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CASE NOTES

HUMAN METAPNEUMOVIRUS: ZOONOSIS OR REVERSE ZOONOSIS?

Jim McDonald, District Veterinarian, Tablelands LHPA, Yass

Posted Flock & Herd March 2012

Introduction

The World Health Organisation defines zoonosis as 'an infection shared in nature by man and animals'. This is an elegant way of describing it and implies that there is no need to coin terms to define the direction of transmission. However, for the sake of clarity, most people regard 'zoonosis' as transmission from animals to man and have, conversely, recently used the term 'reverse zoonosis' for human to animal transmission.

Human metapneumovirus [hMPV] is a recently identified member of the paramyxoviridae, which also includes respiratory syncitial virus and parainfluenza virus. Although identified in 2001, data suggests this is a common virus responsible for human respiratory illness for at least 50 years, and occurring worldwide. Human MPV can cause upper and lower respiratory tract infections in human patients of all ages, especially infants and the elderly.

The origin of this virus, hMPV, will be discussed along with its potential to cause reverse zoonotic disease in some animal species.

IDENTIFICATION IN HUMANS

Human MPV is spread by direct or close contact with respiratory secretions of infected persons, such as sneezing and coughing, or by contact with objects contaminated by their secretions. Infection is common during infancy or early childhood1.

Human MPV was first reported in Nature in 2001 by a virology group from Holland2. This discovery was closely followed by detection at the Royal Children's Hospital in Brisbane3. The Dutch researchers discovered a paramyxovirus, closely related to avian metapneumovirus, in 28 children with respiratory disease. They also demonstrated by serological work on blood taken in 1958 that hMPV has been circulating for more than 50 years and that by the age of 5 years virtually all children have been exposed to the virus1.

Until the Dutch researchers discovery of hMPV, avian metapneumovirus, which causes rhinotracheitis in turkeys, was the sole member of the metapneumovirus genus.

AVIAN METAPNEUMOVIRUS

Avian MPV [aMPV] causes a respiratory infection in turkeys and chickens of all ages and is also known as turkey rhinotracheitis virus [TRT]. Subtypes A & B affect turkeys and chickens in Europe and cause a syndrome called 'swollen big head' in chickens. USA has subtype C, affecting only turkeys4.

ORIGINS OF HUMAN METAPNEUMOVIRUS

Human MPV is closely related to aMPV-C. Because of the similarities, scientists have suggested that hMPV emerged from avian viruses. MPVs have high evolutionary rates similar to influenza. Investigating the history of MPVs using genetic information available for numerous strains of hMPV and aMPV-C circulating in both human and avian populations over the last 20 years, it was calculated that the divergence between hMPV and aMPV-C, based on estimated rate of mutation, occurred approximately 269 years ago [95% likelihood range of 106-382]5,6.

HUMAN METAPNEUMOVIRUS IN TURKEY POULTS

Two week-old turkey poults were inoculated oculonasally with hMPV. These poults showed nasal discharge 4-9 days post exposure with inflammatory changes and mucous accumulation. Specific viral RNA and antigen were detected by RT PCR and immunohistochemical evaluation, respectively, in nasal turbinates of birds exposed to hMPV7. This suggests that hMPV can cause mild disease in turkeys.

HUMAN METAPNEUMOVIRUS IN MOUNTAIN GORILLAS

The world's remaining 786 mountain gorillas live in two areas in central Africa. Principally the Virunga Volcanoes Massif, which combines Volcanoes National Park in Rwanda, Mgahinga National Park in Uganda, and the Virunga National Park in Democratic Republic of Congo. The other area is in Uganda, namely Bwindi Impenetrable National Park. An ecotourism industry for viewing human-habituated mountain gorillas is thriving in the Virunga Volcanoes Massif. This tourism helps ensure the sustainability of the species by generating revenue and awareness of the precarious status of this species in the wild. Tourism also poses a risk of disease transmission from humans to gorillas. Second only to trauma, infectious diseases, primarily respiratory, account for 20% of sudden deaths.

The genetic relatedness of gorillas and humans has led to concerns about the occurrence of reverse zoonoses occurring. Human-to-gorilla transmission may explain hMPV found in 2 wild mountain gorillas that died during a respiratory disease outbreak in Rwanda in 2009.

The Hirwa gorilla group consisted of 12 animals. Moderate to severe respiratory signs developed in 11 of the 12 animals. Five received antimicrobials and recovered. Two untreated animals, 1 adult female and 1 male neonate, died. On June 30, 2009 the adult female was observed coughing and lethargic; on July 3 she left her nest but did not eat. She was found dead on July 4. The neonate was 3 days old when it died. Gross post-mortem examination revealed bronchopneumonia in the adult and unilateral pulmonary congestion and an empty stomach in the neonate. Histologically, the respiratory tract of the adult was characterised by moderate mononuclear tracheitis, laryngitis and air sacculitis; severe pulmonary alveolar histiocytosis; multifocal severe suppuratives pneumonia; pulmonary thrombosis and haemorrhage8.

Multiplex PCR analysis for respiratory pathogens indicated sequences of hMPV in serum, lung tissue, throat, nose, anus and vagina of the adult and lung tissue from the neonate. Streptococcal and Klebsiella spp were detected in lung tissue from the adult, but not the neonate. Bayesian analysis revealed close relationship of the gorilla virus to human isolates from South Africa8.

REVERSE ZOONOSIS

Experimental infections with hMPV have suggested pure infections cause minimal to mild lesions in conducting airways and macrophage accumulation in the alveoli. However, paramyxoviruses, including hMPV, can predispose animals to bacterial pneumonia as appeared to be the case with the Hirwa gorilla group. The hypothesis that hMPV can be fatal for gorillas is supported by a report of respiratory disease in wild chimpanzees at Mahale National Park, Tanzania. During the fatal respiratory outbreaks of 2003, 2005 and 2006, many chimpanzees between 2 months and 2 years and 9 months died. At least 9 were presumed dead after the 2006 outbreak. Analysis of faecal samples taken in 2006 identified the presence of hMPV in the absence of other common respiratory viruses such as measles or influenza9.

Discussion

Reverse zoonosis certainly no rarity. Human MPV has been identified in both gorillas and chimpanzees and can now be included in this category of diseases. Health screening of tourists visiting the habituated gorillas and chimps are under consideration. Minimum approach distances of 5-8 metres from gorillas are adhered to as much as possible.

Closer to home, is the July/August 2009 pandemic influenza A [H1N1] infection of pigs at a 2000 piggery at Dunedoo in the Central West of NSW. This coincided with the epidemic of a swine flu variant of human influenza in this country. This case is very likely to have been introduced to the piggery by piggery workers. The owner and staff at the piggery had previously suffered flu-like symptoms. Farm workers developed symptoms on approximately 19/07/2009 and the pigs were noticed coughing on 24/07/200910. Unfortunately confirmation that the infection had come from the farm workers was not possible11.

There are other documented cases of reverse zoonoses occurring. Human tuberculosis in elephants has occurred in both Africa and Asia12. Bovine Tb has also been transmitted to cattle by a person with renal lesions urinating on cow bedding. Mumps virus causing parotiditis in dogs; Infectious hepatitis A - hepatitis in non-human primates; Corynebacterium diptheria, Staphylococcus aureus, Streptococcus pyogenes - mastitis in cattle and Salmonella as well as influenzas are a few additional examples.

Greatly increased opportunities for diseases to jump hosts will occur in the future. This phenomenon will be driven by the expansion of the human population which will travel more freely around the globe. In addition our food products are travelling more freely between countries and the further contraction of available land that animals occupy will increase human/animal disease transmission opportunities.

The medical profession is now focusing heavily on these factors as they increase the likelihood of zoonoses occurring. These same factors increase the risk of reverse spread as well, with potential and real consequences for wildlife parks and intensive livestock enterprises.

The challenge to the veterinary profession is to identify emerging reverse zoonotic diseases quickly, in not only wildlife, but livestock and companion animals. We will also have a role in examining the epidemiology behind the host jump and assist in minimising the social and economic impacts.

Reviewing biosecurity plans for livestock enterprises, in particular only allowing essential people to enter livestock establishments and then to have access to the stock is a necessary first step. In the light of evidence that some human respiratory viruses can spread to animals, having a policy to exclude staff suffering from illness, especially respiratory complaints, needs to be strongly considered.

There is a role for all veterinarians working with livestock and servicing the livestock industries to be aware and proactively promote to farm managers the necessity for early notification of abnormal signs exhibited by livestock as well as assisting them with biosecurity plans that minimise the potential occurrences of reverse zoonoses.

Acknowledgements

The ecotourism guides from the Virunga National Park, Rwanda.

References

  1. Anthony Harndan, Human metapneumovirus, Brit J Gen Pract. 2005 Feb 1; 55[511]: 84-85
  2. Van den Hoogen BG, de Jong JC, Groen J, et al. A newly discovered human pneumovirus isolated from young children with respiratory tract disease. Nat. Med. 2001; 7:719-724
  3. Norman Swan, Metapneumovirus Broadcast Monday Feb 4, 2002 with virologist Theo Sloots and paediatrician Dr Michael Nissen
  4. Dr Jagdeev M Sharma; Merck Animal Health
  5. Miranda de Graaf, Albert DME Osterhaus, Ron AM Fouchier and Edward C Holmes; Evolutionary dynamics of human and avian metapneumovirues; J Gen Virol, 2008, 89, 2933-2942
  6. Chin-Fen Yang, Chiaoyin K Wang, Sharon J Tollefson, Rohith Piyaratna, Linda D Lintao, Maria Chu, Alexis Liem, Mary Mark, Richard R Spaete, James E Crowe and John V Williams; Genetic diversity and evolution of human metapneumovirus fusion protein over twenty years; Virol. J. 2009, 6:138
  7. Binu T Velayudhan, Kakambi V Nagaraja, Anil J Thachil, Daniel P Shaw, Gregory C Gray and David A Halvorson; Human Metapneumovirus in Turkey Poults; University of Minnesota Foundation with affiliations with Universities of Minnesota, Missouri-Columbia and Iowa USA
  8. Gustavo Palacios, Linda J Lowenstine, Michael R Cranfield, Kirsten V K Gilardi, Lucy Spelman, Magda Lukasik-Braum, Jean-Felix Kinani, Antoine Mudakikwa, Elisabeth Nyirakaragire, Ana Valeria Bussetti, Nazir Savji, Stephen Huctchison, Michael Egholm and W Ian Lipkin; Human Metapneumovirus Infection in Wild Mountain Gorillas, Rwanda. Centres for Disease Control and Prevention, Emerg Infect Dis. 2011, Vol 17, No 4
  9. Kaur, T., Singh, J., Tong, S., Humphrey, C., Clevenger, D., Tan, W., Szekely, B., Wang, Y., Li, Y., Alex Muse, E., Kiyono, M., Hanamura, S., Inoue, E., Nakamura, M., Huffman, M.A., Jiang, B. and Nishida, T. Descriptive epidemiology of fatal respiratory outbreaks and detection of a human-related metapneumovirus in wild chimpanzees [Pan troglodytes] at Mahale Mountains National Park, Western Tanzania. Am. J. Primato. 2008 70:755-765
  10. NSW DPI Biosecurity Bulletin Animals; Chief Veterinary Officer Communication; Influenza infection in piggery near Dubbo; 5 August 2009
  11. AAP NewsWire; Piggery workers not being tested for swine flu industry; 06/08/2009
  12. Arnon Shimshony, DVM; Tuberculosis in elephants: a reverse zoonosis; Infectious Disease News, Dec 2008

 

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