Recurrence and emergence of infectious diseases in Djibouti city.

Research!Recherche Recurrence and emergence of infectious diseases in Djibouti city G.R. Rodier,1' 2 J.-P. Parra,3,4 M. Kamil,3 S.O. Chakib,3 & S.E. Cope1 Public health authorities are now increasingly concerned by changes in the epidemiology of infectious diseases which may have an adverse impact on their budget plans and control strategies. Rapid increases in population and urban migration, various ecological changes, increasing poverty, and a rise in intemational travel have contributed to the worldwide vulnerability of human populations to the emer- gence, recurrence or spread of infectious diseases. In the rapidly growing city of Djibouti in East Africa, public health priorities have been altered during the last 10 years by diseases which were unknown or under control until the early 1980s. These diseases, including malaria, AIDS, tuberculosis, dengue fever and cholera, are consuming considerable resources. This article on Djibouti illustrates the epidemiologi- cal changes in the region. Besides the specific ecological and behavioural changes, which accompany rapid population growth, poverty seems to be a major cause for the emergence and recurrence of infec- tious diseases. Introduction Recurrence of old infectious diseases and the emer- gence of new ones, as revealed by unexpected out- breaks or epidemics, are being reported with increas- ing frequency (1) and could have an adverse impact on health care budgets and disease control strategies. The seriousness of the situation has led to the de- velopment of a prevention strategy by the Centers for Disease Control and Prevention (CDC), which addresses emerging infectious disease threats to the United States (2). This article describes recent changes in the epi- demiology of infectious diseases in the capital city of Djibouti, East Africa, which illustrates the problem of emerging diseases in a rapidly growing city of the developing world. The changes are related to poorly I Risk Assessment Branch, U.S. Naval Medical Research Unit No. 3 (NAMRU-3), Cairo, Egypt. Requests for reprints should be sent to Research Publication Branch, U.S. NAMRU-3, PSC 452 Box 5000, FPO AE 09835-0007, USA. 2 International Health Program, University of Maryland, Balti- more, MD, USA. 3 Ministry of Public Health and Social Affairs, Djibouti. 4 French Cooperation Mission, Djibouti. Reprint No. 5656 documented but significant population movements, including the influx of refugees, in Djibouti follow- ing the Ethiopian and Somali political turmoils since the late 1970s and the periodic regional famines. Findings and discussion The population of Djibouti city was about 15 000 in 1900, 30000 in 1950, 106000 in 1970, 156000 in 1980, 235 000 in 1990, and about 300 000 in 1994 (de Comarmont, Ministry of Urbanism, Djibouti, personal communication, 1994). This increase was primarily due to economic immigrants, high birth rates and the refugees. Although about a third of the national budget has been spent on development since 1977 (de Comarmont, personal communication), the living conditions of Djiboutians remain poor. In an interview to the national newspaper "La Nation" on 7 October 1993. the Djibouti Minister of Urbanism depicted significant difficulties in water supply, sewage system, garbage collection and general hous- ing, and further emphasized the possible adverse consequences on public health. The chronology of the emergence of malaria, HIV/AIDS, multidrug- resistant tuberculosis, dengue fever and cholera in the city of Djibouti is presented in Fig. 1 with the changes in population growth. Bulletin of the World Health Organization, 1995, 73 (6): 755-759 755 G.R. Rodier et al. Fig. 1. Population increase of Djibouti city and chronol- ogy of local epidemiological changes involving infec- tious diseases, 1900-1994. 1993: HIVprevalence 56% in prostitutes, 3.9% in pregnant women; 453 AIDS cases; first cholera epidemic 1992: One strain of M. tuberculosis resistant to 8 antibiotics 1991: First dengue epidemic 1990: Chkoroquine-reasstant malaria 1988: First malaria epidemic 1987: HtVprevalence 4.6% in prostitutes Populaton 1986: First HlVeeropositive patient 1985: Emergence ofmultidrug-resistant tuberculos 1978: Indigenous malaria (rural) 1952: Firs tubercubss controldproranv e Year Malaria In the early 1900s, only two malaria foci were identi- fied, one in Ambouli and the other in Gaanman, two villages located within 4 km of Djibouti city, along the main river valley or wadi (3). Subsequently malaria cases, mostly imported from neighbouring countries, were only infrequently reported until 1973 (4). Recurrence of indigenous malaria was first docu- mented in 1978 in the southern districts, especially Ambouli and Loyada, and then Dikhil and Ali- Sabieh. Malaria, initially unstable with peaks in May-June and November-December, soon became endemic throughout the year, including the dry and torrid summer period. In the following years, cases of malaria occurred for the first time in the northern districts, particularly in Tadjourah. During the 1988-89 winter season, outbreaks of Plasmodium falciparum malaria struck the country, including the capital city and the south-western town of As-Eyla (5). About 3000 malaria cases with significant mor- tality were reported and the importation of malaria parasites by travellers from adjacent countries was suspected (6). Anopheles arabiensis was identified as the main vector (7). In 1991, Djibouti reported 7338 cases of smear-positive malaria, 98% being falcipa- rum malaria and 80% originating from the Ambouli and airport areas of Djibouti city. Although the fig- ure dropped in 1993 to 4770 (74% from the capital city), malaria had become a permanent public health concern in Djibouti city where the marked seasonal pattern had decreased considerably compared to rural areas. The emergence of urban malaria closely fol- lowed the progressive inclusion of the wadi Ambou- li, known for its gardens and wells, in the growing agglomeration of Djibouti. Entomological surveys confirmed the Ambouli area as a major source of Anopheles mosquitos (8). In addition, and following the 1985 report of chloroquine-resistant P. falcipa- rum in Ethiopia (9), P.falciparum strains resistant to chloroquine in vivo, including RII/RIII resistance, was demonstrated in Djibouti in 1990 (NAMRU-3, unpublished data). HIV/AIDS The human immunodeficiency virus (HIV) was un- known in the Republic of Djibouti until the diagnosis of the first HIV-1 seropositive patient in the spring of 1986. In October 1987, the first national serosur- vey showed that HIV-1 was prevalent among 0.8% of males consulting for sexually transmitted diseases (STD), 1.4% of bar hostesses and 4.6% of street prostitutes. Only one serum had antibodies against HIV-2. In March 1988, the first case of acquired immunodeficiency syndrome (AIDS) was diagnosed in a tuberculosis (TB) patient who died 3 weeks later. In June 1988, a second cross-sectional survey (10) showed a low and stable HIV prevalence among male STD patients while the figure rose to 2.7% in bar hostesses and 9% in street prostitutes. In Februa- ry 1990, HIV prevalence was 41.7% in street prosti- tutes, 5% in bar hostesses and 1.9% in STD males (11), while the school population remained HIV-free (12). In 1990 the Republic of Djibouti distributed more than 300 000 free condoms and, in December, reported 58 AIDS cases to WHO (13). In 1993, HIV infection was prevalent in 56.5% of street prostitutes, 23.3% of bar hostesses and 14.4% of men consulting for STD (Djibouti MOH, personal communication, 1994). At that time, HIV prevalence in pregnant women had reached 3.9% versus 1.5% in 1992 and 0.5% in 1991; in 1993, the prevalence was 7.4% in TB patients (14) and 1.2% in blood donors (Djibouti MOH, personal communication, 1994). The cumula- tive numbers of AIDS patients officially reported since 1988 reached 104 in December 1991 (15), 309 in December 1992 (16), and 453 in December 1993 (17). Tuberculosis In 1952, the first national tuberculosis (TB) control programme was launched in Djibouti. The national tuberculosis hospital, built in 1967 in Djibouti city, with an initial capacity of 100 beds was extended to 178 beds in 1974 and 210 in 1987 (18). From 1986 to 1989, the number of newly diagnosed tuberculosis patients in Djibouti was stable around 2000 cases. This figure included a significant percentage of foreigners, primarily Ethiopians and Somali. Since 1989, newly diagnosed tuberculosis cases, in both Djiboutians and foreigners, have increased to a total WHO Bulletin OMS. Vol 73 1995 1 I qA-AnA-AI 756 Recurrence and emergence of infectious diseases in Djibouti city of 3700 in 1992, representing, for the Djiboutians alone, a twofold increase in a four-year period. In 1992, the estimated tuberculosis incidence in Djibou- tians was 280/100 000. The combination of the rapid population growth, the concurrent HIV/AIDS epi- demic, and the deterioration of therapy compliance were certainly key factors for the new tuberculosis burden. In March 1992, an isolate of Mycobacterium tuberculosis, resistant to 8 antibiotics was reported. A retrospective study of antibiotic sensitivity screen- ings demonstrated the growing importance of multi- drug-resistant tuberculosis, which was emerging in 1985 and has been significant since 1989 (19). The frequency of strains sensitive to all frontline drugs (i.e., isoniazid, pyrazinamide, ethambutol and rifam- picin) decreased from 55.5% in 1988 to 16.7% in 1992. Because of the unknown actual importance of primary resistance, surveillance of primary resistance has become a new objective for the Djibouti tubercu- losis control programme. The cost of this programme (18) will continue to increase because of the neces- sary investment for better compliance with treatment, increased laboratory activity, and the use of more expensive drugs. Finally, the growing burden of pro- longed hospitalization of AIDS/tuberculosis patients will soon consume a significant share of the avail- able resources. Dengue In October 1991, an outbreak of acute fever with negative blood smear for malaria was reported in Djibouti city. It involved hundreds of residents, adults and children, locals and foreigners. Reported symptoms included high and acute fever associated with severe headache, fatigue, arthralgia and myal- gia. Rash, pruritus, conjunctivitis, abdominal pain, vomiting and epistaxis were also described. Fever lasted for 4-6 days before spontaneous recovery occurred. Leucopenia, thrombocytopenia and slightly elevated liver enzymes were common. Few patients were hospitalized, with the exception of a suspected case involving a 27-year-old Djiboutian woman who died of shock syndrome and intestinal haemorrhage in the first few days of the epidemic. Aside from this case, no severe haemorrhagic disease was described. The investigation yielded 13% virus isolates of dengue serotype 2 (DEN-2). Cases occurred until February 1992 and the estimated total number was 12 000 (20). A retrospective serologic study and a 1987 sero- survey (21) showed little or no flavivirus activity, supporting the conclusion that DEN-2 virus had recently been introduced. Although dengue transmis- sion had been suspected in neighbouring Somalia and Ethiopia (22), this was the first epidemic report- ed from Djibouti. In 1983, serologically suspected cases of dengue, serotype 2, occurred in expatriates in Mogadishu, Somalia (23), and later, during the 1985-87 period, in the Dam refugee camp near Hargeysa, northern Somalia (24). The presence of Aedes aegypti was not previously reported in Djibou- ti (25), but an entomological survey, conducted in 1992, demonstrated that this species was widespread, abundant and well established in many parts of the city. The predominant larval habitats were 200-litre metal barrels and clay water jars (26). Secondary breeding sites included discarded plastic water bottles and foil-lined milk containers. The spread of A. aegypti had previously been documented in the region, particularly in the coastal cities (25). During the 1993-94 winter, a limited outbreak of serologi- cally suspected dengue fever occurred in Djibouti city (Djibouti MOH, personal communication, 1994). Cholera Cholera has been repeatedly introduced into the region and the seventh cholera pandemic, caused by Vibrio cholerae El Tor, reached the Horn of Africa in 1970, and led to several thousand deaths, particu- larly in Ethiopia; cholera has since been endemic in the region (27). Djibouti's rural areas had limited cholera outbreaks in 1973 and 1985. During summer 1992, cases of cholera were reported among Somali refugees in Yemen (28), but no recrudescence of the disease was observed in Djibouti until 13 July 1993, when the first case of cholera was clinically suspec- ted in the Salines area, one of the poorest quarters of Djibouti city. A control programme was immediately set up, including the inspection and chlorination of all fresh water sources and the establishment of two diarrhoea field hospitals. By 8 August 1993, more than 2000 cases of acute diarrhoeal disease were reported in the capital. About 32% of examined stool samples yielded V. cholerae 01, all of the El Tor biotype, serotype Ogawa, sensitive to most of the antibiotics (NAMRU-3, unpublished data). In late July, water analysis in Djibouti city isolated 4 strains of V. cholerae 01, three from water tanks and one from a well (Djibouti MOH, personal communica- tion, 1993). The epidemic peaked in early August, then was under control by the end of the month and died out in late September; a total of more than 5000 acute diarrhoeal cases were reported. In August, the epidemic also spread to the rural cities of Ali-Sabieh, Dikhil, Arta and Tadjourah and to some refugee camps on the Ethiopian border. Because of the rapid (and free) access of Djibouti residents to the two large rehydration centres, only 32 deaths were recor- ded among the 1428 hospitalized diarrhoeal patients; the global attack rate of suspected cholera in the capital city was 12.2 per 1000 (Djibouti MOH, per- sonal communication, 1993). WHO Bulletin OMS. Vol 73 1995 757 G.R. Rodier et al. Additional changes have been observed since 1990, including the recent recognition of hantavirus in the Rattus norvegicus population of the port area (29) and the emergence of multidrug-resistant strains of Neisseria gonorrhoeae (Djibouti MOH, personal communication, 1994) and Shigella spp. (30). Al- though similar epidemiological changes have been suspected or reported in various places of neighbour- ing Ethiopia (9) and Somalia (22), the city of Dji- bouti was ideal for studying the documented epidem- iological changes within a limited area. Despite some relatively weak data, the trends are clearly present. These epidemiological changes were due to ecologi- cal and behavioural changes including poverty and rapid urbanization. Specific changes and their causes included urban encroachment into a malaria endemic rural area, emergence of multidrug-resistant M. tuberculosis from lack of compliance with anti- tuberculous treatment, introduction of HIV infection and AIDS through prostitution, the absence of an appropriate water supply, the spread of A. aegypti leading to the dengue epidemic, and the influx of ref- ugees into areas of poor sanitation which led to the cholera outbreak. As emphasized in WHO's World Health Report 1995, poverty "conspires with the most deadly and painful diseases to bring a wretched existence to all who suffer from it", and seems to be a major factor in the emergence and recurrence of infectious diseases. Acknowledgements We are grateful to and thank H.E. Mohamed Said Saleh, Djibouti Minister of Health, and his predecessors who strongly supported the monitoring of infectious diseases in Djibouti. We also thank Mrs E. Ismael, WHO Representa- tive, and Dr H. Wassef, her predecessor, Dr Said-Salah Youssouf, Head, Epidemiology and Hygiene Service, and Dr J. Bouloumie, his predecessor, for their full support to NAMRU-3's research efforts in Djibouti. We also acknow- ledge Dr E. Fox, U.S. NAMRU-3, for his initial and deci- sive support to infectious disease research in Djibouti, as well as all the local collaborators, particularly Dr D. Poly- carpe, Dr M. Abdourahman, Dr G. Aur6gan, Dr G. Binson, Dr J.-P. Sevre, Dr D. Daher, Dr F. Marrot, Dr R. Bercion and Mr T. de Comarmont, and thank Dr J. LeDuc, WHO, Geneva, for his critical review of the manuscript. The study was financially supported by Naval Medical Research and Development Command, Naval Medical Command, National Capital Region, Bethesda, MD 20814, Work Unit No B690.00101.EAC.375C. The opinions and assertions in this article are the private ones of the authors and are not to be construed as official or as reflecting the views of the Department of the Navy, the Government of the United States, the Department of Defense, the University of Maryland at Baltimore, the Gov- ernment of Djibouti or the French Cooperation Mission in Djibouti. Resume Reapparition et emergence de maladies infectieuses en ville de Djibouti La r6apparition et 1'6mergence de nouvelles ma- ladies infectieuses, r6v6l6es par des 6pid6mies telles que la pand6mie de SIDA ou la fr6quence croissante de souches bact6riennes resistantes aux antibiotiques, sont devenues un sujet de pr6- occupation pour la sant6 publique, y compris dans les pays d6velopp6s. L'explosion d6mographique, les migrations urbaines massives, les change- ments apport6s a diff6rents ecosystemes, la pau- vrete croissante et I'augmentation spectaculaire des voyages internationaux ont sans aucun doute contribu6 a la vuln6rabilit6 des populations vis-a- vis de l'emergence, de la r6apparition et de la dif- fusion mondiale de certaines maladies infectieu- ses. Dans la capitale de la R6publique de Djibouti, les problemes de sant6 publique ont 6t6 profonde- ment modifies durant ces 10 dernieres ann6es tandis que la ville s'6tendait consid6rablement. Cinq maladies, inconnues ou maltris6es jusqu'au d6but des ann6es 80, jouent maintenant un r6le de premier plan dans les causes de morbidit6 et de mortalit6 chez 1'enfant et l'adulte. Ainsi, la lutte contre le paludisme, le SIDA, la tuberculose, la dengue et le chol6ra ont mobilis6 des ressources considerables. Les donn6es sur la ville de Djibouti illustrent concretement les changements 6pid6- miologiques rencontr6s dans les zones urbaines de la r6gion. En d6pit de certains changements sp6cifiques sur le plan 6cologique, tels que l'int6- gration dans le tissu urbain d'une zone rurale end6mique pour le paludisme, ou sur le plan des comportements (prostitution, stockage de l'eau a domicile) qui peuvent expliquer certains des chan- gements 6pid6miologiques observes, la pauvret6 semble bien etre le principal acteur du retour, ou de l'emergence, de ces maladies infectieuses. References 1. Lederberg J, Shope RE, Oaks SC, eds. Emerging infections, microbial threats to health in the United States. Washington, DC, National Academy Press, 1992. 2. Centers for Disease Control and Prevention. Addressing emerging infectious disease threats. A prevention strategy for the United States. Atlanta, GA, U.S. Department of Health and Human Ser- vices, 1994. 3. Bouffard, Chabaneix. Quelques cas de fievre palu- d6enne a Djibouti, chef-lieu de la C6te de Somalie. 758 WHO Bulletin OMS. Vol 73 1995 Recurrence and emergence of infectious diseases in Djibouti city Annales d'hygiene et de medecine coloniales, 1901, 4: 440-452. 4. Carteron B, Morvan D, Rhodain F. Le probleme de 1'end6mie palustre dans la R6publique de Djibou- ti. M6decine tropicale, 1978, 38: 837-846. 5. Fox E et al. An unprecedented epidemic of malaria in the Republic of Djibouti during the winter season 1988/89. Proceedings of the 38th Annual Meeting of the American Society of Tropical Medicine and Hygiene (abstract 319), 1989. 6. Fox E. et al. Plasmodium falciparum voyage en train d'Ethiopie a Djibouti. M6decine tropicale, 1991, 51: 185-189. 7. Fryauff DJ, Liuberas MA, Bouloumie J. Species composition and density of mosquitoes during inter- mission and epidemic periods of malaria in the Republic of Djibouti. Proceedings of the 39th Annual Meeting of the American Society of Tropical Medi- cine and Hygiene (abstract 292), 1990. 8. Louis JP, Albert JP. Le paludisme en Republique de Djibouti. Une strategie de controle utilisant des larvicides biologiques: poissons larvivores indigenes (Aphanius dispar et toxines bact6riennes. Medecine tropicale, 1988, 48: 107-1 10. 9. Kloos H, Zein ZA. The ecology of health and dis- ease in Ethiopia. Oxford, Westview Press, 1993. 10. Fox E et al. Incidence of HIV infection in Djibouti in 1988. AIDS, 1989, 3: 244-245. 11. Rodier G et al. Trends of HIV-1 infection in female prostitutes and males diagnosed with a sexually transmitted disease in Djibouti, East Africa. Ameri- can Journal of tropical medicine and hygiene, 1993, 48: 682-686. 12. Rodier G et al. HIV infection and secondary school- children in Djibouti, Horn of Africa: knowledge, exposure, and prevalence. East African medical journal, 1993, 70: 414-417. 13. World Health Organization. Global data on AIDS. Weekly epidemiological record, 1991, 66(11): 73-74. 14. Rodier G et al. Clinical features associated with HIV infection in adult patients diagnosed with tuber- culosis in Djibouti, Horn of Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene, 1993, 87: 676-677. 15. World Health Organization. Global data on AIDS. Weekly epidemiological record, 1992, 67(3): 9-10. 16. World Health Organization. Global data on AIDS. Weekly epidemiological record, 1993, 68(3): 9-1 1. 17. World Health Organization. Global data on AIDS. Weekly epidemiological record, 1994, 69(2): 5-8. 18. Foulon G et al. Evaluation du coOt de la lutte anti- tuberculeuse a Djibouti en 1989. Cahiers sant6, 1993, 3: 451-456. 19. Rodier G et al. Multidrug-resistant tuberculosis in the Horn of Africa. Journal of infectious diseases, 1993, 168: 523-524. 20. Rodier G et al. An outbreak of dengue serotype 2 in the city of Djibouti, East Africa. Transactions of the Royal Society of Tropical Medicine and Hygiene (in press). 21. Salah S et al. A negative human serosurvey of haemorrhagic fever viruses in Djibouti. Annales de l'lnstitut Pasteur/Virologie, 1988, 139: 439-442. 22. Oldfield IlIl EC, Rodier G, Gray G. Endemic infec- tious diseases of Somalia. Clinical infectious dis- eases, 1993, 16(suppl. 3): S131-S157. 23. Saleh AS et al. Dengue in north-east Africa. Lan- cet, 1985, 1: 211-212. 24. Botros BA et al. Serological evidence of dengue fever among refugees, Hargueysa, Somalia. Journal of medical virology, 1989, 29: 79-81. 25. Mouchet J. Aedes aegypti et les vecteurs potentiels de la fievre jaune en R6publique D6mocratique de Somali et dans le Territoire fran,ais des Afars et des Issas. Bulletin of the World Health Organization, 1971, 45: 383-394. 26. Cope SE et al. Status of Aedes aegypti in the Republic of Djibouti. Proceedings of the Meeting of the American Mosquito Control Association, 1993. 27. Pankhurst R. The history of cholera in Ethiopia. Medicine history, 1968, 12: 262-269. 28. World Health Organization. Disease notifications. Weekly epidemiological record, 1992, 67(28): 212. 29. Rodier G et al. Presence of antibodies to Hanta- virus in human and rodent populations of Djibouti. Transactions of the Royal Society of Tropical Medi- cine and Hygiene, 1993, 87: 160-161. 30. Cavallo JD, et al. Sensibilit6 aux antibiotiques de 140 souches de Shigella isol6es a Djibouti. Bulletin de la Soci6t6 de Pathologie exotique, 1993, 86: 35-40. WHO Bulletin OMS. Vol 73 1995 759