Persisting leprosy transmission despite increased
control measures in an endemic cluster in Brazil:
the unfinished agenda
CARLOS H. ALENCAR*, ALBERTO N. RAMOS JR*,
JAQUELINE C. BARBOSA*, LIGIA R.F.S. KERR*,
MARIA L.W. DE OLIVEIRA** &
*Department of Community Health, School of Medicine, Federal
University of Ceara ´, Fortaleza, Brazil
**School of Medicine, Federal University of Rio de Janeiro – Rio de
Janeiro (RJ), Brazil
***Anton Breinl Centre for Public Health and Tropical Medicine,
School of Public Health, Tropical Medicine and Rehabilitation
Sciences, James Cook University, Townsville, Australia
Accepted for publication 08 August 2012
Brazil’s high transmission areas.
Design: We obtained data from municipalities in a major disease cluster from
databases for notifiable diseases of four states (Maranha ˜o, Para ´, Tocantins, Piauı ´),
including notifications from 2001 to 2009. Indicators for monitoring and evaluation
of leprosy according to the World Health Organization were evaluated with emphasis
on the rates of new cases presenting grade-2 disabilities and among children
,15 years of age, indicating late diagnosis and active transmission, respectively.
Results:A total of 82,463 leprosy cases were detected in the area (mean annual case
detection rate: 95.9/100,000; RR ¼ 4.56 as compared to the rest of Brazil; 95% CI:
4.45–4.66, P , 0.0001). There was a steady decrease of detection rates in the study
period, from 100.8 to 75.6/100,000 inhabitants. In children ,15 years of age, 9,009
cases of leprosy were detected (28.40/100,000), significantly more than in the rest of
Brazil (RR ¼ 5.80; 95% CI: 5.39–6.25, P , 0.0001). New cases with grade-2
disabilities/100,000 population maintained a stable trend at a high level (4.43 cluster
vs. 1.28 rest of country; RR ¼ 3.46; 95% CI: 3.11–3.84, P , 0.0001), whereas the
proportion of new cases with grade-2 was slightly lower than the country’s average
(5.51% vs. 6.75%; RR ¼ 0.84; 95% CI: 0.81–0.86, P , 0.0001).
To provide an evidence base for improvement of leprosy control in
Correspondence to: J. Heukelbach, Departamento de Sau ´de Comunita ´ria, Universidade Federal do Ceara ´,
Rua Professor Costa Mendes, 1608. 58 andar. Bairro: Rodolfo Teo ´filo. Fortaleza-CE. CEP: 60430-140;
Lepr Rev (2012) 83, 344–353
major active transmission and late diagnosis in the cluster. Further specific actions are
needed to improve early case detection and prompt treatment with the aim to reduce
disease burden in the population, considering social inequities.
Despite recently improved leprosy control measures, there is still
Leprosy is still endemic in Brazil: in 2009, more than 38,000 cases were notified in the
country (93% of cases in the Americas), presenting the highest detection rate worldwide, with
19.64 cases/100,000 inhabitants.1–2There are tremendous regional differences of case
detection rates in Brazil, evidenced by areas with virtually no transmission, mainly in the
southern regions, and other regions with extremely high detection rates.3–5These areas are
also the richest and poorest regions in the country, respectively.
As a consequence, the National Hansen’s Disease Control Program focussed activities
more and more on highly endemic disease clusters. These well-defined clusters are based on
data from compulsory case notification, provided by the nation-wide unique disease
surveillance system, and were identified by spatial analysis.6Due to the nature of analysis,
municipalities with low detection rates geographically close to those with high detection rates
were included in the clusters. By intensifying case finding in these municipalities with low
detection rates, a further reduction of transmission and disease burden caused by hidden
prevalence cases, and improved early case detection, can be expected.4–5
The disease cluster with greatest geographical extension includes parts of the four
states Maranha ˜o, Para ´, Tocantins and Piauı ´ in the north and northeast regions of the country
(Figure 1).4,6The area has a total population of about 10 million. This represents only 1/20
of Brazil’s population, but with its 7,524 new cases detected in 2009 included about 1/5 of
all notified cases. The case detection rate in the cluster was 75.6/100,000 inhabitants in that
Recently, the Brazilian Research Council (Conselho Nacional de Desenvolvimento
Cientı ´fico e Tecnolo ´gico, CNPq) and the Department of Science and Technology of the
Brazilian Ministry of Health (DECIT) provided substantial funding for research projects
in the 10 major and most significant endemic leprosy clusters in collaboration with the
National Hansen’s Disease Control Program. Thus we were able to perform multidiscipli-
nary epidemiological research in the most significant of these clusters (denominated
INTEGRAHANS – MAPATOPI – an acronym derived from the four involved federal states
Maranha ˜o, Para ´, Tocantins, and Piauı ´), to provide an evidence base for improvement of
leprosy control in Brazil’s high transmission areas.8–9
In the present investigation, we analysed epidemiological data from this cluster in detail,
focussing on time trends and indicators for early case detection and active transmission.
All 373 municipalities located in a major leprosy endemic cluster, defined by the National
Hansen’s Disease Control Program were included (Figure 1).6This area is composed of four
states in north and central Brazil with a population distribution as detailed in Table 1.
Persisting leprosy transmission in Brazil345
We obtained secondary epidemiological data from the state databases of notifiable
diseases (Sistema de Informac ¸a ˜o de Agravos de Notificac ¸a ˜o – SINAN) and then merged
datasets. Notifications from 1st January 2001 to 31st December 2009 were included in
analysis. For calculation of leprosy case detection rates, population estimates of the
respective years were obtained from the database of the Brazilian Institute of Geography and
Statistics (Instituto Brasileiro de Geografia e Estatı ´stica – IBGE).10
Table 1. Population data of a high risk leprosy cluster in north Brazil.
Number of Municipalities Population in 2009Proportion of Population (%)
Maranha ˜o State
Para ´ State
Piauı ´ State
All four States
223 3,145,164 39.7
Fig. 1. Cluster of high transmission risk situated in the states Maranha ˜o, Para ´, Tocantins and Piauı ´.
C.H. Alencar et al.346
We calculated the indicators for monitoring and evaluation according to the “Enhanced
Global Strategy for Further Reducing the Disease Burden due to Leprosy” by WHO11: rate
of new cases/100,000 population, rate of new cases with grade-2 disabilities/100,000
population, cure rate (for monitoring progress); proportion of cases presenting with grade-2
disabilities, proportion of child cases, proportion of female patients, and proportion of
multibacillary cases among new cases (for evaluating case detection); and proportion of
new cases verified as correctly diagnosed, proportion of treatment defaulters, and proportion
of relapses (for assessing the quality of services). Indicators were also observed over time.
The proportion of patients who developed new or additional disabilities during multidrug
therapy is not presented, as this information was available in ,50% of cases.
Stata 11 software was used for statistical analysis. Significance of the difference of
relative frequencies was assessed using the Pearson chi squared test. We calculated rate
ratios (RR) and respective exact confidence intervals.
In the period from 2001 to 2009, a total of 82,463 leprosy cases were detected in the cluster.
Table 2 details the indicators for monitoring and evaluation according to the Word Health
Organization’s Enhanced Global Strategy. The mean general case detection rate in the study
period was 95.9/100,000 per year, whereas in the rest of Brazil 21.0 cases/100,000 inhabitants
were notified (RR ¼ 4.56; 95% CI: 4.45–4.66, p, 0.0001). In Para ´, case detection was
Table 2. Indicators for monitoring and evaluation according to the Enhanced Global Strategy for Further Reducing
the Disease Burden due to Leprosy (WHO), in a leprosy endemic cluster in North Brazil, 2001 to 2009.
Maranha ˜o*Para ´* Tocantins*Piauı ´*
Indicators for monitoring progress
New cases detected/100.000 pop.
New cases detected ,15 years/100.000 pop.
New cases with grade-2 disabilities/100.000 pop.
Treatment completion/cure rate
Indicators for evaluating case detection
% assessment of disabilities at diagnosis
% new cases grade-2
% new cases female patients
% clinical form
Indicators for evaluating quality of services
% new cases correctly diagnosed
% treatment defaulters
*Only municipalities in endemic cluster
Persisting leprosy transmission in Brazil 347
During the period of study, the detection rate declined from 100.8 to 75.6/100,000
inhabitants per year in the cluster, with a more pronounced decrease since 2006 (Figure 2).
The largest decrease (63%) was observed in Para ´, but this area still had the highest detection
rate in 2009, as compared to the other states. Tocantins’ municipalities showed a detection
rate of 77.8 to 88.4/100,000 and a tendency of stabilization in the last four years. The
municipalities in Maranha ˜o showed a downward trend since 2005, and Piauı ´ did not reveal
any clear trend. In the rest of Brazil, this indicator was around 16/100,000 inhabitants/year
during the observation period (Figure 2).
The trend in ,15 year-olds showed similar patterns to the general case detection rate,
with elevated rates in all four states (Figure 2). Similar to the general population, the highest
detection rate in children was found in Para ´ (Table 2). In children ,15 years of age, a total of
9,009 cases of leprosy (28.6% of all Brazilian child cases) were detected in the cluster
(detection rate: 28.40/100,000), which was significantly higher as compared to the rest of
Brazil (RR ¼ 5.80; 95% CI: 5.39–6.25, P , 0.0001; Table 2).
2002 20032004 2005
2001 20022003 20042005 20062007 2008 2009
Rest of BrazilTocantins
Rest of BrazilPiauí
New cases/100000 inh·
New cases/100000 inh·
Fig. 2. New cases of leprosy detected/100,000 population per year in a high-risk area in Brazil, 2001 to 2009: (A)
general detection rate; (B) ,15 year-olds.
C.H. Alencar et al. 348
The rate of new cases with grade-2 disabilities/100,000 population was significantly
higher in the cluster than in the rest of Brazil (RR ¼ 3.46; 95% CI: 3.11–3.84, P , 0.0001).
On the other hand, the proportion (%) of new cases with grade-2 was lower than the country’s
average (RR ¼ 0.84; 95% CI: 0.81–0.86, P , 0.0001) (Table 2). The rate of new cases with
grade-2 disabilities/100,000 population showed a similar trend as the general detection rate
(Figure 3). The detection rate showed an inversed trend.
With the exception of Tocantins, defaulter rates were higher than in the rest of Brazil, but
the number of relapses was lower. The proportion of multibacillary cases at the time of
diagnosis was 52.3% in the cluster (RR ¼ 0.98; 95% CI: 0.97–0.98, P , 0.001). The largest
proportion was detected in the State of Maranha ˜o (56%). Borderline or lepromatous clinical
forms represented 50% of cases in the cluster and 52% in the rest of Brazil (RR ¼ 0.96; 95%
CI: 0.95–0.97, P , 0.001); the lowest proportion was in the states of Tocantins (39.7%), and
Piauı ´ (37.6%) (Table 2).
In total, in the cluster there were 84.9% (69,220) leprosy cases with their degree of
disability assessed at diagnosis, less than in the rest of Brazil. Maranha ˜o had the lowest
proportion of cases evaluated (79.0%), whereas in Piauı ´ and Para ´ more than 90% of cases in
the cluster were evaluated (Table 2). Among available cases, 18.1% (13,112) had a disability
of grade-1 and 5.5% (3,811) of grade-2 (Table 2).
In the past years, the Hansen’s Disease Control Program of Brazil’s Ministry of Health has
focussed its actions to a greater extent on defined geographical areas (clusters). The present
study shows that in one of these major clusters which encompasses about 5% of Brazil’s
population, the overall detection rate was more than four times higher than in the rest of the
country, and in ,15 year-olds even about six times. This shows that active leprosy
transmission is continuing at high levels in the region. In addition, the indicators suggest late
diagnosis in many cases. Despite the successes made in the last years, there is thus still a long
Detection rateGrade 2 rate% Grade 2
200420052006 20072008 2009
Rate G2/100000 inh. - %Grade-2
Fig. 3. Trend of new cases detected/100,000 population, rate of new cases with grade-2/100,000 population and
proportion of new cases with grade-2 disabilities in a leprosy endemic cluster in North Brazil, 2001 to 2009.
Persisting leprosy transmission in Brazil349
way to go to reach low detection rates. The study also reinforces that prioritizing and
intensifying control measures in these clusters should be maintained.6
The ascending trend of leprosy detection rates since the 1980s in Brazil seems to have
reached its peak and is expected to show a tendency of stabilisation/reduction in the next few
years.5–6,12The time series from 2001 to 2009 presented in our study shows stable detection
ratesoftheclustermunicipalitiesinthreestates.Para ´ detectionratesdeclinedconsiderably,but
remained at very high levels. This was paralleled by the trend of the detection rate in children.
These trend observations are likely caused by operational factors and not by epidemiological
been established in the observation period, and in fact it can be expected that in future years
detection rates and indicators for late diagnosis will decrease, if the current control
programme’s policy continues. For example, in Para ´ the reduction of detection rates was
Program is almost 100% for several years, lowest values were observed for grade-2 disability/
The decentralised actions of this primaryhealthcare approach may have influenced positively
leprosy control measures.15–16
In 2009, WHO launched a new global target based on grade-2 disabilities/100,000
population, and a reduction goal of at least 35% by the end of 2015 as compared to 2010 was
set.11From 1995 to 2009, Brazil has reduced grade-2 disabilities in newly diagnosed patients/
population by only about 13% every 5 years, which is far away from this target.11,17In the
same period, India and Thailand showed reduction rates of this indicator of 54% and 36%
every 5 years, whereas China reduced this indicator by 8%, after a more pronounced
reduction in the previous years.17On the other hand, these reductions may also be caused by
different operational approaches, and data should be interpreted with care.18
Whereas this new indicator and the target may reflect better the progress of control
measures,19this is still based on entire countries. Clearly, this may be appropriate for small
countries, but care should be taken in the case of nations with continental dimensions such as
Brazil and India, which show tremendous regional differences of leprosy detection rates, with
areas where the disease is virtually nonexistent, and other regions with ongoing
transmission.5As mentioned above, Brazil’s Ministry of Health has approached this
problem by targeting high risk areas for transmission, identified by spatial analysis.6
In the endemic cluster, the rate of new cases with grade-2/100,000 population remained
stable over the study period, with the exception of a peak in 2007. In 2007 a change in the
grade coding was undertaken and not all municipalities used this new code; as a result this
peak should not be considered with the same confidence as data of the other years.20In the
same period, the general detection rate showed a decrease after an initial increase, whereas
the proportion of new cases with grade-2 disabilities showed an inverse trend. This may
reflect established control actions in the area: increased actions to detect leprosy cases
revealed lower proportions of grade-2 disabilities at diagnosis, and early diagnosis improved
over time. On the other hand, there may be other operational problems present, such as the
quality of assessment of disabilities, and possibly over-diagnosis of grade-2.20The rate of
new cases with grade-2 disabilities per 100,000 population has been considered to be less
influenced by operational factors – it focuses attention on prevention of disabilities and
stimulates early detection and is probably a robust marker of the level of the occurrence of the
C.H. Alencar et al.350
disease in the community.19–20In addition, the proportion of grade-2 cases in a population
will give a proxy of the general burden of disease on the population level, independent from
case detection rates and prevalence.17,19
Our analysis also suggests late diagnosis of leprosy to an important extent in the cluster.
The proportion of new cases with grade-2 disabilities was highest in Maranha ˜o, indicating
late diagnosis mainly in this state. In addition, in Maranha ˜o, indeterminate leprosy was less
common and frequency of multibacillary cases highest. Maranha ˜o is one of the poorest states
in Brazil, and decentralisation including population coverage of the Family Health Program
is yet far below the target.
On the other hand, the proportion of female patients and multibacillary cases among new
cases showed higher levels outside the cluster than inside. This may reflect a recent success of
strategies of leprosy control directed to the highly endemic areas of Brazil.5However, leprosy
control should not only focus on areas with a high number of cases, but also on most
vulnerable areas and populations, considering economic and social differences present in low
and middle income countries.21–22
Similar to many other infectious diseases, leprosy has been considered a poverty-related
disease.23–24In Brazilian municipalities with more heterogeneous income distribution, the
chance of leprosy as a public health problem was higher.25In fact, the index of subjective
poverty in the study area is close to 90%, while in the South Region of Brazil, where there is
no active transmission of leprosy,5this index is about 15%.26There is also evidence about
association of leprosy incidence and social conditions in the Amazon region, which
comprises some states of the cluster studied here.27In this context, the ongoing social
governmental policies for reducing extreme poverty will certainly minimise vulnerability of
the population to a variety of diseases, including leprosy.28
Disease Control Program, through the application of Operational Research in collaboration
address areas for improvement of the control programmes at local and state levels.29
The endemic cluster under study presented high levels of leprosy detection rates both in the
general population and in children ,15 years, and of grade-2 disabilities, indicating ongoing
transmission and late diagnosis. Despite established leprosy control in Brazil, in highly
endemic areas, focussed integrated actions are needed to further improve early case detection
and prompt treatment with the aim to reduce disease burden in the population. As leprosy and
its complications are associated with poverty, interventions should also consider social
inequities in the region.
This paper forms part of the MAPATOPI study, an interdisciplinary project providing
evidence for improving the Brazilian Hansen’s Disease Control Program. The project is
co-financed by the Brazilian Research Council (Conselho Nacional de Desenvolvimento
Cientı ´fico e Tecnolo ´gico, CNPq) and the Department of Science and Technology of the
Brazilian Ministry of Health (DECIT). JH and LRFSK are research fellows from CNPq. We
Persisting leprosy transmission in Brazil351
thank Fundac ¸a ˜o Coordenac ¸a ˜o de Aperfeic ¸oamento de Pessoal de Nı ´vel Superior (CAPES,
Brazil) for granting a PhD scholarship to CHA. The State Leprosy Control Programs of the
State Health Secretariats of Maranha ˜o, Para ´, Tocantins and Piauı ´ kindly provided data sets.
1WHO. World Health Organization. Global leprosy situation, 2009. Wkly Epidemiol Rec, 2010; 85: 337–348.
2Brasil. Brası ´lia: Ministe ´rio da Sau ´de; 2010 [cited 2011]; Available from: http://portal.saude.gov.br/portal/saude/
3Magalha ˜es MCC, Rojas LI. Diferenciac ¸a ˜o territorial da hansenı ´ase no Brasil. Epidemiol Serv Sau ´de, 2007; 16:
4Penna ML, Oliveira ML, Penna G. Spatial distribution of leprosy in the Amazon region of Brazil. Emerg Infect
Dis, 2009; 15: 650–652.
5Penna ML, Oliveira ML, Penna GO. The epidemiological behaviour of leprosy in Brazil. Lepr Rev, 2009; 80:
6Brasil. Relato ´rio Executivo do PNCH Ministe ´rio da Sau ´de. Perı ´odo Maio de 2007 a Junho de 2008. Brası ´lia:
Secretaria de Vigila ˆncia em Sau ´de. Programa Nacional de Controle da Hansenı ´ase. Mimeo; 2008
7Alencar CH, Ramos Jr AN, Sena Neto SA, Heukelbach J. Epidemiologia da hansenı ´ase em a ´rea de alto risco de
transmissa ˜o nos estados do Para ´, Tocantins, Maranha ˜o e Piauı ´, 2001 a 2009. Presentation at XLVII Brazilian
Society of Tropical Medicine Congress. Rev Soc Bras Med Trop. 2011.
8Chichava OA, Ariza L, Oliveira AR, Ferreira AC, Marques Da Silva LF, Barbosa JC et al. Reasons for
interrupting multidrug therapy against leprosy: the patients’ point of view. Lepr Rev, 2011; 82: 78–79.
9Heukelbach J, Chichava AO, Oliveira AR, Hafner K, Walther F, Alencar CH et al. Interruption and Defaulting of
Multidrug Therapy against Leprosy: Population-Based Study in Brazil’s Savannah Region. PLoS Negl Trop Dis,
2011; 5: e1031.
10DATASUS. http://tabnet.datasus.gov.br/cgi/deftohtm.exe?ibge/cnv/popbr.def, accessed at July 1st, 2011. 2011.
11WHO. World Health Organization. Enhanced Global Strategy for Further Reducing the Disease Burden due to
Leprosy (Plan Period: 2011–2015). 2009: 28.
12Penna ML, Penna GO. Trend of case detection and leprosy elimination in Brazil. Trop Med Int Health, 2007; 12:
13Penna ML, Oliveira ML, Carmo EH, Penna GO, Tempora ˜o JG. The influence of increased access to basic
healthcare on the trends in Hansen’s disease detection rate in Brazil from 1980 to 2006. Rev Soc Bras Med Trop,
2008; 41(Suppl II): 6–10.
14Brasil. Ministe ´rio da Sau ´de. Departamento de Atenc ¸a ˜o Ba ´sica. Evoluc ¸a ˜o do credenciamento e implantac ¸a ˜o
da estrate ´gia Sau ´de da Famı ´lia. Brası ´lia2011 [01/07/2011]; Available from: http://dab.saude.gov.br/
15Lanza FM, Lana FCF. Decentralization of leprosy control actions in the micro-region of Almenara, State of Minas
Gerais. Rev Latinoam Enfer, 2011; 19: 187–194.
16Atkinson S, Haran D. Back to basics: does decentralization improve health system performance? Evidence from
Cear· in north-east Brazil. Bull World Health Organ, 2004; 82: 822–827.
17Alberts CJ, Smith WCS, Meima A, Wang L, Richardus JH. Potential effect of the World Health Organization’s
2011–2015 global leprosy strategy on the prevalence of grade 2 disability: a trend analysis. Bull World Health
Organ, 2011; 89: 487–495.
18Richardus JH, Habbema JD. The impact of leprosy control on the transmission of M. leprae: is elimination being
attained? Lepr Rev, 2007; 78: 330–337.
19Declercq E. Reflections on the new WHO leprosy indicator: the rate of new cases with grade 2 disabilities per
100,000 population per year. Lepr Rev, 2011; 82: 3–5.
20Oliveira MLW, Grossi MAF, Oliveira CF, Sena Neto SA, Daxbacher E, Penna GO. Commitment to reducing
disability: the Brazilian experience. Lepr Rev, 2010; 81: 342–345.
21Lindoso JAL, Lindoso AABP. Neglected tropical diseases in Brazil. Rev Inst Med Trop Sao Paulo, 2009; 51:
22Mencaroni DA, Pinto Neto JM, Villa TCS, Oliveira MHP. Ana ´lise espacial da endemia hanse ˆnica na a ´rea urbana
do Municı ´pio de Fernando ´polis/SP. Hansen Int, 2004; 29: 12–20.
23Feenstra SG, Nahar Q, Pahan D, Oskam L, Richardus JH. Recent Food Shortage Is Associated with Leprosy
Disease in Bangladesh: A Case-Control Study. PLoS Negl Trop Dis, 2011; 5: e1029.
24Kerr-Pontes LR, Barreto ML, Evangelista CM, Rodrigues LC, Heukelbach J, Feldmeier H. Socioeconomic,
environmental, and behavioural risk factors for leprosy in North-east Brazil: results of a case-control study. Int J
Epidemiol, 2006; 35: 994–1000.
C.H. Alencar et al.352
25Kerr-Pontes LR, Montenegro AC, Barreto ML, Werneck GL, Feldmeier H. Inequality and leprosy in Northeast Download full-text
Brazil: an ecological study. Int J Epidemiol, 2004; 33: 262–269.
26IBGE. Censo Demogra ´fico 2000 e Pesquisa de Orc ¸amentos Familiares - POF 2002/2003. 2003 [cited 2011];
Available from: http://www.ibge.gov.br/estadosat/index.php
27Silva DRX, Ignotti E, Souza-Santos R, Hacon SS. Hansenı ´ase, condic ¸o ˜es sociais e desmatamento na Amazo ˆnia
brasileira. Rev Panam Salud Publica, 2010; 27: 268–275.
28Brasil. Projeto Fome Zero. Instituto de Cidadania, 2002; 3: 1–118.
29Ramos AN, Jr, Heukelbach J, Gomide M, Hinders DC, Schreuder PA. Health systems research training as a tool
for more effective Hansen’s disease control programmes in Brazil. Lepr Rev, 2006; 77: 175–188.
Persisting leprosy transmission in Brazil353