Leishmaniasis worldwide and global estimates of its incidence.
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Journal: 2012/October - PLoS ONE
ISSN: 1932-6203
Abstract:
As part of a World Health Organization-led effort to update the empirical evidence base for the leishmaniases, national experts provided leishmaniasis case data for the last 5 years and information regarding treatment and control in their respective countries and a comprehensive literature review was conducted covering publications on leishmaniasis in 98 countries and three territories (see 'Leishmaniasis Country Profiles Text S1, S2, S3, S4, S5, S6, S7, S8, S9, S10, S11, S12, S13, S14, S15, S16, S17, S18, S19, S20, S21, S22, S23, S24, S25, S26, S27, S28, S29, S30, S31, S32, S33, S34, S35, S36, S37, S38, S39, S40, S41, S42, S43, S44, S45, S46, S47, S48, S49, S50, S51, S52, S53, S54, S55, S56, S57, S58, S59, S60, S61, S62, S63, S64, S65, S66, S67, S68, S69, S70, S71, S72, S73, S74, S75, S76, S77, S78, S79, S80, S81, S82, S83, S84, S85, S86, S87, S88, S89, S90, S91, S92, S93, S94, S95, S96, S97, S98, S99, S100, S101'). Additional information was collated during meetings conducted at WHO regional level between 2007 and 2011. Two questionnaires regarding epidemiology and drug access were completed by experts and national program managers. Visceral and cutaneous leishmaniasis incidence ranges were estimated by country and epidemiological region based on reported incidence, underreporting rates if available, and the judgment of national and international experts. Based on these estimates, approximately 0.2 to 0.4 cases and 0.7 to 1.2 million VL and CL cases, respectively, occur each year. More than 90% of global VL cases occur in six countries: India, Bangladesh, Sudan, South Sudan, Ethiopia and Brazil. Cutaneous leishmaniasis is more widely distributed, with about one-third of cases occurring in each of three epidemiological regions, the Americas, the Mediterranean basin, and western Asia from the Middle East to Central Asia. The ten countries with the highest estimated case counts, Afghanistan, Algeria, Colombia, Brazil, Iran, Syria, Ethiopia, North Sudan, Costa Rica and Peru, together account for 70 to 75% of global estimated CL incidence. Mortality data were extremely sparse and generally represent hospital-based deaths only. Using an overall case-fatality rate of 10%, we reach a tentative estimate of 20,000 to 40,000 leishmaniasis deaths per year. Although the information is very poor in a number of countries, this is the first in-depth exercise to better estimate the real impact of leishmaniasis. These data should help to define control strategies and reinforce leishmaniasis advocacy.
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PLoS ONE. Dec/31/2011; 7(5)
Published online May/30/2012
PMID: 22693548
PMC: 3365071

Leishmaniasis Worldwide and Global Estimates of Its Incidence

Abstract

Introduction

Although estimated to cause the ninth largest disease burden among individual infectious diseases, leishmaniasis is largely ignored in discussions of tropical disease priorities [1], [2]. This consignment to critical oblivion results from its complex epidemiology and ecology, the lack of simple, easily-applied tools for case management and the paucity of current incidence data, and often results in a failure on the part of policy-makers to recognize its importance [3], [4]. Based on the World Health Assembly Resolution 2007/60.13, the World Health Organization (WHO) convened the Expert Committee on Leishmaniasis in March 2010, which subsequently issued the first updated technical report on leishmaniasis in more than 20 years [5], [6]. Both the WHA Resolution and the Expert Committee report highlighted the need to update the epidemiological evidence base in order to plan appropriate approaches to the control of leishmaniasis.

Estimates of disease burden are widely used by policy-makers and funding organizations to establish priorities [7], [8], [9], [10]. These estimates are most commonly expressed as disability-adjusted life years (DALYs) lost, a measurement first promoted in the 1993 World Development Report and the focus of intense scrutiny ever since [11], [12], [13]. The accuracy of this measure depends on the reliability of the incidence, duration, severity and mortality data for a given condition, as well as the underlying assumptions used in the calculations [7], [14]. Although a new round of global disease burden estimation is currently underway, empirical data collection and field validation are neither included nor supported as part of the exercise [15].

10.1371/journal.pone.0035671.t001Table 1
Reported and estimated incidence of visceral leishmaniasis in the American region.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Argentina82004–200820to301
Bolivia02008
Brazil34812003–20074200to63002
Colombia602004–200870to1102
El Salvadorno data
Guatemala152004–200820to302
Honduras62004–20087to102
Mexico72004–20088to122
Nicaragua32003–20073to52
Paraguay482004–2008100to2001
Venezuela402004–200850to702
Region36684500to6800

1Underreporting considered moderate (2–4-fold) based on recent introduction of VL into the country.

2Underreporting considered mild (1.2–1.8-fold) based on data from Brazil [25].

10.1371/journal.pone.0035671.t002Table 2
Reported and estimated incidence of visceral leishmaniasis in the sub-Saharan African region.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Central African Republicno data
Cameroonno data
Chadno data
Cote d’Ivoire02004–2008
DR Congo02004–2008
Gambiano data
Mauritaniano data
Nigerno data
Nigeria12004–2008
Senegal02004–2008
Zambiano data
Region1
10.1371/journal.pone.0035671.t003Table 3
Reported and estimated incidence of visceral leishmaniasis in the East African region.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Djiboutino data
Eritrea1002008200to4001
Ethiopia18602004–20083700to74001
Kenya1452004–2008610to12002
Somalia67920091400to27001
Sudan37422005–200915,700to30,3002
South Sudan17562004–20087400to14,2002
Uganda2882004–2008350to5203
Region856929,400to56,700

1Underreporting considered moderate (2–4-fold).

2Underreporting considered severe (4.2–8.1-fold).

3Underreporting considered mild (1.2–1.8).

10.1371/journal.pone.0035671.t004Table 4
Reported and estimated incidence of visceral leishmaniasis in the Mediterranean region.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Albania1142004–2008140to2101
Algeria1112004–2008130to2001
Bosnia and Herzegovina22002–20052to31
Bulgaria72004–20088to121
Croatia52004–20086to81
Cyprus220082to41
Egypt120081to21
France182004–200820to301
Greece422004–200850to801
Israel22003–20073to41
Italy1342003–2007160to2401
Jordan02004–20080to0
Lebanon02004–20080to0
Libya32004–20085to102
Macedonia72005–20099to131
Malta22002–20053to41
Monacono data
Montenegro32004–20084to51
Morocco1522004–2008300to6102
Palestine52004–200810to202
Portugal152003–200720to301
Sloveniano data
Spain1172004–2008140to2101
Syria142004–200830to602
Tunisia892004–2008110to1601
Turkey292003–200760to1202
Region87512002000

1Underreporting considered mild (1.2–1.8-fold).

2Underreporting considered moderate (2–4-fold).

10.1371/journal.pone.0035671.t005Table 5
Reported and estimated incidence of visceral leishmaniasis in the Middle East to Central Asia.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Afghanistanno data
Armenia72004–200810to301
Azerbaijan282004–200860to1101
China3782004–2008760to15001
Georgia1642004–2008330to6601
Iran (Islamic Republic of)1492004–2008300to6001
Iraq17112004–20083400to68001
Kazakhstan12004–20082to41
Kyrgyzstan02004–2008
Oman12004–20082to41
Pakistanno data
Saudi Arabia342004–200840to602
Tajikistan152004–200830to601
Turkmenistan02004–2008
Ukraine22005–20084to71
Uzbekistan72004–200810to301
Yemen02004–200820to501
Region2496500010,000

1Underreporting considered moderate (2–4-fold).

2Underreporting considered mild (1.2–1.8).

10.1371/journal.pone.0035671.t006Table 6
Reported and estimated incidence of visceral leishmaniasis in the Indian subcontinent and Southeast Asia.
Reported VL cases/yearYears of reportEstimated annual VL incidence
Bangladesh62242004–200812,400to24,9001
Bhutan22005–200910to202
India34,9182004–2008146,700to282,8003
Nepal14772004–20083000to59001
Sri Lankano data6to104
Thailand22006–20105to105
Region42,623162,100to313,600

1Underreporting considered moderate (2.0–4.0-fold; based on lower proportion of cases treated in private sector compared to India).

2Underreporting range based on 2 assessments in Bihar [27], [28].

10.1371/journal.pone.0035671.t007Table 7
Reported and estimated incidence of cutaneous leishmaniasis in the American region.
Reported CL cases/yearYears of reportEstimated annual CL incidence
Argentina2612004–2008730to12001
Belizeno data
Bolivia26472004–20087400to12,2001
Brazil26,0082003–200772,800to119,6001
Colombia17,4202005–200948,800to80,1001
Costa Rica12492002–20063500to57001
Dominican Republicno data0to0
Ecuador17242004–20084800to79001
El Salvadorno data0to0
French Guyana2332004–2008650to11001
Guatemala6842004–20081900to31001
Guyana162006–200850to701
Honduras11592006–20083200to53001
Mexico8112004–20082300to37001
Nicaragua32222003–20079000to14,8001
Panama21882005–20096100to10,1001
Paraguay4312004–20081200to20001
Peru64052004–200817,900to29,5001
Suriname32005–20078to141
Venezuela24802004–20086900to11,4001
REGION66,941187,200307,800

1Underreporting considered mild (2.8–4.6-fold) based on data from Argentina [29].

10.1371/journal.pone.0035671.t008Table 8
Reported and estimated incidence of cutaneous leishmaniasis in the sub-Saharan African region.
Reported CL cases/yearYears of reportEstimated annual CL incidence
Burkina Fasono data
Cameroon552007–2009280to5501
Chadno data
Cote d’Ivoire12004–20085to101
DR Congo02009
Ghana272004–2008140to2701
Guineano data
Guinea-Bissauno data
Mali582004–2008290to5801
Mauritaniano data
Namibiano data
Nigerno data
Nigeria52004–200830to501
Senegal82004–200840to801
South Africano data
REGION155790to15001

1Underreporting considered moderate (5–10-fold).

10.1371/journal.pone.0035671.t009Table 9
Reported and estimated incidence of cutaneous leishmaniasis in the East African region.
Reported CL cases/yearYears of reportEstimated annual CL incidence
Djiboutino data
Eritrea502008250to5001
Ethiopiano data20,000to50,0002
Kenyano data
Sudanno data15,000to40,0003
South Sudanno data
REGION5035,300to90,500

1Underreporting considered moderate (5–10-fold).

2Based on conference report (Armauer Hansen Research Institute, Federal Ministry of Health of Ethiopia and World Health Organization. Consultative meeting for the control of cutaneous leishmaniasis in Ethiopia; June 4–5, 2011; Addis Ababa, Ethiopia).

3Based on estimates by Dr. Nuha Hamid, national project officer, WHO-Khartoum, Sudan (see Annex).

10.1371/journal.pone.0035671.t010Table 10
Reported and estimated incidence of cutaneous leishmaniasis in the Mediterranean.
Reported CL cases/yearYears of reportEstimated annual CL incidence
Albania62004–2008
Algeria44,0502004–2008123,300to202,6001
Bosnia and Herzegovina02008
Bulgaria02008
Croatia22004–20086to101
Cyprus12006–2008
Egypt47120081300to22001
France22004–20086to101
Greece32004–20088to131
Israel5792003–20071600to27001
Italy492003–2007140to2301
Jordan2272004–2008630to10001
Lebanon02004–2008
Libya35402004–20089900to16,3001
Macedonia02008
Malta02008
Monacono data
Montenegro02008
Morocco34302004–20089600to15,8001
Palestine2182005–2009610to10001
Portugal02004–2008
Sloveniano data
Spain02004–2008
Syria22,8822004–200864,100to105,3001
Tunisia76312004–200821,400to35,1001
Turkey24652003–20076900to11,3001
REGION85,555239,500393,600

1Underreporting considered mild (2.8–4.6) [29].

10.1371/journal.pone.0035671.t011Table 11
Reported and estimated incidence of cutaneous leishmaniasis in the Middle East to Central Asia.
Reported CL cases/yearYears of reportEstimated annual CL incidence
Afghanistan22,6202003–2007113,100to226,2001
Armenia02008
Azerbijan172004–200850to802
China02004–2008
Georgia52004–2008
Iran (Islamic Republic of)24,6302004–200869,000to113,3002
Iraq16552004–20088300to16,5003
Kazakhstan152004–200840to702
Kyrgyzstan02004–2008
Mongoliano data
Oman52004–200815to202
Pakistan77522004–200821,700to35,7002
Saudi Arabia34452004–20089600to15,8002
Tajikistan252007–2008125to2503
Turkmenistan992004–2008490to9903
Ukraine22004–200810to203
Uzbekistan1422004–2008710to14003
Yemen6032005–20093000to60003
REGION61,013226,200416,400

1Underreporting considered moderate (5–10-fold) based on estimates of incidence from population-based surveys [30].

2Underreporting considered mild (2.8–4.6) [29].

3Underreporting considered moderate (5–10-fold).

10.1371/journal.pone.0035671.t012Table 12
Reported and estimated incidence of cutaneous leishmaniasis in the Indian subcontinent.
Reported CL cases/yearYears of reportEstimated annual CL incidence
India1562005–20091000to20001
Sri Lanka3222004–2008900to15002
REGION4781900to3500

1Based on estimates by Dr RA Bumb, Department of Skin, STD and Leprosy, SP Medical College, Bikaner, Rajasthan, India.

2Underreporting considered mild (2.8–4.6) [29].

10.1371/journal.pone.0035671.t013Table 13
Global reported and estimated incidence of visceral leishmaniasis.
Reported VL cases/yearCountries with 5 years of dataEstimated annual VL incidence
Americas36628/11 (73%)4500to6800
Sub-Saharan Africa13/11 (27%)
East Africa85695/8 (63%)29,400to56,700
Mediterranean87521/26 (81%)1200to2000
Middle East to Central Asia249614/17 (82%)5000to10,000
South Asia42,6233/6 (50%)*162,100to313,600
Global total58,22754/79 (68%)202,200to389,100

*3/3 (100%) of high burden countries (India, Bangladesh, Nepal) reported 5 years of data. Reports incomplete for Sri Lanka, Bhutan and Thailand.

10.1371/journal.pone.0035671.t014Table 14
Global reported and estimated incidence of cutaneous leishmaniasis.
Reported CLcases/yearCountries with 5 yearsof dataEstimated annual CL incidence
Americas66,94114/20 (70%)187,200to307,800
Sub-Saharan Africa1555/15 (33%)770to1500
East Africa500/6 (0%)35,300to90,500
Mediterranean85,55517/26 (65%)239,500to393,600
Middle East to Central Asia61,01316/18 (89%)226,200to416,400
South Asia3222/2 (100%)1900to3500
Global total214,03653/87 (61%)690,900to1,213,300

The evidence base for the neglected tropical diseases (NTDs) is acknowledged to be particularly problematic [9], [16]. Leishmaniasis, like many other NTDs, occurs in a focal distribution and in remote locations, making extrapolation from official data sources difficult [4]. Visceral leishmaniasis (VL) results in death if not treated, the majority of leishmaniasis deaths go unrecognized, and even with treatment access, VL may result in case-fatality rates of 10–20% [17], [18], [19], [20], [21], [22]. Reported leishmaniasis case figures are widely acknowledged to represent gross underestimates of the true burden, but studies that measure the degree of underreporting are rare [23]. As part of the WHO effort to update the leishmaniasis evidence base, a series of regional meetings were held. National program managers and expert professionals were asked to provide detailed information on epidemiology, ecology, geographical distribution and trends, drug access and management of leishmaniasis for their respective countries. These data, accompanied by literature reviews, are compiled in extensive profiles of each endemic country or territory in the Annex of this publication (see ‘Leishmaniasis Country Profiles Text S1, S2, S3, S4, S5, S6, S7, S8, S9, S10, S11, S12, S13, S14, S15, S16, S17, S18, S19, S20, S21, S22, S23, S24, S25, S26, S27, S28, S29, S30, S31, S32, S33, S34, S35, S36, S37, S38, S39, S40, S41, S42, S43, S44, S45, S46, S47, S48, S49, S50, S51, S52, S53, S54, S55, S56, S57, S58, S59, S60, S61, S62, S63, S64, S65, S66, S67, S68, S69, S70, S71, S72, S73, S74, S75, S76, S77, S78, S79, S80, S81, S82, S83, S84, S85, S86, S87, S88, S89, S90, S91, S92, S93, S94, S95, S96, S97, S98, S99, S100, S101’). This paper focuses on an analysis of the findings, and estimates of leishmaniasis incidence derived from the epidemiological data.

Methods

From 2007 to 2010, WHO organized a series of regional meetings (EMRO countries, Geneva 2007; PAHO countries, Medellin 2008; EURO countries, Istanbul 2009; AFRO countries, Addis Ababa 2010; SEARO countries, Paro 2011). In preparation for each meeting, country representatives were asked to provide yearly reported VL and cutaneous leishmaniasis (CL) incidence data for at least the last 5 years prior to the meeting. In addition, an electronic epidemiological questionnaire was sent to the national control program managers and/or to reputable national scientists to fill information gaps. Data collected included administrative divisions affected, whether VL and CL case notification is mandatory, characteristics of known reservoirs and vector control programs, estimated and reported case numbers, and outbreaks in the previous 5 years.

A comprehensive literature search was also conducted, and the resulting information was used as an independent validation of these data. We reviewed the literature based on MEDLINE searches using the terms leishmaniasis and epidemiology with the name of each endemic country or territory. For the initial search, we included all articles listed in MEDLINE in English, French, Spanish or Russian up to October 2010, when the search was conducted. We selected articles that explicitly addressed incidence, geographic distribution, surveillance and/or trends over time, and preferentially chose articles published since 2000 if available. For countries with sparse data on leishmaniasis, we broadened the review to include all articles that shed light on the occurrence of the disease within that country. We reviewed titles for all references, abstracts when available for those whose titles were not sufficient to lead us to exclude the paper, and the full article when the abstract indicated possible relevance. The search for country-specific literature yielded 3242 potentially relevant articles, of which 340 were retained based on our selection criteria. Five recent review articles were also included. Twenty-six additional unpublished reports were provided by national or international experts. The literature was reviewed by at least 2 authors and regular meetings were held among the authors to discuss the findings in depth.

A MEDLINE search was also performed using the terms leishmaniasis and underreporting to identify articles that would aid in making incidence estimates. This search yielded 8 articles of which 5 presented data on the magnitude of leishmaniasis underreporting. One additional article was identified from author literature collections, yielding 3 articles with empirical data regarding VL and 3 for CL underreporting [24], [25], [26], [27], [28], [29]. These articles were used to establish probable degrees of underreporting for the countries in which their analyses were performed, and were also used for estimates in countries judged similar in their degree of underreporting. National and international experts provided their judgements of the magnitude of underreporting. In addition, for countries where reporting is sparse, but surveys have been performed, the published data were used as a basis to select the appropriate degree of underreporting [30]. Wherever possible, estimated plausible VL and CL incidence ranges were assigned by country and/or region based on reported incidence and multiplication by the probable underreporting factors. Estimates less than 20 were retained as the precise product of the reported case number times the underreporting factor, those between 20 and 1000 were rounded to the nearest 10 and those over 1000 were rounded to the nearest 100. Where reporting was absent but incidence was known to be substantial, estimates were assigned based on the judgment of national and international experts. The regional estimates represent the sum of the country estimates followed by the same rounding process. Similarly, the global estimates represent the sum of the regional estimates followed by rounding as described above. In order to facilitate expert judgment regarding the probable accuracy of the figures presented here, we defined geographical regions consistent with the major ecological foci of leishmaniasis transmission, rather than official WHO regions [31], [32], [33].

A second questionnaire addressed access to antileishmanial medicines, and included specific questions: whether the public sector provides health care free of charge; the existence of a national program for control of leishmaniasis; inclusion of antileishmanial medicines in the National Essential Drug List; the number of different medicines purchased for the public sector or donations received in the last two years; sale of antileishmanial drugs in the private sector and price per tablet or vial; percentage of people using the for-profit private sector versus public sector for leishmaniasis treatment; health care level providing treatment in the public sector; presence of NGOs or other non-profit agencies providing leishmaniasis treatment; and barriers to access for treatment of leishmaniasis. Basic social and health data from each country were obtained from the websites of the relevant international agencies [34], [35], [36], [37], [38].

The epidemiological data were used to produce maps with 2008 as the reference year using ArcGIS 9.3– Desktop (Esri, Redlands, CA) and following WHO guidelines for GIS usage. The numbers of confirmed cases by clinical form (VL, CL, mucocutaneous leishmaniasis) were mapped by official first level administrative division. These data were used to calculate annual incidence rates. A single standard range of values was used for each clinical form to facilitate visual comparison between countries. Draft maps were shared with data providers and other leishmaniasis experts for validation. The following maps were developed for each country: situational map with neighbouring countries and world globe, maps of cases by clinical form, and maps of incidence per 10,000 inhabitants. All maps follow a consistent set of characteristics: five categories of colours in a yellow-to-red scale were chosen for the maps of cases, and six categories of colours in blue tones scale were chosen for the maps of incidence. The sparse information in a few countries required the use of ad hoc scales. Only WHO GIS shapefile databases were used; the maps follow the administrative limits and frontiers recognized by United Nations conventions.

The parasitological information has been reproduced from the WHO Technical Report Series 949 (http://whqlibdoc.who.int/trs/WHO_TRS_949_eng.pdf) published in 2010.

Basic social and health data, results of literature reviews, data on the magnitude of underreporting, maps, data regarding epidemiology, case load, access to treatment and access to drugs, and parasitological information are presented in a series of extensive Profiles of each endemic individual country and territory and are presented in the Annex of this publication (see ‘Leishmaniasis Country Profiles Text S1, S2, S3, S4, S5, S6, S7, S8, S9, S10, S11, S12, S13, S14, S15, S16, S17, S18, S19, S20, S21, S22, S23, S24, S25, S26, S27, S28, S29, S30, S31, S32, S33, S34, S35, S36, S37, S38, S39, S40, S41, S42, S43, S44, S45, S46, S47, S48, S49, S50, S51, S52, S53, S54, S55, S56, S57, S58, S59, S60, S61, S62, S63, S64, S65, S66, S67, S68, S69, S70, S71, S72, S73, S74, S75, S76, S77, S78, S79, S80, S81, S82, S83, S84, S85, S86, S87, S88, S89, S90, S91, S92, S93, S94, S95, S96, S97, S98, S99, S100, S101’).

Results

A total of 98 countries and 3 territories on 5 continents reported endemic leishmaniasis transmission (Tables 1, 2, 3, 4, 5, 6 and 7, 8, 9, 10, 11, 12). In total, official case counts totalled more than 58,000 VL cases and 220,000 CL cases per year (Tables 13 and 14). However, only about two-thirds of countries had reported incidence data for a five-year period; data were sparsest for the foci in Africa. A number of countries are listed here as endemic despite the lack of reported human cases, usually reflecting an absence of surveillance or other investigations. [39] For example, although Mongolia has not reported human CL cases, L. major genetically identical to that found in countries with proven endemic transmission has been isolated on multiple occasions from gerbils. [40] Only countries with circulating species known to be pathogenic to humans are included as endemic. For this reason, Australia is not considered endemic despite reports of CL among red kangaroos caused by a newly described leishmanial species. [41] Human infections due to lower trypanosomatids are also excluded. [42].

There are few published empirical assessments of underreporting in official surveillance data. Two studies from Bihar, India, compared VL case numbers ascertained through active house-to-house surveys to those reported in the official surveillance system; official figures were shown to be 4.2-fold and 8.1-fold lower than the incidence found by active case detection in the two studies, respectively. [27], [28] A study in Brazil used the capture-recapture method to estimate underreporting of VL, based on data from 3 different sources; the degree of underreporting was found to be 1.3- to 1.7-fold. [25] Data from one province in Argentina estimated the degree of CL underreporting to be 2.8 to 4.6-fold; however, studies from Guatemala and Jordan indicate that CL incidence may be underestimated by 40- to 47-fold in national surveillance data. [24], [26], [29] Based on these publications, country-level VL underreporting magnitude was categorized as follows: mild (1.2- to 1.8-fold based on data from Brazil [25]); severe (4.0- to 8.0-fold based on data from India [27], [28]); and an intermediate category of moderate (2.0 to 4.0-fold) underreporting. Despite the high published range of CL underreporting [24], [26], we chose conservative multipliers: mild (2.8 to 4.6-fold based on data from Argentina [29]) and moderate (5.0- to 10.0-fold). No estimates could be made for most countries in sub-Saharan Africa, where almost no data were available.

Based on these estimates, approximately 0.2 to 0.4 million VL cases and 0.7 to 1.2 million CL cases occur each year. More than 90% of global VL cases occur in just six countries: India, Bangladesh, Sudan, South Sudan, Brazil and Ethiopia (Table 13). Cutaneous leishmaniasis is more widely distributed, with about one-third of cases occurring in each of three regions, the Americas, the Mediterranean basin, and western Asia from the Middle East to Central Asia (Table 14). The ten countries with the highest estimated case counts, Afghanistan, Algeria, Colombia, Brazil, Iran, Syria, Ethiopia, North Sudan, Costa Rica and Peru, together account for 70 to 75% of global estimated CL incidence.

Mortality data are extremely sparse and generally represent hospital-based deaths only. The reported case-fatality rate for VL in Brazil in 2006 was 7.2%. In the Indian subcontinent, the focus responsible for the largest proportion of global VL cases, reported case-fatality rates ranged from 1.5% (93 deaths/6224 VL cases from 2004–2008) in Bangladesh to 2.4% (853/34,918) in India and 6.2% (91/1477) in Nepal. However, community-based studies that included active searches for deaths due to kala-azar estimate case-fatality rates of more than 10%, while data from a village-based study in India suggest that as many as 20% of VL patients, disproportionately poor and female, died before their disease was recognized. [43], [44], [45] In South Sudan, one community-based longitudinal study demonstrated a case-fatality rate of 20% in a settled village in peacetime; in areas of conflict, famine or population displacement mortality rates are much higher. [22], [46] A recent study from South Sudan estimated that 91% of all kala-azar deaths went unrecognized. [47] Using an overall case-fatality rate of 10% and assuming that virtually all deaths are from VL, we reach a tentative estimate of 20,000 to 40,000 leishmaniasis deaths per year, in line with previous WHO estimates. [10]

Discussion

The data presented here and in the accompanying Annex (see ‘Leishmaniasis Country Profiles Text S1–S101’) represent the first update of the empirical database for leishmaniasis since 1991. [48], [49] We are acutely cognizant of the uncertainties inherent in the data, and for that reason, have presented rough ranges rather than single estimates for each outcome. We deliberately used conservative assumptions for the underreporting rates and resultant multipliers; true leishmaniasis incidence rates may be substantially higher. Due to the lack of data, we made no estimates for post-kala-azar dermal leishmaniasis, mucocutaneous leishmaniasis, and other less frequent forms of leishmaniasis. Our mortality estimate contains even more uncertainty than the incidence estimate, because studies affirm that a large proportion of kala-azar deaths occur outside of health facilities and the cause likely never recognized, precluding the possibility of accurate passive reporting. [43], [45], [47].

The limitations of these data are obvious: surveillance and vital records reporting in the countries most affected by leishmaniasis are incomplete, and we have very sparse data on which to base correction factors for underreporting. The figures in this report should not be considered precise and should be interpreted with caution. Nevertheless, these data include a more comprehensive review of leishmaniasis incidence than any previous publication, and represent a major improvement in the evidence base for one of the most neglected diseases. [50] Better surveillance systems are urgently needed, in particular in disease foci targeted for more intensive control or elimination. [4], [51] Many key measures of progress, such as validation of trends seen in surveillance data and accurate case-fatality rates, can only be obtained through the active collection of community-based data. [4], [52] We hope the data presented here will allow a more nuanced interpretation of published disease burden estimates, and the uncertainties in these data will spur activities to improve the evidence base for leishmaniasis and other neglected diseases.

Supporting Information

Text S1

Leishmaniasis Country Profiles, Afghanistan.

(DOCX)

pone.0035671.s001.docxClick here for additional data file.
Text S2

Leishmaniasis Country Profiles, Albania.

(DOCX)

pone.0035671.s002.docxClick here for additional data file.
Text S3

Leishmaniasis Country Profiles, Algeria.

(DOCX)

pone.0035671.s003.docxClick here for additional data file.
Text S4

Leishmaniasis Country Profiles, Argentina.

(DOCX)

pone.0035671.s004.docxClick here for additional data file.
Text S5

Leishmaniasis Country Profiles, Armenia.

(DOCX)

pone.0035671.s005.docxClick here for additional data file.
Text S6

Leishmaniasis Country Profiles, Azerbijan.

(DOCX)

pone.0035671.s006.docxClick here for additional data file.
Text S7

Leishmaniasis Country Profiles, Bangladesh.

(DOCX)

pone.0035671.s007.docxClick here for additional data file.
Text S8

Leishmaniasis Country Profiles, Belize.

(DOCX)

pone.0035671.s008.docxClick here for additional data file.
Text S9

Leishmaniasis Country Profiles, Bhutan.

(DOCX)

pone.0035671.s009.docxClick here for additional data file.
Text S10

Leishmaniasis Country Profiles, Bolivia.

(DOCX)

pone.0035671.s010.docxClick here for additional data file.
Text S11

Leishmaniasis Country Profiles, Bosnia.

(DOCX)

pone.0035671.s011.docxClick here for additional data file.
Text S12

Leishmaniasis Country Profiles, Brazil.

(DOCX)

pone.0035671.s012.docxClick here for additional data file.
Text S13

Leishmaniasis Country Profiles, Bulgaria.

(DOCX)

pone.0035671.s013.docxClick here for additional data file.
Text S14

Leishmaniasis Country Profiles, Burkina Faso.

(DOCX)

pone.0035671.s014.docxClick here for additional data file.
Text S15

Leishmaniasis Country Profiles, Cameroon.

(DOCX)

pone.0035671.s015.docxClick here for additional data file.
Text S16

Leishmaniasis Country Profiles, Central African Republic.

(DOCX)

pone.0035671.s016.docxClick here for additional data file.
Text S17

Leishmaniasis Country Profiles, Chad.

(DOCX)

pone.0035671.s017.docxClick here for additional data file.
Text S18

Leishmaniasis Country Profiles, China.

(DOCX)

pone.0035671.s018.docxClick here for additional data file.
Text S19

Leishmaniasis Country Profiles, Colombia.

(DOCX)

pone.0035671.s019.docxClick here for additional data file.
Text S20

Leishmaniasis Country Profiles, Costa Rica.

(DOCX)

pone.0035671.s020.docxClick here for additional data file.
Text S21

Leishmaniasis Country Profiles, Cote d’Ivoire.

(DOCX)

pone.0035671.s021.docxClick here for additional data file.
Text S22

Leishmaniasis Country Profiles, Croatia.

(DOCX)

pone.0035671.s022.docxClick here for additional data file.
Text S23

Leishmaniasis Country Profiles, Cyprus.

(DOCX)

pone.0035671.s023.docxClick here for additional data file.
Text S24

Leishmaniasis Country Profiles, Democratic Republic of the Congo.

(DOCX)

pone.0035671.s024.docxClick here for additional data file.
Text S25

Leishmaniasis Country Profiles, Djibouti.

(DOCX)

pone.0035671.s025.docxClick here for additional data file.
Text S26

Leishmaniasis Country Profiles, Dominican Republic.

(DOCX)

pone.0035671.s026.docxClick here for additional data file.
Text S27

Leishmaniasis Country Profiles, Ecuador.

(DOCX)

pone.0035671.s027.docxClick here for additional data file.
Text S28

Leishmaniasis Country Profiles, Egypt.

(DOCX)

pone.0035671.s028.docxClick here for additional data file.
Text S29

Leishmaniasis Country Profiles El Salvador.

(DOCX)

pone.0035671.s029.docxClick here for additional data file.
Text S30

Leishmaniasis Country Profiles, Eritrea.

(DOCX)

pone.0035671.s030.docxClick here for additional data file.
Text S31

Leishmaniasis Country Profiles, Ethiopia.

(DOCX)

pone.0035671.s031.docxClick here for additional data file.
Text S32

Leishmaniasis Country Profiles, France.

(DOCX)

pone.0035671.s032.docxClick here for additional data file.
Text S33

Leishmaniasis Country Profiles, French Guyana.

(DOCX)

pone.0035671.s033.docxClick here for additional data file.
Text S34

Leishmaniasis Country Profiles, Gambia.

(DOCX)

pone.0035671.s034.docxClick here for additional data file.
Text S35

Leishmaniasis Country Profiles, Georgia.

(DOCX)

pone.0035671.s035.docxClick here for additional data file.
Text S36

Leishmaniasis Country Profiles, Ghana.

(DOCX)

pone.0035671.s036.docxClick here for additional data file.
Text S37

Leishmaniasis Country Profiles, Greece.

(DOCX)

pone.0035671.s037.docxClick here for additional data file.
Text S38

Leishmaniasis Country Profiles, Guatemala.

(DOCX)

pone.0035671.s038.docxClick here for additional data file.
Text S39

Leishmaniasis Country Profiles, Guinea Bissau.

(DOCX)

pone.0035671.s039.docxClick here for additional data file.
Text S40

Leishmaniasis Country Profiles, Guinea.

(DOCX)

pone.0035671.s040.docxClick here for additional data file.
Text S41

Leishmaniasis Country Profiles, Guyana.

(DOCX)

pone.0035671.s041.docxClick here for additional data file.
Text S42

Leishmaniasis Country Profiles, Honduras.

(DOCX)

pone.0035671.s042.docxClick here for additional data file.
Text S43

Leishmaniasis Country Profiles, India.

(DOCX)

pone.0035671.s043.docxClick here for additional data file.
Text S44

Leishmaniasis Country Profiles, Iran.

(DOCX)

pone.0035671.s044.docxClick here for additional data file.
Text S45

Leishmaniasis Country Profiles, Iraq.

(DOCX)

pone.0035671.s045.docxClick here for additional data file.
Text S46

Leishmaniasis Country Profiles, Israel.

(DOCX)

pone.0035671.s046.docxClick here for additional data file.
Text S47

Leishmaniasis Country Profiles, Italy.

(DOCX)

pone.0035671.s047.docxClick here for additional data file.
Text S48

Leishmaniasis Country Profiles, Jordan.

(DOCX)

pone.0035671.s048.docxClick here for additional data file.
Text S49

Leishmaniasis Country Profiles, Kazakhstan.

(DOCX)

pone.0035671.s049.docxClick here for additional data file.
Text S50

Leishmaniasis Country Profiles, Kenya.

(DOCX)

pone.0035671.s050.docxClick here for additional data file.
Text S51

Leishmaniasis Country Profiles, Kuwait.

(DOCX)

pone.0035671.s051.docxClick here for additional data file.
Text S52

Leishmaniasis Country Profiles, Kyrgyzstan.

(DOCX)

pone.0035671.s052.docxClick here for additional data file.
Text S53

Leishmaniasis Country Profiles, Lebanon.

(DOCX)

pone.0035671.s053.docxClick here for additional data file.
Text S54

Leishmaniasis Country Profiles, Libya.

(DOCX)

pone.0035671.s054.docxClick here for additional data file.
Text S55

Leishmaniasis Country Profiles, Malawi.

(DOCX)

pone.0035671.s055.docxClick here for additional data file.
Text S56

Leishmaniasis Country Profiles, Mali.

(DOCX)

pone.0035671.s056.docxClick here for additional data file.
Text S57

Leishmaniasis Country Profiles, Malta.

(DOCX)

pone.0035671.s057.docxClick here for additional data file.
Text S58

Leishmaniasis Country Profiles, Mauritania.

(DOCX)

pone.0035671.s058.docxClick here for additional data file.
Text S59

Leishmaniasis Country Profiles, Mexico.

(DOCX)

pone.0035671.s059.docxClick here for additional data file.
Text S60

Leishmaniasis Country Profiles, Monaco.

(DOCX)

pone.0035671.s060.docxClick here for additional data file.
Text S61

Leishmaniasis Country Profiles, Mongolia.

(DOCX)

pone.0035671.s061.docxClick here for additional data file.
Text S62

Leishmaniasis Country Profiles, Montenegro.

(DOCX)

pone.0035671.s062.docxClick here for additional data file.
Text S63

Leishmaniasis Country Profiles, Morocco.

(DOCX)

pone.0035671.s063.docxClick here for additional data file.
Text S64

Leishmaniasis Country Profiles, Namibia.

(DOCX)

pone.0035671.s064.docxClick here for additional data file.
Text S65

Leishmaniasis Country Profiles, Nepal.

(DOCX)

pone.0035671.s065.docxClick here for additional data file.
Text S66

Leishmaniasis Country Profiles, Nicaragua.

(DOCX)

pone.0035671.s066.docxClick here for additional data file.
Text S67

Leishmaniasis Country Profiles, Niger.

(DOCX)

pone.0035671.s067.docxClick here for additional data file.
Text S68

Leishmaniasis Country Profiles, Nigeria.

(DOCX)

pone.0035671.s068.docxClick here for additional data file.
Text S69

Leishmaniasis Country Profiles, Oman.

(DOCX)

pone.0035671.s069.docxClick here for additional data file.
Text S70

Leishmaniasis Country Profiles, Pakistan.

(DOCX)

pone.0035671.s070.docxClick here for additional data file.
Text S71

Leishmaniasis Country Profiles, Panama.

(DOCX)

pone.0035671.s071.docxClick here for additional data file.
Text S72

Leishmaniasis Country Profiles, Paraguay.

(DOCX)

pone.0035671.s072.docxClick here for additional data file.
Text S73

Leishmaniasis Country Profiles, Peru.

(DOCX)

pone.0035671.s073.docxClick here for additional data file.
Text S74

Leishmaniasis Country Profiles, Portugal.

(DOCX)

pone.0035671.s074.docxClick here for additional data file.
Text S75

Leishmaniasis Country Profiles, Romania.

(DOCX)

pone.0035671.s075.docxClick here for additional data file.
Text S76

Leishmaniasis Country Profiles, Saudi Arabia.

(DOCX)

pone.0035671.s076.docxClick here for additional data file.
Text S77

Leishmaniasis Country Profiles, Senegal.

(DOCX)

pone.0035671.s077.docxClick here for additional data file.
Text S78

Leishmaniasis Country Profiles, Slovenia.

(DOCX)

pone.0035671.s078.docxClick here for additional data file.
Text S79

Leishmaniasis Country Profiles, Somalia.

(DOCX)

pone.0035671.s079.docxClick here for additional data file.
Text S80

Leishmaniasis Country Profiles, South Africa.

(DOCX)

pone.0035671.s080.docxClick here for additional data file.
Text S81

Leishmaniasis Country Profiles, South Sudan.

(DOCX)

pone.0035671.s081.docxClick here for additional data file.
Text S82

Leishmaniasis Country Profiles, Spain.

(DOCX)

pone.0035671.s082.docxClick here for additional data file.
Text S83

Leishmaniasis Country Profiles, Sri Lanka.

(DOCX)

pone.0035671.s083.docxClick here for additional data file.
Text S84

Leishmaniasis Country Profiles, Sudan.

(DOCX)

pone.0035671.s084.docxClick here for additional data file.
Text S85

Leishmaniasis Country Profiles, Surinam.

(DOCX)

pone.0035671.s085.docxClick here for additional data file.
Text S86

Leishmaniasis Country Profiles, Syrian Arab Republic.

(DOCX)

pone.0035671.s086.docxClick here for additional data file.
Text S87

Leishmaniasis Country Profiles, Taiwan.

(DOCX)

pone.0035671.s087.docxClick here for additional data file.
Text S88

Leishmaniasis Country Profiles, Tajikistan.

(DOCX)

pone.0035671.s088.docxClick here for additional data file.
Text S89

Leishmaniasis Country Profiles, Thailand.

(DOCX)

pone.0035671.s089.docxClick here for additional data file.
Text S90

Leishmaniasis Country Profiles, The Former Yugoslav Republic of Macedonia.

(DOCX)

pone.0035671.s090.docxClick here for additional data file.
Text S91

Leishmaniasis Country Profiles, Tunisia.

(DOCX)

pone.0035671.s091.docxClick here for additional data file.
Text S92

Leishmaniasis Country Profiles, Turkey.

(DOCX)

pone.0035671.s092.docxClick here for additional data file.
Text S93

Leishmaniasis Country Profiles, Turkmenistan.

(DOCX)

pone.0035671.s093.docxClick here for additional data file.
Text S94

Leishmaniasis Country Profiles, Uganda.

(DOCX)

pone.0035671.s094.docxClick here for additional data file.
Text S95

Leishmaniasis Country Profiles, Ukraine.

(DOCX)

pone.0035671.s095.docxClick here for additional data file.
Text S96

Leishmaniasis Country Profiles, United States of America.

(DOCX)

pone.0035671.s096.docxClick here for additional data file.
Text S97

Leishmaniasis Country Profiles, Uzbekistan.

(DOCX)

pone.0035671.s097.docxClick here for additional data file.
Text S98

Leishmaniasis Country Profiles, Venezuela.

(DOCX)

pone.0035671.s098.docxClick here for additional data file.
Text S99

Leishmaniasis Country Profiles, West Bank and Gaza Strip.

(DOCX)

pone.0035671.s099.docxClick here for additional data file.
Text S100

Leishmaniasis Country Profiles, Yemen.

(DOCX)

pone.0035671.s100.docx.docxClick here for additional data file.
Text S101

Leishmaniasis Country Profiles, Zambia.

(DOCX)

pone.0035671.s101.docxClick here for additional data file.

Footnotes

Competing Interests: The authors have declared that no competing interests exist.

Funding: The Spanish Agency for International Cooperation for Development (AECID) has provided generous support to the WHO Leishmaniasis program since 2005. This support permitted among many other activities regional meetings with the AFRO, EURO, PAHO and SEARO countries, and provided for short term contracts for IDV, MdB, MH and JS related to the preparation of the country profiles. Sanofi provided a grant for a regional meeting with the EMRO countries and various activities related to the control of cutaneous Leishmaniasis in the EMRO region. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Acknowledgments

The WHO leishmaniasis control team has contributed importantly to this publication and consists of the following members: Daniel Argaw (WHO/HQ), Sujit Bhattacharya (WHO/SEARO), Mikhail Ejov (WHO/EURO), Ana Nilce Elkhouri (WHO/PAHO), José Antonio Ruiz-Postigo (WHO/EMRO), and Joseph Serrano (WHO/HQ). The constant support of Avideh Denereaz within the WHO/NTD/IDM department has been crucial to structure the Leishmaniasis program as a whole but in particular facilitated the three year process of preparing the country profiles. Special thanks are given to colleagues who reviewed the information of some countries or provided accurate data like Byron Arana (WHO/TDR), and in particular to the members of the PECET, University of Medellin in Colombia, namely Sara M Robledo, Karina Mondragón, Andrés Vélez, Liliana López and Luz A. Acosta. Last but not least, we want to highlight our gratitude to all these that participated in the meetings and responded the questionnaires which contributions have been of paramount importance to prepare this publication.

Disclaimer: The boundaries and names shown and the designations used on the maps presented in this paper do not imply the expression of any opinion whatsoever on the part of WHO concerning the legal status of any country, territory, city or area or of its authorities, or concerning the delimitation of its frontiers or boundaries. Dotted lines on maps represent approximate border lines for which there may not yet be full agreement.

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