Sporadic YF epidemics have been reported in eastern Africa since 1940, when the first documented YF epidemic in the region occurred also in the Nuba Mountains of Sudan.5,11
A smaller YF epidemic in Sudan occurred in 1959 in the Blue Nile and Upper Nile states bordering Ethiopia, followed by a large outbreak in Ethiopia during 1960–1962.12
In recent years, sylvatic YF outbreaks have occurred in Kenya in 1992–1993,13–15
and in the Imatong Mountains of southern Sudan in 2003.16,17
Entomologic investigations performed during these epidemics have demonstrated the importance of sylvatic Aedes
vectors in addition to the urban YF vector, Ae. aegypti
, in Sudan. These vectors also transmit CHIKV, which is endemic in Sudan.18–20
Our survey indicates that YFV and CHIKV were recently transmitted in Kortalla, and contributed to the outbreak. The survey results provide a more detailed clinical and laboratory evaluation of the illnesses that would have been reported as suspected YF, confirming that multiple etiologies likely contributed to the 605 suspected YF cases reported from South Kordofan state to the FMoH.4
The history of recent YF vaccination in most of the persons who provided blood samples limits the interpretation of serologic results because we cannot differentiate wild-type YFV infection from vaccination serologically by using ELISA and PRNT. However, the serologic evidence of acute YFV infection in two reportedly unvaccinated persons provides evidence of recent YFV transmission, and the positive result for CHIKV IgM in one person (together with the isolation of CHIKV from two ill persons who lived in Kortalla noted in the introduction to this paper) suggests recent CHIKV transmission. The case-fatality rates in Kortalla of 4% for febrile illness, 8% for YF-like illness, and 23% for severe YF-like illness are consistent with mortality rates reported in prior YF outbreaks in Africa.14,17,21,22
Twelve percent of household members reported an illness suggestive of chikungunya fever. However, one of these persons was a participant with serologic evidence of recent YF, reinforcing the concept that clinical manifestations of arboviral infection overlap and specific diagnosis of arboviral illness requires laboratory evidence of infection with a specific virus. Although antibodies against CHIKV cross-react with the related alphavirus o'nyong-nyong virus, antibodies to o'nyong-nyong virus react only weakly against CHIKV, and neither flavivirus antibody nor alphavirus antibody typically cross-react outside their respective families.23
Serosurvey participants with CHIKV IgG but not IgM may have been infected with CHIKV early during the outbreak, or may have been infected at an undetermined time in the past.
The YF vaccination campaign appeared to be effectively implemented in Kortalla. Recent YF vaccination was reported in 95% of household members, and 99% of vaccinated household members tested had evidence of protective immunity to YFV. Serosurvey participants with no detectable YF IgM may have had a suppressed IgM response because of prior flavivirus exposure.24
Because Sudan has not incorporated YF vaccine into routine immunization programs, and there have been no prior YF vaccination campaigns in South Kordofan, the residents of Kortalla probably had not received any YF vaccination prior to the 2005 campaign.
The results of our survey may be limited by recall bias as well as cultural and language barriers. Such information bias could result in overestimation or underestimation of illness attack rates. The accuracy of our estimates would also be limited if other undetected etiologies, such as malaria, contributed to the symptoms reported in the outbreak. To reduce selection bias, we attempted to choose serosurvey participants randomly. However, all household members were rarely present, and parents often did not want small children to be bled. Residual selection bias is likely manifested in the higher rates of illness reported by serosurvey participants compared with all participants in the household survey (). In addition, because we performed the survey during mid-day, the serosurvey probably underrepresented people who work in the fields and might have greater exposure to the sylvatic YF cycle. This finding is reflected in the demographic differences between the serosurvey group and the reported household demographics. These possible selection biases limit inferences regarding the prevalence of antibody and illness in the community. Finally, estimation of the true attack rates of YF through interpretation of the serologic results is limited by the high coverage of recent YF vaccination.
Despite these limitations, the results of this investigation suggest that CHIKV and YFV contributed to febrile illness in Kortalla during this outbreak. Evidence that both viruses contributed to the wider outbreak in South Kordofan has been previously published.4
Finally, the high reported vaccination rates and serologic evidence of YF immunity indicate that the intensive vaccination campaign conducted in South Kordofan had high coverage and resulted in protective humoral immunity. These results indicate that it is possible to achieve good vaccine coverage in remote areas at high risk for outbreaks of sylvatic YF.