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Leishmaniasis worldwide and global estimates of its incidence.
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MedLine Citation:
PMID:  22693548     Owner:  NLM     Status:  MEDLINE    
Abstract/OtherAbstract:
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.
Authors:
Jorge Alvar; Iván D Vélez; Caryn Bern; Mercé Herrero; Philippe Desjeux; Jorge Cano; Jean Jannin; Margriet den Boer;
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Publication Detail:
Type:  Journal Article; Research Support, Non-U.S. Gov't     Date:  2012-05-31
Journal Detail:
Title:  PloS one     Volume:  7     ISSN:  1932-6203     ISO Abbreviation:  PLoS ONE     Publication Date:  2012  
Date Detail:
Created Date:  2012-06-13     Completed Date:  2012-10-22     Revised Date:  2013-07-12    
Medline Journal Info:
Nlm Unique ID:  101285081     Medline TA:  PLoS One     Country:  United States    
Other Details:
Languages:  eng     Pagination:  e35671     Citation Subset:  IM    
Affiliation:
Department for the Control of Neglected Tropical Diseases (HTM/NTD/IDM), Leishmaniasis Control Program, World Health Organization, Geneva, Switzerland. alvarj@who.int
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MeSH Terms
Descriptor/Qualifier:
Female
Geography
Humans
Internationality*
Leishmaniasis / epidemiology*,  etiology,  mortality
Male
Time Factors
World Health Organization
Investigator
Investigator/Affiliation:
Daniel Argaw / ; Sujit Bhattacharya / ; Mikhail Ejov / ; Ana Nilce Elkhouri / ; José Antonio Ruiz-Postigo / ; Joseph Serrano /
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Journal ID (nlm-ta): PLoS One
Journal ID (iso-abbrev): PLoS ONE
Journal ID (publisher-id): plos
Journal ID (pmc): plosone
ISSN: 1932-6203
Publisher: Public Library of Science, San Francisco, USA
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This is an open-access article, free of all copyright, and may be freely reproduced, distributed, transmitted, modified, built upon, or otherwise used by anyone for any lawful purpose. The work is made available under the Creative Commons CC0 public domain dedication.
Received Day: 6 Month: 12 Year: 2011
Accepted Day: 22 Month: 3 Year: 2012
collection publication date: Year: 2012
Electronic publication date: Day: 31 Month: 5 Year: 2012
Volume: 7 Issue: 5
E-location ID: e35671
ID: 3365071
PubMed Id: 22693548
Publisher Id: PONE-D-11-24894
DOI: 10.1371/journal.pone.0035671

Leishmaniasis Worldwide and Global Estimates of Its Incidence Alternate Title:Leishmaniasis Worldwide and Estimates of Incidence
Jorge Alvar1*
Iván D. Vélez12
Caryn Bern3
Mercé Herrero4
Philippe Desjeux5
Jorge Cano6
Jean Jannin1
Margriet den Boer1
the WHO Leishmaniasis Control Team
Martyn Kirkedit1 Role: Editor
1Department for the Control of Neglected Tropical Diseases (HTM/NTD/IDM), Leishmaniasis Control Program, World Health Organization, Geneva, Switzerland
2PECET, Universidad de Antioquia, Medellin, Colombia
3Division of Parasitic Diseases and Malaria, National Center for Global Health, Centers for Disease Control and Prevention, Atlanta, Georgia, United States of America
4Disease Prevention and Control Programmes, World Health Organization, Addis Ababa, Ethiopia
5Institute of OneWorldHealth, San Francisco, California, United States of America
6National Centre for Tropical Medicine and International Health, Instituto de Salud Carlos III, Madrid, Spain
The Australian National University, Australia
Correspondence: * E-mail: alvarj@who.int
Contributed by footnote: Wrote the paper: JA IV CB MdB. Performed surveys to obtain Individual Country Data: JA IV MdB. Supported Regional Meetings to obtain Individual Country Data: JA IV MH JJ MdB. In addition to these authors the WHO Leishmaniasis Control Team should be mentioned, this consists of Daniel Argaw (WHO/HQ), Sujit Bhattacharya (WHO/SEARO), Mikhail Ejov (WHO/EURO), Ana Nilce Elkhouri (WHO/PAHO), José Antonio Ruiz-Postigo (WHO/EMRO), and Josep Serrano (WHO/HQ). Critical editing of Individual Country Data: PD. Map Design: JC.
[other] ¶ For a full list of the members of the WHO Leishmaniasis Control Team please see the Acknowledgments section.

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].

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 S1S101’) 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.

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Leishmaniasis Country Profiles, Albania.

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Leishmaniasis Country Profiles, Algeria.

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Leishmaniasis Country Profiles, Argentina.

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Leishmaniasis Country Profiles, Armenia.

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Leishmaniasis Country Profiles, Azerbijan.

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Leishmaniasis Country Profiles, Bangladesh.

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Leishmaniasis Country Profiles, Belize.

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Leishmaniasis Country Profiles, Bhutan.

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Leishmaniasis Country Profiles, Bolivia.

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Leishmaniasis Country Profiles, Bosnia.

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Leishmaniasis Country Profiles, Brazil.

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Leishmaniasis Country Profiles, Bulgaria.

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Leishmaniasis Country Profiles, Burkina Faso.

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Leishmaniasis Country Profiles, Cameroon.

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Leishmaniasis Country Profiles, Central African Republic.

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Leishmaniasis Country Profiles, Chad.

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Leishmaniasis Country Profiles, China.

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Leishmaniasis Country Profiles, Colombia.

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Leishmaniasis Country Profiles, Costa Rica.

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Leishmaniasis Country Profiles, Cote d’Ivoire.

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Leishmaniasis Country Profiles, Croatia.

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Leishmaniasis Country Profiles, Cyprus.

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Leishmaniasis Country Profiles, Democratic Republic of the Congo.

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Leishmaniasis Country Profiles, Djibouti.

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Leishmaniasis Country Profiles, Dominican Republic.

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Leishmaniasis Country Profiles, Ecuador.

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Leishmaniasis Country Profiles, Egypt.

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Leishmaniasis Country Profiles El Salvador.

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Leishmaniasis Country Profiles, Eritrea.

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Leishmaniasis Country Profiles, Ethiopia.

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Leishmaniasis Country Profiles, France.

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Leishmaniasis Country Profiles, French Guyana.

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Leishmaniasis Country Profiles, Gambia.

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Leishmaniasis Country Profiles, Georgia.

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Leishmaniasis Country Profiles, Ghana.

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Leishmaniasis Country Profiles, Greece.

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Leishmaniasis Country Profiles, Guatemala.

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Leishmaniasis Country Profiles, Guinea Bissau.

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Leishmaniasis Country Profiles, Guinea.

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Leishmaniasis Country Profiles, Guyana.

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Leishmaniasis Country Profiles, Honduras.

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Leishmaniasis Country Profiles, India.

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Leishmaniasis Country Profiles, Iran.

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Leishmaniasis Country Profiles, Iraq.

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Leishmaniasis Country Profiles, Israel.

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Leishmaniasis Country Profiles, Italy.

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Leishmaniasis Country Profiles, Jordan.

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Leishmaniasis Country Profiles, Kazakhstan.

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Leishmaniasis Country Profiles, Kenya.

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Leishmaniasis Country Profiles, Kuwait.

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Leishmaniasis Country Profiles, Kyrgyzstan.

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Leishmaniasis Country Profiles, Lebanon.

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Leishmaniasis Country Profiles, Libya.

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Leishmaniasis Country Profiles, Malawi.

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Leishmaniasis Country Profiles, Mali.

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Leishmaniasis Country Profiles, Malta.

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Leishmaniasis Country Profiles, Mauritania.

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Leishmaniasis Country Profiles, Mexico.

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Leishmaniasis Country Profiles, Monaco.

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Leishmaniasis Country Profiles, Mongolia.

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Leishmaniasis Country Profiles, Montenegro.

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Leishmaniasis Country Profiles, Morocco.

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Leishmaniasis Country Profiles, Namibia.

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Leishmaniasis Country Profiles, Nepal.

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Leishmaniasis Country Profiles, Nicaragua.

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Leishmaniasis Country Profiles, Niger.

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Leishmaniasis Country Profiles, Nigeria.

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Leishmaniasis Country Profiles, Oman.

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Leishmaniasis Country Profiles, Pakistan.

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Leishmaniasis Country Profiles, Panama.

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Leishmaniasis Country Profiles, Paraguay.

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Leishmaniasis Country Profiles, Peru.

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Leishmaniasis Country Profiles, Portugal.

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Leishmaniasis Country Profiles, Romania.

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Leishmaniasis Country Profiles, Saudi Arabia.

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Leishmaniasis Country Profiles, Senegal.

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Leishmaniasis Country Profiles, Slovenia.

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Leishmaniasis Country Profiles, Somalia.

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Leishmaniasis Country Profiles, South Africa.

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Leishmaniasis Country Profiles, South Sudan.

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Leishmaniasis Country Profiles, Spain.

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Leishmaniasis Country Profiles, Sri Lanka.

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Leishmaniasis Country Profiles, Sudan.

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Leishmaniasis Country Profiles, Surinam.

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Leishmaniasis Country Profiles, Syrian Arab Republic.

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Leishmaniasis Country Profiles, Taiwan.

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Leishmaniasis Country Profiles, Tajikistan.

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Leishmaniasis Country Profiles, Thailand.

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Leishmaniasis Country Profiles, The Former Yugoslav Republic of Macedonia.

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Leishmaniasis Country Profiles, Tunisia.

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Leishmaniasis Country Profiles, Turkey.

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Leishmaniasis Country Profiles, Turkmenistan.

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Leishmaniasis Country Profiles, Uganda.

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Leishmaniasis Country Profiles, Ukraine.

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Leishmaniasis Country Profiles, United States of America.

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Leishmaniasis Country Profiles, Uzbekistan.

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Leishmaniasis Country Profiles, Venezuela.

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Leishmaniasis Country Profiles, West Bank and Gaza Strip.

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Leishmaniasis Country Profiles, Yemen.

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Leishmaniasis Country Profiles, Zambia.

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Notes

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.

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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52. Hirve S,Singh SP,Kumar N,Banjara MR,Das P,et al. Year: 2010Effectiveness and feasibility of active and passive case detection in the visceral leishmaniasis elimination initiative in India, bangladesh, and Nepal.Am J Trop Med Hyg8350751120810811

Tables
[TableWrap ID: pone-0035671-t001] doi: 10.1371/journal.pone.0035671.t001.
Table 1  Reported and estimated incidence of visceral leishmaniasis in the American region.
Reported VL cases/year Years of report Estimated annual VL incidence
Argentina 8 2004–2008 20 to 301
Bolivia 0 2008
Brazil 3481 2003–2007 4200 to 63002
Colombia 60 2004–2008 70 to 1102
El Salvador no data
Guatemala 15 2004–2008 20 to 302
Honduras 6 2004–2008 7 to 102
Mexico 7 2004–2008 8 to 122
Nicaragua 3 2003–2007 3 to 52
Paraguay 48 2004–2008 100 to 2001
Venezuela 40 2004–2008 50 to 702
Region 3668 4500 to 6800

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].


[TableWrap ID: pone-0035671-t002] doi: 10.1371/journal.pone.0035671.t002.
Table 2  Reported and estimated incidence of visceral leishmaniasis in the sub-Saharan African region.
Reported VL cases/year Years of report Estimated annual VL incidence
Central African Republic no data
Cameroon no data
Chad no data
Cote d’Ivoire 0 2004–2008
DR Congo 0 2004–2008
Gambia no data
Mauritania no data
Niger no data
Nigeria 1 2004–2008
Senegal 0 2004–2008
Zambia no data
Region 1

[TableWrap ID: pone-0035671-t003] doi: 10.1371/journal.pone.0035671.t003.
Table 3  Reported and estimated incidence of visceral leishmaniasis in the East African region.
Reported VL cases/year Years of report Estimated annual VL incidence
Djibouti no data
Eritrea 100 2008 200 to 4001
Ethiopia 1860 2004–2008 3700 to 74001
Kenya 145 2004–2008 610 to 12002
Somalia 679 2009 1400 to 27001
Sudan 3742 2005–2009 15,700 to 30,3002
South Sudan 1756 2004–2008 7400 to 14,2002
Uganda 288 2004–2008 350 to 5203
Region 8569 29,400 to 56,700

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

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

3Underreporting considered mild (1.2–1.8).


[TableWrap ID: pone-0035671-t004] doi: 10.1371/journal.pone.0035671.t004.
Table 4  Reported and estimated incidence of visceral leishmaniasis in the Mediterranean region.
Reported VL cases/year Years of report Estimated annual VL incidence
Albania 114 2004–2008 140 to 2101
Algeria 111 2004–2008 130 to 2001
Bosnia and Herzegovina 2 2002–2005 2 to 31
Bulgaria 7 2004–2008 8 to 121
Croatia 5 2004–2008 6 to 81
Cyprus 2 2008 2 to 41
Egypt 1 2008 1 to 21
France 18 2004–2008 20 to 301
Greece 42 2004–2008 50 to 801
Israel 2 2003–2007 3 to 41
Italy 134 2003–2007 160 to 2401
Jordan 0 2004–2008 0 to 0
Lebanon 0 2004–2008 0 to 0
Libya 3 2004–2008 5 to 102
Macedonia 7 2005–2009 9 to 131
Malta 2 2002–2005 3 to 41
Monaco no data
Montenegro 3 2004–2008 4 to 51
Morocco 152 2004–2008 300 to 6102
Palestine 5 2004–2008 10 to 202
Portugal 15 2003–2007 20 to 301
Slovenia no data
Spain 117 2004–2008 140 to 2101
Syria 14 2004–2008 30 to 602
Tunisia 89 2004–2008 110 to 1601
Turkey 29 2003–2007 60 to 1202
Region 875 1200 2000

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

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


[TableWrap ID: pone-0035671-t005] doi: 10.1371/journal.pone.0035671.t005.
Table 5  Reported and estimated incidence of visceral leishmaniasis in the Middle East to Central Asia.
Reported VL cases/year Years of report Estimated annual VL incidence
Afghanistan no data
Armenia 7 2004–2008 10 to 301
Azerbaijan 28 2004–2008 60 to 1101
China 378 2004–2008 760 to 15001
Georgia 164 2004–2008 330 to 6601
Iran (Islamic Republic of) 149 2004–2008 300 to 6001
Iraq 1711 2004–2008 3400 to 68001
Kazakhstan 1 2004–2008 2 to 41
Kyrgyzstan 0 2004–2008
Oman 1 2004–2008 2 to 41
Pakistan no data
Saudi Arabia 34 2004–2008 40 to 602
Tajikistan 15 2004–2008 30 to 601
Turkmenistan 0 2004–2008
Ukraine 2 2005–2008 4 to 71
Uzbekistan 7 2004–2008 10 to 301
Yemen 0 2004–2008 20 to 501
Region 2496 5000 10,000

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

2Underreporting considered mild (1.2–1.8).


[TableWrap ID: pone-0035671-t006] doi: 10.1371/journal.pone.0035671.t006.
Table 6  Reported and estimated incidence of visceral leishmaniasis in the Indian subcontinent and Southeast Asia.
Reported VL cases/year Years of report Estimated annual VL incidence
Bangladesh 6224 2004–2008 12,400 to 24,9001
Bhutan 2 2005–2009 10 to 202
India 34,918 2004–2008 146,700 to 282,8003
Nepal 1477 2004–2008 3000 to 59001
Sri Lanka no data 6 to 104
Thailand 2 2006–2010 5 to 105
Region 42,623 162,100 to 313,600

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].


[TableWrap ID: pone-0035671-t007] doi: 10.1371/journal.pone.0035671.t007.
Table 7  Reported and estimated incidence of cutaneous leishmaniasis in the American region.
Reported CL cases/year Years of report Estimated annual CL incidence
Argentina 261 2004–2008 730 to 12001
Belize no data
Bolivia 2647 2004–2008 7400 to 12,2001
Brazil 26,008 2003–2007 72,800 to 119,6001
Colombia 17,420 2005–2009 48,800 to 80,1001
Costa Rica 1249 2002–2006 3500 to 57001
Dominican Republic no data 0 to 0
Ecuador 1724 2004–2008 4800 to 79001
El Salvador no data 0 to 0
French Guyana 233 2004–2008 650 to 11001
Guatemala 684 2004–2008 1900 to 31001
Guyana 16 2006–2008 50 to 701
Honduras 1159 2006–2008 3200 to 53001
Mexico 811 2004–2008 2300 to 37001
Nicaragua 3222 2003–2007 9000 to 14,8001
Panama 2188 2005–2009 6100 to 10,1001
Paraguay 431 2004–2008 1200 to 20001
Peru 6405 2004–2008 17,900 to 29,5001
Suriname 3 2005–2007 8 to 141
Venezuela 2480 2004–2008 6900 to 11,4001
REGION 66,941 187,200 307,800

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


[TableWrap ID: pone-0035671-t008] doi: 10.1371/journal.pone.0035671.t008.
Table 8  Reported and estimated incidence of cutaneous leishmaniasis in the sub-Saharan African region.
Reported CL cases/year Years of report Estimated annual CL incidence
Burkina Faso no data
Cameroon 55 2007–2009 280 to 5501
Chad no data
Cote d’Ivoire 1 2004–2008 5 to 101
DR Congo 0 2009
Ghana 27 2004–2008 140 to 2701
Guinea no data
Guinea-Bissau no data
Mali 58 2004–2008 290 to 5801
Mauritania no data
Namibia no data
Niger no data
Nigeria 5 2004–2008 30 to 501
Senegal 8 2004–2008 40 to 801
South Africa no data
REGION 155 790 to 15001

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


[TableWrap ID: pone-0035671-t009] doi: 10.1371/journal.pone.0035671.t009.
Table 9  Reported and estimated incidence of cutaneous leishmaniasis in the East African region.
Reported CL cases/year Years of report Estimated annual CL incidence
Djibouti no data
Eritrea 50 2008 250 to 5001
Ethiopia no data 20,000 to 50,0002
Kenya no data
Sudan no data 15,000 to 40,0003
South Sudan no data
REGION 50 35,300 to 90,500

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).


[TableWrap ID: pone-0035671-t010] doi: 10.1371/journal.pone.0035671.t010.
Table 10  Reported and estimated incidence of cutaneous leishmaniasis in the Mediterranean.
Reported CL cases/year Years of report Estimated annual CL incidence
Albania 6 2004–2008
Algeria 44,050 2004–2008 123,300 to 202,6001
Bosnia and Herzegovina 0 2008
Bulgaria 0 2008
Croatia 2 2004–2008 6 to 101
Cyprus 1 2006–2008
Egypt 471 2008 1300 to 22001
France 2 2004–2008 6 to 101
Greece 3 2004–2008 8 to 131
Israel 579 2003–2007 1600 to 27001
Italy 49 2003–2007 140 to 2301
Jordan 227 2004–2008 630 to 10001
Lebanon 0 2004–2008
Libya 3540 2004–2008 9900 to 16,3001
Macedonia 0 2008
Malta 0 2008
Monaco no data
Montenegro 0 2008
Morocco 3430 2004–2008 9600 to 15,8001
Palestine 218 2005–2009 610 to 10001
Portugal 0 2004–2008
Slovenia no data
Spain 0 2004–2008
Syria 22,882 2004–2008 64,100 to 105,3001
Tunisia 7631 2004–2008 21,400 to 35,1001
Turkey 2465 2003–2007 6900 to 11,3001
REGION 85,555 239,500 393,600

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


[TableWrap ID: pone-0035671-t011] doi: 10.1371/journal.pone.0035671.t011.
Table 11  Reported and estimated incidence of cutaneous leishmaniasis in the Middle East to Central Asia.
Reported CL cases/year Years of report Estimated annual CL incidence
Afghanistan 22,620 2003–2007 113,100 to 226,2001
Armenia 0 2008
Azerbijan 17 2004–2008 50 to 802
China 0 2004–2008
Georgia 5 2004–2008
Iran (Islamic Republic of) 24,630 2004–2008 69,000 to 113,3002
Iraq 1655 2004–2008 8300 to 16,5003
Kazakhstan 15 2004–2008 40 to 702
Kyrgyzstan 0 2004–2008
Mongolia no data
Oman 5 2004–2008 15 to 202
Pakistan 7752 2004–2008 21,700 to 35,7002
Saudi Arabia 3445 2004–2008 9600 to 15,8002
Tajikistan 25 2007–2008 125 to 2503
Turkmenistan 99 2004–2008 490 to 9903
Ukraine 2 2004–2008 10 to 203
Uzbekistan 142 2004–2008 710 to 14003
Yemen 603 2005–2009 3000 to 60003
REGION 61,013 226,200 416,400

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).


[TableWrap ID: pone-0035671-t012] doi: 10.1371/journal.pone.0035671.t012.
Table 12  Reported and estimated incidence of cutaneous leishmaniasis in the Indian subcontinent.
Reported CL cases/year Years of report Estimated annual CL incidence
India 156 2005–2009 1000 to 20001
Sri Lanka 322 2004–2008 900 to 15002
REGION 478 1900 to 3500

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].


[TableWrap ID: pone-0035671-t013] doi: 10.1371/journal.pone.0035671.t013.
Table 13  Global reported and estimated incidence of visceral leishmaniasis.
Reported VL cases/year Countries with 5 years of data Estimated annual VL incidence
Americas 3662 8/11 (73%) 4500 to 6800
Sub-Saharan Africa 1 3/11 (27%)
East Africa 8569 5/8 (63%) 29,400 to 56,700
Mediterranean 875 21/26 (81%) 1200 to 2000
Middle East to Central Asia 2496 14/17 (82%) 5000 to 10,000
South Asia 42,623 3/6 (50%)* 162,100 to 313,600
Global total 58,227 54/79 (68%) 202,200 to 389,100

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


[TableWrap ID: pone-0035671-t014] doi: 10.1371/journal.pone.0035671.t014.
Table 14  Global reported and estimated incidence of cutaneous leishmaniasis.
Reported CLcases/year Countries with 5 yearsof data Estimated annual CL incidence
Americas 66,941 14/20 (70%) 187,200 to 307,800
Sub-Saharan Africa 155 5/15 (33%) 770 to 1500
East Africa 50 0/6 (0%) 35,300 to 90,500
Mediterranean 85,555 17/26 (65%) 239,500 to 393,600
Middle East to Central Asia 61,013 16/18 (89%) 226,200 to 416,400
South Asia 322 2/2 (100%) 1900 to 3500
Global total 214,036 53/87 (61%) 690,900 to 1,213,300


Article Categories:
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        • Leishmaniasis
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