This case report reviews experiences with Hendra Virus disease in horses on an affected property at Wollongbar in June / July 2011. It also explores flying fox movements and weather events at the suspected time of virus spillover.
At 6pm on 28th June 2011 a local private veterinarian examined a 16 year old quarter horse gelding. The horse was one of two on a 3.10ha hobby farm near Wollongbar, northern NSW. The horse was febrile; 40.8oC, had increased heart rate of 80/min and increased respiratory rate of 65/min. The mucous membranes were brick red. The horse was stumbling on the left foreleg and had a wide front leg stance. There was no nasal discharge and no cough. It had passed a small amount of firm faeces. The lower lip drooped to the left. It was diagnosed with toxaemia of unknown origin. The horse was tetracycline, penicillin, phenylbutazone, Ketoprofen and a diuretic, frusemide.
At 11am on 26th June the horse was reexamined by the same practitioner. Its cardinal signs had improved; the temperature had dropped to 38.4oC, its heart rate was 65/min and its respiration 48/min. However the neurological signs had progressed. The horse appeared to be blind, walking into walls. The lower lip was drooped and the horse had slight ataxia and stumbling. It was anorexic. The horse was treated was again treated with tetracycline, Ketoprofen and frusemide. A (dry) nasal swab, clotted blood and serum were collected and submitted to EMAI for Hendra virus exclusion.
There was a large fig tree that the horses sheltered under which was frequented by flying foxes at night. Mosquitoes were noted to be active from recent wet weather. The practitioner advised the owners to isolate the horse from its companion and to stay away from the horse until test results were known.
At 1am on the 30th June, the horse was euthanased by the private veterinarian.
On 30th June I was requested by NSWDPI to visit the property to issue disinfection procedures for the horse's disposal and to quarantine the property as a precaution, should the case be positive. This was done and a Biosirt was completed for the case. At this time the companion to the horse was isolated by a single wire away from the house and human contact and a quarantine line established. It was a 4 year old quarter horse mare and in good health.
Later that evening I was notified by DPI that the swab was negative PCR for Hendra and that the blood had given an inconclusive PCR result. I was requested to visit the property to resample the horse at autopsy and oversee the disposal of the body and disinfection.
On the morning of 1st July I collected prescapular and submandibular lymph nodes, blood and nasal swab at autopsy. Copious frothy nasal discharge was noted. I also took bloods and a nasal swab from the companion horse. Full PPE was worn as a precaution, including forced air hood, disposable overalls, gum boots and triple glove.
Just over an hour after leaving the holding I received a phone call from DPI to confirm that the PCR on the blood was indeed positive. I returned to the property to give the results to the owners. One of the owners had close contact with the horse throughout its demise, without any form of PPE. The grief at loosing the horse very quickly turned to shock at their own and the practitioner's exposure to Hendra. The other owner had assisted with the handling and disposal of the carcase, wearing PPE.
I then was sampled by NSW Health, which was repeated at day 21 and day 42, all with negative results. The owners and practitioner were likewise tested.
On 2nd July I returned to the property with Paul Freeman, Dr Hume Fields, Qld DEEDI and a DPI animal health inspector.
Public access areas such as the driveway were disinfected and further quarantine lines established. A twice daily observation schedule commenced for the companion horse. I last saw the companion on 9th July. The following day the mare developed signs of lethargy fever and ataxia. The private veterinarian examined the horse and took blood and nasal swabs. The blood was PCR positive and the nasal swab negative. The horse was euthanased on 12th July.
At the request of DPI I blood sampled the 3 dogs on the property on 6th July. All were negative for Hendra.
I was requested to prepare a report of Flying Fox acivity both on the property as a whole and in the area in general. The fruiting of the large Strangler Fig (Ficus watkinsiana) had almost finished and only small numbers of flying foxes were observed. Tarpaulins were laid under the tree to collect faeces, urine and spats. No virus was isolated. Over the course of the following week I collected weather data, collected information and made observations at local colonies with flying fox carers and researchers.
From this the following report was prepared;
EPIDEMIOLOGY REPORT ON FLYING FOX ACTIVITY
OBSERVATIONS ON THE INFECTED PREMISE
In the centre of a roundabout on the IP there is a large Strangler Fig (Ficus watkinsiana).
The owners gave a history of recent flying fox activity in the tree at night in the time leading up to the horse developing clinical signs. The tree was observed to have a small amount of fruit and evidence of flying fox feeding; part eaten fruit. The tree was observed soon after dusk with a powerful 10 million candle spot light on three evenings for Flying Fox activity. On 2nd July 2011 two flying foxes were seen; one Black Flying Fox (Pteropus alecto) and one Grey Headed Flying Fox (Pteropus poliocephalus). On 4th July four P alecto were seen. Conditions on the evening of 5th July were very windy and none were observed. The general assessment was that the amount of flying fox activity on the IP at that time was low.
SEASONAL ACTIVITY OF FLYING FOX IN THE DISTRICT
The following flying fox camps are located in the proximity of the IP; Boatharbour Reserve Bexhill; 5km, Rotary Park Rainforest Reserve Lismore; 7.5km, Lumley Park Alstonville; 8km, Currie Park, Lismore; 8.5km, Booyong Nature Reserve Booyong; 10km, Ballina Nature Reserve Ballina; 19km and Tuckean Nature Reserve Bagotville 21km.
The Lismore and Alstonville colonies were the most likely source of the flying fox on the IP. Numbers were well down at both colonies, which is typical of the winter months when they move to the coast to feed. An approximately equal proportion of Black and Grey Headed were observed at both colonies.
LONG TERM TRENDS AND ECOLOGY
There are 3 Flying Fox species that can be found in northern NSW. Black Flying Fox (Pteropus alecto), Grey Headed Flying Fox (Pteropus poliocephalus) and the Little Red Flying Fox (Pteropus scapulatus). The seasonal migration pattern of all species is largely dictated by the flowering of fodder trees, in particular Eucalypts, but also Banksias and Callistemons.
Along the east coast P.alecto is steadily moving south and P. poliocephalus numbers are decreasing. P. alecto first entered the Lismore area in 1992. Since that time the numbers of P alecto have steadily increased and the numbers of P poliocephalus have steadily decreased, so that the two species are now in similar numbers on the north coast. P. alecto is steadily moving south each year at a rate that is greater than can be accounted for by climate change; about 1,000km /decade compared with 10-20km latitude shift in the isotherm/decade. The cause of this pattern and the decline of P. poliocephalus (this species is now listed as endangered) is the subject of debate amongst researchers. Both share a similar ecological niche and food sources; both species are nectivores and frugivores. However P. alecto is a more dominant species. Is this long term southward trend of P. alecto related to the apparent southward trend of Hendra cases?
Each year the local Lismore colonies are down in numbers during the winter months, with flying fox moving to the coast for warmer conditions and to feed on Banksia and Melaleuca. Generally most P. alecto move toward the coast; Wardell and Ballina, then north during July, they then return in spring to birth. But each year more P. alecto overwinter in the local area. P. poliocephalus being better cold adapted tend to remain or even move south depending on feed. Both species birth from October to December. However small numbers of P. alecto can be born throughout the year.
The demise of coastal heathlands in southern Queensland and northern NSW to human development in recent decades has reduced the feed source of the two species in the winter months, a critical time of year for flying fox food supply. Is this food shortage a trigger for Hendra virus shedding?
In contrast P. scapulatus is a highly migratory species that is an obligate nectavore. Their movement from camp to camp on the north coast is predictable each year and coincides with Spotted Gum (Corymbia henryi) flowering. In the Richmond 40,000 to 50,000 arrive at Casino in the last week of January each year for about a 2 week period. This is part of their migration north, which initially takes them east from Bonalbo to Casino, then to Evans Head, then north. Some half a million congregate at Gladstone in Queensland to birth each May. Their role in Hendra transmission on the north coast is therefore doubted.
CURRENT SEAONAL TRENDS
The body condition of flying fox locally in the winter of 2011 was good, due to favourable seasonal conditions. In 2010 due to food shortage, there more small short term "splinter" colonies camping at infrequenly used sites. This pattern reflects the general mass food shortages and widespread and prolonged starvation events experienced in southern Queensland and coastal NSW during 2010. This was one of the worst years on record for flying fox starvation events, and followed the break in the drought with Eucalypts putting energy into growth rather than flowering.
WEATHER EVENTS AT THE SUSPECTED TIME OF SPILLOVER FROM FLYING FOXES TO THE INDEX CASE
Flying fox activity on the IP was low at the time of inspection and both species were present. Numbers were higher on the IP two weeks before during a period of cool wet weather. Hendra virus has an incubation period in horses of 4 to 16 days. The first onset of clinical signs was on Tuesday 28th June 2011. Therefore the suspected dates of exposure of the gelding to the virus are 12th to 24th June.
The virus is known to be sensitive to extremes of temperature and to moisture. Transmission from flying fox to horses could therefore be potentially at it greatest during mild, wet or humid weather. Some carers believe that during wet weather flying fox are more frugivorous rather than nectarivorous, as nectar is washed from blossom during wet weather. This accompanied by more fruit on the fig tree could account for higher Flying fox numbers observed by the owners on the IP during wet weather 10 - 14 days before the gelding fell sick.
The horses were stabled during the day of heaviest rain; 13th June and depastured for the remainder of June. In the days that followed this rain event were mild with high relative humidity and overcast; favourable for virus survival.
14th June; mild temperatures (11.9 to 20), showers (19.6), low evaporation (0), moderately high relative humidity (77%), little sun (4.4) and wind to 11 km hour.
15th June; mild temperatures (10.1 to 17.8), little rain (0.4), low evaporation (1.2), moderately high relative humidity (78%), reduced sun (7.4) and wind to 6 km hour.
16th June; mild temperatures (9.9 to 18.2), low evaporation (1.4), moderately high relative humidity (78%), little sun (4.4) and wind to 17 km hour.
17th June; mild temperatures (10 to 20), low evaporation (1.2), moderate relative humidity (68%), sunny and wind to 13 km hour.
Following this time relative humidity was lower and the days sunny to the end of the possible incubation period on the 24th June. The 24th June had cooler temperatures (8.6 to 15), no rain (0), low evaporation (2.6), moderate relative humidity (68%), little sun (1.2) and wind up to 6 km hour.
14th,, 15th, 16th, 17th and 24th June are within the incubation period, had conditions more suited to virus survival may have been the time when the virus was transmitted from flying fox to the affected horse.