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The Mouse Who Couldn't Stop Washing: Pathologic Grooming in Animals and Humans

Published online by Cambridge University Press:  07 November 2014

Jamie D. Feusner ,
Emily Hembacher  and
Katharine A. Phillips
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Abstract

The basic science literature is replete with descriptions of naturally occurring or experimentally induced pathological grooming behaviors in animals, which are widely considered animal models of obsessive-compulsive disorder (OCD). These animal models rely largely on observed similarities between animal behaviors and human OCD behaviors, and on studies of animal pathological grooming disorders that respond to serotonin enhancing drugs. However, current limitations in assessment of complex cognition and affect in animals precludes the field's ability to match the driving primary processes behind observable phenomenology in animal “OCD” with human behavioral disorders. We propose that excessive grooming behaviors in animals may eventually prove to be equally, or possibly more relevant to, other conditions in humans that involve pathological grooming or grooming-like behaviors, such as trichotillomania, body dysmorphic disorder, olfactory reference syndrome, compulsive skin-picking, and onychophagia. Research is needed to better understand pathological grooming behaviors in both humans and animals, as animal models have the potential to elucidate pathogenic mechanisms and inform the treatment of these psychiatric conditions in humans.

Type
Review Article
Information
CNS Spectrums , Volume 14 , Issue 9 , September 2009 , pp. 503 - 513
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

1.Korff, S, Harvey, BH. Animal models of obsessive-compulsive disorder: rationale to understanding psychobiology and pharmacology. Psychiatr Clin North Am. 2006;29:371–390.CrossRefGoogle ScholarPubMed
2.Welch, JM, Lu, J, Rodriguiz, RM, et al.Cortico-striatal synaptic defects and OCD-like behaviours in Sapap3-mutant mice. Nature. 2007;448:894–900.CrossRefGoogle ScholarPubMed
3.Stein, DJ, Shoulberg, N, Helton, K, Hollander, E. The neuroethological approach to obsessive-compulsive disorder. Compr Psychiatry. 1992;33:274–281.CrossRefGoogle ScholarPubMed
4.Lenane, MC, Swedo, SE, Rapoport, JL, Leonard, H, Sceery, W, Guroff, JJ. Rates of Obsessive Compulsive Disorder in first degree relatives of patients with trichotillomania: a research note. J Child Psychol Psychiatry. 1992;33:925–933.CrossRefGoogle ScholarPubMed
5.Bohne, A, Keuthen, N, Wilhelm, S. Pathologic hairpulling, skin picking, and nail biting. Ann Clin Psychiatry. 2005;17:227–232.CrossRefGoogle ScholarPubMed
6.Chosak, A, Marques, L, Greenberg, JL, Jenike, E, Dougherty, DD, Wilhelm, S. Body dysmorphic disorder and obsessive-compulsive disorder: similarities, differences and the classification debate. Expert Rev Neurother. 2008;8:1209–1218.CrossRefGoogle ScholarPubMed
7.Jones, I, Blackshaw, JK. An evolutionary approach to psychiatry. Aust N Z J Psychiatry. 2000;34:8–13.CrossRefGoogle ScholarPubMed
8.Hewson, CJ, Luescher, UA, Parent, JM, Conlon, PD, Ball, RO. Efficacy of clomipramine in the treatment of canine compulsive disorder. J Am Vet Med Assoc. 1998;213:1760–1766.CrossRefGoogle ScholarPubMed
9.Benson, J, Greaves, W, O'Donnell, M, Taglialatela, J. Evidence for symbolic language processing in a Bonobo (Pan paniscus). Journal of Consciousness Studies. 2002;9:33–56.Google Scholar
10.Panksepp, J. Affective consciousness: Core emotional feelings in animals and humans. Conscious Cogn. 2005;14:30–80.CrossRefGoogle Scholar
11.Sachs, BD. The development of grooming and its expression in adult animals. Ann NY Acad Sci. 1988;525:1–17.CrossRefGoogle ScholarPubMed
12.Spruijt, BM, van Hooff, JA, Gispen, WH. Ethology and neurobiology of grooming behavior. Physiol Rev. 1992;72:825–852.CrossRefGoogle ScholarPubMed
13.Moon-Fanelli, AA, Dodman, NH, O'Sullivan, RL. Veterinary models of compulsive self-grooming: parallels with trichotillomania. In: Stein, DJ, Christenson, GA, Hollander, E, eds. Trichotillomania. Arlington, VA: American Psychiatric Publishing, Inc; 1999:63–92.Google Scholar
14.Gardner, R. Psychiatric syndromes as infrastructure for intraspecific communications. In: Chance, MRA, Omark, DR, eds. Social Fabrics of the Mind. London, UK: Lawrence Erlbaum Associates; 1988.Google Scholar
15.Gould, JL. Ethology: The Mechanisms and Evolution of Behavior. New York, NY: W.W. Norton: 1982.Google Scholar
16.Zampiga, E, Hoi, H, Pilastro, A. Preening, plumage reflectance and female choice in budgerigars. Ethology Ecology & Evolution. 2004;16:339–349.CrossRefGoogle Scholar
17.Eckstein, RA, Hart, BL. The organization and control of grooming in cats. Appl Anim Behav Sci. 2000;68:131–140.CrossRefGoogle ScholarPubMed
18.Hart, BL, Powell, KL. Antibacterial properties of saliva: role in maternal periparturient grooming and in licking wounds. Physiol Behav. 1990;48:383–386.CrossRefGoogle ScholarPubMed
19.Gouzoules, S, Gouzoules, H, Smuts, BB, et al.Kinship. In: Smuts, BB, Cheney, DL, Seyfarth, RM, Wrangham, RW, Struhsaker, TT, eds. Primate societies. Chicago, IL: University of Chicago Press; 1987:299–305.Google Scholar
20.Sade, DS. Some Aspects of Parent-Offspring and Sibling Relations in a Group of Rhesus Monkeys, with a Discussion of Grooming. Am J Phys Anthropol. 1965;23:1–17.CrossRefGoogle Scholar
21.Cromwell, HC, Berridge, KC. Implementation of action sequences by a neostriatal site: a lesion mapping study of grooming syntax. J Neurosci. 1996;16:3444–3458.CrossRefGoogle Scholar
22.Berridge, KC. Progressive degradation of serial grooming chains by descending decerebration. Behav Brain Res. 1989;33:241–253.CrossRefGoogle ScholarPubMed
23.Strazielle, C, Lalonde, R. Grooming in Lurcher mutant mice. Physiol Behav. 1998;64:57–61.CrossRefGoogle ScholarPubMed
24.Summerfeldt, LJ, Richter, MA, Antony, MM, Swinson, RP. Symptom structure in obsessive-compulsive disorder: a confirmatory factor-analytic study. Behav Res Ther. 1999;37:297–311.CrossRefGoogle ScholarPubMed
25.Leckman, JF, Grice, DE, Boardman, J, et al.Symptoms of obsessive-compulsive disorder. Am J Psychiatry. 1997;154:911–917.Google ScholarPubMed
26.Phillips, KA, Diaz, SF. Gender differences in body dysmorphic disorder. J Nerv Ment Dis. 1997;185:570–577.CrossRefGoogle ScholarPubMed
27.Phillips, KA. The Broken Mirror. New York, NY: Oxford University Press; 2005.Google Scholar
28.Phillips, KA, Gunderson, C, Gruber, U, Castle, D. Delusions of body malodour; the olfactory reference syndrome. In: Brewer, W, Castle, D, Pantelis, C, eds. Olfaction and the Brain. New York, NY: Cambridge University Press; 2006.Google Scholar
29.Diefenbach, GJ, Mouton-Odum, S, Stanley, MA. Affective correlates of trichotillomania. Behav Res Ther. 2002;40:1305–1315.CrossRefGoogle ScholarPubMed
30.Hayes, SL, Storch, EA, Berlanga, L. Skin picking behaviors: An examination of the prevalence and severity in a community sample. J Anxiety Disord. 2009;23:314–319.CrossRefGoogle Scholar
31.Matthews, PC. Pathological habit disorder. Can J Psychiatry. 1988;33:826–829.CrossRefGoogle ScholarPubMed
32.Diagnostic and Statistical Manual of Mental Disorders. 4th ed, text rev. Washington, DC: American Psychiatric Association; 2000.Google Scholar
33.Mataix-Cols, D, Rosario-Campos, MC, Leckman, JF. A multidimensional model of obsessive-compulsive disorder. Am J Psychiatry. 2005;162:228–238.CrossRefGoogle ScholarPubMed
34.Gilbert, AR, Mataix-Cols, D, Almeida, JR, et al.Brain structure and symptom dimension relationships in obsessive-compulsive disorder: a voxel-based morphometry study. J Affect Disord. 2008;109:117–126.CrossRefGoogle ScholarPubMed
35.Mataix-Cols, D, Wooderson, S, Lawrence, N, Brammer, MJ, Speckens, A, Phillips, ML. Distinct neural correlates of washing, checking, and hoarding symptom dimensions in obsessive-compulsive disorder. Arch Gen Psychiatry. 2004;61:564–576.CrossRefGoogle ScholarPubMed
36.Hill, RA, McInnes, KJ, Gong, EC, Jones, ME, Simpson, ER, Boon, WC. Estrogen deficient male mice develop compulsive behavior. Biol Psychiatry. 2007;61:359–366.CrossRefGoogle ScholarPubMed
37.Faravelli, C, Salvatori, S, Galassi, F, Aiazzi, L, Drei, C, Cabras, P. Epidemiology of somatoform disorders: a community survey in Florence. Soc Psychiatry Psychiatr Epidemiol. 1997;32:24–29.CrossRefGoogle ScholarPubMed
38.Phillips, KA, Taub, SL. Skin picking as a symptom of body dysmorphic disorder. Psychopharmacol Bull. 1995;31:279–288.Google ScholarPubMed
39.O'Sullivan, RL, Phillips, KA, Keuthen, NJ, Wilhelm, S. Near-fatal skin picking from delusional body dysmorphic disorder responsive to fluvoxamine. Psychosomatics. 1999;40:79–81.CrossRefGoogle ScholarPubMed
40.Otto, MW, Wilhelm, S, Cohen, LS, Harlow, BL. Prevalence of body dysmorphic disorder in a community sample of women. Am J Psychiatry. 2001;158:2061–2063.CrossRefGoogle Scholar
41.Rief, W, Buhlmann, U, Wilhelm, S, Borkenhagen, A, Brahler, E. The prevalence of body dysmorphic disorder: a population-based survey. Psychol Med. 2006;36:877–885.CrossRefGoogle ScholarPubMed
42.Phillips, KA, Coles, ME, Menard, W, Yen, S, Fay, C, Weisberg, RB. Suicidal ideation and suicide attempts in body dysmorphic disorder. J Clin Psychiatry. 2005;66:717–725.CrossRefGoogle ScholarPubMed
43.Veale, D, Boocock, A, Gournay, K, et al.Body dysmorphic disorder. A survey of fifty cases. Br J Psychiatry. 1996;169:196–201.CrossRefGoogle ScholarPubMed
44.Hollander, E. Obsessive-compulsive spectrum disorders: an overview. Psychiatric Annals. 1993;23:355–358.CrossRefGoogle Scholar
45.Mataix-Cols, D, Pertusa, A, Leckman, JF. Issues for DSM-V: how should obsessive-compulsive and related disorders be classified? Am J Psychiatry. 2007;164:1313–1314.CrossRefGoogle ScholarPubMed
46.Frost, RO, Steketee, G. Perfectionism in obsessive-compulsive disorder patients. Behav Res Ther. 1997;35:291–296.CrossRefGoogle ScholarPubMed
47.Buhlmann, U, Etcoff, NL, Wilhelm, S. Facial attractiveness ratings and perfectionism in body dysmorphic disorder and obsessive-compulsive disorder. J Anxiety Disord. 2008;22:540–547.CrossRefGoogle ScholarPubMed
48.Stein, DJ, Le Roux, L, Bouwer, C, Van Heerden, B. Is olfactory reference syndrome an obsessive-compulsive spectrum disorder?: two cases and a discussion. J Neuropsychiatry Clin Neurosci. 1998;10:96–99.CrossRefGoogle ScholarPubMed
49.Christenson, GA, Pyle, RL, Mitchell, JE. Estimated lifetime prevalence of trichotillomania in college students. J Clin Psychiatry. 1991;52:415–417.Google ScholarPubMed
50.Christenson, GA, Mackenzie, TB, Mitchell, JE. Characteristics of 60 adult chronic hair pullers. Am J Psychiatry. 1991;148:365–370.Google ScholarPubMed
51.Grant, JE, Odlaug, BL, Potenza, MN. Addicted to hair pulling? How an alternate model of trichotillomania may improve treatment outcome. Harv Rev Psychiatry. 2007;15:80–85.CrossRefGoogle ScholarPubMed
52.Keuthen, NJ, Deckersbach, T, Wilhelm, S, et al.Repetitive skin-picking in a student population and comparison with a sample of self-injurious skin-pickers. Psychosomatics. 2000;41:210–215.CrossRefGoogle Scholar
53.Wilhelm, S, Keuthen, NJ, Deckersbach, T, et al.Self-injurious skin picking: clinical characteristics and comorbidity. J Clin Psychiatry. 1999;60:454–459.CrossRefGoogle ScholarPubMed
54.Arnold, LM, Auchenbach, MB, McElroy, SL. Psychogenic excoriation. Clinical features, proposed diagnostic criteria, epidemiology and approaches to treatment. CNS Drugs. 2001;15:351–359.CrossRefGoogle ScholarPubMed
55.Diefenbach, GJ, Tolin, DF, Meunier, S, Worhunsky, P. Emotion regulation and trichotillomania: a comparison of clinical and nonclinical hair pulling. J Behav Ther Exp Psychiatry. 2008;39:32–41.CrossRefGoogle ScholarPubMed
56.Wells, JH, Haines, J, Williams, CL. Severe morbid onychophagia: the classification as self-mutilation and a proposed model of maintenance. Aust N Z J Psychiatry. 1998;32:534–545.CrossRefGoogle Scholar
57.Man, J, Hudson, AL, Ashton, D, Nutt, DJ. Animal models for obsessive-compulsive disorder. Curr Neuropharmacol. 2004;2:169–181.CrossRefGoogle Scholar
58.Owen, LN. Canine lick granuloma treated with radiotherapy. J Small Anim Pract. 1989;8:454–456.CrossRefGoogle Scholar
59.Shumaker, AK, Angus, JC, Coyner, KS, Loeffler, DG, Rankin, SC, Lewis, TP. Microbiological and histopathological features of canine acral lick dermatitis. Vet Dermatol. 2008;19:288–298.CrossRefGoogle ScholarPubMed
60.Phillips, KA, Hollander, E. Treating body dysmorphic disorder with medication: evidence, misconceptions, and a suggested approach. Body Image. 2008;5:13–27.CrossRefGoogle Scholar
61.Bloch, MH, Landeros-Weisenberger, A, Dombrowski, P, et al.Systematic review: pharmacological and behavioral treatment for trichotillomania. Biol Psychiatry. 2007;62:839–846.CrossRefGoogle ScholarPubMed
62.Virga, V. Behavioral dermatology. Vet Clin North Am Small Anim Pract. 2003;33:231–251, v-vi.CrossRefGoogle ScholarPubMed
63.Overall, KL, Dunham, AE. Clinical features and outcome in dogs and cats with obsessive-compulsive disorder: 126 cases (1989-2000). J Am Vet Med Assoc. 2002;221:1445–1452.CrossRefGoogle ScholarPubMed
64.Rosskopf, WJ Jr., Woerpel, RW. Pet avian conditions and syndromes of the most frequently presented species seen in practice. Vet Clin North Am Small Anim Pract. 1991;21:1189–1211.CrossRefGoogle ScholarPubMed
65.Bordnick, PS, Thyer, BA, Ritchie, BW. Feather picking disorder and trichotillomania: an avian model of human psychopathology. J Behav Ther Exp Psychiatry. 1994;25:189–196.CrossRefGoogle ScholarPubMed
66.van Hierden, YM, de Boer, SF, Koolhaas, JM, Korte, SM. The control of feather pecking by serotonin. Behav Neurosci. 2004;118:575–583.CrossRefGoogle ScholarPubMed
67.Bresnahan, JF, Kitchell, BB, Wildman, MF. Facial hair barbering in rats. Lab Anim Sci. 1983;33:290–291.Google ScholarPubMed
68.van den Broek, FA, Omtzigt, CM, Beynen, AC. Whisker trimming behaviour in A2G mice is not prevented by offering means of withdrawal from it. Lab Anim. 1993;27:270–272.CrossRefGoogle ScholarPubMed
69.Kurien, BT, Gross, T, Scofield, RH. Barbering in mice: a model for trichotillomania. BMJ. 2005;331:1503–1505.CrossRefGoogle Scholar
70.Wynchank, D, Berk, M. Fluoxetine treatment of acral lick dermatitis in dogs: a placebo-controlled randomized double blind trial. Depress Anxiety. 1998;8:21–23.3.0.CO;2-8>CrossRefGoogle ScholarPubMed
71.Seibert, LM, Crowell-Davis, SL, Wilson, GH, Ritchie, BW. Placebo-controlled clomipramine trial for the treatment of feather picking disorder in cockatoos. J Am Anim Hosp Assoc. 2004;40:261–269.CrossRefGoogle ScholarPubMed
72.Grindlinger, HM, Ramsay, E. Compulsive feather picking in birds. Arch Gen Psychiatry. 1991;48:857.CrossRefGoogle ScholarPubMed
73.Aouizerate, B, Guehl, D, Cuny, E, et al.Pathophysiology of obsessive-compulsive disorder: a necessary link between phenomenology, neuropsychology, imagery and physiology. Prog Neurobiol. 2004;72:195–221.CrossRefGoogle ScholarPubMed
74.Graybiel, AM, Rauch, SL. Toward a neurobiology of obsessive-compulsive disorder. Neuron. 2000;28:343–347.CrossRefGoogle Scholar
75.Goodman, WK, McDougle, CJ, Price, LH, Riddle, MA, Pauls, DL, Leckman, JF. Beyond the serotonin hypothesis: a role for dopamine in some forms of obsessive compulsive disorder? J Clin Psychiatry. 1990;51(Suppl:36-43);discussion 55-58.Google ScholarPubMed
76.Green, EJ, Isaacson, RL, Dunn, AJ, Lanthorn, TH. Naloxone and haloperidol reduce grooming occurring as an aftereffect of novelty. Behav Neural Biol. 1979;27:546–551.CrossRefGoogle ScholarPubMed
77.Skapinakis, P, Papatheodorou, T, Mavreas, V. Antipsychotic augmentation of serotonergic antidepressants in treatment-resistant obsessive-compulsive disorder: a meta-analysis of the randomized controlled trials. Eur Neuropsychopharmacol. 2007;17:79–93.CrossRefGoogle ScholarPubMed
78.Stewart, RS, Nejtek, VA. An open-label, flexible-dose study of olanzapine in the treatment of trichotillomania. J Clin Psychiatry. 2003;64:49–52.CrossRefGoogle ScholarPubMed
79.Marroni, SS, Nakano, FN, Gati, CD, Oliveira, JA, Antunes-Rodrigues, J, Garcia-Cairasco, N. Neuroanatomical and cellular substrates of hypergrooming induced by microinjection of oxytocin in central nucleus of amygdala, an experimental model of compulsive behavior. Mol Psychiatry. 2007;12:1103–1117.CrossRefGoogle ScholarPubMed
80.Greer, JM, Capecchi, MR. Hoxb8 is required for normal grooming behavior in mice. Neuron. 2002;33:23–34.CrossRefGoogle ScholarPubMed
81.Zuchner, S, Wendland, JR, Ashley-Koch, AE, et al.Multiple rare SAPAP3 missense variants in trichotillomania and OCD. Mol Psychiatry. 2009;14:6–9.CrossRefGoogle ScholarPubMed
82.Bienvenu, OJ, Wang, Y, Shugart, YY, et al.Sapap3 and pathological grooming in humans: Results from the OCD collaborative genetics study. Am J Med Genet B Neuropsychiatr Genet. 2009;150B:710–720.CrossRefGoogle ScholarPubMed
83.MacLean, PD. Effects of lesions of globus pallidus on species-typical display behavior of squirrel monkeys. Brain Res. 1978;149:175–196.CrossRefGoogle ScholarPubMed
84.Saxena, S, Brody, A, Schwartz, J, Baxter, L. Neuroimaging and frontal-subcortical circuitry in obsessive-compulsive disorder. Br J Psychiatry. 1998;173(suppl 35):26–38.CrossRefGoogle Scholar
85.Graybiel, AM. The basal ganglia and cognitive pattern generators. Schizophr Bull. 1997;23:459–469.CrossRefGoogle ScholarPubMed
86.Rauch, SL, Phillips, KA, Segal, E, et al.A preliminary morphometric magnetic resonance imaging study of regional brain volumes in body dysmorphic disorder. Psychiatry Res. 2003;122:13–19.CrossRefGoogle ScholarPubMed
87.Feusner, JD, Townsend, J, Bystritsky, A, McKinley, M, Moller, H, Bookheimer, S. Regional brain volumes and symptom severity in body dysmorphic disorder. Psychiatry Res. 2009;172:161–167.CrossRefGoogle ScholarPubMed
88.Feusner, JD, Moody, T, Townsend, J, et al.Abnormalities of Visual Processing and Fronto-Striatal Systems in Body Dysmorphic Disorder. Arch Gen Psychiatry. In press.Google Scholar
89.O'Sullivan, RL, Rauch, SL, Breiter, HC, et al.Reduced basal ganglia volumes in trichotillomania measured via morphometric magnetic resonance imaging. Biol Psychiatry. 1997;42:39–45.CrossRefGoogle ScholarPubMed
90.Swedo, SE, Rapoport, JL, Leonard, HL, Schapiro, MB, Rapoport, SI, Grady, CL. Regional cerebral glucose metabolism of women with trichotillomania. Arch Gen Psychiatry. 1991;48:828–833.CrossRefGoogle ScholarPubMed
91.Chamberlain, SR, Blackwell, AD, Fineberg, NA, Robbins, TW, Sahakian, BJ. The neuropsychology of obsessive compulsive disorder: the importance of failures in cognitive and behavioural inhibition as candidate endophenotypic markers. Neurosci Biobehav Rev. 2005;29:399–419.CrossRefGoogle ScholarPubMed
92.Rauch, SL, Wright, CI, Savage, CR, et al.Brain activation during implicit sequence learning in individuals with trichotillomania. Psychiatry Res. 2007;154:233–240.CrossRefGoogle ScholarPubMed
93.McKinney, WT Jr, Bunney, WE Jr.Animal model of depression. I. Review of evidence: implications for research. Arch Gen Psychiatry. 1969;21:240–248.CrossRefGoogle ScholarPubMed
94.Overall, KL. Natural animal models of human psychiatric conditions: assessment of mechanism and validity. Prog Neuropsychopharmacol Biol Psychiatry. 2000;24:727–776.CrossRefGoogle ScholarPubMed
95.Wilner, P. Behavioral models in psychopharmacology. In: Wilner, P, ed. Behavioral models in psychopharmacology: theoretical, industrial, and clinical perspectives. Cambridge, UK: Cambridge University Press; 1991:3–18.Google Scholar
96.Fossella, JA, Casey, BJ. Genes, brain, and behavior: bridging disciplines. Cogn Affect Behav Neurosci. 2006;6:1–8.CrossRefGoogle ScholarPubMed