Comparison between active surveillance and passive detection of zoonotic cutaneous leishmaniasis in endemic rural areas in Central Tunisia, 2009 to 2014

Abstract

Objective: To assess the contribution of active surveillance of zoonotic cutaneous
leishmaniasis (ZCL) in rural areas in Sidi Bouzid from 2009 to 2014 in comparison with the
passive case detection, and describe the pattern of the disease.
Methods: The monitoring was based on the notification of all new cases in primary health care
facilities, among pupils in all schools and a community-based active ZCL surveillance was also
performed. The medical staff of health care facilities reviewed and confirmed cases notified in
schools.
Results: From July 2009 to June 2014, a total of 856 (51.1% male, 48.9% female) cases
were enrolled; the average incidence rate of the disease was 2 514.4 per 100 000 inhabitants.
The median age was 11 years (inter quartile range: 7-28) and 68.9% were aged less than 20
years. Most ZCL lesions arose between August and January and 46.1% of cases were reported
between July 2013 and June 2014. Active surveillance reported more cases mainly in the
delegation of West Sidi Bouzid and most cases (66.7%) were reported by the health care
centers.
Conclusions: The present study showed ZCL was still endemic in rural areas in Sidi Bouzid
Governorate. Active surveillance's cost-effectiveness is not certain thus, it would be rational
to improve routine passive detection of ZCL in Sidi Bouzid than to continue active research of
cases.

Full text

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Epidemiology investigation doi: 10.1016/S2222-1808(15)60827-1 ©2015 by the Asian Pacific Journal of Tropical Disease. All rights reserved.
Comparison between active surveillance and passive detection of zoonotic cutaneous leishmaniasis in
endemic rural areas in Central Tunisia, 2009 to 2014
Hedia Bellali1,2*, Aicha Hchaichi1, Chahida Harizi1, Ali Mrabet2,3, Mohamed Kouni Chahed1,2
1Epidemiology and Statistics Department, A Mami Hospital, Ariana, Tunisia
2Epidemiology and Public Health Department, Medical University of Tunis, Tunisia
3Health Military Directorate, Bab Saadou Tunis, Tunisia
Asian Pac J Trop Dis 2015; 5(7): 515-519
Asian Pacific Journal of Tropical Disease
journal homepage: www.elsevier.com/locate/apjtd
*Corresponding author: Hedia Bellali, Epidemiology and Statistics Department, A
Mami Hospital, Ariana 2080, Tunisia.
Tel: 0021670160361/0021698639824
E-mail: hedia.bellali@gmail.com
Foundation Project: Supported by the International Development Research Center
of Canada (www.crdi.ca) (research project N° 105509-044).
1. Introduction
Leishmaniasis is one of the neglected tropical diseases which are
a group of parasitic diseases and related infections that represent
the most common illnesses of the world’s poorest people[1]. It is
a zoonotic disease endemic in the Mediterranean basin, including
Tunisia[2,3]. Zoonotic cutaneous leishmaniasis (ZCL), caused by
Leishmania major (L. major), is widespread in the Middle East and
North Africa region. The largest number of L. major cases occurs
in the arid and Saharian bioclimatic stages[4-6]. Central Tunisia
is the most endemic area; cases were reported mainly from the
governorate of Sidi Bouzid, Kairouan and Gafsa[7-9].
Public health control measures in any country are strongly
dependent on the information coming from the surveillance
systems. The World Health Organization expert committee
report 2010[2], stated that passive case detection and reporting of
cutaneous leishmaniasis should be the basis for a control program.
In Tunisia, control program of ZCL was implemented since 1990.
The routine surveillance system in Tunisia relies on physicians
and primary health care personal who observe ZCL patients and
the data of notified cases are delivered from primary health care
facilities to regional public health directorate, then to the central
directorate of public health, Ministry of Health. Passive detection
of communicable diseases suffers from severe underreporting
mainly in developing countries and the public health impact of
leishmaniasis is underestimated[10]. This study was part of an
exhaustive population based survey using the ecohealth approach
to improve the understanding of the various interacting climatic,
ecological, epidemiological, agricultural and socio-economic
factors that cause ZCL as well as to investigate possible options for
decreasing the vulnerability of local populations.
ARTICLE INFO ABSTRACT
Objective: To assess the contribution of active surveillance of zoonotic cutaneous
leishmaniasis (ZCL) in rural areas in Sidi Bouzid from 2009 to 2014 in comparison with the
passive case detection, and describe the pattern of the disease.
Methods: The monitoring was based on the notification of all new cases in primary health care
facilities, among pupils in all schools and a community-based active ZCL surveillance was also
performed. The medical staff of health care facilities reviewed and confirmed cases notified in
schools.
Results: From July 2009 to June 2014, a total of 856 (51.1% male, 48.9% female) cases
were enrolled; the average incidence rate of the disease was 2 514.4 per 100 000 inhabitants.
The median age was 11 years (inter quartile range: 7-28) and 68.9% were aged less than 20
years. Most ZCL lesions arose between August and January and 46.1% of cases were reported
between July 2013 and June 2014. Active surveillance reported more cases mainly in the
delegation of West Sidi Bouzid and most cases (66.7%) were reported by the health care
centers.
Conclusions: The present study showed ZCL was still endemic in rural areas in Sidi Bouzid
Governorate. Active surveillance's cost-effectiveness is not certain thus, it would be rational
to improve routine passive detection of ZCL in Sidi Bouzid than to continue active research of
cases.
Contents lists available at ScienceDirect
Article history:
Received 7 Oct 2014
Received in revised form 15 Oct 2014,
2nd revised form 26 Nov 2014
Accepted 15 May 2015
Available online 25 May 2015
Keywords:
Zoonotic infections
Leishmaniasis
Surveillance
Central Tunisia

Hedia Bellali et al./Asian Pac J Trop Dis 2015; 5(7): 515-519
516
In this paper, we assessed the contribution of an active
surveillance system to improve passive case detection and described
characteristics of new cases in terms of date, place and persons.
2. Materials and methods
The surveillance network was implemented in three delegations in
the governorate of Sidi Bouzid since July 2009. Ten rural districts
(Bir Badr, Hichria, Zefzef, Souk Jedid, Rmilia, Sakdel, Gsaira, Garet
Hadid, Friou and Zitouna) with a total population of around 34 044,
were covered by this active detection of ZCL cases.
The monitoring was based on the notification of all new cases
in people who came to primary health care facilities seeking for
treatment, and the active research of other cases among their
neighbors and families by the nursing staff. All schools in this
area have been asked to seek for and notify all ZCL cases among
students. Moreover, a community-based active ZCL surveillance
was performed by the members of the research team. The medical
staff of the health care facilities reviewed and confirmed cases
notified in schools on the basis of clinical diagnosis of the lesion or
scars. Because of the good knowledge of the disease by the medical
staff and the population in this region and the high sensitivity and
specificity of clinical diagnosis, parasitologic diagnosis of ZCL
lesions was not carried out. We organized two conferences in 2010
and 2013 for public health care facilities and schools staff to inform
and aware them of the importance of ZCL reporting. Information on
age, sex, place of residence, date of diagnosis and date of onset of the
lesion, the number and the location of the lesions and the treatment
and evolution were collected using a standardized case record cart.
Data on ZCL from mandatory notification of communicable diseases
was used to compare incidence rates between active and passive
detections. Estimated population data by districts for 2012 was
obtained from the National Institute of Statistics.
3. Results
During the study period, from 2009 to 2014, 856 (51.1% male,
48.9% female) cases of ZCL were enrolled. With an average of 171
new cases occurring each year during 2009-2014 and a population
at risk estimated to be 34 044, the average annual incidence rate of
the disease in this foci was calculated to be approximately 502.9
per 100 000 people and the average total period incidence rate
was calculated to be 2 514.4 cases per 100 000 inhabitants. Table 1
shows number of cases and incidence rate by districts and Figure 1
represents spatial distribution of ZCL cases. The median age was 11
years (inter quartile range: 7-28), ranging from 2 months to 87 years
and most of the patients were assigned to the 0-9 and 10-19 years
age groups with approximately 40% and 30% of the total recorded
ZCL cases respectively for each group. Distribution of cases by
sex and age was shown in Figure 2. In the area under study, the
maximum number of cases (46.1% of total) was recorded between
July 2013 and June 2014 and the least number of cases reported
was in 2009-2010 season with 58 cases (6.8% of total). Recurrent
ZCL was observed in 5.0% of subjects. The lower limb was the most
frequent seat of ZCL lesion (48.0%) and 13.9% had reported face
lesions. About 42.6% had a single lesion and the infection of the
3847000 3854000 3861000 3868000 3875000
3847000 3854000 3861000 3868000 3875000
Zitouna
Sakdel
Souk Jedid
Bir Bader
Rmilia
Zefzef
0 2.5 5 10km
528 000 535 000 542 000 549 000 556 000 563 000 570 000
528000 535000 542000 549000 556000 563000 570000
ZCL cases 2009-2014
Administrative limits
Garaat Njila
Garet Hadid
Bouatouch
N
Hichria
Friou
Figure 1. Spatial distribution of cases by area of residence, active surveillance of ZCL in Central Tunisia, July 2009-June 2014.

Hedia Bellali et al./Asian Pac J Trop Dis 2015; 5(7): 515-519 517
lesion occurred in 7.9% persons. Only 7 subjects were admitted to
hospital, lesions treatment consisted in local disinfection (64.7%)
and antibiotics (21.3%); the spontaneous healing was observed for
95.8% of individuals (Table 2).
Table 1
Number of ZCL and incidence rate by districts, active surveillance in
Central Tunisia, July 2009-June 2014.
Locality Number
of cases
Population Incidence rate
per 100 000
Mean annual incidence
rate per 100 000
Hichria 130 4 250 3 058.8 611.8
Friou 11 4 242 259.3 51.9
Zitouna 12 3 922 305.9 61.2
Garet Hadid 2 3 293 60.7 12.1
Souk Jedid 436 2 758 15 808.6 3 161.6
Gsaira 25 2 263 1 104.7 220.9
Sakdel 14 2 748 509.5 101.9
Rmilia 20 3 281 609.6 121.9
Zefzef 92 3 385 2 717.9 543.6
Bir Badr 114 3 902 2 921.6 584.3
Total 856 34 044 2 514.4 502.9
50
40
30
20
10
0
Percent
0-9 10-19 20-29 30-39 40-49 50-59 60 and over
Age groups (years)
Male Female
Figure 2. Distribution of cases by sex and age group, active surveillance
of ZCL in Central Tunisia, July 2009-June 2014.
Table 2
Epidemiological characteristics of ZCL, active surveillance in Central
Tunisia, July 2009-June 2014.
Characteristics N%
Sex Male 437 51.1
Female 419 48.9
Age in years 0-9 338 39.5
10-19 251 29.3
20-29 56 6.5
30-39 54 6.3
40-49 69 8.1
50-59 43 5.0
60 and over 44 5.1
Season of the lesion
onset
July 2009-June 2010 58 6.8
July 2010-June 2011 198 23.2
July 2011-June 2012 129 15.1
July 2012-June 2013 76 8.9
July 2013-June 2014 394 46.1
Recurrent ZCL Yes 43 5.0
No 813 95.0
Seat of the lesion Face 149 13.9
Trunk 62 5.8
Upper limbs 348 32.4
Lower limbs 516 48.0
Number of lesions 1 364 42.6
2 209 24.4
3 118 13.8
4 and more 164 19.2
Infected lesions Yes 68 7.9
No 788 92.1
Admitted to hospital Yes 7 0.8
No 849 99.2
Treatment Local disinfection 827 64.7
Antibiotic 272 21.3
Local glucantime 174 13.6
Systemic glucantime 5 0.4
Outcome Spontaneous healing 820 95.8
Infection 36 4.2
Active surveillance and passive detection reported respectively a
mean incidence rate of 2 514.4 and 889.8 per 100 000 inhabitants
for the total period. The mean incidence rates calculated from active
surveillance were much higher than those given by passive detection
mainly for the delegation of West Sidi Bouzid (Table 3).
Figure 3. Distribution of cases by the month of lesion onset, active surveillance of ZCL in Central Tunisia, July 2009-June 2014.
Number of ZCL cases
2009
160
140
120
100
80
60
40
20
0
2010 2011 2012
Month of lesion onset
2013 2014
7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6 7 8 9 10 11 12 1 2 3 4 5 6

Hedia Bellali et al./Asian Pac J Trop Dis 2015; 5(7): 515-519
518
Table 3
Incidence rate of ZCL reported from active surveillance and passive
detection, 2009-2014.
Locality Incidence rate per
100 000 inhabitants from
routine notification
Incidence rate per 100 000
inhabitants from active
surveillance
Sidi Bouzid Ouest 930.1 1 660.4
Sidi Bouzid Est 182.9 194.0
Souk Jedid 3 481.5 3 822.8
Total 889.8 2 514.4
The epidemic curve by date of lesion onset showed seasonality of
ZCL occurance. Most ZCL lesions arose between August and January
and the highest incidence was observed in October and November.
An epidemic peak was observed between July 2013 and June 2014
(Figure 3).
A total of 571 (66.7%) cases were reported by the primary health
care centers, 213 (24.9%) cases were reported by the school’s
staff and 72 (8.4%) cases were notified by the community-based
surveillance.
4. Discussion
The existence of national health plans in many countries generates
large databases that can be used for surveillance. In Tunisia,
surveillance activities are supported and managed by a variety
of vertical disease-control programmes such as tuberculosis,
leishmaniasis, malaria and rabies. But, the surveillance function is
far removed from any corresponding action such as disease control
efforts and outbreak response.
ZCL is endemic with periodic outbreaks in Central Tunisia
and outbreaks have an apparent tendency to occur at around 4-7
year intervals and cause disfiguring scars which lead to social
stigmatization[8]. Effective control methods are not available
and surveillance is necessary to study the disease, its patterns of
occurrence and the population at risk. Moreover, there is a need
for baseline data before the implementation of control measures
to monitor and evaluate them, mainly when available data and
alternative sources are not sufficient. Thus, this active surveillance
was established in order to assess the burden of ZCL, analyze its
pattern in terms of time, place and person, study possibilities of
early outbreaks detection and have a baseline database before
implementation of control strategies to monitor progress towards
control or eradication.
We describe characteristics of individuals with new cases of ZCL
and compare incidence rates between active and passive detection.
This study confirmed the high endemicity of ZCL in this area, mainly
in the locality of Souk Jedid and the seasonality of its patterns over
time. ZCL occurs in males and females, but children were the most
vulnerable. Lesions appear on exposed areas of body, mainly lower
limbs, upper limbs and face.
The disease is not fatal, favorable issue and acquired definitive
immunity were often observed. However, ZCL leaves a disfiguring
scars that may cause social impact mainly when the lesion onset is
in the face of women. The mean incidence rates reported from active
surveillance were much higher than those given by passive detection
and the primary health care facilities reported most cases.
This is the first active surveillance system for ZCL in Tunisia which
has included many data sources and collecting procedures to provide
the most accurate information collected in a practical and efficient
manner and to satisfy the goals and objectives of the surveillance
system. The collection of data is the most costly and difficult
component of a surveillance system. The quality of a surveillance
system is only as good as the quality of the data collected. Moreover,
it is essential to establish denominator data for the target population.
As they are paid, reporters and collectors were required to return
the forms monthly. Data could be incomplete since we had not
performed biological diagnosis so that not so typical lesions and
scars should be missed. However, leishmaniasis occurs commonly
in this area so that it is not necessary for all cases to be reported
and this should not reduce the effectiveness of surveillance, since it
is generally the trends of disease occurrence that are important for
decision-making on control and preventive measures.
Incidence rates of ZCL were high attesting that this area is still a
highly endemic region as it was observed in previous studies[7,8].
Souk Jedid reported most cases; however this apparent increase
could not represent true increase, since actors of active surveillance
were mainly medical staff of Souk Jedid health care facility.
Moreover, there was not a big difference in the incidence rate
compared with passive detection; as they are also the actors of
mandatory notification and it is common that active surveillance
enhances reporting from passive detection[11].
The seasonal distribution of ZCL shows that the highest rate of
infection is in autumn, the lowest is in spring and winter and the
peak of the disease occurs in October and November. In Central
Tunisia, Toumi et al. demonstrated that the incidence of the disease
was significantly higher during the group of months from October
to March[8]. A similar seasonal pattern has been reported from other
leishmaniasis endemic countries. In Libya and many provinces
(Arsanjan, Sabzevar, Damghan and Kermanshah) of Iran[12-14], the
highest percentages of patients with ZCL were reported in autumn
and the lowest in winter. Faulde et al. described the seasonality of
ZCL in Mazar-e Sharif, Afghanistan, where the maximum numbers
of ZCL cases were recorded in September and October[15]. The
transmission of leishmaniasis is highly dependent on climate
conditions and the ecology of vector and reservoirs hosts[2]. Each
species of sand fly has an annual cycle, and the highest transmission
occurs at the end of this cycle[16].
The sex distribution was found to be approximately equal in
the present study; this finding was also observed by Bettaieb et
al.[9]. Some studies in Iran have shown an equal proportion of ZCL
infection among the two sexes[17]. However in other endemic regions
of Iran and Mazar-e Sharif, Afghanistan, the frequency of male
patients with ZCL was higher than that of female patients[18]. Such
observations seem to be related to different behavior patterns among
men and women that increase or decrease vector exposure.
In this study, most cases were observed in children, suggesting
exposure of non immune persons to sandfly bite in domestic or
peridomestic places. In ZCL endemic regions of Iran, the highest
risk group is often children aged less than 15 years[17,19,20]. In fact,
in established endemic areas, people become immune against ZCL
when they get older[2].
In this study, it was observed that most of the lesions appeared
on the extremities, feet and hands and this pattern of lesion
development on the limbs is common in ZCL. In a comparative study
of skin lesions observed in three endemic varieties of cutaneous
leishmaniasis in Tunisia, ZCL lesions were often observed on the
limbs[21].
Almost 43% of the ZCL patients in this study had one skin lesion.
Many studies in endemic regions of Iran and one report from
Iraq observed that most patients presented a single lesion[6,13,14].
However, in ZCL due to L. major, multiple lesions might be seen.
In the present study, about 14% of ZCL patients have three lesions
and 19% of them have more than four lesions. Aoun et al. observed
that 75% ZCL lesions in Tunisia were multiple[21]. Likewise, several
workers in different provinces of Iran showed the high frequency
of multiple lesions in ZCL patients[19,22]. A possible explanation is
that sand flies usually have a discontinuous blood-sucking habit and
may sting several times at every attack and cause the development of
multiple lesions on the skin[2].

Hedia Bellali et al./Asian Pac J Trop Dis 2015; 5(7): 515-519 519
The primary health care facilities staff reported most cases
compared to school staff and community-based surveillance.
Indeed, this system was mainly implemented in health care facilities
and schools; detection of cases in the community was made
occasionally when the research team members are in the region
and at the beginning of each season to inform, motivate and boost
surveillance in schools especially. Our surveillance system reported
more cases than passive detection. Active surveillance has been
shown to increase the number and proportion of reported cases,
and to promote closer personal ties between the providers and the
collectors. However, active surveillance is relatively expensive, and
its cost-effectiveness is not entirely clear[11]. In this study, most
cases from active surveillance system were reported by the health
care facilities staff members. The same staff should report some
communicable diseases considered as mandatory notified, including
ZCL cases, to the health authorities. However, this way of reporting
suffers from a severe underreporting and it is decidedly due to the
fact that the staff is not motivate enough to report new cases because
of the absence of feedback information to the people who collect the
data and their low level of awareness concerning the usefulness of
the notified cases.
The present study shows that ZCL is endemic and causes a
major health problem in Central Tunisia. In order to identify all
epidemiological aspects, eco-health approach should be considered,
including climate change and its impact on vector and reservoir
behaviour, and socio-economic characteristics of the local
population.
Recommendations for changes in the surveillance system need to
consider these results so that it would be better to improve passive
detection than to implement active surveillance. Some ways exist to
improve a system such as the awareness of providers, the simplicity
of reporting, the frequent feedback and dissemination of data back
to the people who collected them, the use of multiple sources and
methods, the motivation and the encouragement of providers by legal
requirements, education, participation in projects, making important
clinical and therapeutic information available to those who report,
and by making specific drugs or biologics available to physicians on
notification, and non-monetary or monetary rewards.
Conflict of interest statement
We declare that we have no conflict of interest
Acknowledgements
The authors would like to thank Belgacem Zaafouri from the
Regional Directorate of Public Health of Sidi Bouzid, Tunisia
and Taieb Jlali, from the Regional Directorate of Agriculture of
Sidi Bouzid, Tunisia. This work was financially supported by the
International Development Research Center of Canada (www.crdi.
ca) (research project N° 105509-044).
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