Trypanosomiasis control, Democratic Republic of Congo, 1993-2003.
ABSTRACT In the Democratic Republic of Congo (DRC), human African trypanosomiasis (HAT) reached unprecedented levels in the 1990s. To assess recent trends and evaluate control efforts, we analyzed epidemiologic and financial data collected by all agencies involved in HAT control in DRC from 1993 to 2003. Funds allocated to control populations, as well as to the population screened, doubled from 1993 to 1997 and from 1998 to 2003. The number of cases detected decreased from 26,000 new cases per year in 1998 to 11,000 in 2003. Our analysis shows that HAT control in DRC is almost completely dependent on international aid and that sudden withdrawal of such aid in 1990 had a long-lasting effect. Since 1998, control efforts intensified because of renewed donor interest, including a public-private partnership, and this effort led to a major reduction in HAT incidence. To avoid reemergence of this disease, such efforts should be sustained.
- SourceAvailable from: Carlos Cordon-Obras[Show abstract] [Hide abstract]
ABSTRACT: Trypanosoma brucei gambiense infection is widely considered an anthroponosis, although it has also been found in wild and domestic animals. Thus, fauna could act as reservoir, constraining the elimination of the parasite in hypo-endemic foci. To better understand the possible maintenance of T. b. gambiense in local fauna and investigate the molecular mechanisms underlying adaptation, we generated adapted cells lines (ACLs) by in vitro culture of the parasites in different mammalian sera. Using specific antibodies against the Variant Surface Glycoproteins (VSGs) we found that serum ACLs exhibited different VSG variants when maintained in pig, goat or human sera. Although newly detected VSGs were independent of the sera used, the consistent appearance of different VSGs suggested remodelling of the co-transcribed genes at the telomeric Expression Site (VSG-ES). Thus, Expression Site Associated Genes (ESAGs) sequences were analysed to investigate possible polymorphism selection. ESAGs 6 and 7 genotypes, encoding the transferrin receptor (TfR), expressed in different ACLs were characterised. In addition, we quantified the ESAG6/7 mRNA levels and analysed transferrin (Tf) uptake. Interestingly, the best growth occurred in pig and human serum ACLs, which consistently exhibited a predominant ESAG7 genotype and higher Tf uptake than those obtained in calf and goat sera. We also detected an apparent selection of specific ESAG3 genotypes in the pig and human serum ACLs, suggesting that other ESAGs could be involved in the host adaptation processes. Altogether, these results suggest a model whereby VSG-ES remodelling allows the parasite to express a specific set of ESAGs to provide selective advantages in different hosts. Finally, pig serum ACLs display phenotypic adaptation parameters closely related to human serum ACLs but distinct to parasites grown in calf and goat sera. These results suggest a better suitability of swine to maintain T. b. gambiense infection supporting previous epidemiological results.PLoS ONE 12/2013; 8(12):e85072. · 3.53 Impact Factor
In the Democratic Republic of Congo (DRC), human
African trypanosomiasis (HAT) reached unprecedented lev-
els in the 1990s. To assess recent trends and evaluate con-
trol efforts, we analyzed epidemiologic and financial data
collected by all agencies involved in HAT control in DRC
from 1993 to 2003. Funds allocated to control populations,
as well as to the population screened, doubled from 1993
to 1997 and from 1998 to 2003. The number of cases
detected decreased from 26,000 new cases per year in
1998 to 11,000 in 2003. Our analysis shows that HAT con-
trol in DRC is almost completely dependent on internation-
al aid and that sudden withdrawal of such aid in 1990 had
a long-lasting effect. Since 1998, control efforts intensified
because of renewed donor interest, including a public-pri-
vate partnership, and this effort led to a major reduction in
HAT incidence. To avoid reemergence of this disease, such
efforts should be sustained.
site Trypanosoma brucei. East African HAT is caused by T.
b. rhodesiense and West African HAT, the subject of this
article, by T. b. gambiense. The latter species causes a
slowly progressing fatal disease with few specific symp-
toms or none in its initial stage (1). The only proven effec-
tive way to control T.b. gambiense HATis mass population
screening and treatment of those infected. Well conducted
campaigns reduce the human parasite reservoir and there-
fore HAT incidence (2).
uman African trypanosomiasis (HAT), or sleeping
sickness, is a vectorborne disease caused by the para-
Substantial observational evidence from Sudan (3),
Uganda (4), Equatorial Guinea (5), and the Bandundu
region in former Zaire (6) has shown that intensive screen-
and-treat programs effectively reduce HAT incidence. So
far, no evidence has shown that adding vector control to
active case finding is effective, and vector-control efforts
are limited (5). HAT is one of the so-called neglected dis-
eases that afflict the developing world; the term indicates
the lack of drug research and development for these condi-
tions (7). In the field of HAT, the situation was so bleak by
1998 that production of sleeping sickness drugs was no
longer guaranteed. A public-private partnership was estab-
lished in 2001 between the World Health Organization
(WHO) and Sanofi-Aventis (Paris, France), the main phar-
maceutical manufacturer of anti-HAT drugs. Sanofi-
Aventis donated the 3 most used anti-HAT drugs (DFMO
[difluoromethylornithine], melarsoprol, and pentamidine)
for 5 years and also offered funding for disease control and
innovative research. Bayer AG (Leverkusen, Germany)
has donated a 5-year supply of suramin, another anti-HAT
drug. These donations were welcomed by HAT control
programs, which used to spend up to 46% of their annual
budgets on the purchase of drugs (S. Van Nieuwenhove et
al., unpub. data).
The sustainability of HAT control has been a recurrent
concern, as exemplified by the postcolonial history of
sleeping sickness control in the Democratic Republic of
Congo (DRC). By 1960, the year of DRC’s independence,
HAT was almost completely eliminated, but by 1976,
many new cases were diagnosed. HAT control received
substantial international aid during the 1980s, which
amounted to >90% of DRC’s HAT budget. However, this
international support was suddenly withdrawn after the
massacre of students at the Lubumbashi University in May
1990 (8). Inevitably, sleeping sickness returned to DRC in
Democ ratic Republic of
Pascal Lutumba,*† Jo Robays,† Constantin Miaka mia Bilenge,* Victor Kande Betu Ku Mesu,*
Didier Molisho,‡ Johan Declercq,§ Wim Van der Veken,§ Filip Meheus,¶ Jean Jannin,#
and Marleen Boelaert†
1382Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005
*Programme National de Lutte contre la Trypanosomiase
Humaine Africaine, Kinshasa, Democratic Republic of Congo;
†Institute of Tropical Medicine, Antwerp, Belgium; ‡Fonds Médical
Tropical, Kinshasa, Democratic Republic of Congo; §Coopération
Technique Belge, Kinshasa, Democratic Republic of Congo;
¶Institute of Development Policy and Management, Antwerp,
Belgium; and #World Health Organization, Geneva, Switzerland
full measure. In 1994, donors again allocated financial sup-
port for HAT control as humanitarian emergency aid and
channeled its implementation through nongovernmental
organizations. However, by 1997, the epidemiologic situa-
tion seemed little better than in the 1930s (9,10) and
showed a rising trend that was cause for concern.
Moreover, the HATproblem in DRC was no longer restrict-
ed to remote rural districts: urban areas such as Kinshasa
were reporting cases (11). In 1998, Belgian bilateral aid for
HAT resumed under a 5-year support program, and full
screening and treatment programs were restarted. Several
authors ascribe the reemergence of HAT in DRC primarily
to the interruption of bilateral and multilateral aid that
occurred after 1990 (12–14). The drastic reduction in spe-
cific control activities at a time when the epidemic was
spreading, in the context of overall collapse of the
Congolese health infrastructure, most likely contributed to
the exponential rise in HAT cases after 1990. We examined
the recent trends of HAT in DRC and evaluated the effects
and sustainability of the control program.
DRC has a surface area of 2.345.000 km2and ≈60 mil-
lion inhabitants, for a density of 25 inhabitants/km2.
Administratively, DRC is subdivided into 11 provinces,
and HAT is endemic in 9 of them (Programme National de
Lutte contre la Trypanosomiase Humaine Africaine
[PNLTHA], unpub. data). Since 1990, the country has
been devastated by political turmoil and civil war
(1996–1997 and 1998–2003). The health status of the pop-
ulation has deteriorated because of progressive breakdown
of health infrastructures, disease outbreaks, and the
reemergence of endemic diseases such as tuberculosis and
HAT. The emergence of HIV/AIDS has added to this cata-
log of health disasters.
HAT control in DRC is organized by a national pro-
gram, PNLTHA. This program divides HAT-endemic areas
into 7 regions, each under the responsibility of a regional
coordinator (Figure 1). These regions do not coincide with
the administrative divisions (provinces).
The main control strategy of PNLTHA is to actively
screen the population at risk by specialized mobile teams
(15), who refer patients with confirmed cases to regular
health services and specialized centers for treatment.
Screening was based on the palpation of cervical glands
until 1996, when a serologic screening test (card agglutina-
tion test for trypanosomiasis [CATT]) was added to the
algorithm (16). Each mobile team screens ≈40,000 per-
sons/year. A considerable amount of passive case finding
takes place as well, for example, when the regular health
service staff diagnose HAT in a patient who arrives for a
consultation. PNLTHA’s control strategies also include
We used the PNLTHAepidemiologic surveillance data-
base that included all HAT cases detected by mobile teams
and regular health services since 1926. For 1993–2003, we
examined the monthly reports compiled by the regional
PNLTHA coordinators, with the exception of those from
Maniema-Katanga and the Province Orientale because
they were incomplete and fragmentary as a consequence of
the ongoing war.
We distinguish 2 discrete periods for the analysis of
international aid. From 1993 to 1997, only humanitarian
aid budgets were allocated to HAT control, typically last-
ing for a maximum of 6 months. Because of the political
turmoil at that time in DRC, international aid for HAT was
given as “indirect aid,” i.e., donors would give cash grants
to 3 nongovernmental organizations (NGOs)—Fonds
Médical Tropical (FOMETRO), Medische Missie
Samenwerking (MEMISA), and Médecins sans Frontières
(MSF)—and rely on them for implementation. MEMISA
and MSF would supplement this indirect aid with funds
they had privately raised. Between 1998 and 2003, the
Congolese government again benefitted from long-term
international aid programs, and the Belgian Technical
Cooperation (BTC) launched its own technical assistance
program for HAT control. The same NGOs continued to
play a major role in implementation, as well as partly fund-
ing, these control activities. For the period under study,
WHO funds were donated directly to PNLTHA, while
those from the European Union were given to FOMETRO.
We obtained financial data on budgets and expenditure
for HAT control directly from the various donor agencies
Trypanosomiasis Control, Democratic Republic of Congo
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 20051383
Figure 1. Disease-endemic regions (indicated by shaded areas) in
the Democratic Republic of Congo, as managed by human African
and cross-checked data with all the implementing agencies
(PNLTHA, the 3 NGOs, and the BTC engaged in HAT
control in DRC during the period under study) (Table 1).
Only funds allocated to HAT control were incorporated in
our study; we excluded funds earmarked for research. To
avoid duplication, we categorized financial resources by
donating and not by implementing agency. Over the entire
study period, the Congolese government only allocated
funds for personnel costs, and those were included in our
computations at an average salary of US$12.50 per month
per person. All international aid was donated in cash
directly to the NGOs or BTC.
Expenditure in Belgian francs was converted into US
dollars, according to the exchange rate that applied at time
of expenditure. Expenditure in euros was converted at a
fixed rate of 40.3399 Belgian francs = 1 euro. The
exchange rate between the US dollar and euro was the aver-
age exchange rate per year based on Federal Reserve
Statistical Release (available at http://www.federalreserve.
gov/releases/H10/Hist/). All current dollars were converted
to constant 1998 dollars by using the US Office of Labor
Consumer price Index. All data were stored and analyzed in
an Excel database (Microsoft Corp., Redmond, WA, USA).
PNLTHAdefines a new HAT patient as a person whose
condition has, for the first time, been diagnosed by para-
sitologic examination as sleeping sickness. Relapse cases
are thus not included in this study. The HAT detection rate
is the number of newly detected cases, expressed as a pro-
portion of the screened population. We distinguish the
active detection rate (ADR), in which data are collected
through active case finding, from the overall detection rate,
which also includes cases detected at health facilities. The
coverage rate of the population is the proportion of the
population tested (through active or passive case finding)
divided by the population at risk for HAT. The participa-
tion rate applies only to active case finding and is defined
as the number of persons screened by the mobile teams
divided by the target population. The proportion of treated
patients is the number of persons who received HAT treat-
ment divided by the number of persons detected with HAT.
We structured our evaluation of the HAT control pro-
gram in the form of input, process, output, and outcome
analyses (17) and according to the method of Bouchet et
al. (18) (Table 2). Input represents the human and financial
resources invested in the program. Drug availability, meas-
ured as the number of occasions that the stock ran out dur-
ing the period under study, was also considered as an input.
Process indicators are not reported in this study because
they are relevant only to the daily management of the pro-
gram. Program output was measured through an analysis
of coverage of the population at risk, the participation rate
in screening, the number of detected HAT cases, the pro-
portion of patients with detected HAT patients who
received treatment, and the proportion of patients with
treated cases that have been followed-up correctly. We
report the annual HAT detection rate, both nationally and
for each region, as indicators of program outcome.
Figure 2 represents the evolution in the annual number
of newly detected HAT cases in DRC from 1926 to 2003.
Between 1960 and 1989, the figure shows an increasing
trend with 2 small peaks in 1970 and 1986. This trend was
interrupted in 1990 and 1991, which coincides with the
1384 Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005
sudden arrest of control activities in 1990. When humani-
tarian aid was launched in 1993, the annual number of
detected cases increased markedly. The peak was reached
in 1998, when the control program detected 26,318 new
HAT cases in a screened population of 1,472,674 persons.
After 1998, a marked decline occurred in the number of
HAT cases detected, which was not due to an overall
decrease in screening activities; the number of operational
mobile teams and number of screened persons continued to
increase over that period (Figure 3). The overall HAT
detection rate, based on active case finding, declined from
1.1% in 1994 to 0.3% in 2002. However, this overall
decline in detected HAT cases masks differences between
regions. Figure 4 shows the evolution of the number of
HAT cases and active detection rate, by region, from 1993
In 1990, 25 mobile teams covered the population at
risk. With the reduction in external financial support, 10
teams remained operational from 1991 to 1993. This num-
ber slowly increased to 33 teams in 1998 and to 46 teams
in 2002. These increases were concentrated in the regions
of Bandundu, Equateur-Nord, and Kasai, where the num-
ber of teams rose to 13, 13, and 7, respectively, which
accounts for 33 mobile teams of 46. In 1993, PNLTHA
staff was 250. This number increased progressively to 580
in 2001 and remained stable at 580 in 2003.
From 1993 to 1997, total annual expenditure amounted
to US$1,302,646, while in the period 1998–2003, total
annual expenditure doubled to US$2,786,916. Table 1
shows the amount and the origin of the financial resources.
The budget breakdown was as follows: functioning costs
(fuel, vehicle maintenance, supervision, training, sta-
tionery, etc.) (32.0%), personnel time (26.4%), HAT drugs
(24.3%), laboratory reagents (7.3%), and other material
and equipment (10%). The average expenditure per HAT
case detected and treated is shown in Table 3.
From 1993 to 2001, implementing agencies spent, on
average, 24% of their budgets in purchasing trypanocidal
drugs (range 12%–44%). Though the Sanofi-Aventis/
Bayer donation program was established in 2001, in prac-
tice, implementing agencies could continue working
throughout 2002 with existing drug stocks. For 2003, a
detailed analysis of amount of donated drugs versus pur-
chased drugs consumed was not possible, and we therefore
ignored the in-kind drug donation in Table 1. The full
effect of the donation will only become clear after 2004,
although can be estimated by its monetary value (Table 4).
PNLTHA records the number of patients who have been
treated by drug regimen, and these data allowed us to esti-
mate the quantity of the trypanocidal drugs that were
required, as well as the total cost of those drugs, calculat-
ed according to the preferential price, which was valid
until 2001. We estimated that the total drug cost per year in
DRC, for treating ≈14,000 HAT patients/year, correspond-
ed to ≈US$600,000/year. This value is consistent with the
previous estimate that 24% of budgets are reportedly used
for drugs. Notably, since the public-private partnership
was established in 2001, supplies of trypanocides never
ran short, whereas this problem was a matter of continuous
The population at risk in the DRC has been estimated at
12,600,000 persons (PNLTHA, unpub. data). Screening
and treatment of the at-risk population is estimated to have
risen from 6% in 1993 to 19% in 2003. We observed
notable differences between regions. Equateur-Nord had a
Trypanosomiasis Control, Democratic Republic of Congo
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 20051385
Figure 2. Number of new human African trypanosomiasis new
cases in the Democratic Republic of Congo, 1926–2003.
coverage rate of >50%, while in the other regions the rate
ranged from 10% to 20%. Figure 3 shows that the number
of persons screened each year almost tripled from 1993 to
The participation rate of the population in active case
finding was almost 96% in 1998. By 2002, the rate had
fallen to 78%. The proportion of new patients who
received treatment was ≈95% throughout the whole coun-
try but varied from region to region, from 89% to 100%.
From 2001 to 2003, a total of 44,247 patients were treated
with pentamidine (31.5%), suramin (5.8%), the combina-
tion pentamidine-suramin (0.2%), melarsoprol (55.2%),
eflornithine (0.85%), nifurtimox (2.6%), and the combina-
tion melarsoprol-nifurtimox (3.5%) (because nifurtimox is
not registered for use against HAT in DRC, it was given on
a compassionate basis when no other drugs were available
or when melarsoprol treatment failed).
After the number of cases peaked in 1998 with 26,000
new cases, the annual number of HAT cases reported in
DRC has decreased to 10,900 cases in 2003. From 1993 to
2003, the annual number of persons screened for HAT, as
well as financial resources allocated to HAT control in
DRC, has doubled.
The increase in reported cases and in the detection rate
observed between 1993 and 1997 can be attributed to
increased transmission but also to renewed efforts after
several months when active case finding was interrupted.
However, the striking decrease in HAT cases from 1998 to
2003 cannot be explained by decreased case-detection
efforts because the number of persons screened in the same
period doubled. Changes in detection rates through active
case finding are difficult to interpret because the popula-
tion reached is not the same over time. The additional
number of persons screened might come from populations
that were less at risk in the first place, as happened, for
example, in Ville de Kinshasa, where a new mobile team
started operating in May 2001 in an area with lower preva-
lence. Population movements during the war could, in the-
ory, also explain the observed changes in HAT prevalence,
but no noteworthy migration from disease-endemic to dis-
ease-nonendemic areas or vice versa took place over the
study period. We therefore conclude that the decreasing
trend in HAT case detection observed in DRC since 1999
is real. Most likely this trend is explained by the intensifi-
cation of control efforts, the steep increase in resource allo-
cation since 1998, and a major drug donation in 2001. The
systematic use of CATT as the serologic screening test in
1996 has probably contributed to a decline in transmission,
because it increased screening effectiveness (15).
However, these national figures hide important differ-
ences between regions. In the northern and southern
Equateur regions and in Kinshasa, the absolute number of
HAT cases and detection rates has declined, whereas these
indicators remain stationary in the Bas Congo, Kasai, and
Bandundu regions. In fact, the decline observed at nation-
al level is, to a large extent, based on the decline observed
in 1 region, Equateur-Nord, which experienced a major
1386Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 2005
Figure 3. Population screened per year and number of mobile
teams operating in the Democratic Republic of Congo,
Figure 4. Number of new human African trypanosomiasis cases
and active detection rate (ADR) in Equateur Nord and Bandundu,
Democratic Republic of Congo,1993–2003 (data from additional
regions may be viewed online at www.cdc.gov/ncidod/EID/
outbreak but brought it under control by an intensive and
A similar rapid decrease in the number of HAT cases
has been observed by Van Nieuwenhove and Declercq (19)
in southern Sudan and by Paquet et al. (4) in Uganda.
However, the HAT epidemic reemerged in southern Sudan
after control activities were stopped, indicating that dis-
ease control efforts should be maintained even when
prevalence is low (20–22).
Our analysis showed how HAT control in DRC almost
completely depends on international aid and that the inter-
ruption of financing from 1990 to 1991 had a long-lasting
negative effect on case load. Funding may be discontin-
ued for different reasons, such as changes in donor poli-
cies or priorities, so HAT control remains vulnerable.
Private NGOs have so far accounted for a minor part of
funding in DRC, although they played a role both in advo-
cacy and in program implementation. The recent public-
private alliance with pharmaceutical companies not only
made continued care for HAT patients possible again but
also released substantial financial resources that can be
used in the future for operations in DRC. Moreover,
through direct financial support to research, training, and
rehabilitation, the public-private partnership has con-
tributed to a wider alliance and extension of activities.
However, the fact that the 3 main drugs used to treat HAT
patients are produced and donated by a single company
creates a new type of dependency. Care for HAT patients
may be seriously compromised if production or donation
stopped for any reason, for example, a company takeover,
management changes, or a change in the company’s
The disparities now emerging in disease epidemiology
in different parts of DRC call for the adoption of differen-
tial control strategies in different regions of the country.
Where the ADR has dropped to low levels, screening inter-
vals could be lengthened. Alternatively, and with lower
cost, surveillance methods could be used that detect
emerging epidemics at an early stage, such as serologic
surveys, or that rely on data collection from passive case
finding and enhanced diagnosis in the primary health
structures (23). Where ADR remains high, the program
must identify the reasons for this and find solutions to
make control more effective. Furthermore, the increase in
treatment failures in the southeastern part of the country
should be carefully monitored, and evolving parasite
resistance should be thoroughly investigated.
Our analysis shows that successful HAT control is pos-
sible, but that it depends on continued financial support
and drug availability. Therefore, the governments of dis-
ease-endemic countries and the international community
must make long-term financial commitments to ensure the
continuity of HAT control activities. This necessitates
sound financial sustainability planning for HAT control, as
is already done, for instance, in childhood immunization
(24). Research is necessary on how to rationalize control
Trypanosomiasis Control, Democratic Republic of Congo
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 11, No. 9, September 20051387
activities so that control programs can adopt the most
effective and efficient strategies.
During this study, P. Lutumba was supported by a PhD grant
from the Belgian Directorate-General for International
Cooperation. This sponsor played no role in study design, collec-
tion, analysis, interpretation of data, report writing, or the deci-
sion to submit the paper.
Although Sanofi-Aventis indirectly sponsored part of the
HAT control activities in DRC, and donated HAT drugs, the com-
pany played no role in study design, collection, analysis, interpre-
tation of data, report writing, or the decision to submit the paper.
Dr Lutumba is head of the research unit of the national
sleeping sickness control program of DRC. He has extensive
experience in sleeping sickness control in DRC and participates
in clinical research programs on HAT diagnosis and treatment.
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Address for correspondence: Marleen Boelaert, Epidemiology and
Disease Control Unit, Institute of Tropical Medicine, Nationalestraat 155,
2000 Antwerpen, Belgium; fax: 32-3-247-6258; email: firstname.lastname@example.org
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