a Institute for Medical Research (IMR), Kuala Lumpur, Malaysia.
b Division of Viral and Rickettsial Diseases (DVRD), Centers for Disease Control and Prevention (CDC), Atlanta, GA, USA.
c Centre for Disease Control, Ministry of Health, Kuala Lumpur, Malaysia.
d Negeri Sembilan Health Department, Seremban, Negeri Sembilan, Malaysia.
e Department of Veterinary Services (DVS), Ministry of Agriculture, Kuala Lumpur, Malaysia.
f Members of the Nipah Encephalitis Outbreak Investigation Group: AB Suleiman, AS Tee (Ministry of Health, Malaysia); MA Rahman (DVS, Ministry of Agriculture, Malaysia); F Ong, OC Huck (Sarawak Health Department, Sarawak, Malaysia); D Cannon, P Stockton, L Anderson (DVRD, CDC, Atlanta, GA); WRW Mahiyuddin and ZM Noor (IMR, Kuala Lumpur, Malaysia).
Dr Lye Munn Sunn, Institute for Medical Research, Jalan Pahang, Kuala Lumpur, Malaysia. E-mail: lyems{at}imr.gov.my
Abstract
Background An outbreak of encephalitis primarily affecting pig farmers occurred during 19981999 in Malaysia and was linked to a new paramyxovirus, Nipah virus, which infected pigs, humans, dogs, and cats. Because five abattoir workers were also affected, a survey was conducted to assess the risk of Nipah infection among abattoir workers.
Methods Workers from all 143 registered abattoirs in 11 of 13 states in Malaysia were invited to participate in this cross-sectional study. Participants were interviewed to ascertain information on illness and activities performed at the abattoir. A serum sample was obtained to test for Nipah virus antibody.
Results Seven (1.6 %) of 435 abattoir workers who slaughtered pigs versus zero (0%) of 233 workers who slaughtered ruminants showed antibody to Nipah virus (P = 0.05). All antibody-positive workers were from abattoirs in the three states that reported outbreak cases among pig farmers. Workers in these three states were more likely than those in other states to have Nipah antibody (7/144 [4.86%] versus 0/291 [0%], P < 0.001) and report symptoms suggestive of Nipah disease in pigs admitted to the abattoirs (P = 0.001).
Conclusions Nipah infection was not widespread among abattoir workers in Malaysia and was linked to exposure to pigs. Since it may be difficult to identify Nipah-infected pigs capable of transmitting virus by clinical symptoms, using personal protective equipment, conducting surveillance for Nipah infection on pig farms which supply abattoirs, and avoiding handling and processing of potentially infected pigs are presently the best strategies to prevent transmission of Nipah virus in abattoirs.
Keywords Nipah virus, abattoir workers, Malaysia
Accepted 22 December 2000
Nipah virus is a new paramyxovirus that was discovered in March 1999 during the investigation of an outbreak of encephalitis in Malaysia.13 From September 1998 through May 1999, 265 encephalitis patients (105 [40%] fatal) were reported from hospitals in three states (Perak, Negeri Sembilan, and Selangor) of Malaysia. Most patients showed evidence of Nipah infection. Pigs were implicated as the primary source of human infection;4 most patients were pig farmers, an illness with respiratory and neurological symptoms was observed in pigs on some farms with human patients, and the virus isolates obtained from both human patients and sick pigs showed identical nucleotide sequences.
Nipah virus is most closely related to the Hendra virus (previously known as equine morbillivirus) that was discovered in 1994 after an outbreak of respiratory illness among horses and humans in Australia.57 Three cases of Hendra virus disease among humans have been documented to date; two of these patients have died, one of respiratory failure and the other, one year after his initial infection, of encephalitis.510 Hendra virus is believed to spread from horses to humans through direct contact with secretions and body fluids of an infected animal.11 Although most paramyxoviruses are species specific, both Hendra and Nipah viruses appear to infect a variety of mammals, including bats, cats, horses, pigs, and humans.
Most patients with Nipah encephalitis in Malaysia were pig farmers; however, a few cases were reported in people with other occupational exposure to pigs. Five cases were reported among abattoir workers who slaughtered pigs. Eleven cases of febrile encephalitis or pneumonia resulting in one death were also reported during a concurrent Nipah outbreak among abattoir workers in Singapore.12 The occurrence of these cases prompted this investigation to determine the prevalence of, and types of exposures associated with, infection among workers from 11 of 13 states in Malaysia.
Methods
Abattoirs
Abattoirs in Malaysia are of two types: Class B abattoirs and Class C abattoirs. Class B abattoirs slaughter both pigs and ruminants (cattle and goats) whereas Class C abattoirs slaughter only ruminants. In Class B abattoirs, pigs and ruminants are generally slaughtered in separate buildings and by different personnel. Animals for slaughter are brought to the abattoir on lorries during the day. After unloading, these animals are guided into holding areas where they are held until slaughter. In the evening, animals are guided into the slaughter facility where they are first rendered unconscious by electric shock. Next, they are shackled and hoisted over a blood pit, following which the great vessels of the neck are severed. After bleeding, the carcasses undergo a series of washing and cleaning procedures. Subsequently, the internal organs and the head of the animal are removed, and the carcass is split and readied for distribution to pork sellers.
Study design
Participants for this cross-sectional study were sampled from workers of all 143 registered abattoirs in Peninsular Malaysia. Workers were invited to voluntarily participate in the study after being informed of the study objectives by their respective veterinary officers. Each participant was interviewed between April 6 and April 20 1999, to ascertain information on illness, activities performed at the abattoir, use of personal protective clothing and equipment, and exposure to pigs or pig product in other setting besides the abattoir. Illness information ascertained included signs and symptoms suggestive of Nipah encephalitis, such as fever, cough, sore throat, headache, neck stiffness, rashes, lethargy, and photophobia. Because the Nipah outbreak in Malaysia began in October 1998, the questions on illness pertained to the period from October 1998 through the date of the survey in April 1999. Interviews were conducted in person by trained interviewers using each participant's preferred language. Data were entered using Epi Info, Version 6.04 and were analysed using SPSS 7.5 for Windows.
A single serum sample was drawn from all abattoir workers after obtaining their written consent at the time of the interview. Sera were tested for IgM antibodies using an IgM-capture antibody enzyme immunoassay (EIA) and for IgG antibodies by using an indirect EIA. Hendra virus antigens, which cross-react with antibodies against Nipah virus, were used in the serological assays. At the present, the sensitivity and specificity of these assays are not completely known, but preliminary data suggest that these assays may perform reasonably well in most instances.13
Results
A total of 668 abattoir workers were surveyed, including 435 workers who slaughtered pigs and 233 workers who slaughtered only ruminants (Table 1). Of the 233 workers who slaughtered only ruminants, 230 were from Class C abattoirs, while the other 3 workers as well as all the 435 workers who slaughtered pigs were from Class B abattoirs. Seven (1.6%) of the 435 workers who slaughtered pigs compared with zero (0%) of the 233 workers who slaughtered only ruminants showed antibody against Nipah virus (prevalence odds ratio (POR) = undefined, P = 0.05). All of the infected workers had IgG antibody and six of seven showed IgM antibody.
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Five of the seven Nipah antibody-positive abattoir workers reported that their work involved contact with live pigs. In abattoirs from the three affected states, the prevalence of Nipah antibody was greater among workers who reported contact with live pigs (5/53 [9.4%]) than those who did not (2/91 [2.20%]) but the difference was not statistically significant (P = 0.10). Of the two antibody-positive workers who reported no contact with live pigs, one slaughtered pigs and removed their urinary bladder (this person also worked as a pork seller) while the other packaged pork for distribution.
Of the 144 workers involved in pig slaughter in the affected states, 126 (88%) reported wearing boots, 72 (50%) reported wearing gloves, 65 (45%) reported wearing aprons, 44 (31%) reported wearing masks and 15 (10%) reported wearing goggles at all times while working. However, there were no significance differences between the seven antibody positive workers and the rest of these workers in terms of use of the personal protective equipment and clothing. Also, exposure to pigs in settings other than the abattoir was not significantly associated with infection.
Discussion
In this study, antibody to Nipah virus was detected only among workers from abattoirs located in the three states of Malaysia with reported Nipah encephalitis cases among pig farmers. This finding is consistent with surveillance data showing that infection among pig herds was also primarily confined to farms located in these states and indicates that Nipah disease was not widespread in all states of Malaysia. In abattoirs from the affected states, infection was observed only among workers who slaughtered pigs and not among those who slaughtered ruminants. This observation and the fact that workers reported symptoms in pigs consistent with those of Nipah disease more often in abattoirs from the affected states than those in other states are consistent with pigs being the most likely source of infection. The difference in ethnicity between the groups reflects the fact that Malays do not slaughter pigs because of religious restrictions.
While our data do not allow us to define the exact mode of spread of Nipah virus, the fact that five of the seven antibody-positive workers reported contact with live pigs suggests that secretions and bodily fluids other than blood might be the primary vehicles of transmission. Respiratory secretions may be a vehicle for transmission because infected pigs primarily have a respiratory disease with prominent coughing and immunohistochemical (IHC) studies have demonstrated viral antigen in, and severe inflammation of, both the lower and upper respiratory tract of infected pigs.1,2,14 Urine exposure may also be associated with transmission because Nipah virus antigen has been demonstrated by IHC staining in the renal tubules from pigs and exposure to pig urine was associated with Nipah infection during a concurrent outbreak among abattoir workers in Singapore.1,2 The finding that one infected worker reported no contact with either live pigs or pig urine suggests that other modes of transmission might be responsible for some cases.
Abattoirs in the affected states were temporarily closed after Nipah encephalitis cases were reported in abattoir workers, following which new cases stopped. Similarly, reported encephalitis cases among pig farmers in Malaysia decreased following diminished contact with pigs and the culling of more than one million pigs on farms in the outbreak-affected areas. This study indicates that all abattoir workers handling potentially infected pigs are potentially at risk for Nipah infection and avoiding contact with infected pigs is the only definitive method of eliminating the risk of Nipah infection. However, the symptoms of Nipah disease in pigs may be subtle and can be missed if not specifically sought. In this study, 47% of the workers admitting pigs to abattoirs in the affected states did not observe any signs suggestive of Nipah disease in the pigs. Since it may be difficult to identify Nipah-infected pigs capable of transmitting virus by clinical symptoms, using standard personal protective equipment (e.g. masks, goggles, gloves, boots and aprons), conducting active surveillance for Nipah infection on pig farms which supply abattoirs, and avoiding handling and processing of infected pigs are presently the best strategies to prevent transmission of Nipah virus in abattoirs.
Acknowledgments
We thank Dr Narimah Awin, Director, Institute of Medical Research, Kuala Lumpur, for permission to publish this paper. We thank staff from the state and district health, hospital, and veterinary offices and the following institutions who contributed to this investigation: Environmental Health Research Centre, Kuala Lumpur; Division of Epidemiology and Biostatistics, Institute for Medical Research, Kuala Lumpur.
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