Zoo Prion Disease: review of scientific literature
Database of 82 zoo animals with prion disease
Switcheroo -- mysteries at the MAFF home page
More cheetah TSE 9 years after 'ban'
The case of the missing pumas, tigers, ocelots, and lion
How many house cats really had TSE?
The Bristol Zoo tigers: 1970-77
Horizontal transmission demonstrated in kudu
Eland, nyala, bison, ankole, arabianory, and scimitar-horned oryx
Related References

Zoo Prion Disease: Review of Scientific Literature

"What is man without the beasts?
If the beasts were gone, men would die from a great loneliness of spirit.
For what happens to the beast soon happens to man.
All things are connected."

... attributed to Chief Seattle (Suquamish tribe) 1864.

Below, the entire scientific literature of 46 papers on zoo TSE, many obscure and expensive to obtain, are summarized from full text. The overall picture that emerges is appalling -- the British zoo cover-up has not only affected animals in their own zoos but also other zoos worldwide through the sale of contaminated speciality chows and through export and exchange of rare and endangered species involved in conservation programs.

All the zoos involved are named by name here (unlike in the journal articles). Why protect a zoo that feeds cheetahs split spinal cords from cattle throughout the BSE epidemic? (Better to have tossed them the zoo veterinarian.) Names are important for zoos which would not want to export their healthy animals to these facilities or import possibly preclinical animals for their own endangered species breeding programs or release into wild populations. Medical scientists doing unrelated research want to know if animals in their programs are already incubating prion disease.

Ravensden, Marwell, Chester, Port Lympne, London, Whipsnade, Woburn, and Edinburgh are 8 known BSE affected British zoos. Woburn Safari Park apparently killed the lion by feeding it split cattle spinal cords and skulls.

Zoos not mentioned here could be just as bad or worse; in fact, it is the better zoos that acknowledge their problems (though no zoo yet has really come clean on preclinical animals) and some zoos were simply innocent recipients or donors. In CWD, these are called trace-forward and trace-back facilities.

The issues here are mainly how much penetrance of BSE has there been in preclinical animals, what are the various incubation times relative to life span, and how transmissible (maternally and laterally) is zoo BSE on a species-by-species basis. If your lion enclosure is thoroughly contaminated (like the deer and elk enclosures in Colorado), what do you put in there, fresh endangered asiatic lions caught in the wild? How do you demonstrate that your lion enclosure is not contaminated?

The main dirty trick used by zoos is not to perform the fast and affordable prion IHC (immunohistochemistry ) test on animals that die for whatever reason. It is these animals, not the rare clinical ones, that are the clue to how contaminated that zoo is and how efficiently prion disease is spreading laterally to animals never exposed to BSE per se. Don't ask your local zoo how much TSE it has had, ask rather how many negative IHCs. Zoos with no IHC data need to be placed under immediate quarantine until their incompetent management can be replaced.

The ugly side of zoo BSE is that thousands upon thousands of rare animals have already been exported or loaned to foreign zoos all over the world to maintain genetic diversity (which is already very constrained even before quarantining Britain and France zoos). In those animals in which horizontal transmission is efficient, these conservation programs are ruined.

Uglier still are reintroductions of endangered species into the wild. Here, the last remaining healthy stocks could be infected by horizonatal transmission, as with prion disease in deer and elk and sheep. With zoo animals, BSE, and nvCJD, MAFF is still playing out the 'dead end host' theory, discredited by CWD researchers long before they even began.

Ugliest of all is Britain's refusal to conduct immunohistochemistry on fallen zoo animals to determine the extent of the problem. The CVOs have been fighting this since 1986; it continues to April, 1999. Too expensive? Simply send the frozen samples abroad in triplicate to willing researchers. The medulla oblongata can be removed in 5 minutes or less as is done in CWD and placed in an ice bucket.

All this and worse for the sake of cattle exports which never amounted to an internet startup company in someone's basement.

Prions in primates and other zoo animals

22 April 1999. Contact webmaster with additions or corrections. fax 541-484-0669 US

Four important papers by Noelle Bons and coworkers concerning TSE in primates are summarized on a separate page. The table below summarizes results in the 1999 PNAS paper. Penetrance of the disease is very high and many animals did not yet display symptoms . This paper was the first (and only one) to look at non-symptomatic zoo animals for prion infection (shown below in red). In the TSE column of the table, '+' signs indicate confirmed, 'p' indicates suspicious/probable, '-' means CNS study negative for TSE.(shown as brown), 'pc' means positive diagnosis in preclinical animal.

PNAS 96:4046-4051 199 30 Mar 1999 full text
see comment PNAS 96[9] 4738-4739, April 27, 1999 by Will and Ironside
C R Acad Sci III 1997 Dec;320(12):971-9 N Bons et al.
C R Acad Sci III 1996 Aug;319(8):733-6
Lancet Volume 348, Number 9019  6 July 1996
The 82 zoo animals with BSE:

Id   TSE  Genus     Species  Subsp       Birth  Origin          Death Place of Death
654  x  Microcebus  murinus  -            1997  U.Montpellier   1998  U.Montpellier
656  x  Microcebus  murinus  -            1997  U.Montpellier   1998  U.Montpellier
481  +  Eulemur     fulvus  mayottensis   1974  Madagascar      1992  Montpellier zoo
474  +  Eulemur     fulvus  mayottensis   1974  Madagascar      1990  Montpellier zoo
584  -  Eulemur     fulvus  mayottensis   1984  Montpellier     1991  Montpellier zoo
455  +  Eulemur     fulvus  mayottensis   1983  Montpellier     1989  Montpellier zoo
 -   +  Eulemur     fulvus  mayottensis   1988  Montpellier     1992  Montpellier zoo
 -   +  Eulemur     fulvus  mayottensis   1995  Montpellier     1996  Montpellier zoo
 -   +  Eulemur     fulvus  albifrons     1988  Paris           1992  Montpellier zoo
 -   +  Eulemur     fulvus  albifrons     1988  Paris           1990  Montpellier zoo
 -   +  Eulemur     fulvus  albifrons     1988  Paris           1992  Montpellier zoo
456  +  Eulemur     fulvus  albifrons     1988  Paris           1990  Montpellier zoo
586  +  Eulemur     mongoz  -             1979  Madagascar      1998  Montpellier zoo
 -   p  Eulemur     mongoz  -             1989  Mulhouse        1991  Montpellier zoo
 -   p  Eulemur     mongoz  -             1989  Mulhouse        1990  Montpellier zoo
 -   p  Eulemur     macaco  -             1986  Montpellier     1996  Montpellier zoo
 -   p  Lemur       catta   -             1976  Montpellier     1994  Montpellier zoo
 -   p  Varecia     variegata variegata   1985  Mulhouse        1990  Montpellier zoo
 -   p  Varecia     variegata variegata   1993  xxx             1994  Montpellier zoo
455  +  Macaca      mulatta  -            1986  Ravensden UK    1992  Montpellier zoo
 -   p  Macaca      mulatta  -            1986  Ravensden UK    1993  Montpellier zoo
 -   p  Macaca      mulatta  -            1988  Ravensden UK    1991  Montpellier zoo
 -   p  Saimiri     sciureus -            1987  Frejus France   1990  Frejus zoo
700  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
701  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
702  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
703  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
704  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
705  pc eulemur     hybrid   -               -  Besancon zoo    1998  Besancon zoo
706  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
707  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
708  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
709  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
710  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
711  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
712  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
713  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
714  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
715  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
716  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
717  pc eulemur     hybrid   -               -  Strasbourg zoo  1998  Strasbourg zoo
 x   p  genus       species  -               -  Lille zoo       1996  Lille zoo
 y   p  genus       species  -               -  Lille zoo       1996  Lille zoo
 z   p  genus       species  -               -  Lille zoo       1996  Lille zoo


1    +  Actinonyx   jubatus  cheetah      1986  Marwell zoo     1991  Pearle Coast AU
Duke +  Actinonyx   jubatus  cheetah      1984  Marwell zoo     1992  Colchester zoo? UK
Saki +  Actinonyx   jubatus  cheetah      1986  Marwell zoo     1993  unknown UK
Mich +  Actinonyx   jubatus  cheetah      1986  Whipsnade       1993  Whipsnade UK
Fr1  +  Actinonyx   jubatus  cheetah      1987  Whipsnade       1997  Safari de Peaugres FR
Fr2  +  Actinonyx   jubatus  cheetah      1991  Marwell zoo     1997  Safari de Peaugres Fr
xx   +  Actinonyx   jubatus  cheetah      19xx  xxx zoo         199x  Fota zoo IR
yy   +  Actinonyx   jubatus  cheetah      19xx  yyy zoo         1996+ yyyy zoo UK
zz   +  Actinonyx   jubatus  cheetah      19xx  zzz zoo         1996+ yyyy zoo UK

aaa  +  Felis       concolor puma         1986  Chester zoo     1991  Chester zoo UK
yy   +  Felis       concolor puma         1980  yyy zoo         1995  yyyy zoo UK
zz   +  Felis       concolor puma         1978  zzz zoo         1995  zzzz zoo UK

xxx  +  Felis       pardalis ocelot       1987  xxx             1994  Chester zoo UK
zzz  +  Felis       pardalis ocelot       1980  zzz             1995  zzzz zoo UK

85   +  Felis       catus    cat          1990+ various         1999+ various UK LI NO 
19   +  Canis       familia. dog          1992+ various         1999+ various UK 

Fota +  Panthera    tigris   tiger        1981  xxx zoo         1995  xxxx zoo UK
yy   +  Panthera    tigris   tiger        1983  yyy zoo         1998  yyyy zoo UK

Lump +  Panthera    leo      lion         1986  Woburn SP       1998  Edinburgh zoo UK [since 1994]

1    +  Taurotragus oryx     eland        1987  Port Lympne     1989  Port Lympne zoo UK
Moll +  Taurotragus oryx     eland        1989  xx UK           1991  not Port Lympne UK
Nedd +  Taurotragus oryx     eland        1989  xx UK           1991  not Port Lympne UK
Elec +  Taurotragus oryx     eland        1990  xx UK           1992  not Port Lympne Uk
Daph p  Taurotragus oryx     eland        1988  xx UK           1990  not Port Lympne UK
zzz  +  Taurotragus oryx     eland        1991  zz UK           1994  zzz UK 
yyy  +  Taurotragus oryx     eland        1993  yy UK           1995  yyy UK 


Fran p  Tragelaphus strepsi. kudu         1985  London zoo      1987  London zoo UK
Lind +  Tragelaphus strepsi. kudu         1987  London zoo      1989  London zoo UK
Karl +  Tragelaphus strepsi. kudu         1988  London zoo      1990  London zoo UK
Kaz  +  Tragelaphus strepsi. kudu         1988  London zoo      1991  London zoo UK
Bamb pc Tragelaphus strepsi. kudu         1988  London zoo      1991  London zoo UK
Step -  Tragelaphus strepsi. kudu         1984  London zoo      1991  London zoo UK
346  pc Tragelaphus strepsi. kudu         1990  London zoo      1992  London zoo UK
324  +  Tragelaphus strepsi. kudu         1989  Marwell zoo     1992  London zoo UK

xxx  +  Tragelaphus angasi   nyala        1983  Marwell zoo     1986  Marwell zoo UK

yy   +  Oryx        gazella  gemsbok      1983  Marwell zoo     1986  Marwell zoo UK
zz   +  Oryx        gazella  gemsbok      1994+ zzz zoo         1996+ zzzz zoo UK

xx   +  Oryx        dammah   scim oryx    1990  xxxx zoo        1993  Chester zoo UK

yy   +  Oryx        leucoryx arab oryx    1986  Zurich zoo      1991  London zoo UK

yy   +  Bos         taurus   ankole cow   1987 yyy zoo          1995  yyyy zoo UK
zz   +  Bos         taurus   ankole cow   1986 zzz zoo          1991  zzzz zoo UK

xx   +  Bison       bison    Eu bison     1989 xxx zoo          1996  xxxx zoo UK



Switcheroo -- MAFF web site mysteries

19 Apr 99 webmaster correspondence with MAFF "help" desk
The MAFF staff actually responds helpfully to substantative question about material on their Web site though delays occur. The webmaster wrote MAFFon 16 April 1999 thanking them for their 15 Apr 99 update on animals that have succumbed to confirmed TSE and asking for dates of death on unpublished cases in tigers, ocelots, pumas, and bison that are listed on their site. These animals died some years back but nothing has ever appeared. On 17 Apr 99, the webmaster wrote again about something very puzzling: an allusion to cheetahs on line 15 and 29 whereas no such line numbers existed on the web page.

Evidently they were holding back a line-by-line database of animals that would be very useful to scientists and conservationists around the world.. Very ominiouly, the cheetah lines went up to 29 whereas they showed "only" 5 British cheetahs (at Marwell and Whipsnade) plus 4 exported cheetahs [not furnished but Fota, Pearle Coast, and Safari de Peugres x 2]. There is nothing special about cheetahs and BSE other than they have a shorter incubation time than some of the other felids.

These cheetahs are reported elsewhere to have been fed cattle delicacies such as split spinal cords, whole necks, whole skulls, and split skulls from which the knacker had "removed" CNS material, as late as 1993. No cheetah has ever been autopsied that did not display clinical signs of TSE; 11 cheetahs died at Marwell alone in the mid-90's but apparently were incinerated without autopsy or freezing samples despite the zoo's track record.

The response to my polite inquiry: none. Well, actually there was a response: the MAFF webmaster quietly deleted any mention of the database. The switheroo occured on Mon, Apr 19, 1999 10:59 AM GMT according to Netscape 'document info', taking the site back to an earlier version of the document not mentioning line 15 and 29 and deleting the name of Marwell Zoo (the cheetah BSE factory).

However, I had saved the original page to disk. Here is what the deleted top secret MAFF page actually said:

"Not included above are two cheetahs at zoos in Australia and the Republic of Ireland. Both were apparently litter mates and exported from Marwell zoo, where the cheetahs on lines 15 and 29 were born. Two cases in cheetahs were also confirmed in France, one in January 1997, in an animal born at Whipsnade zoo in 1989. Details are awaited for the second case, but it is reported to have been born in Britain*."

*Why don't they just ring up the French team and find out -- they published the abstract 8 months ago in August of 1998. They gave a presentation at the Chester Zoo published in the Proceedings of the EAZWV on May 24-24, 1998.

MAFF came through (somewhat) on 13 May 1999. Though the names of the zoos could not be supplied and the cheetah line 29 business could not be explained, birth and death dates of zoo BSE animals supplement the published record.

SpeciesBornOnset/Died
Ocelot May 1987 Mar 1994
Ocelot Jul 1980 Oct 1995
Puma 1986 May 1991
Puma 1980 May 1995
Puma 1978 May 1995
Lion Nov 1986 Dec 1998
Tiger 1981 Dec 1995
Tiger Feb 1983 Oct 1998
Ankole 1987 May 1995
Ankole 1986 Feb 1991
Bison 1989/90 Oct 1996

Maff data on 15 May 99
kudu6
gemsbok1
nyala1
oryx2
eland6
cheetah9
puma3
tiger2
ocelot2
bison1
ankole2
lion1

Ankoles and bison are basically cows so no real surprise here; it would have been nice had it been determined whether the prion genes were from 5- or 6- or 7- repeat animals. Ocelot, tiger, lion, and puma prion sequences have unfortunately not been determined.

Pumas are of special interest because of CWD, the theory being that cougars in NE Colorado have been eating a steady diet of mad deer and mad elk. However, UK data on susceptibility to BSE does not provide any specific information on the issue of how long the incubation period might be for oral CWD transmission. Woverines would be another rare species at extreme risk given their dietary practises. Lynx do not eat carrion. There has never been a surveillance programs for animals shot or trapped.

The cheetah epidemic: how many are incubating disease?

20 April 1999. Contact webmaster with additions or corrections. fax 541-484-0669 US

Second French cheetah with TSE

23 August 1998 Iceland TSE Sympostium, Abstract P56
JY Madec, A Pencsik, P Belli, C Vitaud, and Th. Baron
Centre Nation d'Etudes Veterinaaires et Alimentaire, Lyons,France. JYM: tel +33 4 78 72 65 43 fax +33 4 78 61 91 45›
 
"A female cheetah (Actinonyx jubatus) born at Marwell Animal Park in Great Britain in April 1991 and exported to France at 2 years of age was diagnosed in our laboratory with a spongiform encephalopathy in July 1997. This is the second case of TSE in a cheetah imported from GB to France that occured in the same zoologicial park as the first one [Baron et al, Vet Rec 141:270-271 1997]."

As Vitaud works at the Safari de Peaugres at Peaugres, France, this facility probably received this sick cheetah as well as the earlier one from Whipsnade. Note this animal was born well after the Sept 1990 ban so either demonstrates horizontal/maternal transmission or that the ban was flouted by the zoo, or that spinal cord or offal from cattle under 6 months was still infections.

No publication has appeared although 8 months have elapsed since the result was reported at the meeting. The zoo supplying the cheetah has not been released. At the Inquiry, Kirkwood cited this document [on order] which may imply 4 French cases in total:

Clinical observations on four cases of feline spongiform encephalopathy in cheetahs (Acinonyx jubatus).

Proceedings of the European Association of Zoo and Wildlife Veterinarians, Chester, UK, 21st-24th May 1998. Pp 133-138
Vitaud, C., Flach, E.J., Thornton, S.M. & Capello, R. (1998) 
[Document on order]

Spongiform encephalopathy in an imported cheetah in France.

Vet Rec 1997 Sep 13;141(11):270-1
Baron-T, Belli-P Madec-J-Y Moutou-F Vitaud-C Savey-M
CNEVA-Lyon, Laboratoire de Pathologie Bovine, France. 
A male cheetah born at Whipsnade Wild Animal Park in Britain in Sept 1987 was exported to Safari de Peaugres, France in April 1993. Disease onset (hindlimb ataxia) began in early Dec 1996; the animal was euthanized on 20 Jan 97 Immunochemistry with 3F4 confirmed the diagnosis. Thus the onset was at 111 months, the duration was 7 weeks, and the incubation period 3-9 years. This is longer than the other 4 cheetah cases which ranged from 55-91 months for onset.

This cheetah had the same father as a female cheetah (Michelle) that was born at Whipsnade in May 1986, lived all her life there, and died with FSE in Dec 93 (at the animal hospital at Regent's Park). While at Whipsnade, both cheetahs were fed "cuts of meat and bone meal from carcasses of cattle and horses unfit for human consumption, which never included heads, but nevertheless contained sagitally split necks and lumbar regious of cattle." This practise was theoretically banned in Sept 1990 in the UK for cattle over the age of 6 months. The cheetahs were also fed ten species culled deer and antelope zoo species at Whipsnade [see Kirkwood 1995 below], none of them tested for TSE. In France, the cheetah was fed chicken and beef chops fit for human consumption.

In Sep 97 (French publication date), 3 pumas and 1 ocelot had died of TSE. On 24 Sep 94 (submission date), 1 puma and no ocelot cases were known to Kirkwood and Cunningham. This suggests 2 additional pumas and the first ocelot died in a Sept 94- June 97 window and that the second ocelot died in a June 1997-Apr 1999 window (which can be narrowed further by looking at earlier screen captures on this site of the MAFF exotic TSE statistics page). Thus 1 ocelot case was known by 8 July 1996. S. Dealler reports that the Chester Zoo directly confirmed to him one of the ocelot deaths.

SE in in another captive cheetah: Evidence for variation in susceptibility or incubation period between species?

J Zoo Wildlife Medicine 26: 577 1995 (membership-only journal not abstracted by Medline until Mar 1997
American Association of Zoo Veterinarians; no abstracts or even titles prior to vol 29 online.
Kirkwood JK, Cunninghanm AA, Flach EJ, Thornton SM, Wells GAH
This important article was submitted on 24 Sep 94. No tiger, lion, or ocelot TSE case was known to these authors and only 1 puma. This report describes the 4th of 8 cheetahs known at that time. Thus 1 of 2 tigers, 2 more pumas, and 1 ocelot died of TSE before the Sept 97 French cheetah case but still have not been published 3 years later.

This article seeks to mask identities of zoos other than Whipsnade. "Zoo 2" is easily identified via the French paper and Maff as Marwell. Extensive trafficking in cheetahs among zoos is revealed: nearly all the 19 cheetahs shown in Figure 1 had spent time in 2-3 zoos. 11 of the cheetahs ended up an unknown number of unidentified zoos domestic and foreign. Only 5 of the 19 cheetahs were still alive in Sep 94; 4 had confirmed TSE, and 11 were incinerated without neurological testing or sample retention.

This was a lost opportunity for determining the proportion of cheetahs with TSE in progress, greatly exacerbating the risks to zoos receiving these cheetahs of horizontal transmission, even placing worldwide cheetah conservation in some jeopardy. Note that while the exposure and ascertainment expertise resided in Britain, 4 of 8 cheetahs with TSE were confirmed by foreign zoos. This suggests England has sharply unreported its incidence in cheetahs.

A cheetah named Michelle is the subject of this article: born May 1986 and raised at Whipsnade, dying there of TSE on 22 Dec 93 at 91 months of age. The mother, Misty, was born in the Pretoria Zoo in 1978 and arrived at Whipsnade in 1983, dying in Jul 1987 of "interstial nephritis" and was incinerated without neuroautopsy or sample retention. The father was born in 1977 at Howletts Soo in Kent and moved to Whipsnade in 1978, dying in 1988 of "gastric ulcers" but was incinerated without neuroautopsy or sample retention.

Two siblings of Michelle were still alive at unknown British zoos in Sept 1993, one sibling had died of "renal failure" but was incinerated without neuroautopsy or sample retention. One sibling was lost track of in Dec 1988. Three siblings were put in unnamed British zoos in Mar 1987, the fourth in Sept 1987. The current status of these extremely high-risk animals (and their new cagemates and offspring) is unknown.

An unnamed cheetah on line 1, born 16 June 86 at Marwell, exported to the Pearle Coast Zoo [deleted from article] in Broome, Australia on 9 May 89 along with 2 littermates, dying in late Dec 91 at age 66 months after 4 weeks of symptoms of TSE as described by Perth veterinarians. The littermates were euthanized in Aug 92. After diagnosis, all 3 animals were exhumed and incinerated. No CNS study was performed on the littermates. CVL confirmed the diagnosis, finding prion fibrils.

A cheetah named Duke, born at Marwell on 3 Sept 84 spent 6 weeks at Whipsnade (for breeding?) but was exported from there to an unnamed zoo (not back to Marwell) where it died of TSE on 27 Oct 92, according to Peter Bircher [also associated with Marwell in nyala and gemsbok] and John C Lewis of the International Zoo Veterinary Group, West Yorkshire (fax 44 1535 690433), suggesting a British zoo, possibly Colchester Zoo. From Aug 1986 to Dec 1991, Duke had been fed cattle form a knacker's yard but not heads or backbone and occasional whole stillborn calves and soay sheep. A littermate of Duke accompanied him to the same zoo on 17 Aug 86 (after 15 months at Whipsnade) dying in May 1993 without CNS autopsy. Duke's other 3 littermates died at Whipsnade without CNS investigation.

A cheetah named Saki, born 23 Feb 86 at Marwell, spent five months from 18 Sept 90 apparently at Whipsnade, and then was transfered on 22 Feb 91 to a third zoo (with an association to Sean Mckeow), dying on 4 May 93 of TSE some 26 months after arrival. The cheetah death at Fota, Ireland has insufficient released data to associate it with either Saki or Duke.

Marwell remained a very aggressive cheetah exporter despite its history with nyala (first zoo TSE death in July 1986) and gemsbok (born 18 Jun 83, died 8 June 87 at 48 months): only 1 of 11 cheetahs shown here was retained by the facility itself, a female, Misty, the mother of all the Marwell litters in Figure 1, who died without neuro-autopsy or sample retention in Aug 1991. The record is very clear that Marwell knew of the death of its Pearle Coaste zoo cheetah in Jan 1992 and the death of Duke (and perhaps Saki) at the time it shipped another cheetah to Safari de Peugres after April 1993.

All 11 of the exported Marwell cheetahs in Figure 1 had died by Sept 1993 (including 3 to Whipsnade); only 2 of the 11 deaths were investigated by neuro-autopsy, the other 9 were incinerated. One and possibly both of the only neuro-autopsies were conducted by foreign countries. The authors of this paper, 4 of whom are shown as veterinarians with association to Whipsnade, are silent on 3 Whipsnade cheetahs from Marwell that died in Aug 1985, July 1993, and August 1993 and on 3 additional cheetahs from Whipsnade itself that died in Aug 1989, Dec 1988, and Dec 1993.

The first French cheetah case is not shown in Figure 1 (lacks Sept 87 birth at Whipsnade). The second French cheetah case is not shown either: Marwell lacks an April 1991 birth with export to France in 1993 and death in July 1997. This second cheetah argues for horizontal TSE transmission among cheetahs, like that in scrapie and CWD. No details are available on the mother of this cheetah however or for that matter its cagemates.

The UK itself had 5 cheetah deaths by Apr 99. Only one UK death, Michelle, is clear from this paper. Figure 1 has 2 other unassigned cheetah TSE deaths at zoos other than Marwell, Whipsnade, Broome, and France. Fota may be one of these cases. This leaves 3-4 UK cheetah deaths unaccounted for, 4 at unknown zoos.In exotic cats the Maff site now says have now been nine cases in cheetahs (four were diagnosed abroad but originated in Britain), three in pumas, two in ocelots, two in tigers and one in a lion, consistent with the MAFF exotics statistics page.

Whipsnade cheetah were offered whole cattle necks as well as sagitally split necks and lumbar regions. Additionally, surplus animals in 'apparent good health' culled for population control were fed (no CNS check). These animals would have been fed MBM rations like all zoo ungulutes in the UK up until stocks were exhausted after the partial ban. The species feed to cheetah after 1989 at Whipsnade include fallow deer, hog deer, sika deer, reindeer, water deer, nilgai, bison, waterbuck, gemsbok, and scimitar-horned oryx (bold indicates zoo species known to have contracted BSE). These feeding practises were highly irresponsible and completely unnecessary; they should have been stopped in 1986.

Note an important difference between cheetahs eating individual animals and kudus eating pooled MBM product from thousands of rendered cattle (and sheep): the former is hit-or-miss, the latter is low titre but certain.

This paper is the first and only paper to give numbers of captive felids in Britain. At the start of 1990 [source: Mammal Inventory - 1989, FZG PM 1990 London.] members of the Federation of Zoological Gardens of Great Britain and Ireland held

42 cheetahs
66 tigers
51 leopards,
68 lions
25 jaguars
19 snow leopards
1,227 carnivores of 69 species
2,675 artiodactyls of 62 species
This data gave weak chi-squared support to preferential cheetah susceptibility; however subsequent events (2 tigers, 1 lion, 4 cheetahs] eliminate any statistical signficance. Felid prions have proven hard to sequence for unknown reasons; only domestic cat has been reported. Primates data is not mentioned but surely given in the source book. The word 'primate' is never mentioned in any of the 46 articles over 13 years, even after 3 rhesus monkeys from Ravensden proved positive or probable in France.

The authors conclude by saying,

"The pattern of incidence in the kudu suggests that the disease is transmitted between animals through contact, and that the disease could (or has) become endemic in one herd. The epidemiology of the disease ik kudu appears therefore to be more like that of scrapie in sheep and CWD in deer, both of which can be transmitted by direct or indirect contact."

This has horrific implications for conservation because:

"Most herds of zoo animals are small and in order to maintaintheir genetic diversity, animals have to be moved between zoos for breeding, both locally and internationally; these movements are inevitable associated with some risk of accidental disease transmission. "Furthermore, there is growing interest in the reintroduction of captive bred animals to the wild for conservation programmmes and these reintroducions provide a route for the accidental transmission of infections diseases into free-living populations."

The authors note,

"There may also be a possibility that individuals of some species could carry and transmit the disease without showing any clinical signs. It would be prudent to avoid movements of animals that could have been exposed to the BSE agent, or their offspring or in-contacts, into populations that have not been exposed..."

Nowhere in all these articles does Kirkwood ever consider the obvious: prion immunohistochemistry on every fallen animal whether it died with TSE symptoms or not. Nowhere does Kirkwood even suggest freezing CNS samples before incinerating carcasses. There would have been no real expense to this (given a 10 billion dollar epidemic already) and a random subset of the samples could be autopsied initially.

The paper concludes with excellent warnings about the inappropriateness of exposed animals for reintroduction programs and the risks to importing zoos. No action was ever taken by the Federation of Zoological Gardens however and trafficking and reintroductions have probably continued unabated.

December 1998 cheetah holdings in UK, Ireland, and France. All UK animals or UK-history animals must be considered extremely high-risk:

Banham 6
Chester 2
Colchestr 5
Edinburgh 2
Marwell 6
Paignton 1
Whipsnade 5

Belfast 5
Fota 28
total 60 (32 in Britain)

Fontaine 4
La Palmyr 11
Mulhouse 2
Paris Zoo 7 
Peaugres 11
total 35

One supposes that Bradley, the MAFF line officer who passed the disgraceful order from CVO Meldrin to Jeffrey to falsify and delay his 1986 nyala article according to Inquiry transcripts, saw to it that no cheetah was autopsied or had sample retained unless it presented with overt TSE symptoms. Wells has his name on almost every paper on this page, indicating his office had its hand in all veterinary research, even that at private zoos, possibly because of Wells' vast experience or possibly because of CVO orders or both. MAFF similarly fought off autopsies of asymptomatic cows throughout the BSE epidemic; in 1998 was aggressively opposing a random autopsy program for BSE transmitted to sheep; and in 1999 was seeking to halt tonsil surveys of nvCJD in asymptotic humans. There is a pattern here.

With zoos and endangered species, MAFF took a huge gamble with the world's wildlife, hoping that most infected animals would die of other causes and remain hidden, hoping further that horizontal and vertical transmission would not perpetuate the disease the way they had with CWD and scrapie in both captive and wild populations. That same gamble is being taken with human and blood transfusion.

This was Kirkwood's last zoo TSE paper. However he gave a written statement #324 to the BSE Inquiry, observing:

"19. As regards dealings with committees, working parties and government departments: the cases in the ZSL animals (and, as far as I am aware, all the zoo animal cases that occurred in the British Isles) were diagnosed or confirmed at the Central Veterinary Laboratory (CVL)..."

He left the Institute of Zoology at London Zoo in June 1996 and is now the scientific director the Universities Federation for Animal Welfare (UFAW) He now publishes on backyard bird feeders after all his grant applications were rejected by MAFF. Neither the British Veterinary Association nor the Royal College of Veterinary Surgeons would provide an email or fax contact number. However Kirkwood may be found at UFAW.

In wildlife, as Kirkland foresaw in the early 90's, the scheme collapsed with the publication of Noelle Bons' paper in March 1999: the first systematic look for presymptomatic TSE in 13 years of zoo TSE research gave truly shocking results. The true scope of the epidemic must be staggering in felids and ungulates as well as primates -- some animals simply have longer incubation periods than others, that is all that is going on. There is no species barrier. Horizontal transfer may perpetuate the epidemic long after the original animals exposed to BSE feed are gone.

Spongiform encephalopathy in an imported cheetah

Aust Vet J 1992 Jul;69(7):171 
Peet RL, Curran JM
The abstract reads:

"A 5.5-year-old cheetah at the Broome Zoo [in NW Australia, aka Pearle Coast Zoo] was observed to be ataxic and disorientated during December 1991... The animal was killed 4 weeks after the onset of clinical symptoms when it exhibited falling, locomotory weakness and distress... Histopathology showed widespread axonal degeneration and demyelination of all tracts in the spinal cord. Severe spongiform change was visible in the grey matter of the neuroaxis, especially in the corpus striatum, midbrain and thalamic areas. On the basis of neuropathology, a diagnosis of spongiform encephalopathy was made and samples were forwarded to the reference laboratory in Weybridge, UK. The presence of fibrils was confirmed by electron microscopy. Meanwhile, a quarantine order was placed on the zoo and the previously buried carcasses were disinterred and incinerated. [This suggests the littermates were killed as well.]

The cheetah was born at Marwell Zoo in England on 16 June 1986 and imported together with 2 littermates to Australia on 9 May 1989. Marwell Zoo practised a 'feeding in' of culled carcasses to other zoo animals, particularly felids and canids [meaning animals culled at the zoo were fed to carnivores]. The cheetah probably ingested the infective agent while still in England. This is the first diagnosis of spongiform encephalopathy in a cheetah and of spongiform encephalopathy in a zoo animal outside the UK."

The one column article adds little to this. Australia is very concerned about exotic diseases and samples were treated as category 3. The quthorw opine that"the cheetah is considered a 'dead end' host and should not represent a threat to Australian livestock." There is no record of cage decontamination and no tracking of other zoo imports from Marwell Zoo or the UK.

Keepers had noticed a change in gait and disorientation, becoming in two weeks ataxia, locomotor weakness, and distress."Severe spongiform change was visible in the grey matter of the neurozxis, especially in the corpus striatum, midbrain, and thalamic areas."

Large felids with prion disease: years go by without publication

24 Apr 99 Contact webmaster with additions or corrections. fax 541-484-0669 US

Confirmed cases in puma, ocelot, lion, tiger, and cheetahs remain unpublished and the zoos involved secret.

The lion named Lumpy that died in Dec 98 was born in 1986 at Woburn Safari Park and transferred to the transferred to Edinburgh Zoo in 1994. It was 12 years old at death. Matthew Pincbeck at the Edinburgh facility reportedly has expressed concern on lateral transmission, because management had plans to euthanize an 8 year old female (Jody) housed with the FSE lion, based on the recommendation of the EEP coordinator of Asiatic lions in London. However, the CVO has stated there is› "no concern with putting her with other healthy lions who have not been previously exposed to the disease" and the zoo has attempted to place her with another collection (to make room for a new collection of Asiatic lions in Edinburgh)

The Edinburgh case is discussed on the Born Free home page -- the averted death sentence to Jody housed with Lumpy is mentioned, as are two other lions at Woburn which were to be culled because of lack of space/overbreeding, but were saved by public outcry. Also mentioned is a colony of primates which should have similarly be gotten rid of etc. Woburn Safari Park and Woburn Abbey Deer Park are related facilites at the Duke of Beford's 3000 acre drive-through estate; Lumpy resided at the former.

Born Free's Shirley Galligan issued the following statement on 25th Feb 99...

"48 hours ago Woburn Safari Park were arranging to put an end to Bruno and Bantu's lives, they were happy to do this discreetly before they opened their doors to the public on March 9th.› Thanks to information received at the Born Free Foundation offices and our subsequent calls to the UK Media, the plight of Bruno and Bantu became a national concern and an enourmous embarrassment to the management at Woburn Safari Park."

"In a press statement issued by Woburn safari Park they thanked the media for creating new contacts enabling them to find a new home for the lions at Bewdly Safari Park.› The Born Free Foundation would like to ask why only now have Bewdley offered a home for Bruno and Bantu when they were being openly touted on the Zoo Federations animal surplus list, information that is readily available to every zoo and safari park in the UK.› We have seen how safari parks and zoos court the limelight to ensure maximum profits, we at Born Free hope that this is not yet another PR exercise on behalf of this closed industry."

Lion holdings in British zoos as of Dec 98 are available; however, these do not give ages of animals. Mr. Douglas Richardson of the London Zoo Regent's Park heads the EEP program for endangered Asian lions, Panthera leo persicus, that are to be put in the presumbably contaminated enclosure. The years in which other felids died can be inferred from the published record by defining the window between the first mention of a case and the last review failing to mention a case. For example, a tiger case is mentioned by Narang in an article appearing in Apr 96 (but submitted say in Dec 1995 ) whereas Kirkland specifically compares the cheetah situation to the absence of disease in tigers in a comprehenisive published in Sept 1994 (say submitted in June 1994. Kirkland was well-connected as senior veterinary officer at the London and Whipsnade Zoos and conducted extensive interviews with colleagues. This establishes an 18 month window of Jun 94 - Dec 95 for the death of the first tiger and in turn, a 29-47 month delay in publication.

By Sep 13 1997, 2 additional pumas and 1 ocelot, and 1 tiger had died of TSE. The tigers are not included in the list from the WHO meeting 14-16 May 1996, whereas the 2 ocelots and the two additional pumas are: "Seven species of captive wild Bovidae and 18 animals in all have succumbed to SE probably via the same feed source as cattle. Domestic cats (71), puma (3), ocelot (2) and cheetah (4) have developed feline SE.

Epidemiological observations on spongiform encephalopathies in captive wild animals in the British Isles.

Vet Rec 1994 Sep 24;135(13):296-303
Kirkwood JK, Cunningham AA
This is an important summary of zoo TSE based on a 14 Sept 1993 Brussels talk (despite being published a year later). The authors interviewed zoos and staff at 8 affected British institutions about the 19 individual animals and their diet. Since the article was completed 2 additional pumas, 2 ocelots, 2 tigers, 1 lion, a bison, and 3 rhesus monkeys originating in UK zoos have been confirmed.

The scimitar-horned oryx (Oryx dammah) TSE case is described in print for the first time, based on an interview with veterinarians Sandra Scholes [at Veterinary Pathology, University of Liverpool in 1993] and Derek Lyon. The female was born on 12 July 1990 at an unidentified zoo [one with no reported cases] and moved to the Chester zoo [deleted from article but recognizable from puma and D. Lyons involvement] (which had had no ungulate cases but 1 puma), on 25 Apr 91 where it died 21 months later on 29 Jan 1993 at age 30 months.

At the zoo of birth, the scimitar-horned oryx ate proprietary dairy cattle feed but was born 24 months after the (leaky) ban. She was housed with 15 other scimitar-horned oryx, zebra, and red lechwe -- there were 65 scimitar-horned oryx total at this time in the British Isles. At Chester the scimitar-horned oryx was fed a proprietary concentrate lacking ruminant protein after July 1988 (though the manufacturer continued to sell this feed from inventory until Nov 1988) and housed with giraffe, gazelle, roan antelope, and forest buffalo.

From the incubation period the scimitar-horned oryx could have been first exposed to TSE at the unidentified zoo or at Chester Zoo. Both facilities had used tainted feed in the past and may not have realized how ineffective the ban was as a screen for infectivity. The mother was still alive in Sept 1993 but the father had been culled in good health with no CNS tissue saved or examined.

Four cases of TSE in elands had occurred by the time of this article but only one at Port Lympne Zoo in Kent had been written up (by Fleetwood and Furley in 1990). Two subsequent cases have never been described. The 3 elands written up here were at a different collection associated with Martin Hosegood at (Scott Veterinary Clinic, 405 Goldington Road, Bedford, Bedfordshire in 1999; at 49 Howbury St, Bedford in 1993, at Cheadle, Stoke-on-Trent, Staffordshire in 1987). The zoo has not yet been identifed. The herd consisted of 14-26 animals and had been closed since 1982. As the were only 35 elands in all of the British Isles in Jan 90, the zoo could be identified from the NFZG yearbook or current holdings [only Paignton in Devon today on the SW coast; Whipsnade is in Bedfordshire but Kirkwood would identify; Woburn is also in Bedfordshire and is a prime candidate to house the elands]. These animals ate a commercial horse pellet that did not have ruminant protein though bad feed was present on the premises before the births.

An adult female, Daphne, born on 18 April 1988, died on 18 Aug 90 with symptoms very similar to the 3 confirmed cases but brain tissue was discarded without study. This animal might have acquired the disease from feed and passed it horizontally to the others. The elends were also in contact with elephants, rhinos, ankole cows [not the one dying elsewhere of TSE, as per Stanley Kilby], and zebra. Lions and tigers on the premises were fed whole cattle heads up to Aug 88 and then split cattle heads with CNS material removed at the knacker's yard. The authors speculate that material dripping from the meat truck as it crossed the eland enclosure could have contaminated the environment. This zoo is a prime candidate for later tiger and lion cases.

Astonishingly, 2 cases of feline TSE are said by Hosegood to have occurred at this facility in semi-feral cats that scavenged the meat room, euthanized in Jan 91 and Jan 92, with ataxia and other signs consistent with FSE according to Martin Hosegood.

Dates on these 3 elands:

Molly female born 14 Jan 89, died 9 Apr 91 at 27 months.
Neddy male born 10 Jan 89, died 25 May 91 at 28 months.
Electra female born 12 Jan 90, died 253 Jan 92 at 24 months.
[Daphne female born 18 Apr 88, died  18 Aug 90 at 28 months]
The MAFF help desk responded on 27 May 99 to a query about the fifth and sixth elands. One was born in December, 1991 and was euthanized in June of 1994 at the age of 30 months; the other was born in January of 1993 and died in August of 1995 at 32 months.

Cases of BSE in domestic cattle in zoos, including the first case in an ankole cow [Stanley Kilby], are not pursued further here. White tigers at the Bristol Zoo are excluded here because of lack of transmission but see below.

TSE in moufflon, Ovis musimon, are arbitrarily considered scrapie (considering how easily BSE passes to sheep orally); at least 2 British zoos are involved (Wood JLN, Lund IJ, and Done, S Vet Record 130: 25 1992, see below]. However the sheep were pastured (with Soay sheep) and not fed rendered protein according to the article, which does not identify the zoos (or even acknowledge that they are zoos).

Kirkwood in some papers does include the 3 German ostriches reported to have a spongiform encephalopathy, noting they had been fed downer cattle. Dealler writes this site on 20 Apr 99 saying, "The ostriches in Hamburg zoo really did have an infectious form as prions could be shown in the brain tissue: again this has not been published by the various groups in Germany that were involved." Schaetzl sent this site the ostrich prion sequence; the species barrier would not be all that formidable because of the invariance of positions 102-126, the key amyloid domain.

On the other hand, Roland Heynkes wrote saying he had spoken at length in 1997 with the primary pathologists in Germany who said the SE was not a prion disease. And Gibbs writes on 25 Apr 99 saying,

"As to the ostrich situtation. When in Berlin several years ago with Hino Diringer I was asked to look at sections of Ostrich brain that reportedly was being diagnosed as spongiform encephalopathy. As I recall this was archived material. I looked at the brain sections anad although there were vacuoles in the brain it did not present as the type of spongiform encephalopathy I relate to the TSE's. Diringer gave me a small amount of homogenate of the brain which I inoculated in to squirrel monkeys. One animal was held for 6 years and the other for 4 years before dying of intercurrent infections. Neither pathology nor PrPres was detected in their brains. I do not have any of the ostrich brain homogenate left but might be able to find the monkey brains if any are left. "

Further details are given on the gemsbok born 18 Jun 83 at Marwell which died 8 June 87 at 48 months. It was fed the same ruminant derived rations as the nyala. The authors are very confused in this article (but not in others) about the onset of BSE, not realizing that the first cases in cattle occurring in April 1984 implied that the rations had long been contaminated. The gemsbok was died at a time the group numbered 13. Its only calf died on the day it was born, 6 Jan 87. The gemsbok's mother had 6 further calves between 1984 and 1991 before it was euthanized for "old age" with no CNS study nor tissue saved. The calves have not been tracked but are very high risk animals.

Morbidity in captive white tigers

Kelly DF, Pearson H, Wright AI, Greenham LW 
The Comparative Pathology of Animals" editors RJ Montah, G Magaki 
Washington DC Smithsonian Institution Press 1980 pg 183-188
The white tigers that died with spongiform encephalopathy at the Bristol Zoo from 1970 to 1977 are not considered in Kirkland's s review because the condition was not transmittable. However those cases need to be revisited with immunohistochemistry and capillary electrophoresis in both tiger and recipient brains. In one scenario, these tigers could establish that the BSE epidemic had been present at low levels far earlier than ever envisioned (1960's) and had simply been amplified to epidemic levels by a later change in rendering conditions. These tigers would have been fed split spinal cords and the like -- very high risk unpooled material -- possibly several times a week for years on end, thus sampling thousands of spinal cords. Since nothing has been released on 2 confirmed tiger cases in the mid 1990's, family or zoo or enclosure connections cannot be ascertained until the British release more information.

In fact, that may be the very reason that nothing was ever published on the later tiger two cases, one of which was in 1995: these later tigers may also have been white tigers or tigers which had been in Bristol Zoo enclosure.

The paper itself describes spongiform encephalopathy or gliosis or both in the brains of 4 white tigers out of 6 that died with similar behavioral and clinical signs including weight loss, weak unsteady gait (especially in the hind limbs), could not stand without support, head-pressing, constant roaring, periods of unusual aggressiveness and unwillingness to leave the sleeping den.. The course of illness averaged 3 months to death. All of the animals are associated with the Bristol Zoo. Liver problems were also observed. Feeding practises are not disclosed.

Champak, born mar 62, died Jun7 0
Sarala, born May 68, died Oct 71
Sushita, born May 68, died Sep 72
Akbar, born May 68, died Dec 72
Seeta, born May 70, died Feb 73 in New Delhi after Oct 72 export
Shubhra, born May 70, died Sept 77
The Bristol Zoo purchased tweo 15-month old tigers, Champak and Chemeli in June of 1963; the litters above are the second and third. There is no information on the other 18 white tigers born in Bristol between 1967 and 1976. These are the offspring of the original white tiger, Mohan, captured in 1951 by the Maharaja of Rewa. Outbred with a normal tigress and then back-crossed into a daughter, Radha, resulted in the original litters. White tigers are not albinos.

A pilot study of transmission by intracerebral injection into mice from fresh frozen cerebrum and cerebellum from Akbar gave statistically shortened lifespans but no overt illness. Akbar had "striking vacuolation of the neuropil in the grey and white matter and focal cerebral microgliosis. Histological features of classical encephalitis were absent.

Frozen sample material was sent and saved by CJ Gibbs who noted on 25 Apr 99:

"The first I had heard of the death of these tigers was a call from the Director of the National Zoo in Washington, D.C. There had been a meeting of various zoo individuals and during the meeting a pathologist from the Bristol zoo presented data on the death of white tigers in his zoo and described then as having spongiform encephalopathy. Hearsay remarks were made to indicate that other white tigers of the same family living on a private estate in India had died manifesting a similar clinical syndrome. Bristol zoo may have records about the history of these tigers. It is amazing to me that when I brought this issue up at a meeting I held at the CVL shortly after the outbreak of BSE, the door was closed on any further acquisition of white tiger material including slides."

Subsequently the Bristol pathologist sent me some frozen tissues which I inoculated into squireel and capuchin monkeys and which I used to try to extract prion protein. We were not able to identify the abnormal isoform of the prion protein nor were we able to transmitt disease to squirrel monkeys or to capuchin monkeys. In addition a limited number of mice and hamsters were also inoculated at the same time and these remained on for two years before being killed and their brains examined for pathological lesions of spongiform encephalopathy and for the presence of PrPres. All tessts were negative.

The squirrel monkeys were kept under observation (one for 19 years and another is still in our colony- now 20 years); the inoculated capuchin monkeys were held under observation (one for 9 years and the other for 4 years) before dying of intercurrent infections. All three primates were carefully examined neuropathologicaly and for extraction of PrP. All three were negative.

We did not try immunocytochemistry. There is still a piece of cerebellum from one of the tigers but this was received frozen and remains at -80C (.the morphology will be bad.)"

Katherine O'Rourke at WSU notes that "because histology was done on the tigers, there must have been formalin fixed tissues. Since pathologists rarely discard paraffin blocks of tissue, these samples are probably still available. The most efficient way to get IHC done would be to contact Dr. Wells in the UK. He has been immunostaining with one of our antibodies which is predicted to bind the conserved epitope on the feline PrP and probably has access to antibody 3F4. He would have access to FSE tissues from domestic cats for positive controls."

The Bristol Zoo is located in Clifton, Bristol, UK, Tel: 0044-1179-706-176 or 0117 973 8951, fax: 0044-1179-736-814. Geoffrey Greed is director of IUCN programs; J. Bryan Carroll is Operations Manager, EEP coordinator for Pithecia pithecia (white-faced saki), and E.E.P. Studbook keeper for Rachypithecus auratus auratus (Javan leaf monkey/lutung ); Darren A. Webste is EEP studbook keeper for Alouatta caraya (black howler monkey). No emails are provided other than Stephen Woollard at awards@bristolzoo.org.uk or fundraising@bristolzoo.org.uk.

Bristol Zoo Gardens today participates in a total of 82 Conservation Breeding Programmes, of which 30 are for mammals (the zoo has 322 animals of 91 species). "Caring for animals is very expensive. Each year the Zoo spends approximately £100,000 on food, £90,000 on gas and electricity, £50,000 on water and £50,000 on other items such as veterinary fees, cleaning and transport. "

Ironically, the zoo offers a play, The Last Tyger in July 1999 described as, " The Travelling Light Theatre present a richly textured, vibrant and colourful story about the world's last tiger, lost in an urban jungle, and the two city children who find her and decide to set her free. 'Marvellously imaginative' The Stage 'Far too good to miss' Time Out."

Spongiform encephalopathy in a captive puma

Vet Rec. 1992 Nov 7;131(19):431-4. 
Willoughby K, Kelly DF, Lyon DG, Wells GAH
Liverpool Field station South Wirral, Liverpool, Gatehouse Vet Hospital-Lavister-Rossett-Wrexham, CVL
The animal here is a 5 year old puma born and raised at a zoo "in the north of England" that lived alone after 10 months. Now DG Lyon previously investigated anthrax at the Chester Zoo; South Wirral is about 12 miles NW of Chester; and Wrexham is about 12 miles SSW of Chester, a town itself just south of Liverpool. The Chester Zoo itself is officially called the North of England Zoological Society; its director Dr. Gordon Reid, Tel:0044-1244-380280 might be able to confirm this case. One other felid, an ocelot, has been confirmed at Chester.

The Chester Zoo is the UK's largest zoo covering 110 acres and includes around 11 miles of pathways. The zoo is run to support and promote conservation, by breeding rare and threatened animals, with the following co-operative re-introduction programmes completed, in progress or planned by April 1999.

Pňre David's Deer 
*Scimitar-Horned Oryx 
Onager (wild ass) 
Przewalski's Horse 
Cotton-topped Tamarin 
Black and White Ruffed Lemur 
American Bison 
*Cheetah
Chimpanzee 
Bornean Orangutan
Sumatran Orangutan

*These animals have acquired TSEs at various zoos. 
The mother of the puma had been born into the same zoo and the father imported; these died of "non-neurological diseases" but were not autopsied. A cheetah "born in the south of England" mentioned later in the Addendum can be identified as Marwell based on its export to the Pearle Coast Zoo.

The puma at Chester was given cattle carcasses deemed unfit for human consumption and split spinal columns but rarely offal and never cattle heads. All the cattle material came from a single supplier [not identified]. The puma also ate cull meat from 2 elands* born 2 years earlier at the zoo but never sheep or goat and commercially prepared cattle food (ie rations intended for dairy cattle).

Onset of symptoms occured in April 1991 and the animal was put down 6 weeks later, with a postmortem within 3 hours and intensive prion deposits. The MAFF site states that 3 pumas had died in England of TSE; other zoos involved remain undisclosed and no studies have ever been published.

Experimental infection of mink with BSE

J Gen Virol 1994 Sep;75 ( Pt 9):2151-5
Robinson MM, Hadlow WJ, Huff TP, Wells GA, Dawson M, Marsh RF, Gorham JR
Mink were inoculated with bovine brain homogenates from cows affected with BSE, both intracerebrallyand orally. Signs of neurological disease appeared in mink an average of 12 months after intracerebral inoculation and 15 months after feeding. Decreased appetite, lethargy and mild to moderate pelvic limb ataxia were the predominant clinical signs, quite unlike the classic clinical picture of transmissible mink encephalopathy. Although resembling TME, the encephalopathy was distinguishable from it by less extensive changes in the cerebral cortex, by more severe changes in the caudal brainstem and by sparing of the hippocampus.

How many house cats really got TSE?

20 Apr 99 Contact webmaster with additions or corrections. fax 541-484-0669 US

FSE in a cat in Norway

Vet Rec. 1995 Mar 18 136(3) 444
Bratberg, B, Ueland K, GAH Wells
A 6 year old cat near Oslo, Norway was confirmed. Onset (ataxia of gait) to euthanasia took 4 weeks. Extensive prion immunostaining found with monoclonal 3F4. The cat had been fed several imported commercial dry cat food products. The article does not give the brands of cat food nor the name of the Norwegian distributor nor the country of origin of the imported food. The cat itself had no connection to the UK.

Feline spongiform encepalopathy: fibril and PrP studies

Vet Record 131: 307-310  3 Oct 1992
Pearson GR, Wyatt JM, Gruffydd-Jones, Hope J, Chong A, Higgins RJ, Scott, AC, Wells GAH
They looked at 18 cats, 13 of which had been referred with clinical signs potentially indicative of FSE. Of these 13, 5 had FSE histopathology, Prp-res, and prion fibrils; 5 had irrelevent CNS lesions (though one with confirmed meningioma also had Prp-res and fibrils), and 3 had normal histology (though one of these also had prion fibrils). The 5 remaining cats had no clinical signs nor problems on histology and were used as controls. However, one of these had prion fibrils (ie, 20% of the controls).

Thus the authors found 3 of 18 cats (17%) with preclinical disease (including the one undiagnosable from clinical signs and histology). Discounting the clinical FSE cases, 3 of 13 cats is 23%. The control cats had been referred to the Bristol veterinary school for reasons not spelled out but those reasons did not include any type of clinical neurological sign. These cats were in a ":similar age range" as the others [ but see below]. Taken at face value, roughly 20% of the cats in the Bristol area in 1992 were incubating the disease in 1992. If England had 7 million cats in that year and if Bristol was typical, this pencils out to 1,400,000 cases pending in that year.

The cats with overt BSE were 4, 5, 5, 6, and 12 years old (average: 6.4); three had been described previously by Wyatt. The FSE cat with meningioma was 9 years; the FSE cat with neurological sign without CNS pathology was 2. Table 1 shows that several of the cats without prion disease but presenting with neurological problems were significantly younger, 1, 1, 2, 2, 6, 7 (ave: 3.1). Some of these cats may have tested positive had they lived to comparable ages. The negative control cats were 9 weeks, 6 months, 1 year, and 5 years (ave: 1.5 years) whereas the positive control cat was 17 years.

The authors never pursued this line of inquiry, nor did anyone else. It would have been a simple matter to go down the the pound and obtain 100 random cat brains. However, as with cows, sheep, people, and zoo animals, no one really wanted to know how many were incubating BSE. The authors cite an earlier study by Ikegama et al in experimental sheep wherein 3 of 17 preclinical animals had PrP-res in lymph nodes [Vet Record 128: 271 1991], but it has never been politically correct to look for preclinical TSE in any species other than sheep and rodents. The finding of preclinical disease in a small sample of control cats strongly suggests that the overall BSE epidemic in cats was vastly greater than the British have ever stated.

How many cats died from the disease and how many are still incubating FSE today is unknown. The MAFF statistics page is a joke -- where are the control animals?

Do infected cats pass the disease horizontally to other cats or to their owners? This remains unknown; the case in Italy heightens concerns. Question 6 of the official CJD Surveillance Questionaire asks families whether the nvCJD victim shared a home with cats (or dogs or ferrets) since 1980 and in Question 5 whether the subject has ever eaten pet food.

Spongiform encephalopathy in a Scottish cat.

Vet Rec. 1991 Oct 5;129(14):320
Synge BA, et al.  
Cat had been fed tinned beef, no sheep products. Onset at 4 years, euthanized 9 weeks later. 20th case, first in Scotland.

Naturally occurring scrapie-like SE in five domestic cats

Vet Rec 1991 Sep 14;129(11):233-6 
Wyatt JM, Pearson GR, Smerdon, TJ et al.
This summarizes clinical information for 5 cats with FSE:
cat 1, age 5,  from Avon, five cat householdhad onset in Dec 89, was staggering by Jan 90,  was euthanized in April.
cat 2 , age 8, from Gloucestershire, one cat household, excessive salivation  in Feb 90; euthanized 10 weeks later.
cat 3, age 12, from Glamorgan, onset in Apr 90, euthanized in June 90.
cat 4, age 8, from Somerset,  one dog household, onset Apr 90;  euthanized in June 90..
cat 5, age 5, from Warwickshire, cat and dog household, onset Apr 90; euthanized in July 90.
The authors discuss an incident in 4 of 6 tigers of spongiform changes and/or gliosis in tigers from the Bristol zoo in 1980 in which TSE was suspected. Transmission was attempted by CJ Gibbs and DF Kelly in mice, squirrel monkeys, capuchin monkeys, guinea pigs and domestic cats using brain tissue from one of the tigers. No transmission was seen; however experimental details were never published, though page 183 in a textbook alludes to this, Kelly DF, Pearson H, Wright AI, Greenham LW, 'The comparative pathology of zoo animals, Smithsonian Institutional Press, p 183 (1980), Montali and Migaki, editors.

Feline spongiform encephalopathy.

Vet Rec. 1991 Jun 1;128(22):532.
Pearson GR, et al.  
Brief letter. Bristol alone has seen 7 cases of mad cats. Announces prion detection, details to be published in a few months.

A spongiform encephalopathy in a cat.

Vet Rec 1990 Dec 15;127(24):586-8 
Leggett MM, Dukes J, Pirie HM
A 7.5 year old cat from Leicestershire was confirmed. It had been fed proprietary canned food, occasionally supplemented with dry cat food, and had never been boarded. Onset of symptoms was Jan 90; in Apr 90 the cat was afraid to go out and had developed gait abnormalities reminiscent of cows with BSE; it was euthanized around 1 May 90 and confirmed as SE. No plaques were found.

This was the 4th case in cats. [Cite: Anon, Vet Record 127 7 1990]. The authors think the cat will be a 'dead end host,' mysteriously citing mink TSE which is certainly infectious to numberous species and ignoring conclusions about horizontal transmission in deer (though citing Williams et al.). The Pet Food Manufacturer's Association is said to have stopped using suspect offal before the bovine ban for human consumption, citing an anecdote of Meldrin.

Spongiform encephalopathy in a cat.

Vet Rec. 1990 May 19;126(20):513 Wyatt JM, Pearson GR, Smerdon T, et al. A routine referral from a veterinary surgeon [date not provided] to the Bristol veterinary school turned out to be a 5 yr old male siamese cat with ataxia and other symptoms of FSE. Autopsy established the diagnosis of the first prion disease in felids. The animal may be presumed to have eaten BSE-tainted cat food. The date of death and date of submission of the article are not provided. It is possible that substantial delays in reporting occurred.

Keith Meldron, CVO of England, was given comment space in this same issue. He says "nor is there any known connection with the other animal encephalopathies" and requests details of any further confirmed cases be sent to the MAFF divisional officer.

Horizontal transmission shown in kudu

18 April 99. Contact webmasterwith additions or corrections. fax 541-484-0669 US

Spongiform encephalopathy in a greater kudu introduced into an affected group

Vet Rec 1994 Feb 12;134(7):167-8 
Kirkwood JK, Cunningham AA, Austin AR, Wells GA, Sainsbury AW
Two female kudus born at Marwell Zoological Park were transferred to the London Zoo Regent Park on 14 Aug 90. On 22 Nov 92, some 27 months after the transfer, the kudu born on 5 Aug 89 [an animal named 324/90, name deleted here] was euthanized 8 weeks after onset of clinical symptoms (unusually long duration) at age 39 months. No TSE in kudu had been described at Marwell to this date; the father of the kudu was still alive in Feb 93 and the mother (born 2 Nov 82) had died of reticuloperitinitis (no neuro-autopsy done or material saved) sometime after Aug 89. The affected female was born 13 months after the 1988 ban on ruminant-derived protein in ruminant feeds, plus Marwell had stopped this practise even earlier in March of 1997. The London zoo had stopped feeding this material years before the kudu arrived; ruminant protein stocks are not be kept in inventory for more than 2 months by this zoo. The second Marwell kudu was alive in Feb 94. This animal was exposed horizontally both at Marwell and London and by feed at Marwell so must be considered extremely high risk.

Marwell had previously reported TSE in nyala, gemsbok, and cheetah but the affected kudu had never been in contact with these. The ruminants, including the mother of the affected kudu, had been fed rendered bovine protein during the period Mar 86-Mar 87. Yhe cheetah had been fed split spinal chord.

At London, the new kudu were housed with other kudu, two of which subsequently developed TSE. (These were Karla, who died 4 months after the introduction as the offspring of the affected mother Linda, and a second animal born 12 days after the arrival, who died in Feb 92 at 18 months of age with asymptomatic confirmed TSE.) The kudu here had no contact with placental material from this birth nor with ungulates outside this herd.

The kudu described here cannot have acquired its disease from feed either at Marwell or London. Both zoos had ceased feeding suspect material 2 or more years before its birth and feed stocks were kept at most 2 months. Maternal transmission is plausible given the timely exposure of the mother; horizontal transmission is equally plausible given 2 subsequent cases in the herd and an adequate 27 post-arrival incubation period during which Karla was incubating disease. Just as with scrapie, these two scenarios are very difficult to distinguish. This was the 6th and last case of TSE reported in kudu; all were at the London zoo. There are no numbers here for the total numbers of kudus kept in British zoos (nor any reports of negative autopsies from other zoos).

Spongiform encephalopathy in a herd of greater kudu: epidemiological observations

Vet Rec. 1993 Oct 9;133(15):360-364. 
Kirkwood JK, et al.
This is the kudu geneology paper, the only one of its kind, suppling a crude database of this zoo's kudus and their disposition. It addresses a small herd derived from 3 individuals, maintained at the London Zoo since 1970. 5 of 8 animals born since 1987 succumbed to TSE; with at least 4 it is certain that they were not exposed to rendered feed. The authors conclude the disease "has spread among them either by transmission between individuals or through contamination of the environment." This result is very similar to the American experience with CWD.

Koo, male, West African import of 1967
Doo, female, Denmark zoo import 1969
Chester, male, Chester zoo import 1982 born in Munich Zoo in 1975, died 30 Apr 84, brain discarded.
Diana, born 1980, exposed to MBM, still alive in Dec 92.
Steph, born 1984, exposed to MBM, died 1 Feb 91 of hepatopathy, negative light microscopy, brain discarded.
Kaz, male born 14 May 88, culled 6 Jun 91 at age 37 months.
Bambi, male born 29Oct 88, culled in good health on 29 Oct 91 at 36 months.Preclinical TSE
346/90, male born 26 Aug 90, culled 26 Feb 92 at 18 months. Preclinical TSE
Frances, born 28 July 85, died with TSE symptoms 17 Nov 87, brain discarded without examination.
Linda, index case, born 11 Feb 87, died 18 Aug 89 at 30 months, dam of Karla, transmitted to mice.
Karla, born 19 Apr 88 died 13 Nov 90 at 19 months.
324/90, born unknown zoo 5 Aug 89, transferred to LZ at 27 months, died 22 Nov 92 at 39 months
female 1, imported from Marwell in 1990.
female 2, imported from Marwell in 1990.
2 kudu exported to Marwell in 1975-76.
1 kudu exported to Chester zoo in 1980.
1 kudu exported to Cotswold Wildlife Park in 1982.
1 kudu exported to Rotterdam Zoo in 1982.
3 kudu exported to Whipsnade Wild Animal Park in 1987 (Jaime) and 1990 (Kaz and Bambi), latter 2 died there.
Jaime, born 1984, later reimported from Whipsnade in 1989, died 25 Jan 90, negative light microscopy, brain discarded.
Sandra, born to herd, euthanized at 12 months with hip problem, brain discarded without examination.
273/91, born to herd 9 Sep 91, in good health on 16 Dec 92.
276/91, born to herd 7 Sep 91, in good health on 16 Dec 92.
Nick, born early 1986, died 24 Sep 88, brain discarded.

Other kudu in figures 1-2 cannot be identified further.

The animals occupied throughout in a single ungulate facility, Cotton Terraces, with an outdoor padock and three indoor dens exclusive to kudu for over 10 years. While MBM was replaced by fish meal in Feb 87 for all ungulates, MBM continued to be used on zoo premises until June of 1988.

One kudu, the infected but asymptomatic Bambi, was had reared with cattle colostrum and then proprietary sheep milk-replacer. Since 1986, all animals received a serovaccine against E. coli containing hyperimmune antisera prepared in cattle. However, no cases of BSE occurred within these cattle (pers. comm. from manufacturer).

Of 13 kudu that died since 1982, at least three may have had TSE based on clinical signs alone (brains were discarded or just look at with light microscopy). The most conspicuous of these was Fran (same mother as Linda) who died on 17 Nov 87. Diana was the mother or grandmother of all the affected kudu. The prion sequence from kudu was determined but never posted to GenBank by Poidinger et al; the animal is not named; the sequence seems normal.

Kirkwood's Inquiry statement: of 11 Dec 98

"A very cautious approach was taken and the keeper staff used separate tools for cleaning out the kudu dens and paddocks, changed overalls and boots, used latex gloves, and, for a period until it seemed (for reasons mentioned below) less likely that the situation in kudu differed from that in cattle, collected wastes for incineration. Management practices were reviewed again in March 1996 when it was announced that cases of new variant CJD had occurred which might be related to the BSE agent. In order to pre-empt any public concern that might follow this announcement, the walkways past the kudu paddock were closed to the public. No cases have occurred in the kudu group since 1992. "

"During the period we also collated information on cases of SE that occurred in wild animals at or from other zoos in the British Isles. The total number of cases of which I was aware in June 1996, when I presented a review on occurrence of spongiform encephalopathies in zoo animals (at the Royal College of Pathologistsľ Symposium on Transmitting prions: BSE, CJD, and other TSEs, The Royal Society, London, 4th July 1996), was 25, involving 10 species. The animals involved were all from the families Bovidae and Felidae, and comprised: 1 Nyala Tragelaphus angasi, 5 Eland Taurotragus oryx, 6 greater kudu Tragelaphus strepsiceros, 1 Gemsbok Oryx gazella, 1 Arabian oryx Oryx leucoryx, 1 Scimitar-horned oryx Oryx dammah, 4 Cheetah Acinonyx jubatus, 3 Puma Felis concolor 2 Ocelot Felis pardalis, and 1 Tiger Panthera tigris. Since the time the above statistics were published, there has also been a case in a bison."

Transmissible spongiform encephalopathy in greater kudu

Vet Rec. 1993 Jan 16;132(3):68.
Cunningham AA,Wells GAH, Scott AC, Kirkwood, JK, Barnett JEF  
This was a brief but important paper from the London zoo group, the only zoo actively researching TSEs and admitting to having it on the premises (but see Inquiry excerpts). Here they discuss 3 new kudu cases in animals that never received animal protein rations during their lifetimes. Two of these animals were superfluous males and had no clinical symptoms at the time of euthanasia. However both were positive upon prion immunostaining.

The first animal was a male named Kaz [name not provided in paper] born in May, 1988, 8 weeks before the ban on feeding of ruminant derived protein to ruminants. However, the London zoo had taken this step 15 months earlier, in February, 1987, going to fish meal. Clinical onset was at 37 months, in June 1991, progression was rapid, and euthanasia took place the following day. Publication took an additional 18 months.

The second new kudu was a male named Bambi [name not provided in paper] born in Oct 1988 and culled in good health at 36 months (Oct 1991). It had had contact with an earlier TSE kudu (Karla) and was not considered suitable for breeding.

The third kudu was similar: a male named 346/90 [name not provided in paper] born in August 1990 and culled in good health in Feb 1992 at 18 months. (Only one male kudu can be kept in small-enclosure herd.) This is not an instance of early onset because the animal was silently incubating the disease (ie, still preclinical).

The authors tentatively conclude that kudus have horizontal transmission (vertical is ruled out in a later paper). They note that further study many "provide important information for conservation programmes involving the breeding of zoo animals which may have been exposed to infection."

Scrapie-like encephalopathy in a greater kudu which had not been fed ruminant-derived protein

Vet Rec 1992 Apr 25;130(17):365-7 
Kirkwood JK, Wells GA, Cunningham AA, Jackson SI, Scott AC, Dawson M, Wilesmith JW
The calf, Karla (born 19 Apr 89) of a previously described kudu, Linda (born 12 Feb 87) died at 19 months with 12 hours of clinical onset. This animal was not exposed to ruminant-derived protein, not simply because of being born 9 months after a statuatory ban and 26 months after the zoo switched away cattle or sheep products, but because:

"Food purchase, storage, and utilisation practices at the zoo result in the retention of each feed abtch for a maximum of two months. After the modification in Feb 87 the diet of the greater kudu remainied unaltered; it dcontained a vitamen E supplement which included fish meal, but no other animal protein."

The animal was part of a group of 6 kudu that had limited indirect contact with roan antelope, sable antelope and bontebok kept in othr dens in the same house and in the paddock adjacent to the kudu. There was no fence line contact with these species but a common passageway was sometimes used. These species have never been implicated in TSE; however, no neuro-autopsies are known either.

The mother calved in a den separated from the other kudu. The placenta had disappeared when the den was cleaned after 48 hours. The calf was nursed by its mother until it was weaned at the mother's death from TSE on 18 Aug 89.

Feed is ruled out for this calf; maternal and horizonal transmission cannot be distinguished.

Spongiform encephalopathies in ungulates.

Vet Rec. 1991 Mar 30;128(13):311.
Kock R. 
Vapid speculation about Gibson's vapid speculation on Kirkwood paper.
Vet Rec. 1991 Feb 2;128(5):115.
Gibson PH.
Vapid speculation on Kirkwood paper to the effect that ruminant differences in digestion account for the species mix and incubation time seen with TSE.

Spongiform encephalopathy in an arabian oryx (Oryx leucoryx) and a greater kudu.

Vet Rec. 1990 Oct 27;127(17):418-20.
Kirkwood JK, et al.  
The arabian orxy was born at the Zurich Zoo 12 Jan 86 and imported to the London Zoo RP in Oct 86. On 2 Mar 89, after 29 months in Britain at age 38 months, the animal showed clinical signs and died 22 days later. This animal lived in a group of 5. It was fed commercial dairy pellet with meat and bone meal up until Feb 87 when a 13% protein supplement lacking MBM and ruminant derived protein (later identified as containing fish meal as the sole animal protein) was substituted. It had one calf in 1988 that was exported to Saudia Arabia and killed there by incompetent keepers through excessive nutrient intake shortly after arrival on 18 Aug 89 and never examined. Kirkwood stated at the Inquiry that it was retrospective examination of the brain of the Arabian oryx that had died 5 months earlier, indicating brain material had been saved.

On 15 Aug 89, a 30 month old kudu named Linda born on 11 Feb 87 and kept at London developed ataxia. It died 3 days later on 18 Aug 89. A calf named Karla, born 19 Apr 89 was well at the time of this article but died at 19 months on 13 Nov 90 [see 1992 article]. How did this kudu acquire TSE if the zoo had already switched feed in the month of its birth? (The actual date of feed switching was astonishingly not recorded by the zoo and the authors later note that this animal may have been occasionally exposed to MBM on the premises though fish meal was the only animal protein used for ungulates.) The mother of this kudu, Diana, was still healthy in Dec 92. The authors state that 'other' kudus had died at this zoo in the 1985-89 period. One of these, a 2 year old female, Fran, who died on 17 Nov 87 at 28 months with symptoms strongly resembling TSE; this gives chronological paddock overlap. This animal was discarded without neurological examination. Fran is the likliest source of Linda's TSE under horizontal transmission. Fran had no calves.

The authors state that in 1989, the London zoo had 118 artiodactyls of 23 species. Other than the unexamined kudu, none of these had died with symptoms of TSE. Giraffe, gaur, lowland anoa, bongo, camel, vicuna, and llama were also fed the same MBM rations as the affected kudu and oryx. There is no further accounting for these animals. Many would have died for various apparent reasons by now; they were apparently incinerated without neuro-autopsy or sample retention. A scimitar-horned oryx, 5 elands, a bison, and ankole cow on the MAFF site remains unaccounted for among the ungulates.

The authors conclude that there is "a need for a rigorous surveillance fo SE in exotic ungulates and careful consideration before exporting captive-bred exotic ungulates that may have been exposed to [high-risk] feed for reintroduction programs in the wild.

No such surveillance was ever carried out even by the London Zoo, trafficking in zoo animals continued unabated, as apparently did reintroductions to the wild.

Spongiform encephalopathy in an eland.

Vet Rec 1990 May 12;126(19):489-90 
Gibson PH
Vapid speculation subsequent to Fleetwood and Furley eland paper.

Antelopes die of mad cow disease.

Nature. 1990 Mar 15;344(6263):183 N&V
Aldhous P.
This news story cites James Kirkwood, senior veterinary officer at the London zoo, where an Arabian oryx [Oryx leucoryx] and kudu [Tragelaphus strepsiceros] died in 1989, as saying 'conservationists will have to wait to assess the impact of the outbreak on endangered species." London zoo officials have written to other British zoos suggeting that "careful considderation" should be given before animals at risk are exported for foreign zoos or for reintroduction programs. The London zoo circular [not obtainable yet] says that any ungulate fed proprietary meal between 1980 and 1989 may be affected.

The article breifly mentions the nyala and gemsbok [Oryx gazella] at Marwell Zoo near Winchester and an eland at Port Lympne Zoo in Kent. [This zoo has never been mentioned in print other than in this Nature comment piece. 6 elands had died of BSE according to the Maff site by April, 1990; it has not been disclosed whether all of these were from Port Lympne. Kent experienced high initital nvCJD counts and one rendering plant was pumping BSE rendering waste into the groundwater] Geoff Holmes, at Itchen Abbas Maff facility expresses further concerns here about maternal transmission in zoo animals.

Spongiform encephalopathy in an eland.

Vet Rec 1990 Apr 21;126(16):408-9 
Fleetwood AJ, Furley CW
A female eland [Traurotragus oryx], bred and born 6 Apr 87 on zoo premises [not disclosed in article but the Port Lympne Zoo in Kent], three months pregnant, showed clinical signs on 12 Dec 89 and was dead on 20 Dec 89 at 32 months of age. This was the third zoo animal and first of 6 elands. It has not been disclosed where the other 5 elands were located. This eland was part of a small family group that had been "fed an ungulate ration containing procesed animal protein from calfhood to June 1988" and had had no contact with sheep or goats.

Andrew Fleetwood gave a statement to the BSE Inquiry on 15 Sept 98 describing the pathetic state of the supposed feed ban and noting:

"In December 1989, I investigated the appearance of neurological signs in an eland resident at a local zoo. A diagnosis of spongiform encephalophy was made, and the case reported in the Veterinary Record (J/VR/126/408). I used the general test for scrapie on the basis that the disease was uncertain and a broader spectrum of test was suitable (rather than the specific, although quicker, test for BSE). "

Spongiform encephalopathy in a nyala (Tragelaphus angasi)

Vet Pathol. 1988 Sep;25(5):398-9
Jeffrey M, Wells GA
Lasswade Veterinary Laboratory, Midlothian
This is the famous article concerning the first nyala [Tragelaphus angasi] to go down at the Marwell zoo in 1986. Chief Veterinary Officer Keith Meldrun and Bradley personally interfered with to change its title, delete any dates of onset or mention of facility name, any resemblance to scrapie, and to delay its publication by 27 months, as documented at the Inquiry site. On 17 November 1987 Mr Bradley minuted Dr Jeffrey noting that the title to his nyala paper was likely to be unacceptable to "senior management" for "veterinary political reasons" (Inquiry site).

Jeffrey is on record as saying, 'it would have been negligent to try and publish that without a reference to scrapie' and indeed that word did get mentioned 9 times in the article. However, the diet of the nyala was deleted from the final article. In January 1988, J Wilesmith was told Winchester VIC (Geoff Holmes) that both the nyala and a later gemsbok (born 18 Jun 83, died 8 June 87 at 48 months) had received rations containing MBM. Holmes did the original necropsy on the nyala and made a field visit to Marwell Zoo on 21 July 1986.

A 33 month old nyala, born 4 Sep 83 [deleted from article and raised at Marwell Wild Animal Park [zoo deleted in article] developed hindlimb ataxia [date deleted in article] and abnormal head posture and was euthanized after 3 weeks on 18 Jun 86 [deleted from article]. Findings were sufficiently similar to CWD, TME, scrapie, and CJD "to warrant a provisional diagnosis of scrapie-like disease." A "similar encephalopathy" is mentioned in domestic cattle but BSE is not mentioned by name. No antibody was used (this was June of 1986); amyloid and congo red were negative. Like in many subseuent studies, the gastrointestinal epithelia was scrupulously avoided. The incubation periods in 6 strains of mice had the same ranking and pattern as genuine BSE.

The nyala was infected by feed between April 1984 and June of 1986. Assuming a reasonable incubation period, the earlier date is favored. This is why the article created such an internal furor -- the BSE epidemic must have already been rampant and gone through several cycles of amplification before this animal's feed became tainted in, say, June of 1984. (The authors cite an earlier unexplained incident wherein 21 nyalas succumbed to "cardiomyopathy" in 1982.)

The nyala here had no direct contact with sheep or goats and its paddock had not previously been used by them (unlike Colorado's Foothill Research Station). No mink or N. American deer are kept at the facility. The nyala was bottle-fed cow milk [MBM deleted in article]. Only from later BSE Inquiry records do we learn that meal and bone meal from cattle were included in this nyala's diet. The authors exhibit good understanding of the 1982 paper of Williams et al. in which CWD is noted to have become established in the wild.

The nyala was part of a larger group of 5 female nyalas and their calves. The mother of this nyala (which itself was never bred) had 8 other calves from 1985 to 1991; none of these were ever tested. These were kept in a paddock adjacent to 6 sub-adult males, who in turn had fenceline contact with an Arabian oryx. The subsequent history of these animals is not clear, not even if they are still alive. Marwell may have disposed of these animals without autopsy or even exported them. A gemsbok of 36 months of age was diagnosed at this same zoo in 19 June 1987 by SH Done. Marwell exported in mid-1993 a cheetah born in April 1991 (ie, after the Sept 90 feed ban for zoo animals) that died later of TSE at a French zoo, as well as 2 cheetahs dying at the Broome, Australia zoo and the Irish facility at Fota.

Related References

The natural occurrence of scrapie in moufflon.

Vet Rec 1992 Jan 11;130(2):25-7 
Wood JL, Lund LJ, Done SH  {CVL Weybridge]
Six cases of scrapie were confirmed [plus 4 others with scrapie symptoms] in two separately maintained flocks of moufflon, in both of which the disease appeared to be endemic. The clinical signs and histopathology were indistinguishable from those observed in scrapie-affected domesticated sheep. The pathology included lesions in the cerebral cortex which, although commonly present in scrapie-affected sheep, have not previously been described in the natural disease.

Kirkwood identifies both facilities as zoos, not private flocks. Detwiler also briefly mentions moufflon in Rev Sci Tech 1992 Jun;11(2):491-537. Moufflin, a wild sheep from Corsica and Sardinia are maintained today at Besancon (15), Dundee (8), and Whipsnade (1), among many other places. The Scottish herd would be a prime candidate for one of the infected moufflon flocks. This might be confirmed by looking at the mammal inventory book published each year in Britain by the Federation of Zoological Gardens of Great Britain and Ireland.

Flock A, which varied in size to 12 animals, showed 5 scrapie-like deaths among 26 over the years, only 1 of which was confirmed by histopathology. When the flock was down to the last 2 animals, these were culled and found negative by histopathology. The flock was pastured and isolated from domestic sheep for 20 years but animals were shipped back and forth from other moufflon facilities.

In Flock B, 5 confirmed deaths occurred over 5 years in a flock containing 35 animals in 1992. This flock was also pastured; the index case occurred in a moufflon imported from Belgium.

BSE and British zoos

J Zoo Wildlife Medicine 22: 304-308 1991
Cunningham AA.
[Document on order. Rarely cited; apparently first article to spell out implications for conservation of zoo TSEs]

Origin and implications of bovine spongiform encephalopathy

Proc Soc Exp Biol Med 1996 Apr;211(4):306-22 
Narang H
This is an excellent review with deep references. The abstract mentions an affected tiger but not the text body. Two further eland, 2 additional pumas, and 2 more cheetahs died of TSE between the time of submission of this article (say 15 Jan 96) and 15 Apr 99.

Interesting factoids: Switzerland had 40 cases of BSE among a dairy population of 796,000 animals; scrapie was seen in 1 sheep in 1991, 2 sheep in 1993, and a goat in 1993. Denmark, Falkland Islands, and Oman imported their BSE cows from England; France fed local cows imported UK MBM. Spain had 24 million sheep, mainy older, compared to 40.8 in Great Britain, mainly under 1 year. Spain reports scrapie in 30 flocks and 1 flock of goats, all from Aragon; 32% of sheep carcasses are rendered. MBM goes to pigs, poultry, and trout.

The author states for the US that a single case of BSE was suspected , citing a paper of RF Marsh and GR Hartsough, 'Evidence that TME results from feeding infected cattle' in Murphy, BD, Hunter DB, eds, Toronto: Canada Mink Breeders Association. Proc IV Intern Congr Fur Animal Products, pp 204-207 1988.

MM Robinson of USDA, Pullman, Wa., is said to have estimated the adult cattle incidence of BSE in Wisconsin at 1 per 900,000 per year, using various assumption based on various TME outbreaks. The reference given is 'TSE research in the US' in Bradley R, Marchant B, editors. EEC Meeting 1993. Brussels: Proc Consultation BSE Scientific Vet Committee Commision European Communities, pp 261-270, 1994. This estimate agrees with the measured incidence in humans.

1994 Tyrell SEAC Report

Vet Rec. 1995 Mar 18 136(3) 254-5
Anonymous
Summarizes 1994 Tyrell SEAC Report:

"Control measures now in place are adequate to eliminate or reduce any risk to a ngligible level.... rhe risk from BSE to man is remote... satisfactorily protect human and animal health." The paper says no cats with FSE were born after the specified offal ban was extended to protect animals; MAFF has not released birth years of the 29 further UK cats known by April 1999.

The adjacent article describes a RSPCA-driven policy against using wild-caught primates in experimental research (unless licence applicant can establish 'exceptional and special justification' of course)

Spongiform encephalopathies in zoo animals.

Vet Rec. 1994 Nov 12;135(20):488.comment
Benbow G.  
[Document on order]
Vet Rec 1994 Oct 29;135(18):440  comment
Swainston J. 
[Document on order]

Recently described scrapie-like encephalopathies of animals: case definitions.

Research in Veterinary Science 53:1 1992
Wells GAH, McGill JS
[Document is on order. It reportedly has summary data on 6 cases of TSE in 5 zoo bovid species. The abstract at Medline has the tone of a primarily diagnostics review article.]

Spongiform encephalopathy in zoo ungulates: implications for translocation and reintroduction

Proceedings of the American Association of Zoo Veterinarians.  Oakland, California, pp 26-27 1992
Kirkwood JK, Cunningham AA
This is a 2 page sketch of a talk given at a meeting. It gives no new information but reiterates concerns about reintroductions because of loss of conservation value of the population, lack of tests and diagnosis in living animals, and variable incubation periods without overt clinical signs.

Spongiform encephalopathies in captive wild animals in Britain: epidemiological observations

EEC Meeting 1993
Bradley R, Marchant B, editors
Brussels: Proceedings Consultation BSE Scientific Vet Committee
Commision European Communities, pp 29-48 1993
Kirkwood JK, Cunningham AA authors
[This document is not yet available. Please fax to 541-484-0669 if you have it. ]

[TSE in bovids]

Bradley R, Matthews D
Revue Scientifique et Technique de l'Office International des Epizooities 11: 605 1992
[Document on order]

Ultrastructural features of spongiform encephalopathy

Acta Neuropathol (Berl) 1992;84(5):559-69
Jeffrey M, Scott JR, Williams A, Fraser H
A paper strictly focused on histopathology of formalin fixed brain of kudu and nyala transmitted successfully to mice, as compared to authentic fixed and fresh BSE transmitted to mice. The results were very similar and different from scrapie, though no such control was used here. This supports transmission of BSE to zoo animals through feed.

Spongiform encephalopathy in pigs.

Done JT.   
Vet Rec. 1990 Nov 10;127(19):484.
The author makes a plea for veterinarians not to report suspicious signs in pigs fed MBM to the district veterinary officer. Instead, they should wait for MAFF to make TSE in pigs notifiable: "I am not convinced that 'it is mportant that vetrinary surgeons should remain vigilant...'

MPs attack secrecy on zoo animals' BSE

Vet Rec 1990 Apr 7;126(15):322 
no author given
A Labour motion tabled in the Commons expresses concern over secrecy srrounding zoo animal BSE, saying this is of great concern to all involved in wildlife conservation. It urges the MAFF to act to ensure that BSE in zoo stock be made an internationally notifieable disease, to be registr3d with WHO, IUCN, and the International Union of Directors of Zoological Gardens.

The motion called for an immediate ban on movement of all potentially at-risk species between collections, both nationally and internationally, pending more information, and an end to secrecy.

GM Benbow responded to this in the 28 Apr 1990 Vet Record 126(18):441, saying as BVA representative to the National Federation of Zoological Gardens of Grean Britain, he had sent a report to all members of the FZG and all facilities keeping ungulates in May 1989> After 2 cases were confirmed at the London Zoo, further recommendations were made about the risk of exporting animals or using them for reintroduction programs. This report was also sent to all members of the FZG and all facilities keeping ungulates in early 1990. Benbow is indignant about the alleged "secrecy" yet his British Veterinary Association maintained tight secrecy about affected zoos: not a single facility beyond the London Zoo and the associated Whipsnade and rarely Marwell is ever named in 25 publications over 10 years in their flagship journal, Vet. Record.

Secrecy, coupled with continuing exports, creates a very difficult situation for foreign zoos.