Ebola Hemorrhagic Fever Transmission and Risk Factors of Contacts, Uganda

Paolo Francesconi; * Zabulon Yoti; † Silvia Declich; * Paul Awil Onek; ‡ Massimo Fabiani; * Joseph Olango; ‡ Roberta Andraghetti; * Pierre E. Rollin; § Cyprian Opira; † Donato Greco; * Stefania Salmaso*

Disclosures

Emerging Infectious Diseases. 2003;9(11) 

In This Article

Results

The Figure illustrates the three reconstructed chains of transmission; each consisted of three identified generations of cases (excluding the study case-patients). The 27 identified case-patients consisted of, in addition to the 3 laboratory-confirmed patients with whom we began the study, 9 index case-patients (including 3 primary case-patients, all young women whose source of infection was unknown), and 15 collateral case-patients. Of the 24 postprimary patients, 14 (58.3%) lived in the Gulu Town or Municipality, and 10 (41.7%) lived in rural areas of the Gulu District. One patient was a newborn, and three were infants. The remaining 20 patients (83.3%) ranged in age from 14 to 70 years; 14 (70.0%) of these 20 patients were female, and most were housewives or subsistence farmers (70.0%).

Chains of transmission relative to 27 Ebola cases, Gulu District, Uganda (September–October 2000). The numbers above the blocks indicate the total number of healthy contacts identified for that patient. The slashes indicate patients who died. The isolation ward was opened on October 8. *A laboratory facility for serologic diagnosis of Ebola was set up at Lacor Hospital by the Centers for Disease Control and Prevention on October 21. Description of individual cases follows: 1. AF, young woman, admitted at Gulu Hospital Sept. 19, died the same day. She was buried the following day, next to her parents' house, without known identified case-patients among those who attended the burial ceremony; 2. OS, son of AF (4 months old); breastfed even during the last days of his mother's life; admitted to Lacor Hospital; died Sept. 30. 3. OA, father-in-law of AF; nursed his daughter-in-law during the last days of the disease, both at home and in the hospital; reported contact with blood and vomit; died Oct. 7. 4. AR, grandmother of OS; nursed the child after the mother's death; reported contact with feces and urine; survived. 5. ON, cousin of OA, whom ON touched before and after OA's death; no reported contacts with body fluid; died Oct. 16. 6. OR, brother of OA; nursed him during last days; reported contacts with feces; died Oct. 17. 7. OJ, brother of ON; used the blanket left by his brother; survived. 8. AE, young woman who sold beer to soldiers; died Sept. 17. 9. OS, son of AE; breastfed; died Sept. 21. 10. AD, mother of AE; nursed her; reported contact with vomit and feces; prepared the dead body; died Oct. 1. 11. AJ, sister of AE; nursed her; reported contact with feces and vomit; prepared the dead body; died Oct. 4. 12. AV, aunt of OS; nursed the child after the mother's death; reported contact with vomit and feces; died Oct. 11. 13. AN, cousin of OS; they slept together; reported contact with vomit and feces; survived. 14. AV, daughter of AD; nursed her; reported contact with vomit and feces; died Oct. 7. 15. AV, niece of AD; reported direct contact with her during illness; died Oct. 23. 16. AS, daughter of AJ; nursed her, both at home and in the hospital; no reported contact with body fluids; died Oct. 24. 17. AS, co-wife of A J; nursed her; reported contact with blood; died Oct. 24. 18. AE, sister-in-law of AJ; assisted her during delivery on Sept. 28; died Oct. 17. 19. LV, aunt of AJ; assisted her during delivery on Sept. 28; died Oct. 22. 20. OW, son of AJ; born on Sept. 28; died Oct. 9. 21. OJ, husband of LV; nursed her; died Nov. 1. 22. AC, cousin of AV; nursed her; reported contact with feces; survived. 23. AG, young woman; lived next to the barracks; died Oct. 8. 24. AL, sister of AG; nursed her; reported contact with vomit; died Oct. 18. 25. JB, sister of AG; nursed her; reported contact with vomit; died Oct. 26. OR, son of AL; breastfed; died Oct. 21. 27. AF, grandmother of OR; nursed the child after the mother's death; reported contact with feces and vomit; survived.

The 24 postprimary patients had onset of symptoms from September 18 to October 28, 2000. The incubation period (i.e., time elapsed between either the last or the first contact with the index patient and the onset of symptoms) was 1–16 days (median 6 days), when the last contact was considered, and 1–12 days (median 12 days), when the first contact was considered. All three infants had an incubation period of <7 days.

Twenty (83.3%) of the 24 postprimary case-patients were admitted to the hospital; 13 (65.0%) were admitted after the isolation ward had been created. The four patients not admitted to the hospital (a newborn, two infants, and an elderly woman) died within 3 to 11 days of disease onset. Of the 20 hospital patients, 7 were still in the hospital when the laboratory was set up, and 3 were admitted afterwards; all 10 of these patients tested positive for Ebola antigens, IgG, or both.

Of the 20 hospitalized patients, 15 died. Among these 15 patients, the duration of illness (from onset of symptoms to death) was 3–15 days (median 10 days); the duration of hospitalization (from admission to death) was 2–11 days (median 5 days). Among the five surviving patients, the duration of illness (from onset of symptoms to discharge upon clinical recovery) was 10–25 days (median 15 days); the duration of hospitalization was 8–22 days (median 13 days).

Of the 27 patients, all of the primary and secondary case-patients died. Of the remaining 17 patients, 12 (70.6%) died. Of the four persons who died without being admitted to the hospital, two had secondary cases and two had tertiary cases.

In the legend to the Figure, the 27 cases are briefly described 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 family (household contacts) of the case-patients to whom they had been exposed. All but one (95%) had had direct physical contact with the patient who was the likely source of their disease; the remaining person (case-patient 7) had slept wrapped up in a blanket left by his brother, who had just died of EHF.

Among the 20 postprimary case-patients who were ≥14 years of age, 15 (75.0%) reported that they had been exposed 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 point during his or her illness. Twelve of these 18 persons had taken care of the index patient until death, either in the hospital (n = 6) or at home (n = 6). Eleven (55.0%) of these 20 postprimary patients had slept in the same hut or house as the index patient; of these, 5 had slept with the index patient on the same mat or mattress. Six (30.0%) of these 20 postprimary patients had shared meals with index patients (picking up food with their fingers from the same plate). Sixteen (80.0%) of the 20 adult postprimary patients had attended the funeral of their index patient; 11 had also prepared the body for the ceremony or simply touched the dead body; 11 had participated in the communal meal during the ceremony; and 7 had participated in the ritual handwashing during the ceremony.

We also interviewed the 65 apparently healthy contacts of the 9 index patients and 15 collateral case-patients. Notably, not all patients generated contacts, and the six who did not were all third- (n = 5) or fourth-generation case-patients. Five had had onset of symptoms after the isolation ward was created.

Of the 65 healthy contacts, 39 (60.0%) lived in the Gulu Municipality and 23 (35.4%) in rural areas of the Gulu District; information on residence was not available for the remaining three. Two of the healthy contacts (3.1%) were infants, and four (6.2%) were 3–8 years of age The remaining 59 (90.8%) ranged in age from 10 to 70 years; 33 (55.9%) were female; most were housewives or subsistence farmers (60.0%).

One of the two infants had been separated from his sick mother early in the course of the mother's illness; the other infant had been breastfed during his mother's illness. All four of the children 3–8 years of age had slept in the same hut as their sick parent and had had direct physical contact with their sick parent or relative (none of them had taken care of the sick person). None of these four children was reported to have been in contact with the patient's body fluids.

Of the 59 healthy contacts ≥10 years of age, 50 (84.7%) were extended family members of the patient (household contacts); 9 were neighbors of the patient. Forty-seven (79.7%) had had direct physical contact with the case-patient; 15 (25.4%) had been exposed to body fluids; 18 (30.5%) had washed the patient's clothes; and 25 (42.4%) had taken care of the sick person. Of these 25 persons, 11 had taken care of their relative up to the last days of life, either in the hospital (n = 8) or at home (n = 3). Moreover, 13 (22.0%) had slept in the same hut as the patient; 4 had shared the same mat; 7 (11.9%) had shared meals with the index patient (picking up food with their fingers from the same plate).

Thirty-seven (62.7%) of these 59 healthy contacts had attended the funeral of the patient; 14 of them had also touched the dead body. In addition, 14 healthy contacts had participated in the communal meal during the ceremony, and 9 had participated in the ritual handwashing.

Because of their particular exposures, infants ≤2 years were excluded from the analysis of risk factors. Among the 83 remaining contacts, disease developed in 20. Sixty-three contacts remained healthy. Among contacts, neither age (>30 years vs. ≤30 years: PPR = 1.38, 95% CI 0.64 to 2.97) nor sex (women vs. men: PPR = 1.54, 95% CI 0.66 to 3.60) was significantly associated with the disease ( Table 2 ).

Contact with body fluids showed a strong association (PPR = 5.30, 95% CI 2.14 to 13.14). Persons who had had direct physical contact with a sick person were more likely to have acquired the disease (PPR = 3.53, 95% CI 0.52 to 24.11), as were those who had touched the body of the deceased person (PPR = 1.95, 95% CI 0.91 to 4.17), although these associations were not statistically significant.

Regarding indirect transmission, sleeping on the same mat (PPR = 2.78, 95% CI 1.15 to 6.70), participating in the ritual handwashing during the funeral ceremony (PPR = 2.25, 95% CI 1.08 to 4.72), and sharing a communal meal during the funeral ceremony (PPR = 2.84, 95% CI 1.35 to 5.98) were significantly associated with disease. Although the differences were not statistically significant, sharing meals, washing clothes, and sleeping in the same hut were associated with a higher risk of acquiring the disease.

In general, having taken care of a sick person represented a strong risk factor, although the level of risk was lower for persons who had provided care only at the early stage of the disease (PPR = 6.00, 95% CI 1.33 to 27.10), followed by the risk for those who provided care until the index patient's death, either at the hospital (PPR = 8.57, 95% CI 1.95 to 37.66) or at home (PPR = 13.33, 95% CI 3.20 to 55.59) ( Table 3 ).

The risk tended to increase with the increasing number of different types of direct contact (chi square for trend p < 0.001); the risk was higher among persons who were exposed through two (PPR = 1.94, 95% CI 0.30 to 12.94) or three different types of direct contact (PPR = 4.00, 95% CI 0.64 to 25.02), compared with the risk for those who had no direct contact ( Table 3 ).

Factors related to direct and indirect transmission were analyzed separately in multivariate analyses ( Table 4 ). The first model (i.e., factors related to direct transmission) showed that having had contact only with body fluids (adjusted PPR = 4.61, 95% CI 1.73 to 12.29) was strongly associated with the disease, whereas having only touched the patient during illness was not (adjusted PPR = 1.56, 95% CI 0.19 to 13.04). (The weak association found in the univariate analysis was probably confounded by contact with the patient's body fluids.) Having touched the body of the deceased person (adjusted PPR = 1.84, 95% CI 0.95 to 3.55) showed a borderline significant association.

The second model (i.e., factors related to indirect transmission and controlled for the potential confounding effect attributed to the number of different types of direct contact) showed that sleeping in the same hut (adjusted PPR = 2.34, 95% CI 1.13 to 4.84) and sleeping on the same mat (adjusted PPR = 2.93, 95% CI 1.16 to 7.38) were independent risk factors. However, weak associations were found for sharing meals with a sick person and participating in the communal meal during the funeral, whereas the ritual handwashing during the funeral and washing the sick person's clothes were not risk factors.

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