H. Assessing Knowledge, Preventive Attitudes, and Practices Related to Kala-Azar: A Study of Rural Madhepura, Bihar, India. Am J Trop Med Hyg. 2017;98: 857–863. doi: 10.4269/ajtmh.16-0978 29280426

62. Handjani F., Kalafi A. b. Impact of dermatological diseases on family members of the patients using family dermatology life quality index: A preliminary study in Iran. Iran J Dermatology. 2013;16: 128–131.

63. Honório I de M, Cossul MU, Bampi LN da S, Baraldi S. Quality of Life in People with Cutaneous Leishmaniasis. Rev Bras Promoç Saúde. 2016;29: 342–349.

64. Layegh P, Teimourian M, Shiva F, Hebrani P, Momenzadeh A. Quality of life, anxiety and depression in children with cutaneous leishmaniasis: Major concerns or not? Pediatr Dermatol. 2017;34: S152–S153.

65. Pal B, Murti K, Siddiqui NA, Das P, Lal CS, Babu R, et al. Assessment of quality of life in patients with post kalaazar dermal leishmaniasis. Health Qual Life Outcomes. 2017;15: 1–7. doi: 10.1186/s12955-016-0578-4

66. The World Bank. Data for Upper middle income, Lower middle income, Low income [Internet]. 2016 [cited 7 Sep 2018]. Available: https://data.worldbank.org/?locations=XT-XN-XM

67. World Health Organization. WHOQOL-HIV instrument: scoring and coding for the WHOQOL-HIV instruments users manual [Internet]. 2012. Available: https://apps.who.int/iris/handle/10665/77776

68. Abazid N, Jones C, Davies CR. Knowledge, attitudes and practices about leishmaniasis among cutaneous leishmaniasis patients in Aleppo, Syrian Arab Republic. East Mediterr Health J. 2012;18: 7–14. Available: http://www.ncbi.nlm.nih.gov/pubmed/22360005 22360005

69. Nilforoushzadeh MA, Roohafza HR, Jaffary F, Khatuni M. Comparison of quality of life in women suffering from cutaneous leishmaniasis treated with topical and systemic glucantime along with psychiatric consultation compared with the group without psychiatric consultation. J Isfahan Med Sch. 2012;29: 3046–3052. doi: 10.3760/cma.j.issn.0366-6999.2010.07.014

70. Ramdas S, van der Geest S, Schallig HDFH. Nuancing stigma through ethnography: The case of cutaneous leishmaniasis in Suriname. Soc Sci Med. 2016;151: 139–146. doi: 10.1016/j.socscimed.2015.12.044 26802370

71. Reyburn H, Koggel M, Sharifi A. Social and psychological consequences of cutaneous leishmaniasis in Kabul Afghanistan [Internet]. Heal Int Partnersh with Nor Church Aid. 2000. doi: 10.2458/azu_acku_pamphlet_ra644_l25_r493_2000

72. Fernando SD, Siriwardana HVYD, Guneratne K a. RCW, Rajapaksa LC. Some sociological aspects of cutaneous leishmaniasis in patients attending a tertiary referral centre in Colombo, Sri Lanka. Int Health. 2010;2: 69–74. doi: 10.1016/j.inhe.2009.12.002 24037054

73. Copeland NK, Aronson NE. Leishmaniasis: Treatment updates and clinical practice guidelines review. Current Opinion in Infectious Diseases. 2015. doi: 10.1097/QCO.0000000000000194 26312442

74. Bezerra JMT, de Araújo VEM, Barbosa DS, Martins-Melo FR, Werneck GL, Carneiro M. Burden of leishmaniasis in Brazil and federated units, 1990–2016: Findings from Global Burden of Disease Study 2016. PLoS Negl Trop Dis. 2018; doi: 10.1371/journal.pntd.0006697 30188898

75. Wang JY, Cui G, Chen HT, Zhou XN, Gao CH, Yang YT. Current epidemiological profile and features of visceral leishmaniasis in people’s republic of China. Parasites and Vectors. 2012; doi: 10.1186/1756-3305-5-31 22316234

76. Aronson N, Herwaldt BL, Libman M, Pearson R, Lopez-Velez R, Weina P, et al. Diagnosis and treatment of leishmaniasis: Clinical practice guidelines by the infectious diseases society of America (IDSA) and the American Society of tropical medicine and hygiene (ASTMH). American Journal of Tropical Medicine and Hygiene. 2017. doi: 10.4269/ajtmh.16-84256 27927991

77. Nordin K, Påhlman L, Larsson K, Sundberg-Hjelm M, Lööf L. Health-related quality of life and psychological distress in a population-based sample of Swedish patients with inflammatory bowel disease. Scand J Gastroenterol. 2002;37: 450–7. doi: 10.1080/003655202317316097 11989837

78. Halaris A. Inflammation, Heart Disease, and Depression. Curr Psychiatry Rep. 2013;15. doi: 10.1007/s11920-013-0400-5 23975043

79. Faugere M, Micoulaud-Franchi JA, Faget-Agius C, Lançon C, Cermolacce M, Richieri R. Quality of life is associated with chronic inflammation in depression: A cross-sectional study. J Affect Disord. 2017;227: 494–497. doi: 10.1016/j.jad.2017.11.061 29156363

80. Hussein A, MalkAldar M, Hajnoor K, Sidig A, Mohamed El-hadi H. Neurological manifestations of visceral leishmaniasis among lladult sudanese patients. J Neurol Sci. 2017;381: 607. doi: 10.1016/j.jns.2017.08.1712LK - http://rd8hp6du2b.search.serialssolutions.com?sid=EMBASE&issn=18785883&id=doi:10.1016%2Fj.jns.2017.08.1712&atitle=Neurological+manifestations+of+visceral+leishmaniasis+among+lladult+sudanese+patients&stitle=J.+Neurol.+Sci.&title=Journal+of+the+Neurological+Sciences&volume=381&issue=&spage=607&epage=&aulast=Hussein&aufirst=A.&auinit=A.&aufull=Hussein+A.&coden=&isbn=&pages=607-&date=2017&auinit1=A&auinitm=

81. Petersen CA, Greenlee MHW. Neurologic manifestations of Leishmania spp. infection. J Neuroparasit. 2011;2: N110401.

82. Carswell J. Kala-azar at Kitui. East Afr Med J. 1953;30: 287–293. 13095327

83. InfoNTD. NMD Toolkit [Internet]. [cited 9 Jun 2019]. Available: www.infontd.org/Toolkit

84. Bailey F, Mondragon-Shem K, Haines LR, Olabi A, Alorfi A, Ruiz-Postigo JA, et al. Cutaneous leishmaniasis and co-morbid major depressive disorder: A systematic review with burden estimates. PLoS Negl Trop Dis. 2019; doi: 10.1371/journal.pntd.0007092 30802261

85. Bennis I, Thys S, Filali H, De Brouwere V, Sahibi H, Boelaert M. Psychosocial impact of scars due to cutaneous leishmaniasis on high school students in Errachidia province, Morocco. Infect Dis Poverty. 2017;6. doi: 10.1186/s40249-017-0267-5 28385151

86. Peters RMH, Dadun, Zweekhorst MBM, Bunders JFG, Irwanto, van Brakel WH. A Cluster-Randomized Controlled Intervention Study to Assess the Effect of a Contact Intervention in Reducing Leprosy-Related Stigma in Indonesia. PLoS Negl Trop Dis. 2015; doi: 10.1371/journal.pntd.0004003 26485128

87. Van Brakel WH, Cataldo J, Grover S, Kohrt BA, Nyblade L, Stockton M, et al. Out of the silos: Identifying cross-cutting features of health-related stigma to advance measurement and intervention. BMC Med. 2019; doi: 10.1186/s12916-018-1245-x 30764817


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