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  1. Article ; Online: Growth faltering regardless of chronic diarrhea is associated with mucosal immune dysfunction and microbial dysbiosis in the gut lumen.

    Rhoades, Nicholas S / Hendrickson, Sara M / Prongay, Kamm / Haertel, Andrew / Gill, Leanne / Edwards, Robert A / Garzel, Laura / Slifka, Mark K / Messaoudi, Ilhem

    Mucosal immunology

    2021  Volume 14, Issue 5, Page(s) 1113–1126

    Abstract: Despite the impact of childhood diarrhea on morbidity and mortality, our understanding of its sequelae has been significantly hampered by the lack of studies that examine samples across the entire intestinal tract. Infant rhesus macaques are naturally ... ...

    Abstract Despite the impact of childhood diarrhea on morbidity and mortality, our understanding of its sequelae has been significantly hampered by the lack of studies that examine samples across the entire intestinal tract. Infant rhesus macaques are naturally susceptible to human enteric pathogens and recapitulate the hallmarks of diarrheal disease such as intestinal inflammation and growth faltering. Here, we examined intestinal biopsies, lamina propria leukocytes, luminal contents, and fecal samples from healthy infants and those experiencing growth faltering with distant acute or chronic active diarrhea. We show that growth faltering in the presence or absence of active diarrhea is associated with a heightened systemic and mucosal pro-inflammatory state centered in the colon. Moreover, polyclonal stimulation of colonic lamina propria leukocytes resulted in a dampened cytokine response, indicative of immune exhaustion. We also detected a functional and taxonomic shift in the luminal microbiome across multiple gut sites including the migration of Streptococcus and Prevotella species between the small and large intestine, suggesting a decompartmentalization of gut microbial communities. Our studies provide valuable insight into the outcomes of diarrheal diseases and growth faltering not attainable in humans and lays the groundwork to test interventions in a controlled and reproducible setting.
    MeSH term(s) Animals ; Biodiversity ; Biomarkers ; Biopsy ; Chronic Disease ; Diarrhea/complications ; Diarrhea/etiology ; Diarrhea/metabolism ; Diarrhea/pathology ; Disease Models, Animal ; Disease Susceptibility ; Dysbiosis/complications ; Dysbiosis/immunology ; Gastrointestinal Microbiome/immunology ; Growth Disorders/etiology ; Growth Disorders/metabolism ; Immunity, Mucosal/genetics ; Immunohistochemistry ; Intestinal Mucosa/immunology ; Intestinal Mucosa/metabolism ; Intestinal Mucosa/pathology ; Lymphocyte Count ; Macaca mulatta ; Metagenome ; Metagenomics/methods ; Transcriptome
    Chemical Substances Biomarkers
    Language English
    Publishing date 2021-06-22
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2411370-0
    ISSN 1935-3456 ; 1933-0219
    ISSN (online) 1935-3456
    ISSN 1933-0219
    DOI 10.1038/s41385-021-00418-2
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  2. Article ; Online: Reduced infant rhesus macaque growth rates due to environmental enteric dysfunction and association with histopathology in the large intestine.

    Hendrickson, Sara M / Thomas, Archana / Prongay, Kamm / Haertel, Andrew J / Garzel, Laura M / Gill, Leanne / Barr, Tasha / Rhoades, Nicholas S / Reader, Rachel / Galan, Mark / Carroll, Julie M / Roberts, Charles T / Gao, Lina / Amanna, Ian J / Messaoudi, Ilhem / Slifka, Mark K

    Nature communications

    2022  Volume 13, Issue 1, Page(s) 234

    Abstract: Environmental enteric dysfunction is associated with malnutrition as well as infant growth stunting and has been classically defined by villous blunting, decreased crypt-to-villus ratio, and inflammation in the small intestine. Here, we characterized ... ...

    Abstract Environmental enteric dysfunction is associated with malnutrition as well as infant growth stunting and has been classically defined by villous blunting, decreased crypt-to-villus ratio, and inflammation in the small intestine. Here, we characterized environmental enteric dysfunction among infant rhesus macaques that are naturally exposed to enteric pathogens commonly linked to human growth stunting. Remarkably, despite villous atrophy and histological abnormalities observed in the small intestine, poor growth trajectories and low serum tryptophan levels were correlated with increased histopathology in the large intestine. This work provides insight into the mechanisms underlying this disease and indicates that the large intestine may be an important target for therapeutic intervention.
    MeSH term(s) Animals ; Duodenum/pathology ; Female ; Gastrointestinal Tract ; Gene Expression ; Growth Disorders/pathology ; Humans ; Ileum/pathology ; Inflammation ; Intestinal Diseases ; Intestinal Mucosa ; Intestine, Large/pathology ; Intestine, Small/pathology ; Jejunum/pathology ; Macaca mulatta/growth & development ; Male ; Malnutrition
    Language English
    Publishing date 2022-01-11
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2553671-0
    ISSN 2041-1723 ; 2041-1723
    ISSN (online) 2041-1723
    ISSN 2041-1723
    DOI 10.1038/s41467-021-27925-x
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  3. Article ; Online: Maturation of the infant rhesus macaque gut microbiome and its role in the development of diarrheal disease.

    Rhoades, Nicholas / Barr, Tasha / Hendrickson, Sara / Prongay, Kamm / Haertel, Andrew / Gill, Leanne / Garzel, Laura / Whiteson, Katrine / Slifka, Mark / Messaoudi, Ilhem

    Genome biology

    2019  Volume 20, Issue 1, Page(s) 173

    Abstract: Background: Diarrhea is the second leading cause of death in children under 5 years of age. Enhanced understanding of causal pathways, pathogenesis, and sequelae of diarrhea is urgently needed. Although the gut microbiota is believed to play a role in ... ...

    Abstract Background: Diarrhea is the second leading cause of death in children under 5 years of age. Enhanced understanding of causal pathways, pathogenesis, and sequelae of diarrhea is urgently needed. Although the gut microbiota is believed to play a role in susceptibility to diarrheal diseases, our understanding of this association remains incomplete. Infant rhesus macaques (Macaca mulatta) are susceptible to diarrhea making them an ideal model to address this question.
    Results: The maturation of the infant rhesus macaque gut microbiome throughout the first 8 months of life occurs in a similar pattern as that described for human infants. Moreover, the microbiome of the captive reared infant rhesus macaque more closely resembles that of human infants in the developing world than in the western world. Importantly, prior to disease onset, the gut microbiome of infants that later develop diarrhea is enriched in pathways of immunomodulatory metabolite synthesis, while those of infants that remain asymptomatic are enriched in pathways for short-chain fatty acid production. We identify Prevotella strains that are more abundant at 1 month in infants that later develop diarrhea. At 8 months, the microbiomes of animals that experience diarrhea show increased abundance of Campylobacter and a reduction in Helicobacter macacae.
    Conclusion: The composition of the microbial community could provide a phenotypic marker of an infant's susceptibility to diarrheal disease. Given the significant physiological and immunological similarities between human and nonhuman primates, these findings provide potential markers of susceptibility to diarrhea that could be modulated to improve infant health, especially in the developing world.
    MeSH term(s) Aging ; Animals ; Animals, Newborn ; Anti-Bacterial Agents/therapeutic use ; Bacteria/genetics ; Biomarkers/metabolism ; Carrier State/microbiology ; Child ; Child, Preschool ; Developed Countries ; Developing Countries ; Diarrhea/drug therapy ; Diarrhea/microbiology ; Disease Susceptibility ; Female ; Gastrointestinal Microbiome ; Genome, Bacterial ; Humans ; Infant ; Macaca mulatta ; Male ; Metagenomics ; Phylogeny
    Chemical Substances Anti-Bacterial Agents ; Biomarkers
    Language English
    Publishing date 2019-08-26
    Publishing country England
    Document type Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
    ZDB-ID 2040529-7
    ISSN 1474-760X ; 1474-760X
    ISSN (online) 1474-760X
    ISSN 1474-760X
    DOI 10.1186/s13059-019-1789-x
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  4. Article ; Online: The impact of housing on birth outcomes in breeding macaque groups across multiple research centers.

    Haertel, Andrew J / Beisner, Brianne A / Buehler, Margaret S / Capuano, Saverio / Carrol, Kelsey E / Church, Travis / Cohen, Joyce K / Crane, Maria M / Dutton, John W / Falkenstein, Katherine P / Gill, Leanne / Hopper, Lydia M / Hotchkiss, Charlotte E / Lee, Grace H / Malinowski, Carolyn M / Mendoza, Elda / Sayers, Ken / Scorpio, Diana G / Stockinger, Diane /
    Taylor, Joshua M

    American journal of primatology

    2023  Volume 85, Issue 11, Page(s) e23554

    Abstract: Demand for nonhuman primates in research has increased over the past several years, while nonhuman primate supply remains a challenge in the United States. Global nonhuman primate supply issues make it increasingly important to maximize domestic colony ... ...

    Abstract Demand for nonhuman primates in research has increased over the past several years, while nonhuman primate supply remains a challenge in the United States. Global nonhuman primate supply issues make it increasingly important to maximize domestic colony production. To explore how housing conditions across primate breeding colonies impact infant survival and animal production more broadly, we collected medical records from 7959 rhesus macaques (Macaca mulatta) and 492 pigtail macaques (Macaca nemestrina) across seven breeding facilities and used generalized mixed-effect modeling to determine prenatal and infant survival odds by housing type and group size. Infant survival odds for each housing type and group size varied for prenatal, neonatal, early infant, and late infant age groups. Odds of prenatal survival were lowest in paired indoor housing and small and medium outdoor groups. No housing type performed better than large outdoor groups for neonatal survival. Odds of early infant survival was greatest in indoor and mixed indoor/outdoor housing compared to large outdoor enclosures. Large outdoor housing was associated with higher survival odds for late infant survival compared to small and medium outdoor housing. These results may influence housing choices at macaque breeding facilities hoping to maximize infant success, although there are relative care costs, the promotion of species-typical behaviors, and infrastructure factors to also consider. Our study used an interinstitutional collaboration that allowed for the analysis of more infant macaque medical records than ever before and used the broad variations across the seven national primate research centers to make the results applicable to many other facilities housing macaques.
    MeSH term(s) Humans ; Pregnancy ; Female ; Animals ; Macaca mulatta ; Macaca nemestrina ; Housing, Animal ; Breeding
    Language English
    Publishing date 2023-09-29
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.23554
    Database MEDical Literature Analysis and Retrieval System OnLINE

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  5. Article: Maturation of the infant rhesus macaque gut microbiome and its role in the development of diarrheal disease

    Rhoades, Nicholas / Barr, Tasha / Hendrickson, Sara / Prongay, Kamm / Haertel, Andrew / Gill, Leanne / Garzel, Laura / Whiteson, Katrine / Slifka, Mark / Messaoudi, Ilhem

    Genome biology. 2019 Dec., v. 20, no. 1

    2019  

    Abstract: BACKGROUND: Diarrhea is the second leading cause of death in children under 5 years of age. Enhanced understanding of causal pathways, pathogenesis, and sequelae of diarrhea is urgently needed. Although the gut microbiota is believed to play a role in ... ...

    Abstract BACKGROUND: Diarrhea is the second leading cause of death in children under 5 years of age. Enhanced understanding of causal pathways, pathogenesis, and sequelae of diarrhea is urgently needed. Although the gut microbiota is believed to play a role in susceptibility to diarrheal diseases, our understanding of this association remains incomplete. Infant rhesus macaques (Macaca mulatta) are susceptible to diarrhea making them an ideal model to address this question. RESULTS: The maturation of the infant rhesus macaque gut microbiome throughout the first 8 months of life occurs in a similar pattern as that described for human infants. Moreover, the microbiome of the captive reared infant rhesus macaque more closely resembles that of human infants in the developing world than in the western world. Importantly, prior to disease onset, the gut microbiome of infants that later develop diarrhea is enriched in pathways of immunomodulatory metabolite synthesis, while those of infants that remain asymptomatic are enriched in pathways for short-chain fatty acid production. We identify Prevotella strains that are more abundant at 1 month in infants that later develop diarrhea. At 8 months, the microbiomes of animals that experience diarrhea show increased abundance of Campylobacter and a reduction in Helicobacter macacae. CONCLUSION: The composition of the microbial community could provide a phenotypic marker of an infant’s susceptibility to diarrheal disease. Given the significant physiological and immunological similarities between human and nonhuman primates, these findings provide potential markers of susceptibility to diarrhea that could be modulated to improve infant health, especially in the developing world.
    Keywords Campylobacter ; Helicobacter ; Macaca mulatta ; Prevotella ; children ; complications (disease) ; death ; diarrhea ; disease susceptibility ; humans ; infants ; intestinal microorganisms ; metabolites ; microbial communities ; microbiome ; models ; pathogenesis ; phenotype ; rearing ; short chain fatty acids
    Language English
    Dates of publication 2019-12
    Size p. 173.
    Publishing place BioMed Central
    Document type Article
    ZDB-ID 2040529-7
    ISSN 1474-760X ; 1465-6906
    ISSN (online) 1474-760X
    ISSN 1465-6906
    DOI 10.1186/s13059-019-1789-x
    Database NAL-Catalogue (AGRICOLA)

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  6. Article ; Online: Genetic characterization of specific pathogen-free rhesus macaque (Macaca mulatta) populations at the California National Primate Research Center (CNPRC).

    Kanthaswamy, Sree / Kou, Alex / Satkoski, Jessica / Penedo, Maria Cecilia T / Ward, Thea / Ng, Jillian / Gill, Leanne / Lerche, Nicholas W / Erickson, Bethany J-A / Smith, David Glenn

    American journal of primatology

    2010  Volume 72, Issue 7, Page(s) 587–599

    Abstract: A study based on 14 STRs was conducted to understand intergenerational genetic changes that have occurred within the California National Primate Research Center's (CNPRC) regular specific pathogen-free (SPF) and super-SPF captive rhesus macaque ... ...

    Abstract A study based on 14 STRs was conducted to understand intergenerational genetic changes that have occurred within the California National Primate Research Center's (CNPRC) regular specific pathogen-free (SPF) and super-SPF captive rhesus macaque populations relative to their conventional founders. Intergenerational genetic drift has caused age cohorts of each study population, especially within the conventional population, to become increasingly differentiated from each other and from their founders. Although there is still only minimal stratification between the conventional population and either of the two SPF populations, separate derivation of the regular and super-SPF animals from their conventional founders has caused the two SPF populations to remain marginally different from each other. The regular SPF and, especially, the super-SPF populations have been influenced by the effects of differential ancestry, sampling, and lost rare alleles, causing a substantial degree of genetic divergence between these subpopulations. The country of origin of founders is the principal determinant of the MHC haplotype composition of the SPF stocks at the CNPRC. Selection of SPF colony breeders bearing desired genotypes of Mamu-A*01 or -B*01 has not affected the overall genetic heterogeneity of the conventional and the SPF research stocks.Because misclassifying the ancestry of research stocks can undermine experimental outcomes by excluding animals with regional-specific genotypes or phenotypes of importance, understanding founder/descendent genetic relationships is crucial for investigating candidate genes with distinct geographic origins. Together with demographic management, population genetic assessments of SPF colonies can curtail excessive phenotypic variation among the study stocks and facilitate successful production goals.
    MeSH term(s) Animals ; Breeding/methods ; California ; China/ethnology ; Chromosome Mapping ; Cohort Studies ; DNA Primers ; Female ; Gene Frequency ; Genetic Variation ; Genome ; Genotype ; India/ethnology ; Macaca mulatta/genetics ; Male ; Specific Pathogen-Free Organisms/genetics
    Chemical Substances DNA Primers
    Language English
    Publishing date 2010-02-10
    Publishing country United States
    Document type Journal Article ; Research Support, N.I.H., Extramural
    ZDB-ID 1495834-X
    ISSN 1098-2345 ; 0275-2565
    ISSN (online) 1098-2345
    ISSN 0275-2565
    DOI 10.1002/ajp.20811
    Database MEDical Literature Analysis and Retrieval System OnLINE

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