Skip to main content
Top
Published in: Emerging Themes in Epidemiology 1/2017

Open Access 01-12-2017 | Review

Challenges in modeling complexity of neglected tropical diseases: a review of dynamics of visceral leishmaniasis in resource limited settings

Authors: Swati DebRoy, Olivia Prosper, Austin Mishoe, Anuj Mubayi

Published in: Emerging Themes in Epidemiology | Issue 1/2017

Login to get access

Abstract

Objectives

Neglected tropical diseases (NTD), account for a large proportion of the global disease burden, and their control faces several challenges including diminishing human and financial resources for those distressed from such diseases. Visceral leishmaniasis (VL), the second-largest parasitic killer (after malaria) and an NTD affects poor populations and causes considerable cost to the affected individuals. Mathematical models can serve as a critical and cost-effective tool for understanding VL dynamics, however, complex array of socio-economic factors affecting its dynamics need to be identified and appropriately incorporated within a dynamical modeling framework. This study reviews literature on vector-borne diseases and collects challenges and successes related to the modeling of transmission dynamics of VL. Possible ways of creating a comprehensive mathematical model is also discussed.

Methods

Published literature in three categories are reviewed: (i) identifying non-traditional but critical mechanisms for VL transmission in resource limited regions, (ii) mathematical models used for dynamics of Leishmaniasis and other related vector borne infectious diseases and (iii) examples of modeling that have the potential to capture identified mechanisms of VL to study its dynamics.

Results

This review suggests that VL elimination have not been achieved yet because existing transmission dynamics models for VL fails to capture relevant local socio-economic risk factors. This study identifies critical risk factors of VL and distribute them in six categories (atmosphere, access, availability, awareness, adherence, and accedence). The study also suggests novel quantitative models, parts of it are borrowed from other non-neglected diseases, for incorporating these factors and using them to understand VL dynamics and evaluating control programs for achieving VL elimination in a resource-limited environment.

Conclusions

Controlling VL is expensive for local communities in endemic countries where individuals remain in the vicious cycle of disease and poverty. Smarter public investment in control programs would not only decrease the VL disease burden but will also help to alleviate poverty. However, dynamical models are necessary to evaluate intervention strategies to formulate a cost-effective optimal policy for eradication of VL.
Appendix
Available only for authorised users
Literature
1.
go back to reference Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 2007;5(11):873–82.CrossRefPubMed Chappuis F, Sundar S, Hailu A, Ghalib H, Rijal S, Peeling RW, Alvar J, Boelaert M. Visceral leishmaniasis: what are the needs for diagnosis, treatment and control? Nat Rev Microbiol. 2007;5(11):873–82.CrossRefPubMed
3.
go back to reference Mubayi A, Castillo-Chavez C, Chowell G, Kribs-Zaleta C, Ali Siddiqui N, Kumar N, Das P. Transmission dynamics and underreporting of kala-azar in the Indian state of Bihar. J Theor Biol. 2010;262(1):177–85.CrossRefPubMed Mubayi A, Castillo-Chavez C, Chowell G, Kribs-Zaleta C, Ali Siddiqui N, Kumar N, Das P. Transmission dynamics and underreporting of kala-azar in the Indian state of Bihar. J Theor Biol. 2010;262(1):177–85.CrossRefPubMed
6.
go back to reference Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet infect Dis. 2002;2(8):494–501.CrossRefPubMed Guerin PJ, Olliaro P, Sundar S, Boelaert M, Croft SL, Desjeux P, Wasunna MK, Bryceson AD. Visceral leishmaniasis: current status of control, diagnosis, and treatment, and a proposed research and development agenda. Lancet infect Dis. 2002;2(8):494–501.CrossRefPubMed
7.
go back to reference Singh OP, Hasker E, Boelaert M, Sundar S. Elimination of visceral leishmaniasis on the indian subcontinent. Lancet Infect Dis. 2016;16(12):304–9.CrossRef Singh OP, Hasker E, Boelaert M, Sundar S. Elimination of visceral leishmaniasis on the indian subcontinent. Lancet Infect Dis. 2016;16(12):304–9.CrossRef
8.
go back to reference Das VNR, Pandey RN, Siddiqui NA, Chapman LA, Kumar V, Pandey K, Matlashewski G, Das P. Longitudinal study of transmission in households with visceral leishmaniasis, asymptomatic infections and pkdl in highly endemic villages in Bihar, India. PLoS Negl Trop Dis. 2016;10(12):0005196.CrossRef Das VNR, Pandey RN, Siddiqui NA, Chapman LA, Kumar V, Pandey K, Matlashewski G, Das P. Longitudinal study of transmission in households with visceral leishmaniasis, asymptomatic infections and pkdl in highly endemic villages in Bihar, India. PLoS Negl Trop Dis. 2016;10(12):0005196.CrossRef
10.
go back to reference Le Rutte EA, Chapman LA, Coffeng LE, Jervis S, Hasker EC, Dwivedi S, Karthick M, Das A, Mahapatra T, Chaudhuri I, et al. Elimination of visceral leishmaniasis in the Indian subcontinent: a comparison of predictions from three transmission models. Epidemics. 2017;18:67–80.CrossRefPubMedPubMedCentral Le Rutte EA, Chapman LA, Coffeng LE, Jervis S, Hasker EC, Dwivedi S, Karthick M, Das A, Mahapatra T, Chaudhuri I, et al. Elimination of visceral leishmaniasis in the Indian subcontinent: a comparison of predictions from three transmission models. Epidemics. 2017;18:67–80.CrossRefPubMedPubMedCentral
11.
go back to reference Le Rutte EA, Coffeng LE, Bontje DM, Hasker EC, Postigo JAR, Argaw D, Boelaert MC, De Vlas SJ. Feasibility of eliminating visceral leishmaniasis from the Indian subcontinent: explorations with a set of deterministic age-structured transmission models. Parasites Vectors. 2016;9(1):1.CrossRef Le Rutte EA, Coffeng LE, Bontje DM, Hasker EC, Postigo JAR, Argaw D, Boelaert MC, De Vlas SJ. Feasibility of eliminating visceral leishmaniasis from the Indian subcontinent: explorations with a set of deterministic age-structured transmission models. Parasites Vectors. 2016;9(1):1.CrossRef
12.
go back to reference Mondal D, Singh SP, Kumar N, Joshi A, Sundar S, Das P, Siddhivinayak H, Kroeger A, Boelaert M. Visceral leishmaniasis elimination programme in India, Bangladesh, and Nepal: reshaping the case finding/case management strategy. PLoS Negl Trop Dis. 2009;3(1):355.CrossRef Mondal D, Singh SP, Kumar N, Joshi A, Sundar S, Das P, Siddhivinayak H, Kroeger A, Boelaert M. Visceral leishmaniasis elimination programme in India, Bangladesh, and Nepal: reshaping the case finding/case management strategy. PLoS Negl Trop Dis. 2009;3(1):355.CrossRef
14.
go back to reference Chowdhury R, Kumar V, Mondal D, Das ML, Das P, Dash AP, Kroeger A. Implication of vector characteristics of phlebotomus argentipes in the kala-azar elimination programme in the Indian sub-continent. Pathog Global Health. 2016;110(3):87–96.CrossRef Chowdhury R, Kumar V, Mondal D, Das ML, Das P, Dash AP, Kroeger A. Implication of vector characteristics of phlebotomus argentipes in the kala-azar elimination programme in the Indian sub-continent. Pathog Global Health. 2016;110(3):87–96.CrossRef
15.
go back to reference Dhillon G. National vector borne disease control programme—a glimpse. J Indian Med Assoc. 2008;106(10):639.PubMed Dhillon G. National vector borne disease control programme—a glimpse. J Indian Med Assoc. 2008;106(10):639.PubMed
16.
go back to reference Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8(4):1002588.CrossRef Smith DL, Battle KE, Hay SI, Barker CM, Scott TW, McKenzie FE. Ross, macdonald, and a theory for the dynamics and control of mosquito-transmitted pathogens. PLoS Pathog. 2012;8(4):1002588.CrossRef
17.
go back to reference Hasker E, Singh SP, Malaviya P, Picado A, Gidwani K, Singh RP, Menten J, Boelaert M, Sundar S. Visceral leishmaniasis in rural Bihar, India. Emerg Infect Dis. 2012;18(10):1662.CrossRefPubMedPubMedCentral Hasker E, Singh SP, Malaviya P, Picado A, Gidwani K, Singh RP, Menten J, Boelaert M, Sundar S. Visceral leishmaniasis in rural Bihar, India. Emerg Infect Dis. 2012;18(10):1662.CrossRefPubMedPubMedCentral
18.
go back to reference Dhiman R, Sen A. Epidemiology of kala-azar in rural Bihar (India) using village as a component unit of study. Indian J Med Res. 1991;93:155–60.PubMed Dhiman R, Sen A. Epidemiology of kala-azar in rural Bihar (India) using village as a component unit of study. Indian J Med Res. 1991;93:155–60.PubMed
19.
go back to reference Ranjan A, Sur D, Singh VP, Siddique NA, Manna B, Lal CS, Sinha PK, Kishore K, Bhattacharya SK. Risk factors for indian kala-azar. Am J Trop Med Hyg. 2005;73(1):74–8.PubMed Ranjan A, Sur D, Singh VP, Siddique NA, Manna B, Lal CS, Sinha PK, Kishore K, Bhattacharya SK. Risk factors for indian kala-azar. Am J Trop Med Hyg. 2005;73(1):74–8.PubMed
20.
go back to reference Sinha P, Ranjan A, Singh V, Das V, Pandey K, Kumar N, Verma N, Lal C, Sur D, Manna B, et al. Visceral leishmaniasis (kala-azar)| the Bihar (India) perspective. J Infect. 2006;53(1):60–4.CrossRefPubMed Sinha P, Ranjan A, Singh V, Das V, Pandey K, Kumar N, Verma N, Lal C, Sur D, Manna B, et al. Visceral leishmaniasis (kala-azar)| the Bihar (India) perspective. J Infect. 2006;53(1):60–4.CrossRefPubMed
21.
go back to reference Bern C, Haque R, Chowdhury R, Ali M, Kurkjian KM, Vaz L, Amann J, Wahed M, Wagatsuma Y, Breiman RF, et al. The epidemiology of visceral leishmaniasis and asymptomatic leishmanial infection in a highly endemic Bangladeshi village. Am J Trop Med Hyg. 2007;76(5):909–14.PubMed Bern C, Haque R, Chowdhury R, Ali M, Kurkjian KM, Vaz L, Amann J, Wahed M, Wagatsuma Y, Breiman RF, et al. The epidemiology of visceral leishmaniasis and asymptomatic leishmanial infection in a highly endemic Bangladeshi village. Am J Trop Med Hyg. 2007;76(5):909–14.PubMed
22.
go back to reference Nandy A, Neogy A, Chowdhury A. Leishmanin test survey in an endemic village of indian kala-azar near Calcutta. Ann Trop Med Parasitol. 1987;81(6):693–9.CrossRefPubMed Nandy A, Neogy A, Chowdhury A. Leishmanin test survey in an endemic village of indian kala-azar near Calcutta. Ann Trop Med Parasitol. 1987;81(6):693–9.CrossRefPubMed
23.
go back to reference Barnett PG, Singh S, Bern C, Hightower AW, Sundar S. Virgin soil: the spread of visceral leishmaniasis into Uttar Pradesh, India. Am J Trop Med Hyg. 2005;73(4):720–5.PubMed Barnett PG, Singh S, Bern C, Hightower AW, Sundar S. Virgin soil: the spread of visceral leishmaniasis into Uttar Pradesh, India. Am J Trop Med Hyg. 2005;73(4):720–5.PubMed
24.
go back to reference Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, et al. Risk factors for kala-azar in Bangladesh. Emerg Infect Dis. 2005;11:655.CrossRefPubMedPubMedCentral Bern C, Hightower AW, Chowdhury R, Ali M, Amann J, Wagatsuma Y, Haque R, Kurkjian K, Vaz LE, Begum M, et al. Risk factors for kala-azar in Bangladesh. Emerg Infect Dis. 2005;11:655.CrossRefPubMedPubMedCentral
25.
go back to reference Bern C, Joshi AB, Jha SN, Das ML, Hightower A, Thakur G, Bista MB. Factors associated with visceral leishmaniasis in Nepal: bed-net use is strongly protective. Am J Trop Med Hyg. 2000;63(3):184–8.CrossRefPubMed Bern C, Joshi AB, Jha SN, Das ML, Hightower A, Thakur G, Bista MB. Factors associated with visceral leishmaniasis in Nepal: bed-net use is strongly protective. Am J Trop Med Hyg. 2000;63(3):184–8.CrossRefPubMed
26.
go back to reference Schenkel K, Rijal S, Koirala S, Koirala S, Vanlerberghe V, Van der Stuyft P, Gramiccia M, Boelaert M. Visceral leishmaniasis in southeastern Nepal: a cross-sectional survey on leishmania donovani infection and its risk factors. Trop Med Int Health. 2006;11(12):1792–9.CrossRefPubMed Schenkel K, Rijal S, Koirala S, Koirala S, Vanlerberghe V, Van der Stuyft P, Gramiccia M, Boelaert M. Visceral leishmaniasis in southeastern Nepal: a cross-sectional survey on leishmania donovani infection and its risk factors. Trop Med Int Health. 2006;11(12):1792–9.CrossRefPubMed
27.
go back to reference Saha S, Ramachandran R, Hutin YJ, Gupte MD. Visceral leishmaniasis is preventable in a highly endemic village in West Bengal, India. Trans R Soc Trop Med Hyg. 2009;103(7):737–42.CrossRefPubMed Saha S, Ramachandran R, Hutin YJ, Gupte MD. Visceral leishmaniasis is preventable in a highly endemic village in West Bengal, India. Trans R Soc Trop Med Hyg. 2009;103(7):737–42.CrossRefPubMed
28.
go back to reference Rukunuzzaman M, Rahman M. Epidemiological study of risk factors related to childhood visceral leishmaniasis. MMJ. 2008;17(1):46–50.PubMed Rukunuzzaman M, Rahman M. Epidemiological study of risk factors related to childhood visceral leishmaniasis. MMJ. 2008;17(1):46–50.PubMed
29.
go back to reference Dinesh D, Ranjan A, Palit A, Kishore K, Kar S. Seasonal and nocturnal landing/biting behaviour of phlebotomus argentipes (diptera: Psychodidae). Ann Trop Med Parasitol. 2001;95(2):197–202.CrossRefPubMed Dinesh D, Ranjan A, Palit A, Kishore K, Kar S. Seasonal and nocturnal landing/biting behaviour of phlebotomus argentipes (diptera: Psychodidae). Ann Trop Med Parasitol. 2001;95(2):197–202.CrossRefPubMed
30.
go back to reference Artzy-Randrup Y, Alonso D, Pascual M. Transmission intensity and drug resistance in malaria population dynamics: implications for climate change. PLoS ONE. 2010;5(10):13588.CrossRef Artzy-Randrup Y, Alonso D, Pascual M. Transmission intensity and drug resistance in malaria population dynamics: implications for climate change. PLoS ONE. 2010;5(10):13588.CrossRef
31.
go back to reference Parham PE, Michael E. Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect. 2010;118(5):620.CrossRefPubMed Parham PE, Michael E. Modeling the effects of weather and climate change on malaria transmission. Environ Health Perspect. 2010;118(5):620.CrossRefPubMed
32.
go back to reference Gorahava KK, Rosenberger JM, Mubayi A. Optimizing insecticide allocation strategies based on houses and livestock shelters for visceral leishmaniasis control in Bihar, India. Am J Trop Med Hyg. 2015;93:114–22.CrossRefPubMedPubMedCentral Gorahava KK, Rosenberger JM, Mubayi A. Optimizing insecticide allocation strategies based on houses and livestock shelters for visceral leishmaniasis control in Bihar, India. Am J Trop Med Hyg. 2015;93:114–22.CrossRefPubMedPubMedCentral
33.
go back to reference Peters D, Yazbeck A, Ramana G, Sharma R, Pritchett L, Wagstaff A. Raising the sights: better health systems for India’s poor. The World Bank (Health, Nutrition, Population Sector Unit) 2001;173. Peters D, Yazbeck A, Ramana G, Sharma R, Pritchett L, Wagstaff A. Raising the sights: better health systems for India’s poor. The World Bank (Health, Nutrition, Population Sector Unit) 2001;173.
34.
go back to reference Van de Poel E, Speybroeck N. Decomposing malnutrition inequalities between scheduled castes and tribes and the remaining indian population. Ethn Health. 2009;14(3):271–87.CrossRefPubMed Van de Poel E, Speybroeck N. Decomposing malnutrition inequalities between scheduled castes and tribes and the remaining indian population. Ethn Health. 2009;14(3):271–87.CrossRefPubMed
35.
go back to reference Pascual Martinez F, Picado A, Roddy P, Palma P. Low castes have poor access to visceral leishmaniasis treatment in Bihar, India. Trop Med Int Health. 2012;17(5):666–73.CrossRefPubMed Pascual Martinez F, Picado A, Roddy P, Palma P. Low castes have poor access to visceral leishmaniasis treatment in Bihar, India. Trop Med Int Health. 2012;17(5):666–73.CrossRefPubMed
36.
go back to reference Matlashewski G, Arana B, Kroeger A, Battacharya S, Sundar S, Das P, Sinha PK, Rijal S, Mondal D, Zilberstein D, et al. Visceral leishmaniasis: elimination with existing interventions. Lancet Infect Dis. 2011;11(4):322–5.CrossRefPubMed Matlashewski G, Arana B, Kroeger A, Battacharya S, Sundar S, Das P, Sinha PK, Rijal S, Mondal D, Zilberstein D, et al. Visceral leishmaniasis: elimination with existing interventions. Lancet Infect Dis. 2011;11(4):322–5.CrossRefPubMed
37.
go back to reference Den Boer M, Argaw D, Jannin J, Alvar J. Leishmaniasis impact and treatment access. Clin Microbiol Infect. 2011;17(10):1471–7.CrossRef Den Boer M, Argaw D, Jannin J, Alvar J. Leishmaniasis impact and treatment access. Clin Microbiol Infect. 2011;17(10):1471–7.CrossRef
38.
go back to reference Rijal S, Koirala S, Van der Stuyft P, Boelaert M. The economic burden of visceral leishmaniasis for households in Nepal. Trans R Soc Trop Med Hyg. 2006;100(9):838–41.CrossRefPubMed Rijal S, Koirala S, Van der Stuyft P, Boelaert M. The economic burden of visceral leishmaniasis for households in Nepal. Trans R Soc Trop Med Hyg. 2006;100(9):838–41.CrossRefPubMed
39.
go back to reference Magalhães DFd, Silva JAd, Haddad JPA, Moreira EC, Fonseca MIM, Ornelas MLLd, Borges BKA, Luz ZMPd. Dissemination of information on visceral leishmaniasis from schoolchildren to their families: a sustainable model for controlling the disease. Cadernos de Saúde Pública. 2009;25(7):1642–6.CrossRefPubMed Magalhães DFd, Silva JAd, Haddad JPA, Moreira EC, Fonseca MIM, Ornelas MLLd, Borges BKA, Luz ZMPd. Dissemination of information on visceral leishmaniasis from schoolchildren to their families: a sustainable model for controlling the disease. Cadernos de Saúde Pública. 2009;25(7):1642–6.CrossRefPubMed
40.
go back to reference Uranw S, Ostyn B, Dorlo TP, Hasker E, Dujardin B, Dujardin J-C, Rijal S, Boelaert M. Adherence to miltefosine treatment for visceral leishmaniasis under routine conditions in Nepal. Trop Med Int Health. 2013;18(2):179–87.CrossRefPubMed Uranw S, Ostyn B, Dorlo TP, Hasker E, Dujardin B, Dujardin J-C, Rijal S, Boelaert M. Adherence to miltefosine treatment for visceral leishmaniasis under routine conditions in Nepal. Trop Med Int Health. 2013;18(2):179–87.CrossRefPubMed
41.
go back to reference Mittal C, Gupta S, et al. Noncompliance to dots: how it can be decreased. Indian J Commun Med. 2011;36(1):27.CrossRef Mittal C, Gupta S, et al. Noncompliance to dots: how it can be decreased. Indian J Commun Med. 2011;36(1):27.CrossRef
42.
go back to reference Uranw S, Ostyn B, Rijal A, Devkota S, Khanal B, Menten J, Boelaert M, Rijal S. Post-kala-azar dermal leishmaniasis in Nepal: a retrospective cohort study (2000–2010). PLoS Negl Trop Dis. 2011;5(12):1433.CrossRef Uranw S, Ostyn B, Rijal A, Devkota S, Khanal B, Menten J, Boelaert M, Rijal S. Post-kala-azar dermal leishmaniasis in Nepal: a retrospective cohort study (2000–2010). PLoS Negl Trop Dis. 2011;5(12):1433.CrossRef
43.
go back to reference Desjeux P, Ghosh R, Dhalaria P, Strub-Wourgaft N, Zijlstra E. Report of the post kala-azar dermal leishmaniasis (pkdl) consortium meeting, New Delhi, India, 27–29 June 2012. Parasit Vectors. 2013;6:196.CrossRefPubMedPubMedCentral Desjeux P, Ghosh R, Dhalaria P, Strub-Wourgaft N, Zijlstra E. Report of the post kala-azar dermal leishmaniasis (pkdl) consortium meeting, New Delhi, India, 27–29 June 2012. Parasit Vectors. 2013;6:196.CrossRefPubMedPubMedCentral
44.
go back to reference Thakur C, Meenakshi Thakur AK, Thakur S, et al. Newer strategies for the kala-azar elimination programme in india. Indian J Med Res. 2009;129(1):102–4.PubMed Thakur C, Meenakshi Thakur AK, Thakur S, et al. Newer strategies for the kala-azar elimination programme in india. Indian J Med Res. 2009;129(1):102–4.PubMed
45.
go back to reference Mubayi A, Zaleta CK, Martcheva M, Castillo-Chavez C. A cost-based comparison of quarantine strategies for new emerging diseases. Math Biosci Eng. 2010;7(3):687–717.CrossRefPubMed Mubayi A, Zaleta CK, Martcheva M, Castillo-Chavez C. A cost-based comparison of quarantine strategies for new emerging diseases. Math Biosci Eng. 2010;7(3):687–717.CrossRefPubMed
46.
go back to reference Rock KS, le Rutte EA, de Vlas SJ, Adams ER, Medley GF, Hollingsworth TD. Uniting mathematics and biology for control of visceral leishmaniasis. Trends Parasitol. 2015;31(6):251–9.CrossRefPubMed Rock KS, le Rutte EA, de Vlas SJ, Adams ER, Medley GF, Hollingsworth TD. Uniting mathematics and biology for control of visceral leishmaniasis. Trends Parasitol. 2015;31(6):251–9.CrossRefPubMed
47.
go back to reference Dye C, Wolpert DM. Earthquakes, influenza and cycles of indian kala-azar. Trans R Soc Trop Med Hyg. 1988;82(6):843–50.CrossRefPubMed Dye C, Wolpert DM. Earthquakes, influenza and cycles of indian kala-azar. Trans R Soc Trop Med Hyg. 1988;82(6):843–50.CrossRefPubMed
48.
go back to reference Hasibeder G, Dye C, Carpenter J. Mathematical modelling and theory for estimating the basic reproduction number of canine leishmaniasis. Parasitology. 1992;105(01):43–53.CrossRefPubMed Hasibeder G, Dye C, Carpenter J. Mathematical modelling and theory for estimating the basic reproduction number of canine leishmaniasis. Parasitology. 1992;105(01):43–53.CrossRefPubMed
49.
go back to reference Dye C, Killick-Kendrick R, Vitutia MM, Walton R, Killick-Kendrick M, Harith AE, Guy MW, Cañavate M-C, Hasibeder G. Epidemiology of canine leishmaniasis: prevalence, incidence and basic reproduction number calculated from a cross-sectional serological survey on the island of Gozo, Malta. Parasitology. 1992;105(01):35–41. doi:10.1017/S0031182000073662.CrossRefPubMed Dye C, Killick-Kendrick R, Vitutia MM, Walton R, Killick-Kendrick M, Harith AE, Guy MW, Cañavate M-C, Hasibeder G. Epidemiology of canine leishmaniasis: prevalence, incidence and basic reproduction number calculated from a cross-sectional serological survey on the island of Gozo, Malta. Parasitology. 1992;105(01):35–41. doi:10.​1017/​S003118200007366​2.CrossRefPubMed
50.
51.
go back to reference Stauch A, Sarkar RR, Picado A, Ostyn B, Sundar S, Rijal S, Boelaert M, Dujardin J-C, Duerr H-P. Visceral leishmaniasis in the indian subcontinent: modelling epidemiology and control. PLoS Negl Trop Dis. 2011;5(11):1405.CrossRef Stauch A, Sarkar RR, Picado A, Ostyn B, Sundar S, Rijal S, Boelaert M, Dujardin J-C, Duerr H-P. Visceral leishmaniasis in the indian subcontinent: modelling epidemiology and control. PLoS Negl Trop Dis. 2011;5(11):1405.CrossRef
52.
go back to reference Stauch A, Duerr H-P, Dujardin J-C, Vanaerschot M, Sundar S, Eichner M. Treatment of visceral leishmaniasis: model-based analyses on the spread of antimony-resistant l. Donovani in Bihar, India. PLoS Negl Trop Dis. 2012;6(12):1973.CrossRef Stauch A, Duerr H-P, Dujardin J-C, Vanaerschot M, Sundar S, Eichner M. Treatment of visceral leishmaniasis: model-based analyses on the spread of antimony-resistant l. Donovani in Bihar, India. PLoS Negl Trop Dis. 2012;6(12):1973.CrossRef
53.
go back to reference Stauch A, Duerr H-P, Picado A, Ostyn B, Sundar S, Rijal S, Boelaert M, Dujardin J-C, Eichner M. Model-based investigations of different vector-related intervention strategies to eliminate visceral leishmaniasis on the indian subcontinent. PLoS Negl Trop Dis. 2014;8(4):2810.CrossRef Stauch A, Duerr H-P, Picado A, Ostyn B, Sundar S, Rijal S, Boelaert M, Dujardin J-C, Eichner M. Model-based investigations of different vector-related intervention strategies to eliminate visceral leishmaniasis on the indian subcontinent. PLoS Negl Trop Dis. 2014;8(4):2810.CrossRef
54.
go back to reference ELmojtaba IM, Mugisha J, Hashim MH. Mathematical analysis of the dynamics of visceral leishmaniasis in the Sudan. Appl Math Comput. 2010;217(6):2567–78. ELmojtaba IM, Mugisha J, Hashim MH. Mathematical analysis of the dynamics of visceral leishmaniasis in the Sudan. Appl Math Comput. 2010;217(6):2567–78.
55.
go back to reference ELmojtaba IM, Mugisha J, Hashim MH. Modelling the role of cross-immunity between two different strains of leishmania. Nonlinear Anal Real World Appl. 2010;11(3):2175–89.CrossRef ELmojtaba IM, Mugisha J, Hashim MH. Modelling the role of cross-immunity between two different strains of leishmania. Nonlinear Anal Real World Appl. 2010;11(3):2175–89.CrossRef
56.
go back to reference ELmojtaba IM, Mugisha J, Hashim MH. Vaccination model for visceral leishmaniasis with infective immigrants. Math Methods Appl Sci. 2013;36(2):216–26.CrossRef ELmojtaba IM, Mugisha J, Hashim MH. Vaccination model for visceral leishmaniasis with infective immigrants. Math Methods Appl Sci. 2013;36(2):216–26.CrossRef
57.
go back to reference Sevá AP, Ovallos FG, Amaku M, Carrillo E, Moreno J, Galati EA, Lopes EG, Soares RM, Ferreira F. Canine-based strategies for prevention and control of visceral leishmaniasis in Brazil. PLoS ONE. 2016;11(7):0160058.CrossRef Sevá AP, Ovallos FG, Amaku M, Carrillo E, Moreno J, Galati EA, Lopes EG, Soares RM, Ferreira F. Canine-based strategies for prevention and control of visceral leishmaniasis in Brazil. PLoS ONE. 2016;11(7):0160058.CrossRef
58.
go back to reference Aparicio JP, Castillo-Chavez C. Mathematical modelling of tuberculosis epidemics. Math Biosci Eng. 2009;6(2):209–37.CrossRefPubMed Aparicio JP, Castillo-Chavez C. Mathematical modelling of tuberculosis epidemics. Math Biosci Eng. 2009;6(2):209–37.CrossRefPubMed
59.
go back to reference Lipsitch M, Levin B. Population dynamics of tuberculosis treatment: mathematical models of the roles of non-compliance and bacterial heterogeneity in the evolution of drug resistance. Int J Tuberc Lung Dis. 1998;2(3):187–99.PubMed Lipsitch M, Levin B. Population dynamics of tuberculosis treatment: mathematical models of the roles of non-compliance and bacterial heterogeneity in the evolution of drug resistance. Int J Tuberc Lung Dis. 1998;2(3):187–99.PubMed
60.
go back to reference Vaughan PW, Rogers EM, Singhal A, Swalehe RM. Entertainment-education and HIV/AIDS prevention: a field experiment in Tanzania. J Health Commun. 2000;5(sup1):81–100.CrossRefPubMed Vaughan PW, Rogers EM, Singhal A, Swalehe RM. Entertainment-education and HIV/AIDS prevention: a field experiment in Tanzania. J Health Commun. 2000;5(sup1):81–100.CrossRefPubMed
61.
go back to reference Mason JE, England DA, Denton BT, Smith SA, Kurt M, Shah ND. Optimizing statin treatment decisions for diabetes patients in the presence of uncertain future adherence. Med Decis Mak. 2012;32(1):154–66.CrossRef Mason JE, England DA, Denton BT, Smith SA, Kurt M, Shah ND. Optimizing statin treatment decisions for diabetes patients in the presence of uncertain future adherence. Med Decis Mak. 2012;32(1):154–66.CrossRef
62.
go back to reference Hallett TB, Gregson S, Mugurungi O, Gonese E, Garnett GP. Assessing evidence for behaviour change affecting the course of hiv epidemics: a new mathematical modelling approach and application to data from Zimbabwe. Epidemics. 2009;1(2):108–17.CrossRefPubMed Hallett TB, Gregson S, Mugurungi O, Gonese E, Garnett GP. Assessing evidence for behaviour change affecting the course of hiv epidemics: a new mathematical modelling approach and application to data from Zimbabwe. Epidemics. 2009;1(2):108–17.CrossRefPubMed
63.
go back to reference Mushayabasa S, Bhunu C, et al. Assessing the impact of educational campaigns on controlling hcv among women in prison settings. Commun Nonlinear Sci Numer Simul. 2012;17(4):1714–24. Mushayabasa S, Bhunu C, et al. Assessing the impact of educational campaigns on controlling hcv among women in prison settings. Commun Nonlinear Sci Numer Simul. 2012;17(4):1714–24.
64.
go back to reference Fenichel EP, Castillo-Chavez C, Ceddia M, Chowell G, Parra PAG, Hickling GJ, Holloway G, Horan R, Morin B, Perrings C, et al. Adaptive human behavior in epidemiological models. Proc Natl Acad Sci. 2011;108(15):6306–11.CrossRefPubMedPubMedCentral Fenichel EP, Castillo-Chavez C, Ceddia M, Chowell G, Parra PAG, Hickling GJ, Holloway G, Horan R, Morin B, Perrings C, et al. Adaptive human behavior in epidemiological models. Proc Natl Acad Sci. 2011;108(15):6306–11.CrossRefPubMedPubMedCentral
65.
go back to reference Perrings C, Castillo-Chavez C, Chowell G, Daszak P, Fenichel EP, Finnoff D, Horan RD, Kilpatrick AM, Kinzig AP, Kuminoff NV, et al. Merging economics and epidemiology to improve the prediction and management of infectious disease. EcoHealth. 2014;11(4):464–75.CrossRefPubMedPubMedCentral Perrings C, Castillo-Chavez C, Chowell G, Daszak P, Fenichel EP, Finnoff D, Horan RD, Kilpatrick AM, Kinzig AP, Kuminoff NV, et al. Merging economics and epidemiology to improve the prediction and management of infectious disease. EcoHealth. 2014;11(4):464–75.CrossRefPubMedPubMedCentral
68.
go back to reference Pandey A, Mubayi A, Medlock J. Comparing vector-host and sir models for dengue transmission. Math Biosci. 2013;246(2):252–9.CrossRefPubMed Pandey A, Mubayi A, Medlock J. Comparing vector-host and sir models for dengue transmission. Math Biosci. 2013;246(2):252–9.CrossRefPubMed
69.
go back to reference Rogers L. Fevers in the tropics. London: H. Frowde, Hodder & Stoughton; 1908. Rogers L. Fevers in the tropics. London: H. Frowde, Hodder & Stoughton; 1908.
70.
go back to reference Young TM. Fourteen years’ experience with kala-azar work in Assam. Trans R Soc Trop Med Hyg. 1924;18(3):81–18786397.CrossRef Young TM. Fourteen years’ experience with kala-azar work in Assam. Trans R Soc Trop Med Hyg. 1924;18(3):81–18786397.CrossRef
71.
go back to reference Sen Gupta P, et al. A report on kala-azar in Assam. Indian Med Gaz. 1951;86(6 & 7):266–71. Sen Gupta P, et al. A report on kala-azar in Assam. Indian Med Gaz. 1951;86(6 & 7):266–71.
72.
go back to reference Olliaro PL, Guerin PJ, Gerstl S, Haaskjold AA, Rottingen J-A, Sundar S. Treatment options for visceral leishmaniasis: a systematic review of clinical studies done in India, 1980–2004. Lancet Infect Dis. 2005;5(12):763–74.CrossRefPubMed Olliaro PL, Guerin PJ, Gerstl S, Haaskjold AA, Rottingen J-A, Sundar S. Treatment options for visceral leishmaniasis: a systematic review of clinical studies done in India, 1980–2004. Lancet Infect Dis. 2005;5(12):763–74.CrossRefPubMed
Metadata
Title
Challenges in modeling complexity of neglected tropical diseases: a review of dynamics of visceral leishmaniasis in resource limited settings
Authors
Swati DebRoy
Olivia Prosper
Austin Mishoe
Anuj Mubayi
Publication date
01-12-2017
Publisher
BioMed Central
Published in
Emerging Themes in Epidemiology / Issue 1/2017
Electronic ISSN: 1742-7622
DOI
https://doi.org/10.1186/s12982-017-0065-3

Other articles of this Issue 1/2017

Emerging Themes in Epidemiology 1/2017 Go to the issue