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Date Palm Sap Linked to Nipah Virus Outbreak in Bangladesh, 2008

Muhammad Aziz Rahman
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Mohammad Jahangir Hossain
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Sharmin Sultana
Institute of Epidemiology, Disease Control and Research, Dhaka, Bangladesh.

Nusrat Homaira
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Salah Uddin Khan
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Mahmudur Rahman
Institute of Epidemiology, Disease Control and Research, Dhaka, Bangladesh.

Emily S. Gurley
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Pierre E. Rollin
Centers for Disease Control and Prevention, Atlanta, Georgia.

Michael K. Lo
Centers for Disease Control and Prevention, Atlanta, Georgia.

James A. Comer
Centers for Disease Control and Prevention, Atlanta, Georgia.

Lowe
Centers for Disease Control and Prevention, Atlanta, Georgia.

Paul A. Rota
Centers for Disease Control and Prevention, Atlanta, Georgia.

Thomas G. Ksiazek
Centers for Disease Control and Prevention, Atlanta, Georgia.

Eben Kenah
Department of Biostatistics, University of Washington, Seattle

Yushuf Sharker
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Stephen P. Luby
International Centre for Diarrhoeal Disease Research, Bangladesh, Dhaka, Bangladesh.

Abstract/ Executive Summary:

ntroduction: We investigated a cluster of patients with encephalitis in the Manikgonj and Rajbari Districts of Bangladesh in February 2008 to determine the etiology and risk factors for disease.

Methods: We classified persons as confirmed Nipah cases by the presence of immuno globulin M antibodies against Nipah virus (NiV), or by the presence of NiV RNA or by isolation of NiV from cerebrospinal fluid or throat swabs who had onset of symptoms between February 6 and March 10, 2008. We classified persons as probable cases if they reported fever with convulsions or altered mental status, who resided in the outbreak areas during that period, and who died before serum samples were collected. For the case–control study, we compared both confirmed and probable Nipah case-patients to controls, who were free from illness during the reference period. We used motion-sensor-infrared cameras to observe bat's contact of date palm sap.

Results: We identified four confirmed and six probable case-patients, nine (90%) of whom died. The median age of the cases was 10 years; eight were males. The outbreak occurred simultaneously in two communities that were 44km apart and separated by a river. Drinking raw date palm sap 2–12 days before illness onset was the only risk factor most strongly associated with the illness (adjusted odds ratio 25, 95% confidence intervals 3.3–N, p < 0.001). Case-patients reported no history of physical contact with bats, though community members often reported seeing bats. Infrared camera photographs showed that Pteropus bats frequently visited date palm trees in those communities where sap was collected for human consumption.

Conclusion: This is the second Nipah outbreak in Bangladesh where date palm sap has been implicated as the vehicle of transmission. Fresh date palm sap should not be drunk, unless effective steps have been taken to prevent bat access to the sap during collection.

Keywords: Date Palm Sap, Nipah Virus, Bangladesh

Location: Doulatpur Upazila (subdistrict) of Manikgonj District and Baliakandi Upazila of Rajbari District in central-western region of Bangladesh

Start Date:

End Date:

Program Area: Risk Management in Agriculture

Commodity: Date, Nipah virus

Objectives:

The objectives of the investigation were to determine the cause of the outbreak, identify risk factors for illness, and develop strategies for prevention.

Methodology:

Study Site and Study Population

The communities affected by the outbreak were located in Doulatpur Upazila (subdistrict) (population 155,674) of Manikgonj District and Baliakandi Upazila (population 186,562) of Rajbari District in central-western region of Bangladesh (Bangladesh Bureau of Statistics, 2010). These sites are located 44km apart and are separated by a river. Date palm sap is widely harvested, sold, and consumed in both areas.

Case Identification and Sample Collection

The investigation team sought for suspect cases who had fever and convulsions or altered mental status in the outbreak areas between February 6 and March 10, 2008. First, we visited the hospitals where the patients were treated. We identified the suspect case patients and interviewed them or their proxy respondents. Then we searched for additional case-patients in the affected villages. We collected blood, cerebrospinal fluid (CSF), and throat swab samples from all the living suspect case-patients. The serum and CSF samples were aliquoted locally. The samples were transported to ICDDR, B in cold pack or in liquid nitrogen for storage in −70°C freezer.

We classified persons as confirmed Nipah case-patients by the presence of immunoglobulin M (IgM) antibodies against NiV or by the presence of NiV RNA or by isolation of NiV from CSF or throat swabs. The probable cases were defined as suspect cases who died before sample collection or who had no IgM against NiV in serum collected within 8 days of onset of illness and who died before a follow-up serum sample could be obtained.

Case–Control Study

The investigation team returned to the outbreak communities to conduct a case-control study from March 5 to 10, 2008, to determine the risk factors for illness. We enrolled all confirmed and probable case patients as cases. Individuals who lived in the same communities as the cases, and who were close in age and were free from any febrile illness with convulsions or altered mental status between February 6 and March 10, 2008, were eligible to be enrolled as controls. We identified controls by visiting the fourth closest house to the case-patient's, confirming that no one in the house met the case definition, and identifying the household resident closest in age to the case-patient. We enrolled only one control per household. If the household resident closest in age to the case-patient declined to participate in the study; no other person in the household was sought as a control. This process was repeated at the next closest household until four controls were enrolled for each case-patient.

Data Collection

Trained interviewers collected information from cases and controls using a standardized structured questionnaire in Bengali language, based upon the questionnaires used in previous Nipah outbreak investigations in Bangladesh. We collected a detailed exposure history to previously identified risk factors for cases and respective controls for 1 month preceding the onset of illness of cases. For each case-patient who had died or was unable to respond and for each of the controls who were < 10 years of age, we identified proxy respondents. Proxy respondents included spouses, family members, friends, and neighbors who were knowledgeable about the illness or the exposures of the case-patients and controls. We also conducted informal interviews with several date palm sap collectors and local community residents about the date palm sap collection procedure, recognition of bats in the areas, and possible contamination of date palm sap by bats. We used global positioning system to determine the location of the outbreak areas.

Laboratory Analysis

Serum and CSF samples were tested for IgM and IgG antibodies against NiV using IgM-capture and indirect IgG enzyme immunoassay (Daniels et al., 2001). CSF and throat swab specimens from five patients were tested at the U.S. Centers for Disease Control and Prevention (CDC) laboratory for molecular detection and virus isolation of NiV. Real-time RT-polymerase chain reaction (rRT-PCR) was performed using the following primers that amplified a 112- nucleotide (nt) fragment spanning from position 538 to 660 in the NiV N gene: forward primer NVBNF2B-5′-CTGGTCTCTGCAGTTAT CACCATCGA-3′, reverse primer NVBN593R 5′-ACGTACT TAGCCCATCTTCTAGTTTCA-3′, and probe NVBN542P 5′-CAGCTCCCGACACTGCCGAGGAT-3′, with the FAM dye incorporated at the 5′ end and a BHQ1 molecule at the 3′ end. PCR products were sequenced as previously described (Chadha et al., 2006), and were analyzed using Sequencher 4.10.1 software (Gene Codes).

Date Palm Sap Evaluation

The field team also collected date palm sap early in the morning from both the outbreak areas from February 27 to March 5, 2008. Two separate aliquots for a sample were collected from a tree: one in viral transport medium and another in trizol. The sap specimens were stored in a cold box maintaining temperature around 2°C–8°C and transferred to liquid nitrogen within several hours and later stored in −70°C. The sap was tested at CDC for the presence of NiV RNA by rRT-PCR; the sap was also cultured for NiV.

Infrared Camera Observation

We identified seven date palm trees where sap was collected for the cases' consumption in Manikgonj and Rajbari District outbreak sites. To identify the possible contamination of date palm sap by bats' secretions and to understand bat sap contamination behavior, we mounted one motion-sensor-infrared camera focusing on date palm trees' shaved surface, sap stream, tap, and collection pot in each of the seven trees for a full night (5:00 PM to 6:00 AM).

Data Analysis

We used exact logistic regression to estimate the univariate odds ratios (ORs) with 95% confidence intervals (CIs) between exposures and case status. We stratified on the case–control pairs to account for the matched design. We assessed for confounding by constructing a multivariate exact logistic regression model. We included all exposures during multivariate analysis that had (p < 0.20) in the initial model and removed those exposures one at a time that were not significantly associated with case status. We performed all statistical analyses with STATA version 10.0.

Ethics

Interviewers obtained voluntary informed consent from all participants or proxies; for those <18 years of age, the team obtained individual assent as well as parental consent. This investigation was part of an emergency response to the outbreak, and so a complete human subjects review of all activities was not possible, but the Ethical Review Committee at ICDDR,B had previously reviewed and approved a general protocol for Nipah surveillance and response to outbreaks.

Source of Information: Institute of Medicine (US). Improving Food Safety Through a One Health Approach: Workshop Summary. Washington (DC): National Academies Press (US); 2012.

Article Link (Online Journal):

Funding Source:

Budget:

Total Budget (Tk.) :

Achievement/Findings:

There is evidence of recurrent fatal outbreaks from 2001 through 2007 by the transmission of NiV from its fruit-bat reservoirs to humans in Bangladesh. The present investigation also suggests that date palm sap is an important pathway for this transmission. Drinking fresh date palm sap was the most strongly associated risk factor among the exposures investigated for this outbreak of human NiV infection in this study. The outbreak ended following local warning against drinking fresh date palm sap from the Government of Bangladesh. To prevent this illness, date palm sap should not be drunk fresh unless effective steps have been taken to prevent bat access to the sap during collection. We are working with local date palm sap collectors to develop socially acceptable low cost technologies to prevent bats' access to the date palm sap producing parts of the tree. Studies in Bangladesh involving local date palm sap collectors suggest that using a bamboo-skirt to cover the shaved part of the date palm tree and sap collection pot might be a practical, affordable method to prevent bats' access to the date palm sap (Nahar et al., 2008; Drinking raw date palm sap is a long-practiced tradition in Bangladesh, so public health recommendations to avoid drinking fresh date palm sap are unlikely to be universally followed. Research to identify culturally acceptable approaches to produce safe date palm sap may provide an additional lifesaving prevention strategy.

Knowledge Management: Report/Proceedings