The authors have declared that no competing interests exist.
Conceived and designed the experiments: DMP PSu PSa FP. Performed the experiments: DMP PSu PNL JBMM DBBI BMD MK JJTM. Analyzed the data: DMP PSu MB FP PTL BCdJ. Wrote the paper: DMP PSu PTL BCdJ FP MB.
Cutaneous infection by
We conducted a cross-sectional survey (July–August 2008) using the door-to-door method simultaneously in the two rural health zones (RHZ) of the Songololo Territory (RHZ of Kimpese and Nsona-Mpangu), each containing twenty health areas. Cases were defined clinically as active BU and inactive BU in accordance with WHO-case definitions.
We detected 775 BU patients (259 active and 516 inactive) in a total population of 237,418 inhabitants. The overall prevalence of BU in Songololo Territory was 3.3/1000 inhabitants, varying from 0 to 27.5/1000 between health areas. Of the 259 patients with active BU, 18 (7%) had been reported in the hospital-based reporting system at Kimpese in the 6–8 months prior to the survey.
The survey demonstrated a huge variation of prevalence between health areas in Songololo Territory and gross underreporting of BU cases in the hospital-based reporting system. Data obtained may contribute to better targeted and improved BU control interventions, and serve as a baseline for future assessments of the control program.
Buruli ulcer (BU) is a necrotizing bacterial infection of skin, subcutaneous tissue and bone, caused by an environmental pathogen,
Cutaneous infection by
BU is considered as one of the Neglected Tropical Diseases (NTDs) with a poorly known global prevalence
Year of report | Country | Study area | Overall prevalence active & inactive BU rate per 1000 | Prevalence Active BU rate per 1000 | Reference |
2001 | Ivory Coast | Nation-wide | - | 0.3 | Kanga and Kacou |
2002 | Ghana | Nation-wide | 0.31 | 0.21 | Amofah and others |
Amansie West District | - | 1.51 | |||
2004 | Cameroon | Valley of Nyong river | 4.42 | 2.05 | Noeske and others |
2005 | Benin | Lalo District | 8.66 | 1.84 | Johnson and others |
2009 | Cameroon | Akonolinga District | 4.70 | 2.50 | Porten and others |
BU: Buruli ulcer.
In the Democratic Republic of Congo (DRC), more than 500 BU cases had been reported before 1980
The Congolese Ministry of Health granted approval to conduct the survey. We obtained ethical clearance for this study from the Institutional Review Board of IME (N° IME/CS/01/2008). All patients, or their guardian in the case of minors, provided written informed consent for all diagnostic and treatment procedures and publication of any or all images derived from the management of the patient, including clinical photographs that might reveal patient identity. After informed consent had been given, data were recorded on a Community BU Form recommended by WHO. Patient care was free of charge.
The case search covered two rural health zones (RHZ), Kimpese and Nsona-Mpangu, both located in Songololo Territory (
A. Map of Africa showing the location of the Democratic Republic of Congo. B. Map of the Democratic Republic of Congo showing the location of the province of Bas-Congo. C. Map of the Province of Bas-Congo showing the location of the two health zones surveyed in 2008.
Songololo Territory is limited in the north by the Congo River, in the west by Sekebanza Territory, in the east by Mbanza-Ngungu Territory and in the south by the northern border of Angola. Each RHZ is subdivided into 20 health areas (
We conducted a cross-sectional survey (July–August 2008) using the door-to-door method simultaneously in the two RHZ of the Songololo Territory (i.e., Kimpese and Nsona-Mpangu), each containing twenty health areas. Cases were defined clinically as active BU and inactive (healed) BU in accordance with WHO-case definitions
This study was conducted in two phases: a preparatory phase and an investigation phase. During the preparatory four-week phase (June 2008), the purpose of the study was explained to the local political and health authorities, and their approval was obtained. Then, 80 CHW, i.e., 40 per RHZ, were trained in the use of the survey tools (BU community form, pictorial document to recognize BU) and in the identification of suspected BU cases in their communities. We also trained six physicians (working in the RHC of both RHZ), two nurse-supervisors of the leprosy and tuberculosis program (LT), and 40 head nurses (in charge of peripheral health areas), in active case-finding of BU cases and in the use of the survey tools.
For the survey, each RHZ was provided with 1 motor bike, 1 Global Position System device, 4 digital photo cameras, 30 bicycles (at least 1 for each health area), 25 megaphones (at least 1 for each health area), drugs and required medical and laboratory consumables.
The investigation phase was divided in two periods. The first period (two to three weeks depending on health area) consisted of making an inventory of all BU-like cases by the CHW, using the door-to-door approach in all villages and in each section of two cities in Songololo Territory (Songololo city and Kimpese city). The recommendation to CHW was to visit 40 households per day. A pictorial document, showing different clinical manifestations of BU, was presented to the head of the household or his/her representative asking if any household members presented similar lesions. If the head of the household was not present, the household was revisited once. The second period (6 weeks) included the clinical validation of suspected BU cases by trained health professionals. The eight validation teams were each composed of two people: firstly, a team member of the BU Project (physician or nurse), or another physician, or a LT supervisor, and secondly one of the head nurses.
The diagnostic confirmation process of suspected cases involved the collection of swabs from ulcerative lesions and fine needle aspirates from non-ulcerative lesions, followed by laboratory analyses (bacteriology and/or molecular biology) according to WHO recommendations
The study was carried out simultaneously in the different health areas of both RHZ. Data were recorded on a standardized Case Registry Form elaborated by WHO (BU02), entered into an Excel database (Microsoft Corporation, Redmond, WA) and analyzed with Epi-Info version 3.3.2 (Centers for Diseases Control and Prevention, Atlanta, GA). The Pearson chi-square test was used to compare proportions with a significance level set at 5%, and the Fisher's exact test when an expected cell value was less than 5. Coverage was calculated as the number of active cases detected who had visited the BU reference center in IME Hospital. We produced the distribution maps of BU in Songololo Territory using ArcGIS 9.2 (ESRI, Redlands, CA, USA).
The CHW visited a total of 39,044 households distributed across 9 sections of two cities (Kimpese and Songololo), 46 hamlets and camps, and 547 villages of the Songololo Territory. The estimated coverage of the study was 98.6%. During the household visits, the CHW inventoried 2,516 persons with BU-like lesions, among which 775 (30.8%) were validated in a second step as probable cases of BU, all forms included (i.e., 259 with active and 516 with inactive lesions). A total of 72 out of 241 (30%) patients with active lesions in whom a sample could be taken were confirmed by at least one positive laboratory test for
Health Zone | Population | Number BU case Total | Number Active BU | Number Inactive BU | Global prevalence/103 | Active BU prevalence/103 | Inactive BU prevalence/103 |
Kimpese | 146,108 | 376 | 141 | 235 | 2.6 | 1 | 1.6 |
Nsona-Mpangu | 91,310 | 399 | 118 | 281 | 4.4 | 1.3 | 3.1 |
Total | 237,418 | 775 | 259 | 516 | 3.3 | 1.1 | 2.2 |
BU: Buruli ulcer.
Sixty percent of the identified patients in the RHZ of Nsona-Mpangu were from 3 health areas, Kisonga, Nkamuna, and Songololo (
The age distribution of all cases ranged from 2 to 94 years (Median 27, Interquartile range (IQR) 14–44) with no significant differences between active and inactive cases. The supplementary tables provide the detailed information.
We observed a predominance of female gender (60%) among the recorded cases. Among the 259 patients with active lesions, no sex difference was observed, as 130 (50.2%) were female. The proportion of new cases was far higher (94%) than the relapses. The ages ranged from 2 to 94 years (Median 27 years; IQR 11–47 years), and the distributions in the two RHZ were similar. Among these 259 patients, 192 (74%) had ulcerative lesions and 62 (23.9%) were diagnosed with functional joint limitations. Lesions on the limbs were predominant, representing 90% of the sites of lesions. Regarding the patients' categorization, 48.8% were in category I, 31.5% category II, and 19.7% category III. The proportion of patients with ulcerative lesions was higher (p<0.001) in the RHZ of Kimpese (83%) compared to the RHZ Nsona-Mpangu (63.6%). Less than half of the patients of the RHZ of Kimpese (41.2%) and more than half (57.6%) in the RHZ of Nsona-Mpangu were in category I (p = 0.031) (
Female patients predominated amongst active confirmed cases compared to unconfirmed cases; on the other hand, male patients were more frequent in active unconfirmed patients (p = 0.029). No differences in the age distribution were observed between active confirmed and unconfirmed patients. The lower limb locations were significantly more frequent amongst active unconfirmed patients (p<0.001). Upper limb sites predominated (p<0.001) amongst active confirmed patients (
Characteristic | Active confirmed (n = 72) | Active unconfirmed (n = 187) | p-value |
|
n (%) | n (%) | |||
Gender | Female | 44 (61.1) | 86 (46.0) | 0.029 |
Male | 28 (38.9) | 101 (54.0) | ||
Age | ≤15 years | 27 (37.5) | 61 (32.6) | 0.298 |
16–49 years | 35 (48.6) | 84 (44.9) | ||
>49 years | 10 (13.9) | 42 (22.5) | ||
Classification of cases | New case | 64 (88.9) | 179 (95.7) | 0.078 |
Relapse | 8 (11.1) | 8 (4.3) | ||
Clinical forms | ||||
Ulcerated simple | 55 (76.4) | 123 (65.8) | 0.200 | |
Ulcerated mixed | 4 (5.6) | 10 (5.3) | ||
Non ulcerated | 13 (18.0) | 54 (28.9) | ||
Category of lesion | I | 36 (50.0) | 88 (48.4) |
0.740 |
II | 24 (33.3) | 56 (30.8) |
||
III | 12 (16.7) | 38 (20.9) |
||
Functional limitation | Yes | 22 (30.6) | 40 (21.4) | 0.121 |
No | 50 (69.4) | 147 (78.6) | ||
Site of lesion | Lower limb | 39 (53.4) |
136 (72.7) | <0.001 |
Upper limb | 29 (39.7) |
31 (16.6) | ||
Other | 5 (6.8) |
20 (10.7) | ||
Rural Health Zone | Kimpese | 41 (56.9) | 100 (53.5) | 0.615 |
Nsona Mpangu | 31 (43.1) | 87 (46.5) |
X2 test unless otherwise specified.
†Two-sided Fisher exact test (An expected cell value was less than 5).
‡n = 182 because of 5 missing data.
Ωn = 73 because of one case with disseminated lesions.
Features of active cases in the two RHZ were quite similar, with a few exceptions. The ulcerated forms (p<0.001) and functional limitations on diagnosis (p<0.001) predominated in the RHZ of Kimpese. Features of inactive cases in the two RHZ were similar but functional limitations were more often observed in the RHZ of Kimpese (p = 0.005) (
Only 25 BU patients were admitted and notified at the General Hospital IME/Kimpese between January and August 2008, amongst which 18 were still under treatment for active BU during the survey. Thus, 93% of all active BU patients at the time of the community survey were not captured by the hospital-based reporting system, corresponding to a ratio of 1 reported case for approximately 13 unreported cases.
The present study is the first exhaustive population-based survey in DRC aiming to assess the prevalence and distribution of BU in a well-circumscribed endemic region. The survey demonstrated a huge variation in prevalence between health areas and gross underreporting of BU cases in Songololo Territory, compared with the ongoing hospital-based reporting system.
Case-definition during the survey was essentially clinical. Case validation was performed by physicians from the BU project and physicians working in the area, well-trained in BU diagnosis, assisted by either a nurse from the BU project or a LT-supervisor, with the nurse responsible for the health area. We are aware of the limitations of clinical diagnosis, which is dependent on the range of experience of health professionals. This may account for certain non-BU cases included in this study. In endemic regions, depending on the clinical stage of the disease, BU may be confused with many other conditions such as nodular onchocerciasis, cyst, lipoma, lymphadenitis, phagedenic tropical ulcer, pyomyositis, necrotizing fasciitis
Despite these limitations, we suggest that our results reflect the endemicity of BU in Songololo Territory reasonably well. In fact, the areas previously established as most endemic were corroborated through this survey, as were the non- or hypoendemic areas
When considering only active lesions, no sex difference was observed, similar to findings in other studies
Among the 259 patients with active lesions, the majority (66%) were over age 15, similar to previous findings in the same area
The results presented in
The clinical presentation of BU was different in the two health zones (
Although the number of BU patients admitted at the hospital has increased in recent years, the survey results have demonstrated that the coverage of the population at risk was still insufficient. Of the 259 patients with active BU, 18 (7%) had been reported in the hospital-based reporting system. Porten et al. reported a coverage of 16%, limited to the area close to the Akonolinga hospital in Cameroon, where Médecins Sans Frontières (MSF) opened a BU programme in 2002. The need for improved access to care in the high prevalence areas was emphasized
The survey demonstrated large variations in prevalence between health areas within an endemic health zone consistent with previous studies in other African BU-endemic regions
Therefore, priority in case detection should be given to the most endemic health areas. A close collaboration with the provincial Leprosy & Tuberculosis control officers may facilitate the integration of BU activities at the primary health care centers. In fact, the use of the same case-confirmation network or the organization of integrated supervisions would help to reduce the BU intervention costs.
Data obtained in this survey may contribute to better targeted and improved BU control interventions, and serve as a baseline for future assessments of the control program.
STROBE Checklist.
(DOC)
Distribution of confirmed active BU cases in the Songololo Territory, July–August 2008.
(TIF)
Distribution of inactive BU cases in the Songololo Territory, July–August 2008.
(TIF)
Distribution of active and inactive BU cases in the Rural Health Zone of Kimpese (July–August 2008).
(DOCX)
Distribution of active and inactive BU cases in the Rural Health Zone of Nsona Mpangu (July–August 2008).
(DOCX)
Comparison of active case features in the two Rural Health Zones of Songololo Territory, July–August 2008.
(DOCX)
Comparison of inactive case features in the two Rural Health Zones of Songololo Territory, July–August 2008.
(DOCX)
We are grateful to all participants in this study, the staff of the IME/Kimpese Hospital, community health workers and health professionals in the health zones of Kimpese and Nsona-Mpangu, as well as the staff of the Mycobacteriology Unit and the Unit of Epidemiology and Disease Control of the ITM/Antwerp.
We particularly thank Dr WM Meyers for his unconditional support for all projects on Buruli ulcer in the Lower Congo for more than 40 years.