Congo DRC, Kamwiziku. Mycoses 2021

Received: 8 April 2021ꢀ ꢀRevised: 1 June 2021ꢀ ꢀAccepted: 10 June 2021 <ul style="display: flex;"><li style="flex:1">|</li><li style="flex:1">|</li></ul>DOI: 10.1111/myc.13339 R E V I E W A R T I C L E Serious fungal diseases in Democratic Republic of Congo – Incidence and prevalence estimates Guyguy K. Kamwiziku1 ꢀ| Jean-Claude C. Makangara1 ꢀ| Emma Orefuwa2ꢀ| David W. Denning2,3 1Department of Microbiology, Kinshasa Abstract University Hospital, University of Kinshasa, Kinshasa, Democratic Republic A literature review was conducted to assess the burden of serious fungal infections of Congo in the Democratic Republic of the Congo (DRC) (population 95,326,000). English and French publications were listed and analysed using PubMed/Medline, Google Scholar and the African Journals database. Publication dates spanning 1943–2020 were in- cluded in the scope of the review. From the analysis of published articles, we estimate a total of about 5,177,000 people (5.4%) suffer from serious fungal infections in the DRC annually. The incidence of cryptococcal meningitis, Pneumocystis jirovecii pneumonia in adults and invasive aspergillosis in AIDS patients was estimated at 6168, 2800 and 380 cases per year. Oral and oesophageal candidiasis represent 50,470 and 28,800 HIV-infected patients respectively. Chronic pulmonary aspergillosis posttuberculosis incidence and prevalence was estimated to be 54,700. Fungal asthma (allergic bronchopulmonary aspergillosis and severe asthma with fungal sensitization) probably has a prevalence of 88,800 and 117,200. The estimated prevalence of recurrent vulvovaginal candidiasis and tinea capitis is 1,202,640 and 3,551,900 respectively.Further work is required to provide additional studies on opportunistic infections for improving diagnosis and the implementation of a national surveillance programme of fungal disease in the DRC. 2Global Action Fund for Fungal Infections, Geneva, Switzerland 3Manchester Fungal Infection Group, The University of Manchester, Manchester Academic Health Science Centre, Manchester, UK Correspondence Guyguy K. Kamwiziku, Department of Microbiology, Kinshasa University Hospital, University of Kinshasa, Congo. Email: <a href="mailto:[email protected]" target="_blank">[email protected] </a>K E Y W O R D S aspergillosis, candidiasis, cryptococcosis, fungal infection, HIV/AIDS, Pneumocystis, tinea capitis, Tuberculosis 1ꢀ |ꢀ INTRODUCTION tertiary care provision responsibility. The provincial level provides technical supervision, monitoring and translation of directives and With a surface area of 2,345,000 km², DRC is the second largest country in Africa after Algeria. It has a population of around 95,326,000 inhabitants of which more than 60% live in rural areas.1,2 The DRC shares 9,165 kilometres of border with 9 countries (Figure 1).3 The country is currently ranks 176 out of 189 countries on the Human Development Index. In 2019, GDP per capita $545, a 2.13% decline from 2018.4 With regards to health system architecture, the Ministry of Public Health is structured in the form of a 3-level pyramid. The national level has normative, regulatory and offers secondary reference health care. The operational level includes 516 Health Zones (HZ) with 393 General Reference Hospitals and 8,504 planned Health Areas (HA) of which 8,266 have a Health Centre. The function of this level is to implement the primary health care strategy. At this level, there are 2004 health centres for the detection and treatment of tuberculosis (CSDT) and 4,587 sites for the detection and treatment of HIV (SDT). In 2019, the DRC integrated 1752 existing CSDTs into the management of HIV-TB co-infection. A HZ is a geographically limited space covering a theoretical |Mycoses. 2021;00:1–11. <a href="/goto?url=http://www.wileyonlinelibrary.com/journal/myc" target="_blank">wileyonlinelibrary.com/journal/myc </a>© 2021 Wiley-VCH GmbH. ꢀ ꢀ1 2ꢀ ꢀꢀꢁ KAMWIZIKU et Al. |population of 100,000 to 150,000 inhabitants with a general reference hospital (GRH). The health system also integrates private for-profit and not-for-profit sector health facilities (health services of non-governmental organisations and faith-based organisations). The majority of GRHs lack intensive care, laboratory services (with parasitology, biochemistry, bacteriology and haematology services) and imaging X-ray, ultrasound, electrocardiogram, non stress test, Optical coherent tomography, etc). In the same way, the three University Clinics are under-equipped to serve as tertiary reference facilities. The DRC has 29 pharmaceutical industry companies, and wholesale supply and distribution is provided by 150 authorised establishments.5,6 There is an imbalance in the organisation of training courses and in the equitable distribution of health workers between rural and urban areas and between health structures. Health staff are concentrated in the capital Kinshasa and in the urban centres of the provinces. Health workforce indicators are low, using the benchmark ratio of 1 doctor per 10,000 inhabitants, only three out of ten provinces have staff numbers that meet or exceed international standards.3 Communicable diseases with epidemic potential are an ongoing issue in the DRC.3,4 The Director General for Disease Control has placed certain infectious diseases under epidemiological surveillance, including acute flaccid paralysis, cholera, leprosy, neonatal tetanus, plague, viral haemorrhagic fever, yellow fever, monkey-pox, measles, avian flu, bloody and simple diarrhoea, meningitis, malaria, typhus, pertussis, typhoid fever, acute respiratory infections, sexually transmitted infections, several neglected tropical diseases (NTDs), AIDS and tuberculosis (TB). Despite their known association with co-infections such as HIV and TB, fungal diseases are a glaring omission from the priority list of infectious diseases being surveilled. DRC is in a phase of epidemiological transition, characterised by an FI G U R E 1ꢀMap of the Democratic Republic of Congo with the neighbouring countries FI G U R E 2ꢀlocalisation of main institutions publishing articles in Democratic Republic of Congo KAMWIZIKU et Al. ꢀꢁꢀ ꢀ 3 |increase in the incidence of non-communicable diseases such as cancer and diabetes which heighten the need to address fungal infections as a public health issue of growing significance. information from multiple sources, all described in Table 2. The assumptions used to compute annual incidence or prevalence are also shown. There is no surveillance programme for fungal diseases in the DRC.6 Given the poor availability and accessibility of diagnostics in the DRC, fungal infections unfortunately remain grossly underestimated. Despite the paucity of data, some studies have been conducted in DRC which allow for baseline modelling to be carried out. The aim of this literature review is to take stock of the current incidence and prevalence of fungal infections in DRC. 3ꢀ |ꢀ RESULTS 3.1ꢀ |ꢀ Country's profile In the DRC, endemic diseases have a high mortality: malaria is the leading cause of death with a prevalence of 23%. HIV/AIDS and TB are also common. The DRC is among 30 countries with the highest burden of TB ranking 11th in the world and 3rd in Africa. It is also one of 13 countries facing the dual challenge of HIV-TB co-infection and drug resistance at the same time.3,14 Although HIV prevalence is declining in the DRC, at 0.8%, its epidemiology is complex. It is higher among women in some provinces and four times higher in urban areas. Apart from HIV and TB co-infection, which are well supported and documented, the prevalence and incidence of other opportunistic infections is not known due to the lack of any diagnostic capability in most health facilities. 2ꢀ |ꢀ MATERIALS AND METHODS This literature review was based on articles about fungal infections using the Google Scholar and PubMed/Medline search engines, African newspapers, health reports, epidemiological journals in DRC and WHO reports (Figure 2). The articles searched were mostly in English. The keywords searched were: fungal infection, opportunistic disease, HIV/AIDS, tuberculosis, chronic pulmonary, cryptococcosis, histoplasma, all associated with DRC. The oldest article retrieved was from 1943 and the most recent was from 2020. There are few studies on fungal diseases in the DRC and many of them are more than a decade old so we extended our searches to studies in border countries that have already estimated the burden of some fungal infections. We first considered Central African Countries and then, other sub-Saharan African countries. The countries chosen were those that are close to the four major universities in the DRC that use published articles. Where no article was found from the DRC or neighbouring countries, we used data from other countries within Africa and if this was not available, then data from other countries outside the African region. The socio-demographic data were taken from the National Health Development Plan 2016-2020 reports and the 2017 reports of the National Statistics Institute (Table 1). The HIV prevalence and deaths were taken from the 2019 UNAIDS report. To evaluate the incidence of children and adults at risk of developing the OIs, we have assessed different factors impacting on OI incidence in the literature.7 Considering that people living with HIV infection (PLWHIV) who are not on ART generally develop profound immunodeficiency over 7 years for adults and 5 years for children and that the rate failure of ART is 11%, we estimated the population of PLWHIV at risk.8 TB rates were taken from the WHO Global report 2019, and we derived the pulmonary TB survivors. Asthma prevalence in adults living in Kinshasa was assumed to apply to the 3.2ꢀ |ꢀ Review of serious fungal infections The scarcity of articles on fungal infections has prompted us to use prevalence or incidence from other countries to estimate the burden in the DRC. The summary shown in Table 2 and 3 is derived from the various populations at risk and the rate per 100,000 inhabitants. Each year in DRCongo approximately 5,079,278 people are affected by fungal diseases, 5.32% of the whole population. 3.2.1ꢀ |ꢀ Fungal skin infections: Tinea capitis and neglected tropical diseases In children, tinea capitis is the most common superficial fungal infection. Our estimation is 3,551,862 children have tinea capitis, a rate of 3,726 per 100,000. An old study (1959) gave a disparate prevalence of tinea capitis by region, the lowest prevalence was 2.9% in the middle part of the DRC and the high was 20% in the East part.42,43 No recent study is published, but it is a common problem. Neglected tropical skin fungal diseases have not been reported recently. An old study from the Belgian Congo (currently DRC) found 9 cases of my- cetoma in 1954.44 A strain of Catenulostroma chromoblastomycosum is deposited with the information that it is from a case of chromoblastomycosis from Zaire (currently DRC).45 Sporothrix schenckii is a ubiquitous fungus, causing mostly non-life-threatening localised infections of the skin and subcutaneous tissues - only one case is reported from DRC in an HIV patient.46 No data was found for basidi- obolomycosis, chromoblastomycosis, rhinoporidioisis or Conidiobolus or Emergomyces infections. They are probably rare. whole country.9 Chronic obstructive pulmonary disease (COPD) 10 <ul style="display: flex;"><li style="flex:1">prevalence was taken from the Cameroon </li><li style="flex:1">and it was assumed </li></ul>that 10.5% were admitted to hospital each year, as in Algeria.11 Lung 12 cancer was taken from Global cancer observatory (Globocan) and acute myeloid leukaemia from the WHO expert committee.13 No stem cell or organ transplantation procedures are done in the DRC. We used the various populations and denominators and estimated prevalence or incidence of different fungal diseases using 4ꢀ ꢀꢀꢁ KAMWIZIKU et Al. |TA B L E 1ꢀThe basic demographics of the country <ul style="display: flex;"><li style="flex:1">Data </li><li style="flex:1">Number </li><li style="flex:1">Reference </li><li style="flex:1">Comments </li></ul>2<ul style="display: flex;"><li style="flex:1">Population </li><li style="flex:1">95 326 400 </li></ul>520 000 233 520 3 551 860 380 2019 15 16 2<ul style="display: flex;"><li style="flex:1">HIV infection </li><li style="flex:1">Prevalence 2019 </li></ul>Annual incidence 2019 With 2019 population Annual incidence Pulmonary tuberculosis Asthma numbers in adults Acute myeloid leukaemia 17 Abbreviation: HIV, Human Immunodeficiency Virus. TA B L E 2ꢀAssumptions underlying the assessment of serious fungal diseases burden <ul style="display: flex;"><li style="flex:1">Fungal disease </li><li style="flex:1">Underlying condition </li><li style="flex:1">Assumptions made </li><li style="flex:1">References </li></ul>18 <ul style="display: flex;"><li style="flex:1">Cryptococcal meningitis </li><li style="flex:1">HIV/AIDS </li></ul>HIV/AIDS 12.2% of AIDS patients 19 Pneumocystis pneumonia 10% PCP as newly diagnosed HIV/AIDS adults over 2 years 20,21 22-26 Disseminated histoplasmosis Invasive aspergillosis <ul style="display: flex;"><li style="flex:1">HIV/AIDS </li><li style="flex:1">1.5% of advanced HIV disease </li></ul><ul style="display: flex;"><li style="flex:1">HIV/AIDS; COPD; Leukaemia; lung cancer </li><li style="flex:1">10% of AML patients develop IA. Rate </li></ul>in non-AML same as in AML. 1.3% of admitted COPD patients, 2.6% of lung cancer patients and 4 per 1000 HIV/ AIDS patients develop IA 27-29 <ul style="display: flex;"><li style="flex:1">Chronic pulmonary aspergillosis (CPA) </li><li style="flex:1">Tuberculosis, COPD </li><li style="flex:1">22% of TB survivors with cavities, 2% of </li></ul>those without cavities and assumed pulmonary TB is the underlying diagnosis in 80% of all CPA cases 30 31 Allergic Broncho pulmonary aspergillosis Asthma (ABPA) 2.5% of adult asthmatics 32 Severe asthma with fungal sensitisation (SAFS) <ul style="display: flex;"><li style="flex:1">Severe asthma </li><li style="flex:1">33% of worst 10% of adult asthmatics. </li></ul>33 <ul style="display: flex;"><li style="flex:1">Candidaemia </li><li style="flex:1">5/100,000 (mean of 2-11/100,000) with </li></ul>30% in ICU (critical care and postsurgical patients) and 70% in cancer and other immunocompromised patients 34 Candida peritonitis <ul style="display: flex;"><li style="flex:1">Pancreatitis, major abdominal surgery </li><li style="flex:1">1 patient with hospital-acquired (almost </li></ul>all post-operative) Candida peritonitis for every 2 patients with candidaemia, in ICU 35,36 37,38 <ul style="display: flex;"><li style="flex:1">Oral candidiasis </li><li style="flex:1">HIV/AIDS </li></ul>HIV/AIDS 90% of untreated HIV patients <ul style="display: flex;"><li style="flex:1">Oesophageal candidiasis </li><li style="flex:1">20% of patients not on ARVs and 0.5% of </li></ul>those on ARVs 39 40 Recurrent candida vaginitis (≥4x/year) 6% of adult women <ul style="display: flex;"><li style="flex:1">Mucormycosis </li><li style="flex:1">Affects 2 per million of the population </li></ul>based on data from Europe 41 <ul style="display: flex;"><li style="flex:1">Tinea capitis </li><li style="flex:1">7.38% of school-age children </li></ul>Abbreviations: AML, Acute myeloid leukaemia; ARV, antiretroviral; COPD, Chronic obstructive pulmonary disease; HIV/AIDS, Human Immunodeficiency Virus/ Acquired ImmunoDeficiency Syndrome; IA, invasive aspergillosis; ICU, Intensive Care Unit; PCP, Pneumocystis pneumonia; TB, Tuberculosis. Other data from Cameroon found 34.8% of women had vaginal can- 3.2.2ꢀ |ꢀ Candida diseases didiasis, suggesting this problem is more frequent than in Europe and the USA, and likely to be underestimated by our estimate.47 Although blood culture is fairly widespread in DRC, there are no data on the frequency of candidaemia. Using a low average country incidence, of 5/100 000,48 we estimate ~4,770 patients annually. In France, the ratio of candidaemia to intra-abdominal candidiasis No data on recurrent vulvovaginal candidiasis (rVVC), candidaemia and Candida peritonitis were found. The prevalence of rVVC is thought to be 2523/100 000, using a 6% proportion of women aged between 15 and 54, or to affect about 1.2 million women.39 KAMWIZIKU et Al. ꢀꢁꢀ ꢀ 5 |TA B L E 3ꢀEstimate of serious fungal infections in Republic Democratic of Congo No underlying disease Critical <ul style="display: flex;"><li style="flex:1">care </li><li style="flex:1">Serious Fungal </li></ul>Infection Respiratory Cancer disease Total <ul style="display: flex;"><li style="flex:1">Burden </li><li style="flex:1">Estimate </li><li style="flex:1">HIV/AIDS </li><li style="flex:1">+immunocompromised +surgery Rate/100,000 </li></ul>Cryptococcal meningitis <ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">–</li></ul>––<ul style="display: flex;"><li style="flex:1">6168 </li><li style="flex:1">–</li><li style="flex:1">–</li></ul>–– ––– 6.5 2.9 0.6 6168 <ul style="display: flex;"><li style="flex:1">Pneumocystis </li><li style="flex:1">I</li></ul>I 2800 595 –– 2800 595 pneumonia adult Pneumocystis pneumonia children <ul style="display: flex;"><li style="flex:1">Pneumocystis </li><li style="flex:1">I</li></ul>I –– 3016 380 <ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">–</li></ul>– 3.2 3.2 3016 3063 pneumonia total <ul style="display: flex;"><li style="flex:1">Invasive </li><li style="flex:1">2560 </li><li style="flex:1">123 </li></ul>aspergillosis CPA post TB CPA post TB CPA – all <ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">–</li></ul>––––––––<ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">11,580 </li><li style="flex:1">–</li></ul>–––– ––––– 12.1 38.3 57.4 93.2 123 5.0 11,580 36,500 54,700 88,800 117,200 4770 PPPPI<ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">36,500 </li></ul><ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">54,700 </li></ul><ul style="display: flex;"><li style="flex:1">ABPA </li><li style="flex:1">–</li><li style="flex:1">88,800 </li></ul><ul style="display: flex;"><li style="flex:1">SAFS </li><li style="flex:1">–</li><li style="flex:1">117,200 </li></ul>Candidaemia Candida peritonitis Oral candidiasis <ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">–</li></ul>–––<ul style="display: flex;"><li style="flex:1">3340 </li><li style="flex:1">1430 </li></ul><ul style="display: flex;"><li style="flex:1">715 </li><li style="flex:1">I</li><li style="flex:1">–</li><li style="flex:1">–</li></ul>––<ul style="display: flex;"><li style="flex:1">0.8 </li><li style="flex:1">715 </li></ul><ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">50,470 </li></ul>28,800 –– 52.9 30.2 50,470 <ul style="display: flex;"><li style="flex:1">28,800 </li><li style="flex:1">Oesophageal </li></ul>candidiasis I Recurrent Candida vaginitis (>4x/ year) <ul style="display: flex;"><li style="flex:1">1,202,640 </li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">2523 </li><li style="flex:1">1,202,640 </li></ul>Mucormycosis Histoplasmosis Fungal keratitis Tinea capitis <ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">190 </li><li style="flex:1">–</li></ul>–––<ul style="display: flex;"><li style="flex:1">0.2 </li><li style="flex:1">190 </li></ul><ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">840 </li><li style="flex:1">–</li></ul>––<ul style="display: flex;"><li style="flex:1">0.9 </li><li style="flex:1">840 </li></ul><ul style="display: flex;"><li style="flex:1">I</li><li style="flex:1">12,680 </li></ul>3,551,900 4,767,220 <ul style="display: flex;"><li style="flex:1">–</li><li style="flex:1">–</li><li style="flex:1">13.3 </li></ul>3726 12,680 3,551,900 5,177,427 <ul style="display: flex;"><li style="flex:1">P</li><li style="flex:1">–</li><li style="flex:1">–</li></ul><ul style="display: flex;"><li style="flex:1">Total burden </li><li style="flex:1">92,229 </li><li style="flex:1">312 180 </li><li style="flex:1">3653 </li><li style="flex:1">2145 </li></ul>Abbreviations: ABPA, Allergic bronchopulmonary aspergillosis; CPA, Chronic pulmonary aspergillosis; I, incidence; P, prevalence; SAFS, Severe asthma with fungal sensitisation; TB, tuberculosis.

Congo DRC, Kamwiziku. Mycoses 2021

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