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Cited by 124Primate Behavior and EcologyAnimal Behavior and Welfare StudiesPosttraumatic Stress Disorder Research

Signs of mood and anxiety disorders in chimpanzees

Open access
Ferdowsian, Hope R., Durham, Debra L., Kimwele, Charles, Kranendonk, Godelieve, Otali, Emily, Akugizibwe, Timothy, Mulcahy, J. B., Ajarova, Lilly +1 more·2011·PLoS ONE
DOI 10.1371/journal.pone.0019855PMC PMC3116818
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Abstract

BACKGROUND: In humans, traumatic experiences are sometimes followed by psychiatric disorders. In chimpanzees, studies have demonstrated an association between traumatic events and the emergence of behavioral disturbances resembling posttraumatic stress disorder (PTSD) and depression. We addressed the following central question: Do chimpanzees develop posttraumatic symptoms, in the form of abnormal behaviors, which cluster into syndromes similar to those described in human mood and anxiety disorders? METHODOLOGY/PRINCIPAL FINDINGS: In phase 1 of this study, we accessed case reports of chimpanzees who had been reportedly subjected to traumatic events, such as maternal separation, social isolation, experimentation, or similar experiences. We applied and tested DSM-IV criteria for PTSD and major depression to published case reports of 20 chimpanzees identified through PrimateLit. Additionally, using the DSM-IV criteria and ethograms as guides, we developed behaviorally anchored alternative criteria that were applied to the case reports. A small number of chimpanzees in the case studies met DSM-IV criteria for PTSD and depression. Measures of inter-rater reliability, including Fleiss' kappa and percentage agreement, were higher with use of the alternative criteria for PTSD and depression. In phase 2, the alternative criteria were applied to chimpanzees living in wild sites in Africa (n = 196) and chimpanzees living in sanctuaries with prior histories of experimentation, orphanage, illegal seizure, or violent human conflict (n = 168). In phase 2, 58% of chimpanzees living in sanctuaries met the set of alternative criteria for depression, compared with 3% of chimpanzees in the wild (p = 0.04), and 44% of chimpanzees in sanctuaries met the set of alternative criteria for PTSD, compared with 0.5% of chimpanzees in the wild (p = 0.04). CONCLUSIONS/SIGNIFICANCE: Chimpanzees display behavioral clusters similar to PTSD and depression in their key diagnostic criteria, underscoring the importance of ethical considerations regarding the use of chimpanzees in experimentation and other captive settings.

AI snapshot

Written from the paper’s full text.

TL;DR

This two-phase study applied DSM-IV and behaviorally anchored alternative criteria for PTSD and major depression to chimpanzees, finding symptom clusters similar to human mood and anxiety disorders. In phase 2, sanctuary chimpanzees with histories of trauma met alternative criteria for depression and PTSD far more often than wild chimpanzees.

Key findings

  • In phase 1, among 20 published chimpanzee case reports, average diagnoses per rater were 3 of 20 for PTSD and 1 of 20 for major depression using DSM-IV criteria; using alternative criteria, averages were 3 of 20 for PTSD and 1.6 of 20 for major depression.
  • Reliability was higher with alternative criteria: for PTSD, DSM-IV median percentage agreement was 43% and median Fleiss’ kappa was 0, versus 82% and 0.50 for alternative criteria; for depression, DSM-IV median agreement was 48% and median kappa was −0.10, versus 87% and 0.50 for alternative criteria.
  • In phase 2, 58% of sanctuary chimpanzees (n = 168) met alternative criteria for depression versus 3% of wild chimpanzees (n = 196; p = 0.04), and 44% of sanctuary chimpanzees met alternative criteria for PTSD versus 0.5% of wild chimpanzees (p = 0.04).
  • Where duration was reported, approximately 89% of individual alternative-criteria items for depression and PTSD persisted for at least 1 year; retest intra-rater percentage agreement averaged 81%–97%, with Cohen’s kappa averaging 0.40–0.80 across eight sites.

Methods

  • Phase 1 searched PrimateLit for genus *Pan* using the term “nonadaptive,” screened results to 20 individually identifiable chimpanzee cases from 12 published papers, and had three raters apply DSM-IV PTSD and major depression criteria. The authors then developed behaviorally anchored alternative criteria using chimpanzee ethograms and consultation with primatology, ethology, psychology, and psychiatry experts.
  • Phase 2 applied the alternative criteria at eight sites: three wild sites (n = 196) and five sanctuary sites (n = 168), including African sanctuaries and sanctuaries housing former laboratory chimpanzees. Three observers per chimpanzee completed surveys independently and were masked to study hypotheses; medical and behavioral records were also reviewed.
  • Prevalence differences were tested with Mann-Whitney U tests using an alpha of 0.05 in SPSS version 18.0; test-retest reliability was assessed in a random subsample with questionnaires repeated after approximately 2 weeks.

Limitations

  • Stated in the paper: chimpanzees cannot clearly articulate thoughts, feelings, and experiences; phase 1 relied on published case reports that may have contained biases or insufficient detail; some alternative-criteria items had low inter-rater reliability; there is no gold standard for assessing mood and anxiety disorders in chimpanzees, so external validity cannot be established; phase 2 was not longitudinal, did not allow full assessment of symptom duration or severity, was not designed for simultaneous observations, and relied on observer recall over differing time periods.
  • Stated in the paper: comparability of wild and sanctuary data collection is a possible concern, though the authors argue wild chimpanzees are observed systematically and physiological reactions such as heavy or irregular breathing would likely be underestimated rather than overestimated.
  • Evident from the text: the alternative criteria were developed and selected using the phase 1 case reports and expert consultation, then applied in phase 2, but the paper does not report independent validation against an external diagnostic standard; phase 2 prevalence estimates are based on caregiver/observer reports rather than direct clinical diagnosis.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1371/journal.pone.0019855

Cites

76 of 76 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

0 of 18 cited sources checked · 0 supported · 0 flagged

  • Findingown data

    The third hypothesis, that chimpanzees would display clusters of symptoms that are similar to disorders such as PTSD and depression, was supported.

    “The third hypothesis, that chimpanzees would display clusters of symptoms that are similar to disorders such as PTSD and depression, was supported.”
    Quote in the paperSubstantial claim
  • Findingown data

    In phase 2, there were differences between chimpanzees living in sanctuaries and those living in the wild in the percentages of abnormal behaviors (alternative criteria) reported.

    “In phase 2, there were differences between chimpanzees living in sanctuaries and those living in the wild in the percentages of abnormal behaviors (alternative criteria developed in phase 1) reported, as shown in Figures 1 and 2.”
    Quote in the paperSubstantial claim
  • Findingown data

    Where duration of behavior was reported, approximately 89% of the individual items for alternative criteria for depression and PTSD were reported to persist for at least 1 year.

    “Where duration of behavior was reported, approximately 89% of the individual items for alternative criteria for depression (Figure 1) and PTSD (Figure 2) were reported to persist for at least 1 year.”
    Quote in the paperNot a substantial claim
  • Findingown data

    There was 100 percent agreement (K = 1.0) among raters for the diagnosis of PTSD when testing the set of alternative criteria in phase 1.

    “It was reassuring that there was 100 percent agreement (K = 1.0) among raters for the diagnosis of PTSD, when testing the set of alternative criteria in phase 1.”
    Quote in the paperNot a substantial claim
  • Findingown data

    In phase 2, 44% of chimpanzees in sanctuaries met the set of alternative criteria for PTSD, compared with 0.5% of chimpanzees in the wild (p = 0.04).

    “44% of chimpanzees in sanctuaries met the set of alternative criteria for PTSD, compared with 0.5% of chimpanzees in the wild (p = 0.04).”
    Quote in the paperSubstantial claim
  • May combine two claims. 19
  • The quote only partly states this claim. 1
  • Classified as probably not a substantial claim. 15

  • May combine two claims.

    Findingown data

    For alternative depression criteria, percentage agreement among the three raters for each item ranged from 63% to 100% (median = 87%), and inter-rater reliability K values ranged from 0.10 to 1.0 (median = 0.50).

    “In contrast, percentage agreement among the three raters for each of the items in the alternative criteria for depression ranged from 63% to 100% (median = 87%) and inter-rater reliability Κ values ranged from 0.10 to 1.0 (median = 0.50).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Although a number of chimpanzees met DSM-IV criteria for PTSD and depression in phase 1, measures of inter-rater reliability were low.

    “Although a number of chimpanzees met DSM-IV criteria for PTSD and depression in this phase, measures of inter-rater reliability were low.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    For major depression in phase 1, one rater deemed three chimpanzees met DSM-IV criteria, while the other two raters found no chimpanzees who met DSM-IV criteria for major depression.

    “For major depression, one rater deemed three chimpanzees met DSM-IV criteria. However, the other two raters found no chimpanzees who met DSM-IV criteria for major depression.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For PTSD in phase 1 using DSM-IV criteria, one rater deemed four chimpanzees met criteria, another rater deemed two, and another rater deemed three.

    “For PTSD, using the DSM-IV criteria, one rater deemed that four chimpanzees met criteria; another rater deemed that two chimpanzees met criteria; and another rater deemed that three chimpanzees met criteria.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingnone given

    Mawa met alternative criteria for depression and PTSD.

    “Mawa met alternative criteria for depression and PTSD.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    For DSM-IV major depression, percentage agreement among the three raters for each of the 13 items ranged from 12% to 67% (median = 48%), and inter-rater reliability K values ranged from −0.40 to 0.40 (median = −0.10).

    “The percentage agreement among the three raters for each of the 13 DSM-IV items for major depression ranged from 12% to 67% (median = 48%), and the inter-rater reliability Κ values for the three raters ranged from −0.40 to 0.40 (median Κ = −0.10).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    For PTSD, percentage agreement among the three raters for each of the 21 DSM-IV items ranged from 27% to 73% (median = 43%), and inter-rater reliability K values ranged from −0.30 to 0.30 (median = 0).

    “For PTSD, percentage agreement among the three raters for each of the 21 items for the DSM-IV criteria ranged from 27% to 73% (median = 43%), while the inter-rater reliability Κ values for the three raters ranged from −0.30 to 0.30 (median = 0).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    For alternative PTSD criteria, percentage agreement among the three raters for each item ranged from 63% to 100% (median = 82%), and inter-rater reliability K values ranged from 0.10 to 0.70 (median = 0.50).

    “In contrast, percentage agreement among the three raters for each of the items in the alternative criteria for PTSD ranged from 63% to 100% (median = 82%), and inter-rater reliability Κ values ranged from 0.10 to 0.70 (median = 0.50).”
    Quote in the paperSubstantial claim

  • The quote only partly states this claim.

    Findingown data

    Measures of inter-rater reliability, including Fleiss' kappa and percentage agreement, were higher with use of the alternative criteria for PTSD and depression than with DSM-IV criteria.

    “Measures of inter-rater reliability, including Fleiss' kappa and percentage agreement, were higher with use of the alternative criteria for PTSD and depression.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Upon retest, percentage agreement within raters for individual symptoms averaged from 81% to 97%, with Cohen's kappa averaging from 0.40 to 0.80 at the eight sites.

    “Upon retest, percentage agreement within raters for individual symptoms averaged from 81% to 97%, with Cohen's kappa averaging from 0.40 to 0.80 at the eight sites.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingreasoning

    Negra met alternative criteria for depression and PTSD.

    “Negra met alternative criteria for depression and PTSD.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    The PrimateLit search returned 384 results that met the initial criteria.

    “The search returned 384 results that met our initial criteria.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Findingown data

    44% of chimpanzees in sanctuaries met the definition for PTSD based on alternative criteria, compared with 0.5% of chimpanzees in the wild (p = 0.04).

    “Similarly, 44% of chimpanzees in sanctuaries met the definition for PTSD based on alternative criteria, compared with 0.5% of chimpanzees in the wild (p = 0.04).”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Findingown data

    Using the optimal set of alternative criteria for depression, one rater deemed three chimpanzees met criteria, another rater deemed two, and another rater deemed none.

    “Using the optimal set of alternative criteria for depression we identified, one rater deemed that three chimpanzees met criteria; another rater deemed two chimpanzees met criteria; and another rater deemed that no chimpanzees met criteria.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S4 (based).

    Study design and conductnone given

    Chimpanzees at the wild sites are typically observed for five days per week from dawn to dusk as part of systematic behavioral study.

    “Therefore, it is important to note that chimpanzees at the wild sites are typically observed for five days per week from dawn to dusk as part of systematic behavioral study.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    In phase 2, responses were made independently and without consultation.

    “Responses were made independently and without consultation.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Inter-rater reliability was assessed by calculating Fleiss' kappa and percentage agreement for each item.

    “Inter-rater reliability was assessed by calculating Fleiss' kappa (Κ) and the percentage agreement for each item.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    The inability of nonhuman primates to report symptoms presents obstacles similar to those in pediatrics, psychiatry, and geriatrics, often requiring special investigative methods, including gathering information from relevant third parties.

    “The inability of nonhuman primates to report symptoms presents obstacles similar to those in pediatrics, psychiatry, and geriatrics, often requiring special investigative methods, including gathering information from relevant third parties [48]–[52].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [48]–[52]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductown data

    In phase 2, respondents were masked to the study hypotheses.

    “While respondents were informed that the study related to primate behavior, all were masked to the study hypotheses.”
    Quote in the paperNot a substantial claim

  • Classified as probably not a substantial claim.

    Study design and conductnone given

    Intra-rater percentage agreement was used to determine the reliability of the raters' assessments.

    “Intra-rater percentage agreement was used to determine the reliability of the raters' assessments.”
    Quote in the paperSubstantial claim

  • Classified as probably not a substantial claim. May combine two claims.

    Study design and conductnone given

    Three raters who were aware of the purpose of the study rated all 20 phase 1 cases independently.

    “Three raters who were aware of the purpose of the study rated all 20 cases independently.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    Other unfavorable rearing conditions, social isolation, prolonged captivity, sensory deprivation, and use in laboratory experimentation have been reported to be contributors to behavioral pathology in nonhuman primates.

    “Likewise, other unfavorable rearing conditions, social isolation, prolonged captivity, sensory deprivation, and use in laboratory experimentation have been reported to be contributors to behavioral pathology in nonhuman primates [13]–[16].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [13]–[16]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    The association of pathological behaviors with captivity in nonhuman primates has been noted for decades.

    “The association of pathological behaviors with captivity in nonhuman primates has been noted for decades [1]–[9].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [1]–[9]

      Not checked in the free run.

  • May combine two claims.

    Study design and conductnone given

    The study had a robust sample size in phase 2 representing a wide age range of both sexes, reports of trained observers, a broad spectrum of behaviors assessed, and the ability for caregivers to report observations in a relatively unrestricted but structured setting.

    “Strengths of the current study include a robust sample size in phase 2 representing a wide age range of both sexes, as well as reports of trained observers, the broad spectrum of behaviors assessed, and the ability for caregivers to report observations in a relatively unrestricted but structured setting.”
    Quote in the paperSubstantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Several authors have demonstrated the prevalence of abnormal behaviors, ranging from whole-body stereotypies to self-injurious behaviors, in chimpanzees and other nonhuman primates in captivity.

    “Several authors have demonstrated the prevalence of abnormal behaviors, ranging from whole-body stereotypies to self-injurious behaviors, in chimpanzees and other nonhuman primates in captivity [6], [15], [17], [18].”
    Quote in the paperNot a substantial claim0 of 3 sources checked
    • cites [6] LT Nash, 1999, Variables influencing the origins of diverse abnormal behaviors in a large sample of captive chimpanzees (Pan troglodytes)., Am J Primatol source

      Not checked in the free run.

    • cites [15] C Lutz, 2003, Stereotypic and self-injurious behavior in rhesus macaques: a survey and retrospective analysis of environment and early experience., Am J Primatol source

      Not checked in the free run.

    • cites [17] MA Hook, 2002, Inter-group variation in abnormal behavior in chimpanzees (Pan troglodytes) and rhesus macaques (Macaca mulatta)., Appl Anim Behav Sci source

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Abnormalities of the hypothalamic-pituitary-adrenal axis have been described in animals subjected to confinement, restraint, isolation, or surgical procedures.

    “Abnormalities of this axis have been described in animals subjected to confinement, restraint, isolation, or surgical procedures [22], [23].”
    Quote in the paperNot a substantial claim0 of 2 sources checked
    • cites [22] FD McMillan, 2005, Mental health and well-being in animals source

      Not checked in the free run.

    • cites [23] NG Gregory, 2004, Physiology and behavior of animal suffering

      Not checked in the free run.

  • May combine two claims.

    Study design and conductreasoning

    In phase 2, the design was not longitudinal and therefore did not allow for full assessment of the duration of symptoms and impeded the assessment of severity.

    “In phase 2, the design was not longitudinal and therefore did not allow for full assessment of the duration of symptoms and impeded the assessment of severity.”
    Quote in the paperSubstantial claim

  • May combine two claims.

    Premisecitation

    Complex PTSD, depression, and other psychiatric conditions have been diagnosed in other species, including chimpanzees.

    “Complex PTSD, depression, and other psychiatric conditions have been diagnosed in other species, including chimpanzees [14], [22], [23], [41]–[46], although it is unclear how appropriate the DSM-IV (Diagnostic and Statistical Manual of Mental Disorders, 4th Ed.) criteria [47] or other traditional methods of assessing psychopathology are for use in species other than humans.”
    Quote in the paperSubstantial claim0 of 3 sources checked
    • cites [14] GA Bradshaw, 2008, Building an inner sanctuary: complex PTSD in chimpanzees., J Trauma Dissociation source

      Not checked in the free run.

    • cites [22] FD McMillan, 2005, Mental health and well-being in animals source

      Not checked in the free run.

    • cites [23] NG Gregory, 2004, Physiology and behavior of animal suffering

      Not checked in the free run.

  • Classified as probably not a substantial claim.

    Premisecitation

    Mood and anxiety disorders such as PTSD and depression are commonly diagnosed among humans exposed to significant acute, recurrent, or persistent trauma.

    “Mood and anxiety disorders such as PTSD and depression are commonly diagnosed among humans exposed to significant acute, recurrent, or persistent trauma [72]–[76].”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [72]–[76]

      Not checked in the free run.

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The greater reliability among raters when testing alternative criteria is likely partly attributable to attempts to reduce the need to make inferences about thoughts or feelings.

    “This is likely partly attributable to attempts to reduce the need to make inferences about thoughts or feelings.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Cohen's kappa was calculated to produce the most conservative estimate of intra-rater reliability.

    “Cohen's kappa (K) was calculated to produce the most conservative estimate of intra-rater reliability.”
    Quote in the paperNot a substantial claim

  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Study design and conductnone given

    Test-retest was assessed in a random sub-sample of raters and chimpanzees at each site.

    “Test-retest was assessed in a random sub-sample of raters and chimpanzees at each site.”
    Quote in the paperNot a substantial claim

  • May combine two claims.

    Study design and conductreasoning

    The study was not designed to capture simultaneous observations, therefore making it difficult to assess inter-rater reliability.

    “The study was not designed to capture simultaneous observations, therefore making it difficult to assess inter-rater reliability.”
    Quote in the paperNot a substantial claim
33 of 33

  • The paper relies on this without support.

    It is uncommon to study psychopathology in nonhuman primates using the terms and tools of human psychiatry.

    “Despite the many similarities between humans and nonhuman primates, it is uncommon to study psychopathology in nonhuman primates using the terms and tools of human psychiatry.”

  • The paper relies on this without support.

    Pathological behaviors in nonhuman primates are often described in isolation without being distilled into recognizable syndromes.

    “Moreover, pathological behaviors in these individuals are often described in isolation without being distilled into recognizable syndromes.”

  • The paper relies on this without support.

    Diagnostic criteria for mood and anxiety disorders typically require verbal descriptions from subjects of their experiences and internal states.

    “Diagnostic criteria for mood and anxiety disorders typically require verbal descriptions from subjects of their experiences and internal states.”

  • The paper relies on this without support.

    Changes, disruption, or dysfunction of common neuropsychiatric systems can result in similar patterns of symptom expression.

    “Similarly, changes, disruption, or dysfunction of common neuropsychiatric systems can result in similar patterns of symptom expression.”

  • The paper relies on this without support.

    Chimpanzees cannot clearly articulate their thoughts, feelings, and experiences to humans.

    “Chimpanzees cannot clearly articulate their thoughts, feelings, and experiences to humans, although a few have learned to communicate using sign language.”

  • The paper relies on this without support.

    There is no gold standard for the assessment of mood and anxiety disorders in chimpanzees.

    “Since there is no gold standard for the assessment of mood and anxiety disorders in chimpanzees, it is not possible to establish the external validity of the alternative criteria we developed.”

  • The paper relies on this without support.

    The alternative criteria for PTSD and depression are valid indicators of these disorders in chimpanzees.

    “We propose that these diagnostic terms be used, when applicable, in chimpanzees and offer criteria for their use.”

  • The paper relies on this without support.

    Sanctuary chimpanzees are previously traumatized relative to wild chimpanzees.

    “The significant differences we found in phase 2 between the wild and sanctuary populations in the percentage of chimpanzees who met a set of alternative diagnostic criteria for PTSD and depression suggest that syndromes similar to PTSD and depression are identifiable in previously traumatized chimpanzees.”
8 of 8

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Captive apes that have experienced early trauma, isolation or abuse often show disturbed behavior and social interactions compared to those who have not.

    “Captive apes, for example, have often experienced early trauma, lived in isolation or have suffered abuse. Those that have, often show disturbed behavior and social interactions compared to those who have not (Ferdowsian et al., 2011; Clay and de Waal, 2013).”

    From Endogenous peripheral oxytocin measures can give insight into the dynamics of social relationships: a review (2014) · cites this paper as Ferdowsian et al., 2011

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

  • Average alternative-criteria depression diagnoses is misrounded

    Minor

    The three raters diagnosed 0, 2, and 3 cases, for an average of 1.67 cases per rater. Rounded to one decimal place, this is 1.7, not the reported 1.6.

    Reported 1.6 · recomputed 1.666667

1 of 1

Cites

Flagged first, then by citations

Research works printed but not linked: 3

  1. 2000, Diagnostic and statistical manual of mental disorders, fourth edition (text revision)
  2. SM Howell, 1997, Treating chronic regurgitation behavior: a case study., Lab Anim, 26, 30
  3. EJ Struthers, 1990, A case history of a decrement in maternal competence in a captive chimpanzee (Pan troglodytes)., Brown University Lab Primate Newsletter, 29, 3

Cited by

Sorted by citations

Related

Authors
Ferdowsian, H. R., Durham, D. L., Kimwele, C., Kranendonk, G., Otali, E., Akugizibwe, T., Mulcahy, J. B., Ajarova, L., & Johnson, C. M.
Affiliations
  • Physicians Committee for Responsible Medicine (US)
  • University of Nairobi (KE)
  • Kibale Chimpanzee Project (UG)
  • Wildlife Conservation Society Uganda (UG)
Corresponding author
Ferdowsian, Hope R.
ORCID
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2011-06-16
Volume
6
Issue
6
Pages
e19855
ISSN
1932-6203 (ISSN-L)
DOI
10.1371/journal.pone.0019855
PMC
PMC3116818
OpenAlex
W2098756499
Semantic Scholar
d9a5cc906e3214a5c0e35fe3448286e16061aa5a
Cited by
124
References
76
Citations by year
2026: 4 · 2025: 8 · 2024: 7 · 2023: 7 · 2022: 9 · 2021: 7 · 2020: 20 · 2019: 6 · 2018: 4 · 2017: 4 · 2016: 6 · 2015: 13 · 2014: 11 · 2013: 4 · 2012: 13
FWCI
12.62
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • PLoS ONE (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • WBI Studies Repository (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • University of Nairobi Research Archive (University of Nairobi) (submittedVersion)
Funders
  • Arcus Foundation
  • Ministrstvo za visoko šolstvo, znanost in tehnologijo
Topics
  • Social Sciences › Psychology › Social Psychology › Primate Behavior and Ecology
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Social Sciences › Psychology › Clinical Psychology › Posttraumatic Stress Disorder Research
Keywords
chimpanzees, post-traumatic stress disorder, depression, mood disorders, anxiety disorders, traumatic events, maternal separation, social isolation, animal experimentation, wild chimpanzees, diagnostic criteria, ethogram, inter-rater reliability, animal welfare ethics
MeSH terms
Animals, Anxiety, Pan troglodytes, Female, Male, Mood Disorders

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Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Claims read by deepseek-v4.1-flash under definition version 3 (extract-v3) on 2026-10-09.

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