Cited by 5Antifungal resistance and susceptibilityAnimal Behavior and Welfare StudiesFungal Infections and Studies

Nationwide Survey about the Occurrence of Aspergillosis in Captive Penguins in Zoos and Aquariums in Japan

Open access
Itoh, Megumi, Matsumoto, Naoya, Hagino, Kyogo, Sawayama, Nanako, Kuwayama, Miki, Yamada, Kazutaka, Toyotome, Takahito·2023·Animals

Abstract

We surveyed the facilities that were members of the Japan Association of Zoos and Aquariums to clarify the incidence of aspergillosis, which is a major cause of death in captive penguins, and to discern effective preventive measures. Responses were obtained for 2910 penguins in 64 facilities; 73 penguins (2.5%) in 35 facilities had died from aspergillosis during the past 5 years from April 2016 to March 2021. Answers to questions about the rearing environment indicated that aspergillosis occurred significantly more often in facilities where penguins were reared outdoors, were in contact with soil, or were moved outside of the rearing enclosure. Answers to questions about their dead penguins indicated that 76% may have been at individual risk (e.g., young age, old age, molting period, and breeding season) and 54% were thought to be reared in uncomfortable environments (e.g., high temperature, high humidity). Aspergillosis may occur when individual risk factors and uncomfortable environmental factors are added to the risk factors of exposure to Aspergillus, such as the presence of soil. These conditions must be recognized as risk factors for aspergillosis, and appropriate preventive measures, such as avoiding penguin contact with the soil where Aspergillus is expected to be present, can minimize aspergillosis-related deaths.

AI snapshot

Written from the paper’s full text.

TL;DR

A nationwide JAZA questionnaire found that 73 of 2910 captive penguins (2.5%) died from aspergillosis across 35 of 64 responding facilities in Japan from April 2016 to March 2021. Risk was significantly associated with outdoor enclosures, movement outside rearing enclosures, and soil contact, while most deaths also had individual or environmental risk factors.

Key findings

  • Of 64 responding facilities (72.0%), 35 reported penguin deaths from aspergillosis; 73 of 2910 penguins (2.5%) died over the 5 years from April 2016 to March 2021.
  • Statistically higher death rates were reported for southern rockhopper (11.4%), little (10.2%), and Magellanic penguins (33.3%), but cases clustered in single facilities; excluding those facilities, there was no significant difference in death rate by species.
  • Aspergillosis occurred significantly more often in groups using outdoor enclosures (35/74, 47% vs. 6/45, 13%; p < 0.01), moved outside rearing enclosures (19/35, 54% vs. 22/84, 26%; p < 0.01), and in contact with soil (20/32, 63%; p < 0.01). For Antarctic/sub-Antarctic penguins, outdoor vs. indoor housing was significant (p = 0.007); for temperate penguins, moving outside (p = 0.009) and soil contact (p = 0.019) were significant.
  • In the additional survey of 54 dead penguins, 41 (76.0%) had at least one individual risk factor, 29 (53.7%) were thought to have been in an uncomfortable environment, and 26 (48.1%) had contact with soil; 52 of 54 had at least one individual, environmental, or soil-exposure risk factor. No significant reduction in aspergillosis was detected in facilities with five or more preventive measures.

Methods

  • In September 2021, a questionnaire was sent through JAZA to 89 zoos and aquariums that bred penguins; 64 facilities responded, providing data on 2910 penguins of 11 species. The primary survey asked about species and numbers, aspergillosis deaths from April 2016 to March 2021, indoor/outdoor rearing environment, movement outside enclosures, preventive measures, and free-text comments.
  • An additional questionnaire was sent to the 35 facilities reporting aspergillosis deaths; 30 responded regarding 54 dead penguins, with questions on month of occurrence, sex, age, transfer within the past year, molting or breeding period, suspected cause of death, hot/humid conditions, soil or plant contact, nesting box type, and bedding materials.
  • Statistical analyses used chi-square test and residual analysis for species mortality, chi-square or Fisher’s exact test for environmental associations, and Wilcoxon rank-sum test for number of preventive measures; p < 0.05 was considered significant, using Excel add-in Statcel4.

Limitations

  • The paper states that it did not obtain information on the type of soil used as basement material, and that the analysis did not confirm whether Aspergillus spores in the air or outdoor unsuitable temperature/humidity are risk factors.
  • The paper notes that the earlier 1960s survey used different methods, so simple comparisons with the present mortality rate are difficult.
  • Evident from the methods: case ascertainment and risk-factor attribution relied on facility questionnaires and respondent-reported causes, with no independent diagnostic confirmation or environmental sampling described in this survey; the 72.0% response rate and clustering of cases in single facilities may also affect species-level comparisons.

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

Integrity signals

Registry

Crossref · 10.3390/ani13121913

Cites

34 of 34 references verified0 citation errors · 0 not checkable

Statistics

Nothing to recompute.

Claims the paper makes

31 of 51 cited sources checked · 16 supported · 0 flagged · accuracy not yet measured

  • Interpretationreasoning

    Various improvements in zoos and aquariums, such as reference to and adherence to penguin breeding manuals and preventive management, were thought to have reduced the number of deaths.

    “Although the climate in Japan is hot and humid for penguins, various improvements in zoos and aquariums, such as reference to and adherence to penguin breeding manuals [33] and preventive management [28,29,30], were thought to have reduced the number of deaths.”
    Quote in the paperNot a substantial claim3 of 4 sources checked
    • cites [33] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source

      The paper describes preventive management at one aquarium, including washing penguins’ feet, avoiding a suspected contaminated route, and disinfecting affected areas. It reports that deaths from aspergillosis were no longer observed, but it does not establish that improvements across zoos and aquariums reduced penguin deaths generally. The relevant passages are labelled Abstract in our copy; no page number is supplied. (LLM, conf=0.83)

      Experimental — accuracy not yet measured
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source

      The Abstract and Conclusion describe preventive measures at one aquarium and report no new aspergillosis cases in its captive penguins since 2016. They do not report a reduction in penguin deaths across zoos and aquariums. The breeding-manual example is attached to a different citation in the citing sentence. (LLM, conf=0.85)

      Experimental — accuracy not yet measured
    • cites [30] Hocken, 2000, Cause of death in Blue penguins (Eudyptula m. minor) in North Otago, New Zealand, N. Z. J. Zool. source

      The Abstract (page not provided) reports causes of death among blue penguins collected in North Otago, not whether preventive management reduced deaths in zoos or aquariums. Searches for preventive management, predator control, and reduced mortality found no passage addressing that claim. The breeding-manual citation [33] is separate from the citations being assessed here. (LLM, conf=0.72)

      Experimental — accuracy not yet measured
    • Rests on an assumption: The climate in Japan is hot and humid for penguins.
  • Premisecitation

    Soil is the major habitat of Aspergillus.

    “Soil is the major habitat of Aspergillus [4,14,35].”
    Quote in the paperSubstantial claim1 of 3 sources checked
    • cites [4] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

    • cites [14] Chamilos, 2019, Aspergillus fumigatus and Aspergillosis in 2019, Clin. Microbiol. Rev. source

      The Introduction (page unavailable) identifies soil as the ecological niche of A. fumigatus. That supports the claim for this species, but the cited passage does not establish that soil is the major habitat of the entire Aspergillus genus. (LLM, conf=0.85)

      Experimental — accuracy not yet measured
    • cites [35] Summerbell, 1989, Potted plants in hospitals as reservoirs of pathogenic fungi, Mycopathologia source
  • Premisecitation

    Compost is one of the major sources of Aspergillus.

    “As shown in some publications, compost is one of the major sources of Aspergillus [37].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [37] Zhang, 2017, A Novel Environmental Azole Resistance Mutation in Aspergillus Fumigatus and a Possible Role of Sexual Reproduction in Its Emergence, MBio source

      The Introduction (page not specified) describes compost as an important biological niche for A. fumigatus with high densities of spores, and the Results report A. fumigatus in samples from two compost heaps. The paper does not establish that compost is one of the major sources of Aspergillus generally; the Discussion says compost could be a source of resistant A. fumigatus. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Premisecitation

    Prevention of access to soil was a useful measure for reducing aspergillosis in an aquarium.

    “As shown in our previous study, the prevention of access to soil was a useful measure for reducing aspergillosis in an aquarium [28,29].”
    Quote in the paperSubstantial claim2 of 2 sources checked
    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source
  • Premisecitation

    Even when housed indoors, air conditioners are associated with a risk of contamination with fungi including Aspergillus species.

    “For example, even when housed indoors, air conditioners are associated with a risk of contamination with fungi including Aspergillus species.”
    Quote in the paperNot a substantial claim2 of 2 sources checked
    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source
  • Classified as probably not a substantial claim. 28
  • May combine two claims. 29
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing). May combine two claims.

    Premisecitation

    To prevent aspergillosis, contact with Aspergillus must be minimized in penguins and the health of each penguin should be maintained.

    “Therefore, to prevent aspergillosis, contact with Aspergillus must be minimized in penguins, and the health of each penguin should be maintained [28,29,30,31].”
    Quote in the paperNot a substantial claim3 of 4 sources checked
    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source

      The paper describes avoiding a suspected A. fumigatus contamination site, washing penguins’ feet, and disinfecting contaminated areas—measures consistent with minimizing exposure (passage [6], section labeled Abstract; page unavailable). The passages do not recommend maintaining the health of each individual penguin, so that part of the claim is unsupported. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source
    • cites [30] Hocken, 2000, Cause of death in Blue penguins (Eudyptula m. minor) in North Otago, New Zealand, N. Z. J. Zool. source

      The Abstract reports that aspergillosis was the commonest natural disease among the blue penguins examined, but it does not discuss prevention. Searches for Aspergillus exposure and penguin health found no passage recommending either measure in the claim. (LLM, conf=0.72)

      Experimental — accuracy not yet measured
    • cites [31] Miller, R.E., and Fowler, M.E. (2015). Zoo and Wild Animal Medicine, Elsevier Saunders. [8th ed.].

      Not checked in the free run.

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

    Premisecitation

    Aspergillus spores are hydrophobic and approximately 2.5 μm in diameter, allowing them to pass through the trachea to reach the air sacs and lungs and cause aspergillosis in immunocompromised humans and animals.

    “Their spores are hydrophobic and extremely small, with a diameter of approximately 2.5 µm. Therefore, they easily pass through the trachea to reach the air sacs and lungs, which causes aspergillosis, a respiratory infection in immunocompromised humans and animals [4,20].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [4] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

    • cites [20] Mateos, 2010, Polyclonal Aspergillus fumigatus infection in captive penguins, Vet. Microbiol. source

      The Introduction (p. 2) describes aspergillosis as a fungal infection in birds, and §2.1 (Animals) reports A. fumigatus infection and lesions in the lungs and air sacs of penguins. Our copy does not state that spores are hydrophobic or approximately 2.5 µm across, that they pass through the trachea, or that this mechanism causes disease in immunocompromised humans and animals. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Aspergillus species are common fungi found in the environment, such as soil and air.

    “The Aspergillus species [4,5,6,7,8,9,10,11,12,13] are common fungi found in the environment, such as soil and air [14,15,16,17,18,19].”
    Quote in the paperNot a substantial claim4 of 6 sources checked
    • cites [14] Chamilos, 2019, Aspergillus fumigatus and Aspergillosis in 2019, Clin. Microbiol. Rev. source
    • cites [15] Snelders, 2009, Possible environmental origin of resistance of Aspergillus fumigatus to medical triazoles, Appl. Environ. Microbiol. source
    • cites [16] Verweij, 2009, Azole resistance in Aspergillus fumigatus: A side-effect of environmental fungicide use?, Lancet Infect. Dis. source
    • cites [17] Sewell, 2019, Elevated prevalence of azole resistant Aspergillus fumigatus in urban versus rural environments in the United Kingdom, Antimicrob. Agents Chemother. source

      The Introduction describes A. fumigatus as ubiquitous, with a soil niche and airborne conidia; the Environmental A. fumigatus isolates section also reports its recovery from soil samples. These passages support the claim for A. fumigatus, but do not establish it for Aspergillus species generally. (LLM, conf=0.82)

      Experimental — accuracy not yet measured
    • cites [18] Hirose, 2022, Diversity and distribution of Aspergillus fumigatus and its related species in Izu and Ogasawara islands, Japan, Med. Mycol. J. source
    • cites [19] Toyotome, 2022, Azole-resistant Aspergillus fumigatus as an emerging worldwide pathogen, Microbiol. Immunol. source
  • May combine two claims.

    Premisecitation

    In a previous report from the authors' aquarium, six aspergillosis cases occurred between 2009 and 2015, and no aspergillosis occurred from 2016 to 2020 after implementing measures to minimize penguin contact with soil.

    “As a result, although the aquarium had six aspergillosis cases between 2009 and 2015, there was no incidence of aspergillosis from 2016 to 2020 [28,29].”
    Quote in the paperSubstantial claim2 of 2 sources checked
    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source

      Split into 2 atoms — 0 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 1 unverifiable. Expand the claim to see per-atom verdicts.

      Experimental — accuracy not yet measured
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source
  • Classified as probably not a substantial claim.

    Premisecitation

    Aspergillosis is considered an opportunistic infectious disease.

    “Aspergillosis is considered an opportunistic infectious disease [4,20].”
    Quote in the paperSubstantial claim1 of 2 sources checked
    • cites [4] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

    • cites [20] Mateos, 2010, Polyclonal Aspergillus fumigatus infection in captive penguins, Vet. Microbiol. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    A. fumigatus is the most pathogenic Aspergillus species causing severe respiratory symptoms in wild birds and poultry.

    “In particular, A. fumigatus is the most pathogenic species that causes severe respiratory symptoms in wild birds and poultry [21,22].”
    Quote in the paperNot a substantial claim1 of 2 sources checked
    • cites [21] Thomas, N.J., Hunter, D.B., and Atkinson, C.T. (2008). Infectious Diseases of Wild Birds, Blackwell Publishing Professional. source
    • cites [22] Obendorf, 1980, Mortality in little penguins (Eudyptula minor) along the coast of Victoria, Australia, J. Wildl. Dis. source

      The penguin findings (section labelled “Contracaecum spiculigerum”; page unavailable) report pulmonary aspergillosis in two wild birds, and Histopathology describes lesions in their lungs and air sacs. The paper does not identify A. fumigatus, compare the pathogenicity of Aspergillus species, report severe respiratory symptoms, or address poultry. (LLM, conf=0.84)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S2 (checkable), S3 (load-bearing).

    Interpretationcitation

    New technologies such as diagnosis with image analysis, plasma biomarkers, and probiotic-based vaccination might be useful in reducing the incidence of aspergillosis among penguins.

    “New technologies, such as diagnosis with image analysis [25,27], plasma biomarkers [38], and probiotic-based vaccination [39], might be useful in reducing the incidence of aspergillosis among penguins.”
    Quote in the paperNot a substantial claim4 of 4 sources checked
    • cites [25] Itoh, 2020, Characteristic imaging findings of the respiratory ssystem in penguins with suspected aspergillosis in an aquarium, J. Vet. Med. Sci. source

      The Discussion says CT findings, combined with blood screening, could help diagnose aspergillosis early and initiate treatment in penguins. It suggests early detection could prevent deaths, but does not show that imaging reduces the incidence of infection. The plasma-biomarker and probiotic-vaccination parts of the citing sentence have separate citations and are not attributed to this paper. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [27] Matsumoto, 2022, Evaluation of the air sac volume of penguins with respiratory diseases using computed tomography, J. Vet. Med. Sci. source
    • cites [38] Desoubeaux, 2018, Application of 3-Hydroxybutyrate measurement and plasma protein electrophoresis in the diagnosis of aspergillosis in African penguins (Spheniscus demersus), J. Zoo Wildl. Med. source

      The conclusion (section labeled “200”) says 3-hydroxybutyrate measurement may help diagnose aspergillosis in penguins, especially alongside plasma protein electrophoresis. This supports the plasma-biomarker part of the citing sentence, but the paper does not establish that these tests reduce the incidence of aspergillosis. (LLM, conf=0.86)

      Experimental — accuracy not yet measured
    • cites [39] Thorel, 2022, Assessment of the safety and efficacy of an oral probiotic-based vaccine against Aspergillus infection in captive-bred Humboldt penguins (Spheniscus humboldti), Front. Immunol. source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In our previous study, Aspergillus fumigatus was detected from air conditioner vents.

    “In our previous study [28,29], A. fumigatus was detected from air conditioner vents.”
    Quote in the paperNot a substantial claim2 of 2 sources checked
    • cites [28] Matsumoto, 2020, Detection of Aspergillus fumigatus in the captive environment and preventive measures leading to the eradication of penguin aspergillosis in an aquarium, Jpn. J. Zoo Wildl. Med. source
    • cites [29] Toyotome, 2022, Countermeasures against aspergillosis in captive penguins, Med. Mycol. J. source

      The section discussing the previous study reports that swabs detected A. fumigatus on air conditioners and exhaust fans in the penguin rearing facility. It does not identify the sampled surfaces as air-conditioner vents specifically. (LLM, conf=0.83)

      Experimental — accuracy not yet measured
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    In the case of Okinawa rail, the authors described the environmental source of the causative agent.

    “In the case of Okinawa rail, the authors described the environmental source of the causative agent [36].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [36] Kano, 2021, Antifungal drugs-low-susceptibility in Aspergillus Flavus isolated from a captively reared Okinawa rail (Hypotaenidia okinawae), J. Vet. Med. Sci. source

      The paper describes soil and dead leaves in the rail’s enclosure as a possible source of Aspergillus infection. It also states that the authors found no evidence of the route of infection in this case, so it does not establish the environmental source of the causative agent. (LLM, conf=0.88)

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

    Premisecitation

    A mass outbreak of aspergillosis in kākāpō and one case in Okinawa rail were reported.

    “Recently, a mass outbreak of aspergillosis in kākāpō (Strigops habroptilus) and one case in Okinawa rail (Hypotaenidia okinawae) were reported [34,36].”
    Quote in the paperNot a substantial claim2 of 2 sources checked
    • cites [34] Winter, 2022, A single fungal strain was the unexpected cause of a mass aspergillosis outbreak in the world’s largest and only flightless parrot, iScience source
    • cites [36] Kano, 2021, Antifungal drugs-low-susceptibility in Aspergillus Flavus isolated from a captively reared Okinawa rail (Hypotaenidia okinawae), J. Vet. Med. Sci. source
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    In the mass outbreak in kākāpō, a single strain caused aspergillosis, and the association between the ambient environment and aspergillosis was considered an important risk factor.

    “In the mass outbreak in kākāpō, a single strain caused aspergillosis, and the association between the ambient environment and aspergillosis was considered an important risk factor [34].”
    Quote in the paperNot a substantial claim1 of 1 sources checked
    • cites [34] Winter, 2022, A single fungal strain was the unexpected cause of a mass aspergillosis outbreak in the world’s largest and only flightless parrot, iScience source
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingown data

    The main reason for moving penguins outside of the rearing enclosures was walking exercise (68% of groups).

    “The main reason for moving penguins outside of the rearing enclosures was for walking exercise (68% of groups).”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    Statistically higher aspergillosis death rates were reported among southern rockhopper (11.4%), little (10.2%), and Magellanic penguins (33.3%).

    “Statistically higher death rates were reported among southern rockhopper (11.4%), little (10.2%), and Magellanic penguins (33.3%; Table 2).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: The causes of death reported by keepers and veterinarians as aspergillosis were accurate.
  • May combine two claims.

    Findingown data

    Among Antarctic/sub-Antarctic penguins, contact with soil was associated with a higher incidence of aspergillosis (2/3 vs 6/43), but the difference was not significant (p = 0.073).

    “Penguins that had contact with soil had a higher incidence of aspergillosis (2 of 3 groups) than those that did not have contact with soil in the rearing environment (6 of 43 groups). However, there was no significant difference between with and without aspergillosis groups (p = 0.073; Table 4).”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Contact with soil is a valid proxy for exposure to Aspergillus spores.
  • May combine two claims.

    Findingown data

    26 of 54 dead penguins had contact with soil, and at least 48.1% were at risk of exposure to Aspergillus spores.

    “Furthermore, 26 of 54 dead penguins had contact with soil, and at least 48.1% of the penguins were at risk of exposure to Aspergillus spores.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The Adélie penguin was reared indoors and had no contact with soil.

    “it was also reared indoors and had no contact with soil.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The occurrence of aspergillosis in penguins was strongly related to outdoor enclosures of penguins (p < 0.01), moving of penguins outside the rearing enclosures (p < 0.01), and contact with soil (p < 0.01).

    “In accordance with these results, the occurrence of aspergillosis in penguins was strongly related to outdoor enclosures of penguins (p < 0.01), moving of penguins outside the rearing enclosures (p < 0.01), and contact with soil (p < 0.01).”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    The individual risk factors were being younger than a year, older than 20 years, or transferred from other facilities within the past year.

    “That is, they were younger than a year, were older than 20 years, or had been transferred from other facilities within the past year.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    In this study, only uncomfortable environmental factors were detected in one penguin, and only exposure to Aspergillus spores was detected in four penguins.

    “In this study, only uncomfortable environmental factors were detected in one penguin, and only exposure to Aspergillus spores was detected in four penguins.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Findingown data

    For Antarctic/sub-Antarctic penguin species, the correlation between aspergillosis occurrence and contact with soil was not significant, but the number of facilities where these species had access to soil was less.

    “The correlation between the occurrence of aspergillosis and contact with soil was not significant for the Antarctic/sub-Antarctic penguin species; however, the number of facilities where these species had access to soil was less.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingown data

    One Adélie penguin died of aspergillosis, and this was the only case of death due to aspergillosis among 500 penguins at the facility.

    “One Adélie penguin died of aspergillosis, but this was the only case of death due to aspergillosis among 500 penguins at the facility.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Findingnone given

    Some facilities include soil and plants in outdoor penguin enclosures to resemble their habitats in the wild.

    “Some facilities include soil and plants in outdoor penguin enclosures to resemble their habitats in the wild.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Findingreasoning

    Many facilities had implemented various countermeasures to decrease the incidence of aspergillosis among penguins, including prevention, early detection, and preemptive aggressive treatment, of which some are crucial.

    “Many facilities had implemented various countermeasures to decrease the incidence of aspergillosis among penguins, including prevention, early detection, and preemptive aggressive treatment, of which some are crucial.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Findingreasoning

    In this study, aspergillosis was not observed in emperor penguins, chinstrap penguins, or northern rockhopper penguins.

    “Aspergillosis was not observed in emperor penguins, chinstrap penguins, or northern rockhopper penguins in this study.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    According to the AZA Penguin Care Manual, optimal air temperature ranges are −6 °C to 7 °C for Antarctic/sub-Antarctic penguins and 4.5 °C to 26.5 °C for temperate penguins.

    “For Antarctic/sub-Antarctic penguin species, the optimal air temperature ranges from −6 °C to 7 °C. However, the optimal air temperature of temperate penguins ranges from 4.5 °C to 26.5 °C.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

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

    Premisecitation

    Aspergillosis might occur in stressed conditions, and putative stressors include inadequate heat or cold environment, stressful relocation, breeding, and molting.

    “Aspergillosis might occur in stressed conditions. Putative stressors have been associated with inadequate heat or cold environment, stressful relocation, breeding, and molting [4].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [4] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

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

    Premisenone given

    Aspergillus is ubiquitous in soil.

    “Aspergillus is ubiquitous in soil.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Waterbirds in captivity are more susceptible to aspergillosis than land birds.

    “Hllgarth and Kear [23] revealed that waterbirds in captivity are more susceptible to aspergillosis than land birds.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [23] Hillgarth, 1979, Diseases of seaducks in captivity, Wildfowl
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Premisecitation

    The three most common Aspergillus species causing aspergillosis are A. fumigatus, A. niger, and A. flavus, which are also major producers of mycotoxin aflatoxin.

    “The three most common species of the Aspergillus genus that cause aspergillosis are A. fumigatus, A. niger, and A. flavus, which are also major producers of mycotoxin aflatoxin [21].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [21] Thomas, N.J., Hunter, D.B., and Atkinson, C.T. (2008). Infectious Diseases of Wild Birds, Blackwell Publishing Professional. source
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationown data

    Environmental interventions, such as keeping away from soil, might be effective in further reducing the incidence of aspergillosis.

    “As further measures, environmental interventions, such as keeping away from soil, might be effective in further reducing the incidence of aspergillosis.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S2 (checkable).

    Interpretationreasoning

    Combined measures focusing on individual and environmental risk factors and consultation with keepers, veterinarians, and microbiologists can be useful in controlling the incidence of aspergillosis.

    “Combined measures focusing on individual and environmental risk factors as well as consultation of keepers, veterinarians, and microbiologists, such as mycobiologists, regarding rearing environment can be useful in controlling the incidence of aspergillosis.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing), S4 (based).

    Interpretationreasoning

    Clothes and items brought into rearing facilities cause the invasion of Aspergillus spores in facilities.

    “Moreover, Aspergillus is extremely common in the environment, which suggests that clothes and items brought into rearing facilities cause the invasion of Aspergillus spores in facilities.”
    Quote in the paperNot a substantial claim
    • Rests on an assumption: Aspergillus is extremely common in the environment.
  • May combine two claims.

    Interpretationreasoning

    In temperate penguin species, contact with other penguins and soil increased exposure to Aspergillus spores, which might be a risk factor for aspergillosis.

    “Even in temperate penguin species, contact with other penguins and soil increased exposure to Aspergillus spores, which might be a risk factor for aspergillosis.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Flach et al. reported that chicks (≤1 year) of gentoo penguins were the most susceptible.

    “Flach et al. [7] reported that chicks (≤1 year) of gentoo penguins were the most susceptible.”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Flach, 1990, Aspergillosis in gentoo penguins (Pygoscelis papua) at Edinburgh Zoo, 1964–1988, Vet. Rec.
  • May combine two claims.

    Interpretationreasoning

    The death rate from aspergillosis in captive penguins in Japan is currently much lower, and the preventive measures implemented are effective as basic measures.

    “However, the death rate is currently much lower, and the preventive measures implemented are effective as basic measures.”
    Quote in the paperSubstantial claim
  • Classified as probably not a substantial claim.

    Study design and conductnone given

    We did not obtain information on the type of soil used for the basement in this survey.

    “However, we did not obtain information on the type of soil used for the basement in this survey.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Aspergillosis in captive penguins was caused by the combination of individual risk factors (young and old ages), uncomfortable environments (high temperature and humidity), and rearing environments susceptible to exposure to Aspergillus spores (such as contact with soil).

    “As demonstrated in this study, aspergillosis was caused by the combination of individual risk factors, such as young and old ages; uncomfortable environments, such as high temperature and humidity; and rearing environments susceptible to exposure to Aspergillus spores, such as contact with soil.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Interpretationreasoning

    The results obtained in this study agree with our previous results.

    “The results obtained in this study agree with our previous results.”
    Quote in the paperNot a substantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing). May combine two claims.

    Study design and conductreasoning

    The methods of investigation of the earlier research differed from ours; therefore, simple comparisons are difficult to make.

    “The methods of investigation of the earlier research differed from ours; therefore, simple comparisons are difficult to make.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Premisecitation

    To the best of the authors' knowledge, surveys of aspergillosis in captive penguins have not been reported in Japan for several decades, and a nationwide survey on the occurrence of aspergillosis, rearing conditions, and countermeasures has not been performed for several decades in Japan.

    “To the best of our knowledge, surveys of aspergillosis in captive penguins have not been reported in Japan for several decades.”
    • Also stated in: § Simple Summary · plain
      “In addition, a nationwide survey on the occurrence of aspergillosis, rearing conditions, and countermeasures has not been performed for several decades in Japan.”
    Quote in the paperSubstantial claim0 of 1 sources checked
    • cites [32] Inokashira park zoo (1971). A survey of captive penguins in Japan (Japanese). J. Jpn. Assoc. Zool. Gard. Aquar., 13, 62–69.

      Not checked in the free run.

  • May combine two claims.

    Interpretationnone given

    Captive penguins in Japan are exposed to hot and humid conditions, and their immune systems may be weakened as a result of young or old age.

    “In addition, captive penguins are exposed to hot and humid conditions in Japan, and their immune systems may be weakened as a result of young or old age.”
    Quote in the paperSubstantial claim
    • Rests on an assumption: The climate in Japan is hot and humid for penguins.
  • Probably not a substantial claim: may not pass S2 (checkable). May combine two claims.

    Interpretationreasoning

    Environmental interventions might be an effective and easy method for decreasing the risk of aspergillosis, which should be considered a priority.

    “However, environmental interventions might be an effective and easy method for decreasing the risk of aspergillosis, which should be considered a priority.”
    Quote in the paperNot a substantial claim
  • May combine two claims.

    Interpretationown data

    The trends in temperate penguin species are similar to those of Antarctic/sub-Antarctic penguin species, with out-of-home migration and contact with soil as the major risk factors for aspergillosis development.

    “The trends in temperate penguin species, as shown in Table 4, are similar to those of Antarctic/sub-Antarctic penguin species as discussed above, with out-of-home migration and contact with soil as the major risk factors for aspergillosis development.”
    Quote in the paperSubstantial claim
  • May combine two claims.

    Interpretationown data

    Uncomfortable environmental factors were a source of stress for the penguins and a possible risk factor for the development of aspergillosis.

    “These uncomfortable environmental factors were a source of stress for the penguins and a possible risk factor for the development of aspergillosis.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Aspergillosis is common among birds younger than 1 year.

    “According to a previous report, aspergillosis is common among birds younger than 1 year [7].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [7] Flach, 1990, Aspergillosis in gentoo penguins (Pygoscelis papua) at Edinburgh Zoo, 1964–1988, Vet. Rec.
  • May combine two claims.

    Interpretationreasoning

    Multiple risk factors were involved in the development of aspergillosis, but other risks were not validated in this study.

    “Although multiple risk factors were involved in the development of aspergillosis, other risks were not validated in this study.”
    Quote in the paperSubstantial claim
  • Probably not a substantial claim: may not pass S3 (load-bearing).

    Premisecitation

    Antarctic/sub-Antarctic penguins are already recommended to be housed in cooler temperatures than temperate species.

    “The Antarctic/sub-Antarctic penguins are already recommended to be housed in cooler temperatures than temperate species [3].”
    Quote in the paperNot a substantial claim0 of 1 sources checked
    • cites [3] AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

      Not checked in the free run.

47 of 47
  • The paper relies on this without support.

    Aspergillosis is a major cause of mortality in captive penguins.

    “Aspergillosis is a fungal respiratory infectious disease in humans and animals and a major cause of mortality in captive penguins.”
    “Aspergillosis is one of the leading causes of death in captive penguins.”
  • The paper relies on this without support.

    The efficacy of rearing conditions and countermeasures in preventing aspergillosis has not been investigated sufficiently.

    “However, their efficacy has not been investigated sufficiently.”
  • The paper relies on this without support.

    In Japan, nationally standardized guidelines for the care of penguins have not been established.

    “In Japan, nationally standardized guidelines for the care of penguins have not been established.”
  • The paper relies on this without support.

    The causes of death reported by keepers and veterinarians as aspergillosis were accurate.

    “species and the number of penguins that had died of aspergillosis in the 5 years from April 2016 to March 2021”
    “cause of death suspected by respondents”
  • The paper relies on this without support.

    Contact with soil is a valid proxy for exposure to Aspergillus spores.

    “Moreover, the probability of contact between penguins and soil as a risk factor for exposure to Aspergillus spores was aggregated.”
  • The paper relies on this without support.

    The 64 responding facilities are representative of JAZA facilities that rear penguins.

    “we sent a questionnaire (Supplementary File S1) about aspergillosis in penguins to 89 zoos and aquariums (members of JAZA) that bred penguins. Sixty-four facilities responded to the questionnaire with information on 2910 penguins belonging to 11 species (Table 1), and these data were used in the analysis.”
  • The paper relies on this without support.

    The questionnaire responses accurately reflect the rearing environments and preventive measures at the facilities.

    “Based on these responses, we initially determined the number and mortality rate of aspergillosis in each penguin species.”
  • The paper relies on this without support.

    The number of preventive measures taken is a valid measure of preventive effort against aspergillosis.

    “We examined the association between the number of measures and incidence of aspergillosis.”
  • The paper relies on this without support.

    Aspergillus is extremely common in the environment.

    “Moreover, Aspergillus is extremely common in the environment, which suggests that clothes and items brought into rearing facilities cause the invasion of Aspergillus spores in facilities.”
  • The paper relies on this without support.

    Kākāpō, Okinawa rail, and penguins are flightless birds, and they walk on the soil.

    “Kākāpō, Okinawa rail, and penguins are flightless birds, and they walk on the soil.”
  • The paper relies on this without support.

    Aspergillus is ubiquitous both in soil and in the air.

    “Aspergillus is ubiquitous both in soil and in the air; therefore, it is difficult to eliminate contact with Aspergillus outdoors and even indoors.”
  • The paper relies on this without support.

    The climate in Japan is hot and humid for penguins.

    “Although the climate in Japan is hot and humid for penguins, various improvements in zoos and aquariums, such as reference to and adherence to penguin breeding manuals [33] and preventive management [28,29,30], were thought to have reduced the number of deaths.”
12 of 12

Self-check

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

Each contradiction between two passages listed here was confirmed by an independent check.

  • Conflicting totals for Magellanic penguin deaths

    Minor

    The Results report 13 Magellanic penguin deaths from aspergillosis, but the Discussion describes the same single-facility cluster as four of eight deaths. Both passages say four deaths occurred at one facility, but they give different totals.

1 of 1

Cites

Flagged first, then by citations

2 of the 36 references couldn’t be matched to a known paper.

Research works printed but not linked: 5

  1. AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.
  2. AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.
  3. Xavier, 2011, Clinical and pathological findings of Aspergillosis in Magellanic penguins (Spheniscus magellanicus), Ciênc Anim. Bras., 12, 520
  4. Miller, R.E., and Fowler, M.E. (2015). Zoo and Wild Animal Medicine, Elsevier Saunders. [8th ed.].
  5. AZA Penguin Taxon Advisory Group (2014). Penguin (Spheniscidae) Care Manual, Association of Zoos and Aquariums.

Cited by

Sorted by citations

Authors
Itoh, M., Matsumoto, N., Hagino, K., Sawayama, N., Kuwayama, M., Yamada, K., & Toyotome, T.
Affiliations
  • Obihiro University of Agriculture and Veterinary Medicine (JP)
  • Azabu University (JP)
  • Noboribetsu Marine Park Nixe, Noboribetsu 059-0492, Hokkaido, Japan
  • Chiba University (JP)
Corresponding author
Toyotome, Takahito
Venue
Animals
Publisher
MDPI AG
Published
2023-06-08
Volume
13
Issue
12
Pages
1913
ISSN
2076-2615 (ISSN-L)
OpenAlex
W4379882519
Cited by
5
References
36
Citations by year
2026: 1 · 2025: 2 · 2024: 2
FWCI
0.93
Type
journal article
Language
en
Open access
Locations
  • Animals (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Institutional Repositories DataBase (IRDB) (submittedVersion)
Funders
Japan Society for the Promotion of Science KAKENHI (C) (21K05931)
Topics
  • Health Sciences › Medicine › Infectious Diseases › Antifungal resistance and susceptibility
  • Health Sciences › Veterinary › Small Animals › Animal Behavior and Welfare Studies
  • Health Sciences › Medicine › Epidemiology › Fungal Infections and Studies
Keywords
aspergillosis, captive penguins, zoo animals, aquarium animals, Aspergillus, disease incidence, risk factors, environmental risk factors, soil exposure, preventive measures

About these checks

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 2026-10-27.

Classified by jev-1.13-20260917 (gold-guideline-v0.2) on 2026-10-27.

Cited sources are checked by gpt-6-sol.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review