State Department of Health. Dr. Britt is Former Epidemic Intellig- ence Service Officer, Field Services Branch,Epidemiology Program, located in the Oregon State ...
Skunks are now the most frequently reported rabid animal in the United States and the major source of human rabies. The skunk's adaptability to living near man and its use as a pet increase the potential for human exposure to rabies. Since 1958, reports of 131 rabid or possibly rabid pet skunks have been received by the Center for Disease Control. One hundred eighty-two humans are known to have received bites from these skunks. The most recent episode involved 366 persons and 69 possibly rabid skunks. The ecology of rabies in wild skunks indicates that these animals will continue to be a threat to man in the near future. However, control of breeding, quarantine, and vaccination could prevent the sale of rabid pet skunks.
Skunk Rabies: The Risk to Manor Never Trust a Skunk Introduction In the United States since 1960, skunks have become the most frequently reported rabid animal and the most common source of human rabies."2 Although due in large part to successful reduction of domestic rabies, the predominance of skunk rabies also reflects an epizootic of wildlife rabies which began several decades ago.3'4 Along with the resurgence of feral skunk rabies has come another problem: rabies in pet skunks. Although all of the reported cases of skunkassociated human rabies have been the result of bites by wild animals, human exposures to rabid pet skunks are frequently reported to the Center for Disease Control. This paper presents details of a wide reaching episode involving 366 persons and 69 possibly rabid pet skunks and reviews the present problem of rabies in wild and pet skunks.
Pet Skunk Rabies: Pacific Northwest 1970 On July 17, 1970, a Seattle woman was bitten on the arm and leg by her pet striped skunk (Mephitis mephitis), which had become irritable and ferocious in the preceding week. The skunk was shown to be rabid by the fluorescent antibody test.5 The woman was treated with a 23-dose course of duck embryo vaccine plus equine antirabies serum, and has remained well. The rabid skunk was one of 69 striped skunks caught in the wild by a skunk farmer in Oregon, and sold in Portland and Seattle. After capture, all the skunks were mixed with each other, so all could have contracted rabies. The owners of each of the 69 skunks were located by the end of July with the help of public health personnel and radio, television, and newspaper coverage in Oregon, Washington, California, and Canada. Fifty-one skunks were recovered and examined in the laboratory; 50 proved negative, and one (mentioned above) was positive for rabies by the fluorescent antibody test. The other 18 skunks were lost or dead and therefore unavailable for laboratory examination. Since those skunks might have been rabid, 14 persons bitten by them received post-exposure rabies prophylaxis. 1080
AJPH DECEMBER, 1973, Vol. 63, No. 12
Michael A. W. Hattwick, M.D.; Edgar K. Marcuse, M.D.; Michael R. Britt, M.D.; Reynoldson B. Zehmer, D.V.M.; Russell W. Currier, 11, D.V.M.; and William N. Elledge, M.D. Individual interviews with the owners of each skunk revealed that 366 persons had been in contact with the 69 skunks (Table 1). Eighty of these had been bitten, The risk of being bitten was highest among the members of the immediate household; but many casual contacts were also bitten. (Table 2) The one proven rabid skunk bit the only person it had access to, its owner. Fifty-eight per cent of the 36 skunks sold in Oregon bit one or more persons. Sixteen per cent of all contacts of these skunks and 21 per cent of the members of the household in which the skunks were kept were bitten. Members of households in which at least one person was bitten had an even higher incidence of bites, 40 per cent having been bitten. Even within the pet store prior to sale, 9 per cent of the persons contacting the skunks were bitten. Non-household contacts of the pet skunks had a similar risk of being bitten, 13 per cent receiving bites. An estimate of the number of pet skunks present in the Portland and Seattle at cas -was based on information supplied by the pet stores and veterinarians of these cities. Twenty-one of the 57 pet stores in Portland and Seattle sold skunks. One hundred eighty-two skunks were sold in 1969 and 149 in 1970, with ten pet shops accounting for over 95 per cent of the sales. The source of the skunks for the retail market varied widely with approximately two-thirds of the skunks supplied by two skunk farmers in Oregon and Washington, and a national supplier from the Midwest. The skunks sold in pet stores were descented by the suppliers prior to delivery to the stores. In addition to the skunks sold in pet stores, some skunks are locally captured in the wild by private individuals. In the Portland area, four veterinary hospitals descented approximately 74 such skunks each year for private individuals. By adding the number of skunks descented to the number of skunks sold in retail pet shops, we estimate that at least 180 pet skunks are introduced into
Table 1-Persons In Contact With or Bitten by Possibly Rabid Pet Skunks: Washington and Oregon, 1970
Exposure to
Contacts Persons Bitten No. of Total House Total House skunks persons hold Animals persons hold
Proven rabid skunk Proven not rabid skunk Unexamined skunk Skunks prior to sale
1 50 18
1 259 49 57
1 118 24
0 45 8
1 60 14 5
1 26 4
Total Washington Total Oregon
24 45
65 301
ND 142
17 36
31 49
ND 30
Total both states
69
366
142*
53
80
30*
ND'Not Determined 'Oregon data only
Table 2-Summary of Pet Skunk Behavior Pacific Northwest 1970 Total bite rate
-
Persons bitten Human contacts
=
80 = 22% 366
Oregon total bite rate*
-
Persons bitten Human contacts
=
49 301
Non-household bite rate*
=
Visitors bitten Persons visiting
=
14 = 13% 112
Household bite rate*
-
Members of household bitten People in household
=
30 = 21% 142
_
30 = 40% 75
=
5 = 57
=
21 36
Bite rate, households of biting skunk* Pet store bite rate
-
Persons bitten Contacts prior to sale
= 16%
9%
Percentage of skunks which bit one or more persons
= 58%
*Oregon data only, based on individual interviews.
the Portland area alone each year. This estimate is probably low, because additional skunks may be caught and descented by private individuals.
Surveillance of Pet Skunk Rabies Including the above episode, 32 cases of confirmed rabies in pet skunks have been reported to the CDC since 1958, usually involving at least one bitten human ([able 3). An additional 99 skunks were reported as possibly rabid, without laboratory confirmation. In all cases where the species was specified, it was the common striped skunk (Mephitis mephitis). A total of 117 persons required postexposure prophylaxis against rabies because of bites by these rabid or possibly rabid skunks. The skunk had been in the
household as a pet for as long as 18 months in one case prior to developing rabies. Many of these skunks were purchased in retail pet shops which had obtained them from wholesale pet dealers. In several the animal was shipped or carried from one state to another. In all probability the rabid animals were exposed to rabies in the wild prior to capture, as in the episode described above. Understanding pet-skunk rabies, therefore, requires awareness of the problem in wildlife.
Feral Rabies Surveillance of wildlife rabies is based on data submitted to the Center for Disease Control from the various states. Figure 1 compares the number of rabid skunks with all rabid SKUNK RABIES
1081
Table 3-Reported Rabies in Pet Skunks 1959-1970 No. Skunks confirmed rabid
No. Human Source of skunk
Length of* contact
Reference
LC Pet shop in Ky. LC
2 mos.
15
1 wk. 7 mos.
16 17
21 2
NR LC
NR 3 wks.
Unpublished 18
5 4
5 4
NR NR
3
10
10
Pet shop
NR
Unpublished
4
3
8
8
NR
NR
Unpublished
Illinois
1
1
1
1
NR
NR
Unpublished
Michigan
3
2
5
5
NR
Unpublished
Illinois
3
3
10
10
Pet shop in Iowa Pet shop in Iowa
NR
Unpublished
Tennessee
1
1
1
1
NR
8
Illinois
2
2
3
3
NR
Unpublished
Kentucky
7 4
2
Georgia
1
10 4
10 2
NR 2 wks.
Unpublished 19
Washington Illinois
1 1
1 1
20 2
11 2
LC Pet shop in Okla. Pet shop LC
4 mos. NR
20 Unpublished
OregonWashington Illinois
69 1
1 1
366 2
80 2
Pet shop LC
2 mos. NR
Unpublished
131
32
484
182
Total skunks
contacts reported
No. Humans bitten
Year
State
1959 1960
Louisiana Alabama
4 7
1 2
1 7
0
Washington
2
1
2
1
1961
Michigan Arkansas
8 2
NR 1
21 2
1962
Ohio Michigan
5 1
5 NR
1963
Kentucky
5
1964
Michigan
1965
1966
1968
1969
1970
Totals
4
3 wks.- 18 mos. 7 NR Unpublished
Pet dealer in Fla. NR
NRzNot reported LC&Locally captured skunk *Duration skunk was kept as a pet prior to onset of rabies.
Table 4-Skunk Rabies Prevalence Selected Studies
State
Year
Oregon Illinois Arizona
1970 1959-60 1970 1960-62
Illinois Illinois 4-5/61 Ohio 1962 California 1950-63 California 1964-68 1969 California 1082
Known epizootic activity
Associated human case
No No Yes? Yes Peak period Yes Yes Yes Yes
No No Yes No No No Yes No No
AJPH DECEMBER, 1973, Vol. 63,
No. 12
No. examined
No. positive
47 122 290 124 18 502
0 0 3 20 10 311
1,988 3,003 1,045
1,028 927 245
% positive 0 0 1 16.1 55 62 51.7 30.9 24
Technique Trapping Trapping Trapping Trapping Trapping Various Various Various Various
animals reported to the CDC from 1946 through 1970. Skunks have been the most frequently reported rabid animal since 1960, making up approximately one-third of all rabid animals and one-half of the wild rabid animals reported each year. Distribution of rabid skunks is nationwide with concentration in the mid-continent and California (Figure 2). Since these data are based on animals submitted to health departments for laboratory examination, they give only minimum estimates of rabies incidence and distribution. The prevalence of rabies among wild skunks may be approximated roughly by the percentage of all skunks submitted to a diagnostic laboratory which are found to be rabid (Table 4). In states where rabies is not epizootic, this percentage is rarely over one per cent, but with epizootic activity it may exceed 60 per cent.6'7 These data may tend to overestimate the prevalence of rabies since animals frequently are submitted because of abnormal behavior. However, more precise estimates of the true prevalence of skunk rabies obtained by intensive trapping campaigns in relatively welldefined animal populations confirm these general estimates.6'8'9
Figure 1-Animal Rabies, United States, 1946-1970 11,000 --
10.000-
--
ALL ANIMALS ALL WILD ANIMALS SKUNKS
9.000-
8.0001 7,000
5,000-
Discussion Human rabies in the United States has been reduced from an average of 30 cases a year in the 1940s to less than two cases a year since 1960, largely as a result of rabies control in cats and dogs. Further reduction in human rabies requires attention to the wildlife vectors that are currently causing human exposure. ' The skunk has become the major problem at the present time. When rabid, skunks are a particularly threatening source of human rabies for several reasons. Rabies virus may be excreted in skunk saliva as much as 18 days prior to death, and the titer of rabies virus in skunk saliva is significantly higher than in fox or dog saliva.'0 Thirty-six to 83 per cent of skunks that die of rabies have virus in the salivary glands, although not all of these have virus in the saliva. 11, 12, 13The prolonged period of virus secretion and the high titers of rabies virus in saliva combine to enhance the risk of rabies from skunk bites. In addition, the ecology of skunks make them a particularly likely source of human exposure to rabies. The majority of rabid skunks are caught in the second quarter of the year, a time when human activity outdoors is also high.6' 7 Usually nocturnal and shy, skunks when rabid may be seen in daylight, and attack rather than run away. At night they may enter campers' tents and sleeping bags and bite without provocation. ' Rabid skunks often do not scent, eliminating another factor that might reduce human exposure. Even in the wild, skunks tolerate close proximity to man, often living near houses or suburban homes. Moreover, their tolerance for man is reciprocated, and the skunk has been brought into the home as one of the more common exotic pets.'4 All of these factors combine to enhance the likelihood of human exposure to rabies. Controlling zoonotic rabies in wild skunks is difficult. The standard technique relies on population reduction by wild trapping or poisoning with strychnine-laced egg bait. These techniques are of only limited effectiveness. Moreover, application of these techniques requires knowledge of the areas of high rabies activity, and wildlife rabies surveillance programs give only a rough indication of where these areas are. Even in areas in which high rabies prevalence has been demonstrated, population reduction only transiently alleviates the local skunk rabies. There is no realistic likelihood that the prevalence or distribution of rabies in feral skunks will be significantly altered in the near future.
4,000-
3.000
\
"I 2.000
x
S
v
1,000-
oL, 1945
'-I~~oo I-~~~~, '-I/ /
-
s-
/
i
"\%.Ol/ '50
'66
;55
'65
70
YEAR
On the other hand, we can control rabies in skunks destined for use as pets with current techniques. In view of the inability to control rabies in feral skunks, no wild trapped skunk can be considered rabies-free. Moreover, the incubation period of rabies in skunks varies from 14 to at least 177 days,'0 so no wild trapped skunks should be released for use as a pet without a minimum of six months' quarantine. Since the market for pet skunks is largely limited to the sale of baby skunks, this would require that the mother skunk be in captivity for at least six months before giving birth to a skunk that will be sold for use as a pet. All susceptible pets, including skunks, should be vaccinated against rabies. In the case of skunks, only inactivated rabies vaccines should be used. Vaccination of skunks with live rabies vaccines has been associated with clinical rabies in the animal confirmed by laboratory examination of the animal's brain. In such a case it may be impossible to tell whether the skunk acquired rabies in the wild or as a result of the modified live virus vaccine.9 Effective regulations limiting the sale of skunks to vaccinated offspring of animals not captured within the previous six months should reduce the risk of human exposure to rabies. If skunk bites caused only pain, local infection, and tetanus, the above data would make one wonder whether keeping skunks as pets makes sense. Since skunks not only can but often do get rabies, and since we still have no reliable SKUNK RABIES
1083
Figure 2-Skunk Rabies, United States, 1961-1970
AVERAGE NUMBER REPORTED ANNUALLY: *w| LC]|
NONE R.EPORTED
Y
E 1-10 ~~~~I1
9 ~~~~~~~~~~10-tOO
1to-zoo
post-exposure treatment for rabies in man, there is a powerful argument for prohibiting skunks as pets. Some states have already adopted such a ban. Whether available data justify legislation prohibiting the keeping of pet skunks is open to question. Raising rabies-free skunks is theoretically possible, with a combination of quarantine, domestic breeding, and vaccination. If such measures cannot be assured or are impractical, the risk of the animal's having rabies will be real, and selling such animals in retail pet stores should be prohibited.
References 1. Hattwick, M. A. W.; Hochberg, F. H.; Landrigan, P. J.; and Gregg, M. B. Skunk-associated human rabies, JAMA, 222:44-47, 1972. 2. Center for Disease Control: Zoonoses Surveillance, Rabies Annual Summary 1970 (Atlanta). 3. Johnson, H. N. Rabies. In: Viral and Rickettsial Infections of Men. Edited by Horsfall and Tamm, Philadelphia: J. B. Lippincott and Co., 1%5, pp. 814-840. 4. Johnson, H. N. General epizootology of rabies. Rabies Proceedings of Working Conference on Rabies. Tokyo, Oct 12-14, 1970, Univ. Tokyo Press, 1971. 5. Goldwasser, R. A. and Kissling, R. E. Fluorescent antibody staining of street and fixed rabies virus antigens. Proc. Soc. Exp. Biol. (NY) 98:219-223, 1958. 6. Verts, B. J. Rabies. In the Biology of the Striped skunk. Urbana: Univ. of Illinois Press, 1%7, pp. 144-190. 7. Schnurrenberger, P.; Beck, J. R.; and Pedan, D. Skunk rabies in Ohio. Public Health Rep. 79:161-166, 1964. 1084
AJPH DECEMBER, 1973, Vol. 63, No. 12
8. Center for Disease Control: Zoonoses Surveillance, Rabies Annual Summary 1968 (Atlanta). 9. Center for Disease Control: Zoonoses Surveillance, Rabies Annual Summary 1969 (Atlanta). 10. Parker, R. L. and Wilsnack, R. E. Pathogenesis of skunk rabies virus: Quantitation in skunks and foxes. Amer. J. Vet. Res. 116:33-38, 1966. 11. Wilsnack, R. E. and Parker, R. L. Pathogenesis of skunk rabies virus: Rabies inhibiting substance. Amer. J. Vet. Res. 27:39-43, 1966. 12. Sikes, R. K. Pathogenesis of rabies in wildlife. I. Comparative effect of varying doses of rabies virus inoculated into foxes and skunks. Amer. J. Vet. Res. 23:1041-1047, 1962. 13. Carski, J. R.; Wilsnack, R.; and Sikes, R. K. Pathogenesis of rabies in wildlife. II. Fluorescent antibody studies. Amer. J. Vet. Res. 23:1048-1052, 1962. 14. Hume, C. How to raise and train a skunk. TFH Publications, Inc., Jersey City, New Jersey, 1967. 15. Center for Disease Control: Veterinary Public Health Notes, Nov. 1959, p. 12 (Atlanta). 16. Center for Disease Control: Veterinary Public Health Notes, Aug. 1960, p. I (Atlanta). 17. Center for Disease Control: Veterinary Public Health Notes, Mar. 1960, p. 12 (Atlanta). 18. Center for Disease Control: Veterinary Public Health Notes, Dec. 1961, pp. 1-2 (Atlanta). 19. Center for Disease Control: Veterinary Public Health Notes, Sept. 1969, p. 1 (Atlanta). 20. Center for Disease Control: Morbidity and Mortality Weekly Rep 18(40): 347, 4 Oct 1969 (Atlanta). Dr. Hattwick is Chief, Respiratory and special Pathogens Unit, Viral Diseases Branch, Epidemiology Program, CDC, Atlanta, Georgia.
Dr. Marcuse is former Epidemic Intelligence Service Officer, Field Services Branch, Epidemiology Program, located in the Washington State Department of Health. Dr. Britt is Former Epidemic Intelligence Service Officer, Field Services Branch, Epidemiology Program, located in the Oregon State Department of Health. Dr. Zehmer is Epidemic Intelligence Service Officer, Office of Veterinary Public
Health, Services, Epidemiology Program, CDC, Atlanta, Georgia. Dr. Currier is Veterinary Epidemiologist, CDC, located in the Alabama State Department of Health, and Dr. Elledge is Epidemic Intelligence Service Officer, Field Services Branch, Epidemiology Program, located in the Washington State Department of Health. This paper was submitted for publication in November, 1971.
American Public Health Association NEW 40-YEAR MEMBERS-1973 Dewitt S. Abell, Beacon, NY (Environment) Anna M. Baetjer, D.Sc., Baltimore, MD (Occupational Health and Safety) Chester S. Bowers, M.P.H., Myrtle Beach, SC (Public Health Education) W. Arkell Browne, M.D., M.P.H., New Bern, NC (Health Administration) Harold D. Chope, M.D., Dr.P.H., Belmont, CA (Health Administration) Florence C. Drach, Monroe, LA (Laboratory) Vivian V. Drenckhahn, M.P.H., Minneapolis, MN (Public Health Education) Roy F. Feemster, M.D., Dr.P.H., Amherst, NH (Laboratory) Franklin M. Foote, M.D., Dr.P.H., Newington, CT (Health Administration) Grace Frauens, R.N., Pleasant Hill, TN (Public Health Nursing) Clarissa Gibson, Kensington, MD (Public Health Nursing) G. Howard Gowen, M.D., Gaithersburg, MD (Epidemiology) Hattie Hemschemeyer, R.N., Bethlehem, CT (Public Health Nursing) Edward C. Holmblad, M.D., Chicago, IL (Occupational Health and Safety) Hugh R. Leavell, M.D., Dr.P.H., Richmond, VA (Public Health Education) Bernard J. McMorrow, Honolulu, HI (Environment) Charles W. Meinershagen, M.D., M.P.H., Jefferson City, MO (Health Administration) Margaret M. Nicholson, M.D., Washington, DC (Maternal and Child Health) Ella Oppenheimer, M.D., Washington, DC (Maternal and Child Health) Donna Pearce, R.N., Knoxville, TN (Public Health Nursing) George St. J. Perrott, Bethesda, MD (Medical Care) Ruth R. Puffer, Dr.P.H., Lynn, MA (Statistics) Mervyn B. Starnes, D.V.M., M.P.H., Dallas, TX (Veterinary Public Health) Roger W. Truesdail, Ph.D., Los Angeles, CA (Food and Nutrition) Israel Weinstein, M.D., Brooklyn, NY (Public Health Education) Arthur W. Wright, M.D., Albany, NY (Laboratory)
SKUNK RABIES
1085
