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Ebola Hemorraghic

Ebola Hemorraghic

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From August 2000 through January 2001, a large epi-demic of Ebola hemorrhagic fever occurred in Uganda, with425 cases and 224 deaths. Starting from three laboratory-confirmed cases, we traced the chains of transmission for three generations, until we reached the primary case-patients (i.e., persons with an unidentified source of infec-tion). We then prospectively identified the other contacts inwhom the disease had developed. To identify the risk fac-tors associated with transmission, we interviewed bothhealthy and ill contacts (or their proxies) who had beenreported by the case-patients (or their proxies) and whomet the criteria set for contact tracing during surveillance.The patterns of exposure of 24 case-patients and 65healthy contacts were defined, and crude and adjustedprevalence proportion ratios (PPR) were estimated for dif-ferent types of exposure. Contact with the patient’s bodyfluids (PPR = 4.61%, 95% confidence interval 1.73 to12.29) was the strongest risk factor, although transmissionthrough fomites also seems possible.
E
 bola hemorrhagic fever (EHF) is a severe viral diseasecaused by three of the four species of “Ebola-likeviruses” (1), which are probably maintained in an as-yet-undefined natural reservoir in the rain forests of Africa (2).Epidemics occur when an infectious case-patient is intro-duced into a susceptible population. The first recognizedepidemics occurred almost simultaneously in 1976 insouthern Sudan (284 cases and 117 deaths) (3) and in anearby region of the Democratic Republic of Congo (318cases and 280 deaths) (4). Amajor mode of transmissionwas within hospitals, especially in the early stages of theoutbreaks. Person-to-person transmission also occurredoutside the hospital setting, with numerous community-acquired cases (3,4).In 1995, another large epidemic occurred in Kikwit, inthe Democratic Republic of Congo, with 315 cases and244 deaths (5). The primary mode of transmission was per-son-to-person transmission to household members whohad had direct contact with sick persons or their body flu-ids, especially during the late stage of the disease (6).However, the source of infection remained unknown for 12case-patients, which led to the suspicion that the virus wastransmitted by airborne particles or fomites (7).The largest epidemic (425 presumptive cases and 224deaths) occurred from August 30, 2000 (i.e., the earliest presumptive case), to January 9, 2001 (i.e., onset of the lastcase), in the Republic of Uganda, which borders both theDemocratic Republic of Congo and Sudan (8–11). Sincethen, epidemics have been occurring with increasing fre-quency. Specifically, between December 2001 and March2002, outbreaks occurred in the Republic of Gabon (65cases and 53 deaths) (12,13) and in the neighboringRepublic of Congo (57 cases and 43 deaths) (12). InFebruary 2003, cases again began to be reported in theRepublic of Congo, where 13 laboratory-confirmed case- patients and 127 epidemiologically linked case-patients,including 123 deaths, have been reported to date (14).During the epidemic in Uganda, a national task force, incollaboration with an international team of health profes-sionals, conducted activities for controlling the epidemicand managing cases (11). The area in which the epidemicwas mainly concentrated was the Gulu District, a savannaharea located in the north and mainly inhabited by Nilotic
1430Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 9, No. 11, November 2003
RESEARCH
Ebola Hemorrhagic Fever Transmission and Risk Factors of Contacts,Uganda
1
Paolo Francesconi,* Zabulon Yoti,† Silvia Declich,* Paul Awil Onek,‡ Massimo Fabiani,* Joseph Olango,‡ Roberta Andraghetti,* Pierre E. Rollin,§ Cyprian Opira,† Donato Greco,* and Stefania Salmaso*
*Istituto Superiore di Sanità, Rome, Italy; †St. Mary’s HospitalLacor, Gulu, Uganda; ‡Ministry of Health, Kampala, Uganda; and§Centers for Diseases Control and Prevention, Atlanta, Georgia,USA
1
This paper is dedicated to Dr. Matthew Lukwiya, MedicalSuperintendent of St. Mary's Hospital Lacor, and the other healthstaff who contracted and died of Ebola while taking care of hospi-tal patients.
 
tribes. Most of the district’s 400,000 inhabitants live inGulu Town or in one of several camps, located in ruralareas, for persons who have been internally displaced because of the insecurity caused by the activity of insur-gents. On October 8, an outbreak of EHF was suspected at StMary’s Hospital Lacor (hereafter termed Lacor Hospital),a nonprofit facility located several kilometers from GuluTown. Two days later, isolation wards were set up in thedistrict’s major hospitals, i.e., Lacor Hospital and the GuluGovernment Hospital. In Lacor Hospital, only the hospitalstaff provided patient care in the isolation ward, whereas inthe Gulu Government Hospital, relatives were allowed tocontribute, which is the usual practice in Ugandan hospi-tals. The staff of both hospitals adopted strict barrier nurs-ing precautions (e.g., gloves, masks, gowns, aprons, rubber  boots); in the Gulu Government Hospital, these precau-tions were partially extended to patients’relatives. OnOctober 15, the outbreak was confirmed, and a system of daily case reporting, including a computerized database,was established. Acase-patient was defined as a personwho experienced at least one of the following events(9,10): 1) unexplained bleeding; 2) abrupt onset of fever and three or more of the following symptoms or signs:headache, vomiting, anorexia, diarrhea, weakness, or severe fatigue, abdominal pain, body aches or joint pain,difficulty in swallowing, difficulty in breathing, and hic-cups; and 3) death from unexplained causes.On October 21, 2000, the Centers for Disease Controland Prevention (CDC) set up a laboratory for performingenzyme-linked immunosorbent assays (ELISAs) for Ebolaantigens and antibodies and reverse transcriptase-poly-merase chain reaction (RT-PCR) at Lacor Hospital.Laboratory confirmation (positive result for Ebola virusantigen or Ebola immunoglobulin [Ig] G antibody) wasobtained for 218 (51.3%) of the total 425 presumptivecases involved in the epidemic (9,10).At approximately the same time, a surveillance systemfor contact tracing and case finding was established. Acontact was defined as a person who had at least one of thefollowing exposures: 1) physical contact with a case- patient, alive or dead; 2) slept in the same hut or housewith a case-patient during the disease period; 3) contactwith a case-patient’s body fluids during the disease period;and 4) contact with a case-patient’s linens or other possiblefomites during the disease period and just after death.Members of the surveillance teams and the hospital staff were not considered contacts, even if they were exposed toa case-patient, because they had been taught how to protectthemselves. For each case-patient, a list of contacts wascreated; all contacts were followed by daily home visits for 21 days (maximum incubation period) from the last con-tact with the case-patient (11).In November and December 2000, we collected addi-tional data from a group of contacts (or their proxies) con-cerning the nature and timing of their exposure to case- patients. Our objective was to trace chains of transmissionand identify risk factors for transmission among a group of exposed persons in the community. This study, the resultsof which are reported here, was fully integrated into thesurveillance activities described above and was authorized by the director of the Gulu District Health Services and theUgandan Ministry of Health.
Methods
Study Design and Population
To retrospectively trace the chain of transmission, weinterviewed three laboratory-confirmed case-patients inthe Lacor Hospital who had onset of symptoms October 23–28 (referred to as “study case-patients”; see Table 1 for other definitions). We asked them to identify the personsfrom whom they had probably acquired the disease(referred to as index patients). In turn, the index patients(or their next of kin living in the same village if they haddied, as was usually the case) were then asked to identifythe persons from whom they had probably acquired thedisease (also referred to as index patients). This processwas repeated until we reached the patients whose source of infection could no longer be identified (referred to as pri-mary case-patients). For each of the index patients and pri-mary case-patients, we then reviewed the list of persons
Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 9, No. 11, November 20031431
RESEARCH
Table 1. Definitions used in the chain of transmission of Ebola hemorrhagic fever
Classification Definition Study patients The three laboratory-confirmed case- patients from whom we retrospectively identified the other case-patients and their contacts Index patients The nine case-patients retrospectively identified from the study patients as the source of infection (including primary case-patients) Primary case-patients The three earliest patients for whom we were not able to identify the source of infection Collateral case-patients Cases generated by the index patients, or  by other collateral case-patients, and identified by matching the list of contacts of these persons with the list of reported cases Postprimary case-patients Case-patients for whom we were able to identify the source of infection Contacts Persons exposed to a case-patient, listed  by the surveillance teams using the definition reported in the background section. Healthy contacts Contacts in whom the disease did not develop within 21 days of the last exposure
 
with whom they had been in contact since the onset of their symptoms; such information had been routinely collectedas part of surveillance. Then, as 21 days had passed sincethe last exposure, each name on the list was matched witha name on the list of reported case-patients in order toidentify the contacts in whom the disease had developed(collateral case-patients). The process was then repeated prospectively with the collateral case-patients for as manygenerations as possible.To identify risk factors, we interviewed all of the iden-tified contacts (or their proxies) of the primary, index, andcollateral case-patients, irrespective of their status (patientor healthy contact). To this end, we developed a question-naire that focused on the exact type and timing of exposureto index patients.
Data Analysis and Statistical Methods
We performed univariate analyses to evaluate thestrength of associations between the different types of expo-sure and disease, by comparing disease prevalence among persons with a given exposure to that among persons with-out that exposure and by testing the resulting differenceswith the chi-square test or, when appropriate, the Fisher exact test. Those risk factors independently associated withthe disease were evaluated in multivariate analyses by usinglog-binomial regression models after we ascertained theabsence of a significant multiple colinearity among thevariables. The crude and adjusted prevalence proportionratios (PPR) and their 95% confidence intervals (CI) wereused to describe the strength of the associations (15).
Results
Chains of Transmission
The Figure illustrates the three reconstructed chains of transmission; each consisted of three identified genera-tions of cases (excluding the study case-patients). The 27identified case-patients consisted of, in addition to the 3laboratory-confirmed patients with whom we began thestudy, 9 index case-patients (including 3 primary case- patients, all young women whose source of infection wasunknown), and 15 collateral case-patients. Of the 24 post- primary patients, 14 (58.3%) lived in the Gulu Town or Municipality, and 10 (41.7%) lived in rural areas of theGulu District. One patient was a newborn, and three wereinfants. The remaining 20 patients (83.3%) ranged in agefrom 14 to 70 years; 14 (70.0%) of these 20 patients werefemale, and most were housewives or subsistence farmers(70.0%).The 24 postprimary patients had onset of symptomsfrom September 18 to October 28, 2000. The incubation period (i.e., time elapsed between either the last or the firstcontact with the index patient and the onset of symptoms)was 1–16 days (median 6 days), when the last contact wasconsidered, and 1–12 days (median 12 days), when thefirst contact was considered. All three infants had an incu- bation period of <7 days.Twenty (83.3%) of the 24 postprimary case-patientswere admitted to the hospital;13 (65.0%) were admittedafter the isolation ward had been created. The four patientsnot admitted to the hospital (a newborn, two infants, andan elderly woman) died within 3 to 11 days of diseaseonset. Of the 20 hospital patients, 7 were still in the hospi-tal when the laboratory was set up, and 3 were admittedafterwards; all 10 of these patients tested positive for Ebolaantigens, IgG, or both.Of the 20 hospitalized patients, 15 died. Among these15 patients, the duration of illness (from onset of symp-toms to death) was 3–15 days (median 10 days); the dura-tion of hospitalization (from admission to death) was 2–11days (median 5 days). Among the five surviving patients,the duration of illness (from onset of symptoms to dis-charge upon clinical recovery) was 10–25 days (median 15days); the duration of hospitalization was 8–22 days(median 13 days).Of the 27 patients, all of the primary and secondarycase-patients died. Of the remaining 17 patients, 12(70.6%) died. Of the four persons who died without beingadmitted to the hospital, two had secondary cases and twohad tertiary cases.In the legend to the Figure, the 27 cases are brieflydescribed and the mode of transmission is summarized for the 24 postprimary cases. The newborn (case-patient 20)was delivered by a sick woman 4 days after the onset of symptoms, and the other three infants (case-patients 2, 9,and 26) had been breastfed by sick mothers. The other 20 postprimary cases were all members of the extended fam-ily (household contacts) of the case-patients to whom theyhad been exposed. All but one (95%) had had direct phys-ical contact with the patient who was the likely source of their disease; the remaining person (case-patient 7) hadslept wrapped up in a blanket left by his brother, who had just died of EHF.Among the 20 postprimary case-patients who were >14years of age, 15 (75.0%) reported that they had beenexposed to the body fluids of their index patient; 11(55.0%) had washed the index patient’s clothes; and 18(90.0%) had taken care of the index patient at some pointduring his or her illness. Twelve of these 18 persons hadtaken care of the index patient until death, either in the hos- pital (n = 6) or at home (n = 6). Eleven (55.0%) of these 20 postprimary patients had slept in the same hut or house asthe index patient; of these, 5 had slept with the index patient on the same mat or mattress. Six (30.0%) of these20 postprimary patients had shared meals with index patients (picking up food with their fingers from the same
1432Emerging Infectious Diseases • www.cdc.gov/eid • Vol. 9, No. 11, November 2003
RESEARCH

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