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Human metapneumovirus infections in chimpanzees and their keeper in Ljubljana Zoo

I Grmek Kosnik1, N Lalek2,  P Kvapil3 , M Kastelic3,  M Petrovec4

Institute of Public Health Kranj, Slovenia 
University Clinic for Respiratory Diseases and Allergy Golnik, Slovenia 
Zoo Ljubljana, Slovenia
4.   Institute of Microbiology and Imunology, Slovenia

Abstract
A case of human metapneumovirus (hMPV) infection spread from human to chimpanzee and back is described. Four out of 6 members of chimpanzee family developed bronchopneumonia and latter two died. hMPV and Klebsiella spp were isolated. Two days later the chimpanzee's keeper got ill with hMPV detected in nasopharingeal swab. We assume that chimpanzees got infected from an infected visitor as there is only a narrow space (1.3 m) between visitors and the inner fence. The keeper most likely got infected by aerosols or body fluids from chimpanzees, since he had daily close contacts with them.


Chimpanzees are a big attraction for children in zoological parks (Zoos). In Ljubljana, Slovenia Zoo, chimpanzee family consisted of 6 members. In 2013 chimpanzees were let in the outdoor cage only in the middle of June, since the weather was to cold in May and beginning of June.�At that time the number of the visits increased to over 2000 per day , while a lot of schools and kindergartens were having end of the school year trip there. 

On June 19th four of the youngest chimpanzees (10 to 15 years old) started to show signs of a cold with snorting. Veterinarians suspected a viral infection but because of the possibility of secondary bacterial infection they started to treat chimpanzees with amoxicillin/clavulanic acid. The next day, clinical signs of pneumonia or pleural effusion appeared. The youngest chimpanzee died of respiratory failure on June 22rd. Autopsy revealed acute bronchopneumonia. Human metapneumovirus (hMPV) and Klebsiella spp were isolated from tissue. In the same day health condition of all the other chimpanzees deteriorated. Second youngest chimpanzee with symptoms of acute respiratory distress was sedated, ventilated and treated with infusions, bronchodilators and intravenous antibiotics, however he died on June 24th due to bronchopneumonia. In remaining two chimpanzees clinical signs and symptoms gradually vaned in 6 days.

Chimpanzee's keeper was a 31 year old male, nonsmoker, with known history of persistent allergic rhinoconjunctivitis and childhood asthma. He reported signs of a cold on the morning of June 21st. In the next 2 days his symptoms worsened with body temperature 37.5�C, sore throat, chills, muscle and joint pain, headache and dry cough. He visited the emergency department on Sunday June 23rd. Next day nasopharyngeal and throat swab for pathogenic bacteria and respiratory viruses were taken and hMPV  was confirmed in the nasopharingeal swab sample by PCR later in the same day,. On the June 24th his general practitioner, unaware of the positive virology report, prescribed him amoxicillin/ clavulanic acid. After two days of treatment with antibiotic diarrhea developed, and amoxicillin/clavulanic acid was replaced with azithromycin 500 mg . However, on July 1st the patient was referred to University Clinic for Respiratory Diseases and Allergy Golnik because of chest tightness and whizzing. On examination, his clinical status revealed inspiratory and expiratory wheezing and also crepitations. His laboratory findings were normal except for high leukocyte count (12*109/L) and liver alanine transaminase (0.76 �kat/L). Chest roentgenogram was normal. As hMPV is one of the more frequent etiologic agents associated with bronchiolitis, high resolution computed tomography was performed which excluded that diagnosis, but revealed mucus plugs in the bronchi for posterobasal segments of the right lung with segmental air trapping. Pulmonary function testing showed normal spirometry and highly elevated diffusing capacity for CO (132 % predicted). Patient had elevated sputum eosinophil count. He was treated with methylprednisolone 32 mg per day and salbutamol 4 puffs on regular intervals. Crepitation and chess tightness eventually subsided and the patient was discharged on the July 4th with recommendation to continue treatment for asthma with inhaled fluticasone propionate 500 mcg 2 times daily and salbutamol on demand until check up. 

This case is interesting because of the way the infection spread. We assume that chimpanzees got infected from an infected child in one of the visiting groups. Infection could have been spread by airborne route. There is a narrow space between visitors and the inner fence with minimal distance only 1.3 meters in Ljubljana Zoo. Respiratory disease is the most important cause of morbidity and mortality among wild great apes habituated to human presence, for research or tourism, and thus presents major conservation concerns. Transmission of hMPV from human to monkey has already been described (1). Frequent contact between humans and wild primates increase the likelihood of pathogen exchange between human and nonhuman primates (2). Anthropozoonotic transmission of the paramyxoviruses respiratory syncytial virus (HRSV) and human metapneumovirus (HMPV) from humans to wild chimpanzees resulting in several respiratory disease outbreaks has been shown in the Tai National Park, Cote d�Ivoire and in Mahale, Tanzania (3,4). 
Another possibility is that the monkeys got sick by infected food. It is not uncommon that visitors throw food like candies that falls on the cages floor to animals. We were not able to identify a source of infection among the monkeys. The keeper most likely got infected by aerosols or body fluids from chimpanzees, since he had daily close contacts with them. The keeper did not have own children and he did not have close contact with children that time.

Human metapneumovirus (hMPV) is common respiratory pathogens in humans causing lower respiratory tract disease in both the very young and the frail elderly, first isolated in 2001. hMPV has a seasonal variation. In temperate climates it circulates in late winter to early spring (5,6). 
In young children, symptoms range from mild upper respiratory tract infections to severe lower respiratory tract infections (eg. bronchiolitis, croup, and pneumonia). In adults, hMPV infection typicaly presents with colds and flulike clinical manifestations (7). The elderly, the imunocompromised patients and patients with cardiac or pulmonary impairment are particularly at risk (8). HMPV is associated with severe infection in patient with pulmonary disease and chronic obstructive pulmonary disease. Studies on hMPV in BALB/c in mice and cotton rats show airway obstruction and hyperresponsiveness after infection. Initially hMPV infection in the lung is characterized by interstitial inflammation with alveolitis starting on day 3 with a peak on day 5 and subsequently decreasing inflammation (9). 
HMPV is thought to be transmitted by direct or close contact with contaminated secretions whereRNA is found five days to two weeks after the beginning of the symptoms (10-12). Based on two single cases of nosocomial hMPV infections the incubation period of hMPV is estimated to be 4 to 6 days (8). 

Viral RNA hMPV could be find in feces chimpanzees as soon as 3-4 days after the first symptoms , and was detectable until day 26 (2). Excretion via feces presents a possible route of transmission, however, epidemiologically, this will be a minor factor since chimpanzees live in close social contact and transmission via smear infection or aerosols is more likely (2,13).
Virus culture is relatively difficult, because hMPV grows slowly in conventional cell culture and has mild cytopathic effects. Detection of viral RNA by NAAT such as reverse transcriptase-PCR (RT-PCR) assay is the most sensitive method for diagnosis of hMPV infection (14). The diagnosis of hMPV infection can be made also by detection of viral RNA, antigen detection or the detection of rising antibody titers.

Ape family is our closest relatives and are therefore susceptible to a large number of human pathogens. There have been several cases of transmission of human disease to gorillas and chimpanzees in zoos that are well documented but have never been published (4). In �Ljubljana's�Zoo chimpanzees are raised since year 1974, and they never had a case of such a severe or even fatal case of viral respiratory infection. �In both cases of dead chimpanzees infection with hMPV and superinfection with bacteria was confirmed. However, we were unable to find any report in the literature of the transmission of hMPV from chimpanzees to human. 

References

Van den Hoogen BG, Herfst S, de Graaf M, Sprong L, van Lavieren R, van Amerongen G, Yuksel S, Fouchier RA, Osterhaus AD, de Swart RL. Experimental infection of macaques with human metapneumovirus induces transient protective immunity. J Gen Virol 2007; 88:1251-9.

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