In mid-July 2002, Madagascar health authorities were notified of a high number of deaths due to acute respiratory illness in the village of Sahafata (population 2160), located in the rural highlands of Fianarantsoa Province. This region is approximately 450–500 km south of the capital Antananarivo. In late July, a similar alert was reported from Ikongo District, Fianarantsoa Province. Staff from the Ministry of Health (MOH) and the Institut Pasteur, Madagascar (IPM) investigated both events. Pharyngeal swab specimens were collected from ill persons for viral culture. Four influenza A viruses were isolated at the IPM; two were sub-typed as A (H3N2) viruses. In 7 August, the MOH requested assistance from the World Health Organisation (WHO). In response, the Global Outbreak Alert and Response Network (GOARN) mobilised an international team comprised of three medical epidemiologists from the Institut de Veille Sanitaire (InVS), France, and Centers for Disease Control and Prevention (CDC), USA, two microbiologists from the Institut Pasteur, France, and WHO Regional Office for Africa (AFRO), and a logistician from WHO Global Alert and Response (GAR). The team arrived in Madagascar on 14 August. This report summarises preliminary epidemiological and virological findings.

Epidemiological findings

Nationwide surveillance for influenza-like illness cases implemented by the MOH revealed that the outbreak peaked during the week of 22 August. As of 19 September, 30 304 cumulative cases and 754 deaths had been reported from 13 of 111 health districts and 4 of 6 provinces (Map); 85% of cases were reported from Fianarantsoa Province. Most illnesses occurred in rural areas and 95% of deaths occurred away from health facilities and could not be investigated. No standardised case definition was used and the degree of over-reporting or under-reporting of influenza-like illness cases is uncertain.

Field investigations were conducted in 3 districts of Fianarantsoa Province where high numbers of cases and deaths had been reported. The investigations’ objectives were to confirm the aetiology of the outbreak, and to make recommendations based upon the epidemiological findings. An analysis of acute respiratory illness (ARI) data from 1999–2002 collected at health centres showed that ARI cases peaked each year during the winter months in highland districts. The peaks in ARI cases coincided with peaks of mortality from all causes and from respiratory conditions such as pneumonia for the years that data were available. In Ikongo District (population 161 494), the numbers of ARI cases evaluated at health centres and deaths from all causes that occurred during July–August 2002 were substantially higher than during the identical periods in previous years. However, the proportion of deaths to ARI cases appeared to be similar to the proportions during previous years.

In Ikongo District, 54% of the reported deaths due to ARI that occurred in July–August 2002 were among children under 5 years, but the highest mortality rate was among persons aged 60 years and over. A survey of a remote village (population 750) in Ikongo District showed an attack rate for acute febrile respiratory illness of 67% and an estimated case fatality ratio of 2%. In contrast, no unusually high morbidity or mortality was reported among the population of the province’s capital (Fianarantsoa town), or in Antananarivo (population 1.25 million), where morbidity and virologic surveillance for influenza are conducted year-round by the IPM.

Virological data

Between 19 July and 22 August, a total of 152 respiratory specimens were collected for viral isolation from ill persons in three areas of Fianarantsoa Province (Sahafata, Ikongo and Manandriana) where outbreaks occurred. The international team also used rapid influenza antigen tests to test specimens in the field. Influenza A viruses were isolated from specimens collected from ill persons in each area that was investigated. There were 27 influenza isolates that were antigenically characterised at the IPM and confirmed by the WHO Collaborating Centre for Reference and Research on Influenza, London, UK, and all isolates were A/Panama/2007/99-like (H3N2) viruses. The H3N2 component of both the 2002 Southern Hemisphere and 2002–03 Northern Hemisphere influenza vaccines are well matched to the outbreak strain.

The outbreak appears attributable to influenza A/Panama/2007/99-like (H3N2) viruses, which have been in circulation worldwide for a number of years. Several factors may have contributed to the widespread ARI morbidity and unusually high mortality reported from rural highlands of Madagsacar. Crowdedliving conditions during a cold and wet winter may have facilitated person-to-person transmission of influenza among highly susceptible populations. In Fianarantsoa, 40% of under five children suffer from chronic malnutrition and access to basic health care is poor for most villages. These factors may have been further exacerbated by civil unrest that plagued the country from December 2001 to June 2002.

Conclusions

This outbreak illustrated several important lessons for controlling influenza outbreaks in developing countries and for global pandemic influenza planning. Since it occurred primarily in remote areas, awareness of the outbreak and response by health authorities were delayed. Although influenza surveillance is conducted in Antananarivo by the IPM’s WHO-recognised national influenza laboratory, no data were available for the most impacted areas. In Madagascar, as in many developing countries, problems such as malnutrition, poor access to health care, difficulties in reaching populations in rural areas, limited communicable disease surveillance, shortages of antibiotics to treat secondary bacterial complications, the unavailability of influenza vaccine, and lack of awareness about influenza complicated efforts to assess and control the outbreak (1, 2).

The team’s recommendations included: expanding influenza surveillance, educating the public and health care providers about influenza, improving access to health care in rural areas, and ensuring that adequate supplies of antibiotics are available at health centres to treat bacterial complications of influenza. Influenza vaccination was not recommended because the outbreak was already widespread in August, and the ability to distribute vaccine in remote areas was extremely limited.

Acknowledgments: this report reflects important contributions by

L Rasoazanamiarina, AL Rakotonjanabelo, D Randrianasolo, C Ravaonjanahary, (Ministry of Health, Madagascar); A. Ndikuyeze, B. Andriamahefazafy (WHO Madagascar); G Razafitrimo, R Migliani, M Ratsitorahina, P Grosjean, N Rasolofonirina, L Rabarijaona, (Institut Pasteur, Madagascar); J Rasamizanaka, H Ravokatsoa, L Razafilahy, B Tanjaka, P Rakotoarisoa, E Raharilalao (Public Health Services, Fianarantsoa Province, Madagascar); R Arthur, N Shindo, K Ströhr (WHO/CSR Geneva); A Hay (WHO Collaborating Centre for Reference and Research on Influenza, London, U.K); S Harper, K Fukuda, J LeDuc (CDC USA).

* The WHO-GOARN teams was composed of (alphabetical order):

M. Kamel Ait-Ikhlef, CSR/GAR WHO Geneva; Dr Isabelle Bonmarin; Infectious Diseases Department, InVS, France; Pr Bréhima Koumare, WHO AFRO IPC/EMC, Abidjan; Dr Jean-Claude Manuguerra, WHO Collaborating Center for Research and Reference on Influenza and Other Respiratory Viruses, National Reference Center for Influenza (North France), Institut Pasteur, France; Dr Christophe Paquet (team leader) International Health Department, InVS, France; Dr Timothy Uyeki, Influenza Branch, Division of Viral and Rickettsial Diseases, CDC, USA.