The Gottingen minipig is a model of the hematopoietic acute radiation syndrome: g-colony stimulating factor stimulates hematopoiesis and enhances survival from lethal total-body γ-irradiation

Moroni, Maria; Ngudiankama, Barbara F.; Christensen, Christine; Olsen, Cara H.; Owens, Rossitsa; Lombardini, Eric D.; Holt, Rebecca K.; Whitnall, Mark H.

doi:10.1016/j.ijrobp.2013.04.041

Cited by 68Effects of Radiation ExposureHematopoietic Stem Cell TransplantationImmunotoxicology and immune responses

The Gottingen minipig is a model of the hematopoietic acute radiation syndrome: g-colony stimulating factor stimulates hematopoiesis and enhances survival from lethal total-body γ-irradiation

Open access

Moroni, Maria, Ngudiankama, Barbara F., Christensen, Christine, Olsen, Cara H., Owens, Rossitsa, Lombardini, Eric D., Holt, Rebecca K., Whitnall, Mark H.·2013·International Journal of Radiation Oncology*Biology*Physics

DOI 10.1016/j.ijrobp.2013.04.041PMC PMC3710733

Open this paper in CoChat — free account

Abstract

Purpose We are characterizing the Gottingen minipig as an additional large animal model for advanced drug testing for the acute radiation syndrome (ARS) to enhance the discovery and development of novel radiation countermeasures. Among the advantages provided by this model, the similarities to human hematologic parameters and dynamics of cell loss/recovery after irradiation provide a convenient means to compare the efficacy of drugs known to affect bone marrow cellularity and hematopoiesis. Methods and materials Male Gottingen minipigs, 4 to 5 months old and weighing 9 to 11 kg, were used for this study. We tested the standard off-label treatment for ARS, rhG-CSF (Neupogen, 10 μg/kg/day for 17 days), at the estimated LD70/30 total-body γ-irradiation (TBI) radiation dose for the hematopoietic syndrome, starting 24 hours after irradiation. Results The results indicated that granulocyte colony stimulating factor (G-CSF) enhanced survival, stimulated recovery from neutropenia, and induced mobilization of hematopoietic progenitor cells. In addition, the administration of G-CSF resulted in maturation of monocytes/macrophages. Conclusions These results support continuing efforts toward validation of the minipig as a large animal model for advanced testing of radiation countermeasures and characterization of the pathophysiology of ARS, and they suggest that the efficacy of G-CSF in improving survival after total body irradiation may involve mechanisms other than increasing the numbers of circulating granulocytes.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1016/j.ijrobp.2013.04.041

Cites

20 of 20 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

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?

In addition to clinical experience in radiological accident victims, there is a wealth of literature evaluating the efficacy of colony stimulating factors in well-controlled, randomized studies in canine, swine, and non-human primate models.
“However, in addition to clinical experience in radiological accident victims, there is a wealth of literature evaluating the efficacy of colony stimulating factors in wellcontrolled, randomized studies in canine, swine, and non-human primate models (MacVittie et al., 1991;Moroni et al., 2013;Legesse et al., 2019).”
From Medical countermeasures for the hematopoietic-subsyndrome of acute radiation syndrome in space (2022) · cites this paper as Moroni et al., 2013
Split into 2 atoms — 1 confirmed, 1 partially supported, 0 disputed, 0 misattributed, 0 unverifiable. Expand the claim to see per-atom verdicts.
Experimental — accuracy not yet measured
Those studies provide strong evidence for an acceleration of recovery from myelosuppression with a reduced risk for infection and bleeding leading to an improvement in the likelihood of survival.
“In total, those studies provide strong evidence for an acceleration of recovery from myelosuppression with a reduced risk for infection and bleeding leading to an improvement in the likelihood of survival.”
From Medical countermeasures for the hematopoietic-subsyndrome of acute radiation syndrome in space (2022) · cites this paper as Moroni et al., 2013
The Discussion reports that G-CSF shortened neutropenia and thrombocytopenia and improved survival in irradiated minipigs. But the Results report similar microscopic hemorrhage in both groups and bacterial pneumonia in about half of each group, so the claimed reduction in infection and bleeding risk is not supported by these observations. Our copy provides no page numbers for these passages. (LLM, conf=0.88)
Experimental — accuracy not yet measured

Self-check

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

The self-check needs the paper’s full text.

1 retracted

RETRACTED: CD163 and its expanding functional repertoire
Akila, P., Prashant, A., Suma, M., Prashant, S., & Chaitra, T. R. (2012) · Clinica Chimica Acta · doi:10.1016/j.cca.2012.01.028 · Cited by 50 · see citing works
Retracted
Medical Management of the Acute Radiation Syndrome: Recommendations of the Strategic National Stockpile Radiation Working Group
Waselenko, J. K., MacVittie, T. J., Blakely, W. F., Pesik, N., Wiley, A. L., Dickerson, W. E., Tsu, H., Confer, D. L., Coleman, C. N., Seed, T., et al. (2004) · Annals of Internal Medicine · doi:10.7326/0003-4819-140-12-200406150-00015 · Cited by 766 · see citing works
Platelet-derived microparticles bind to hematopoietic stem/progenitor cells and enhance their engraftment
Janowska‐Wieczorek, A., Majka, M., Kijowski, J., Baj‐Krzyworzeka, M., Reca, R., Turner, A. R., Ratajczak, J., Emerson, S. G., Kowalska, M. A., & Ratajczak, M. Z. (2001) · Blood · doi:10.1182/blood.v98.10.3143 · Cited by 354 · see citing works
Filgrastim improves survival in lethally irradiated nonhuman primates
Farese, A. M., Cohen, M. V., Katz, B. P., Smith, C. P., Gibbs, A., Cohen, D. M., & MacVittie, T. J. (2013) · Radiation Research · doi:10.1667/rr3049.1 · Cited by 187 · see citing works
Membrane markers of the immune cells in swine: an update
Piriou-Guzylack, L., & Salmon, H. (2008) · Veterinary Research · doi:10.1051/vetres:2008030 · Cited by 149 · see citing works
First global consensus for evidence-based management of the hematopoietic syndrome resulting from exposure to ionizing radiation
Dainiak, N., Gent, R. N., Carr, Z., Schneider, R., Bader, J., Buglova, E., Chao, N., Coleman, C. N., Ganser, A., Gorin, C., et al. (2011) · Disaster Medicine and Public Health Preparedness · doi:10.1001/dmp.2011.68 · Cited by 107 · see citing works
Multipotent mesenchymal stem cell grafting to treat cutaneous radiation syndrome: Development of a new minipig model
Agay, D., Scherthan, H., Forcheron, F., Grenier, N., Hérodin, F., Meineke, V., & Drouet, M. (2010) · Experimental Hematology · doi:10.1016/j.exphem.2010.06.008 · Cited by 107 · see citing works
DEFINING THE FULL THERAPEUTIC POTENTIAL OF RECOMBINANT GROWTH FACTORS IN THE POST RADIATION-ACCIDENT ENVIRONMENT: THE EFFECT OF SUPPORTIVE CARE PLUS ADMINISTRATION OF G-CSF
MacVittie, T. J., Farese, A. M., & Jackson, W. (2005) · Health Physics · doi:10.1097/01.hp.0000173143.69659.5b · Cited by 99 · see citing works
Autologous Adipocyte Derived Stem Cells Favour Healing in a Minipig Model of Cutaneous Radiation Syndrome
Forcheron, F., Agay, D., Scherthan, H., Riccobono, D., Hérodin, F., Meineke, V., & Drouet, M. (2012) · PLoS ONE · doi:10.1371/journal.pone.0031694 · Cited by 86 · see citing works
Phenotypic and functional heterogeneity of porcine blood monocytes and its relation with maturation
Chamorro, S., Revilla, C., Álvarez, B., Alonso, F., Ezquerra, Á., & Domı́nguez, J. (2004) · Immunology · doi:10.1111/j.1365-2567.2004.01994.x · Cited by 84 · see citing works
Single administration of stem cell factor, FLT-3 ligand, megakaryocyte growth and development factor, and interleukin-3 in combination soon after irradiation prevents nonhuman primates from myelosuppression: long-term follow-up of hematopoiesis
Drouet, M., Mourcin, F., Grenier, N., Leroux, V., Denis, J., Mayol, J.-F., Thullier, P., Lataillade, J., & Hérodin, F. (2003) · Blood · doi:10.1182/blood-2003-05-1400 · Cited by 81 · see citing works
Hematological Changes as Prognostic Indicators of Survival: Similarities Between Gottingen Minipigs, Humans, and Other Large Animal Models
Moroni, M., Lombardini, E., Salber, R. E., Kazemzedeh, M., Nagy, V., Olsen, C. H., & Whitnall, M. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025210 · Cited by 75 · see citing works
Self-citation
Validating Animal Models for Preclinical Research: A Scientific and Ethical Discussion
Varga, O., Hansen, A. K., Sandøe, P., & Olsson, I. A. S. (2010) · Alternatives to Laboratory Animals · doi:10.1177/026119291003800309 · Cited by 74 · see citing works
Hematopoietic Radiation Syndrome in the Gottingen Minipig
Moroni, M., Coolbaugh, T. V., Lombardini, E., Mitchell, J., Moccia, K. D., Shelton, L. J., Nagy, V., & Whitnall, M. H. (2011) · Radiation Research · doi:10.1667/rr2481.1 · Cited by 70 · see citing works
Self-citation
Combination therapy for radiation-induced bone marrow aplasia in nonhuman primates using synthokine SC-55494 and recombinant human granulocyte colony-stimulating factor
MacVittie, T. J., Farese, A. M., Hérodin, F., Grab, L. B., Baum, C. M., & McKearn, J. (1996) · Blood · doi:10.1182/blood.v87.10.4129.bloodjournal87104129 · Cited by 67 · see citing works
Antiapoptotic cytokines in combination with pegfilgrastim soon after irradiation mitigates myelosuppression in nonhuman primates exposed to high irradiation dose
Hérodin, F., Roy, L., Grenier, N., Delaunay, C., Baugé, S., Vaurijoux, A., Grégoire, E., Martin, C., Alonso, A., Mayol, J.-F., et al. (2007) · Experimental Hematology · doi:10.1016/j.exphem.2007.04.017 · Cited by 52 · see citing works
5-AED enhances survival of irradiated mice in a G-CSF-dependent manner, stimulates innate immune cell function, reduces radiation-induced DNA damage and induces genes that modulate cell cycle progression and apoptosis
Grace, M. B., Singh, V. K., Rhee, J. G., Jackson, W. E., Kao, T., & Whitnall, M. H. (2012) · Journal of Radiation Research · doi:10.1093/jrr/rrs060 · Cited by 49 · see citing works
Self-citation
Haematological Effects of RhGM-CSF in Dogs Exposed to Total-body Irradiation with a Dose of 2·4 Gy
Nothdurft, W., Selig, C., Fliedner, T. M., Hintz-Obertreis, P., Kreja, L., Krumwieh, D., Kurrle, R., Seiler, F. R., & Weinsheimer, W. (1992) · International Journal of Radiation Biology · doi:10.1080/09553009214551281 · Cited by 30 · see citing works
Vascular access port implantation and serial blood sampling in a Gottingen minipig (Sus scrofa domestica) model of acute radiation injury.
Moroni, M., Coolbaugh, T. V., Mitchell, J., Lombardini, E., Moccia, K. D., Shelton, L. J., Nagy, V., & Whitnall, M. H. (2011) · PubMed Central · Cited by 24 · see citing works
Self-citation
RhG-CSF Improves Radiation-induced Myelosuppression and Survival in the Canine Exposed to Fission Neutron Irradiation
Yu, Z.-Y., Li, M., Han, A.-R.-N., Xing, S. J., Ou, H., Xiong, G.-L., Xie, L., Yan-Fang, Z. H. A. O., Xiao, H., Shan, Y., et al. (2011) · Journal of Radiation Research · doi:10.1269/jrr.10103 · Cited by 15 · see citing works

Flagged first, then by citations

Sorted by citations

Filgrastim improves survival in lethally irradiated nonhuman primates
Farese, A. M., Cohen, M. V., Katz, B. P., Smith, C. P., Gibbs, A., Cohen, D. M., & MacVittie, T. J. (2013) · Radiation Research · doi:10.1667/rr3049.1 · Cited by 187 · see citing works
A review of radiation countermeasures focusing on injury-specific medicinals and regulatory approval status: part I. Radiation sub-syndromes, animal models and FDA-approved countermeasures
Singh, V. K., & Seed, T. M. (2017) · International Journal of Radiation Biology · doi:10.1080/09553002.2017.1332438 · Cited by 176 · see citing works
Mechanisms of radiation-induced endothelium damage: Emerging models and technologies
Wijerathne, H., Langston, J. C., Yang, Q., Sun, S., Miyamoto, C. T., Kilpatrick, L. E., & Kiani, M. F. (2021) · Radiotherapy and Oncology · doi:10.1016/j.radonc.2021.02.007 · Cited by 175 · see citing works
Animal models for acute radiation syndrome drug discovery
Singh, V. K., Newman, V. L., Berg, A. N., & MacVittie, T. J. (2015) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2015.1023290 · Cited by 139 · see citing works
Pegfilgrastim improves survival of lethally irradiated nonhuman primates
Hankey, K. G., Farese, A. M., Blaauw, E. C., Gibbs, A. M., Smith, C. P., Katz, B. P., Tong, Y., Prado, K. L., & MacVittie, T. J. (2015) · Radiation Research · doi:10.1667/rr13940.1 · Cited by 129 · see citing works
Pharmacological management of ionizing radiation injuries: current and prospective agents and targeted organ systems
Singh, V. K., & Seed, T. M. (2020) · Expert Opinion on Pharmacotherapy · doi:10.1080/14656566.2019.1702968 · Cited by 126 · see citing works
Colony-stimulating factors for the treatment of the hematopoietic component of the acute radiation syndrome (H-ARS): A review
Singh, V. K., Newman, V. L., & Seed, T. M. (2014) · Cytokine · doi:10.1016/j.cyto.2014.08.003 · Cited by 121 · see citing works
Radiation countermeasure agents: an update (2011 – 2014)
Singh, V. K., Newman, V. L., Romaine, P. L. P., Wise, S. Y., & Seed, T. M. (2014) · Expert Opinion on Therapeutic Patents · doi:10.1517/13543776.2014.964684 · Cited by 112 · see citing works
Radiation countermeasures for hematopoietic acute radiation syndrome: growth factors, cytokines and beyond
Singh, V. K., & Seed, T. M. (2021) · International Journal of Radiation Biology · doi:10.1080/09553002.2021.1969054 · Cited by 88 · see citing works
Modeling Hematopoiesis and Responses to Radiation Countermeasures in a Bone Marrow-on-a-Chip
Torisawa, Y., Mammoto, T., Jiang, E., Jiang, A. R., Mammoto, A., Watters, A. L., Bahinski, A., & Ingber, D. E. (2016) · Tissue Engineering Part C Methods · doi:10.1089/ten.tec.2015.0507 · Cited by 72 · see citing works
Survival Efficacy of the PEGylated G-CSFs Maxy-G34 and Neulasta in a Mouse Model of Lethal H-ARS, and Residual Bone Marrow Damage in Treated Survivors
Chua, H. L., Plett, P. A., Sampson, C. H., Katz, B. P., Carnathan, G. W., MacVittie, T. J., Lenden, K., & Orschell, C. M. (2013) · Health Physics · doi:10.1097/hp.0b013e3182a4df10 · Cited by 54 · see citing works
Medical countermeasures for unwanted CBRN exposures: part II radiological and nuclear threats with review of recent countermeasure patents
Singh, V. K., Romaine, P. L. P., Newman, V. L., & Seed, T. M. (2016) · Expert Opinion on Therapeutic Patents · doi:10.1080/13543776.2016.1231805 · Cited by 42 · see citing works
Subject-Based versus Population-Based Care after Radiation Exposure
Yu, J.-Z., Lindeblad, M., Lyubimov, A., Neri, F., Smith, B., Szilagyi, E., Halliday, L. C., MacVittie, T., Nanda, J. P., & Bartholomew, A. M. (2015) · Radiation Research · doi:10.1667/rr13918.1 · Cited by 35 · see citing works
Impact of Abbreviated Filgrastim Schedule on Survival and Hematopoietic Recovery after Irradiation in Four Mouse Strains with Different Radiosensitivity
Satyamitra, M. M., Kumar, V. P., Biswas, S., Cary, L. H., Dickson, L., Venkataraman, S., & Ghosh, S. P. (2017) · Radiation Research · doi:10.1667/rr14555.1 · Cited by 33 · see citing works
Use of Growth Factors and Other Cytokines for Treatment of Injuries During a Radiation Public Health Emergency
DiCarlo, A. L., Horta, Z. P., Aldrich, J. T., Jakubowski, A. A., Skinner, W., & Case, C. M. (2019) · Radiation Research · doi:10.1667/rr15363.1 · Cited by 32 · see citing works
Specific Members of the Gut Microbiota are Reliable Biomarkers of Irradiation Intensity and Lethality in Large Animal Models of Human Health
Carbonero, F. G., Mayta, A., Bolea, M., Yu, J.-Z., Lindeblad, M., Lyubimov, A., Neri, F., Szilagyi, E., Smith, B., Halliday, L. C., et al. (2018) · Radiation Research · doi:10.1667/rr14975.1 · Cited by 31 · see citing works
The hunt for radiation biomarkers: current situation
Kultová, G., Tichý, A., Řehulková, H., & Myslivcova-Fucikova, A. (2019) · International Journal of Radiation Biology · doi:10.1080/09553002.2020.1704909 · Cited by 31 · see citing works
Addressing the Symptoms or Fixing the Problem? Developing Countermeasures against Normal Tissue Radiation Injury
Williams, J. P., Calvi, L. M., Chakkalakal, J. V., Finkelstein, J. N., O’Banion, M. K., & Puzas, E. J. (2016) · Radiation Research · doi:10.1667/rr14473.1 · Cited by 30 · see citing works
Rescue from lethal acute radiation syndrome (ARS) with severe weight loss by secretome of intramuscularly injected human placental stromal cells
Pinzur, L., Akyuez, L., Levdansky, L., Blumenfeld, M., Volinsky, E., Aberman, Z., Reinke, P., Ofir, R., Volk, H., & Gorodetsky, R. (2018) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12342 · Cited by 29 · see citing works
Development of a combined radiation and full thickness burn injury minipig model to study the effects of uncultured adipose-derived regenerative cell therapy in wound healing
Foubert, P., Doyle‐Eisele, M., Gonzalez, A. D., Berard, F., Weber, W., Zafra, D., Alfonso, Z., Zhao, S., Tenenhaus, M., & Fraser, J. K. (2016) · International Journal of Radiation Biology · doi:10.1080/09553002.2017.1242814 · Cited by 29 · see citing works
The delayed effects of acute radiation exposure (DEARE): characteristics, mechanisms, animal models, and promising medical countermeasures
Wu, T., & Orschell, C. M. (2023) · International Journal of Radiation Biology · doi:10.1080/09553002.2023.2187479 · Cited by 27 · see citing works
Radioprotective effects of Sipunculus nudus L. polysaccharide combined with WR-2721, rhIL-11 and rhG-CSF on radiation-injured mice
Jiang, S., Shen, X., Liu, Y., He, Y., Jiang, D., & Chen, W. (2015) · Journal of Radiation Research · doi:10.1093/jrr/rrv009 · Cited by 26 · see citing works
Development of a Model of the Acute and Delayed Effects of High Dose Radiation Exposure in Jackson Diversity Outbred Mice; Comparison to Inbred C57BL/6 Mice
Patterson, A. M., Plett, P. A., Chua, H. L., Sampson, C. H., Fisher, A., Feng, H., Unthank, J. L., Miller, S. J., Katz, B. P., MacVittie, T. J., et al. (2020) · Health Physics · doi:10.1097/hp.0000000000001344 · Cited by 25 · see citing works
Establishing Pediatric Mouse Models of the Hematopoietic Acute Radiation Syndrome and the Delayed Effects of Acute Radiation Exposure
Patterson, A. M., Sellamuthu, R., Plett, P. A., Sampson, C. H., Chua, H. L., Fisher, A., Vemula, S., Feng, H., Katz, B. P., Tudor, G. L., et al. (2021) · Radiation Research · doi:10.1667/rade-20-00259.1 · Cited by 25 · see citing works
2013 Dade W. Moeller Lecture
Moulder, J. E. (2014) · Health Physics · doi:10.1097/hp.0000000000000082 · Cited by 25 · see citing works
A comparative analysis of gut microbiota disturbances in the Gottingen minipig and rhesus macaque models of acute radiation syndrome following bioequivalent radiation exposures
Carbonero, F. G., Mayta-Apaza, A. C., Yu, J.-Z., Lindeblad, M., Lyubimov, A., Neri, F., Szilagyi, E., & Bartholomew, A. M. (2018) · Radiation and Environmental Biophysics · doi:10.1007/s00411-018-0759-0 · Cited by 24 · see citing works
Phospholipase D1 is upregulated by vorinostat and confers resistance to vorinostat in glioblastoma
Kang, D. W., Hwang, W. C., Noh, Y. N., Kang, Y., Jang, Y., Kim, J., & Min, D. S. (2020) · Journal of Cellular Physiology · doi:10.1002/jcp.29882 · Cited by 23 · see citing works
Impact of Age, Sex, and Genetic Diversity in Murine Models of the Hematopoietic Acute Radiation Syndrome (H-ARS) and the Delayed Effects of Acute Radiation Exposure (DEARE)
Orschell, C. M., Wu, T., & Patterson, A. M. (2022) · Current Stem Cell Reports · doi:10.1007/s40778-022-00214-z · Cited by 23 · see citing works
Granulocyte Colony-Stimulating Factor in the Treatment of Acute Radiation Syndrome: A Concise Review
Hofer, M., Pospíšil, M., Komůrková, D., & Hoferová, Z. (2014) · Molecules · doi:10.3390/molecules19044770 · Cited by 20 · see citing works
Neulasta regimen for the hematopoietic acute radiation syndrome: effects beyond neutrophil recovery
Legesse, B., Kaur, A., Kenchegowda, D., Hritzo, B., Culp, W. E., & Moroni, M. (2019) · International Journal of Radiation Oncology*Biology*Physics · doi:10.1016/j.ijrobp.2018.11.043 · Cited by 20 · see citing works
Self-citation
Development of a minipig model for lung injury induced by a single high-dose radiation exposure and evaluation with thoracic computed tomography
Lee, J. G., Park, S., Bae, C., Jang, W.-S., Lee, S., Lee, D. N., Myung, J. K., Kim, C. H., Jin, Y.-W., Lee, S., et al. (2015) · Journal of Radiation Research · doi:10.1093/jrr/rrv088 · Cited by 19 · see citing works
Selective Insulin-like Growth Factor Resistance Associated with Heart Hemorrhages and Poor Prognosis in a Novel Preclinical Model of the Hematopoietic Acute Radiation Syndrome
Kenchegowda, D., Legesse, B., Hritzo, B. A., Olsen, C. H., Aghdam, S. Y., Kaur, A., Culp, W. E., Derrien-Colemyn, A., Severson, G., & Moroni, M. (2018) · Radiation Research · doi:10.1667/rr14993.1 · Cited by 19 · see citing works
Self-citation
Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Stem Cell Research & Therapy · doi:10.1186/s13287-024-03743-y · Cited by 18 · see citing works
Medical countermeasures for the hematopoietic-subsyndrome of acute radiation syndrome in space
Kernagis, D. N., Balcer-Kubiczek, E., Bazyar, S., Orschell, C. M., & Jackson, I. L. (2022) · Life Sciences in Space Research · doi:10.1016/j.lssr.2022.06.002 · Cited by 16 · see citing works
Transient Inhibition of mTORC1 Signaling Ameliorates Irradiation-Induced Liver Damage
Yang, W., Shao, L., Zhu, S., Li, H., Zhang, X., Ding, C., Wu, X., Xu, R., Yue, M., Tang, J., et al. (2019) · Frontiers in Physiology · doi:10.3389/fphys.2019.00228 · Cited by 16 · see citing works
Effects of a granulocyte colony stimulating factor, Neulasta, in mini pigs exposed to total body proton irradiation
Sanzari, J. K., Krigsfeld, G. S., Shuman, A. L., Diener, A., Lin, L., Maï, W., & Kennedy, A. R. (2015) · Life Sciences in Space Research · doi:10.1016/j.lssr.2015.03.002 · Cited by 16 · see citing works
Tocols induce G-CSF and mobilise progenitors that mitigate radiation injury
Singh, V. K., Romaine, P. L. P., Newman, V. L., & Seed, T. M. (2014) · Radiation Protection Dosimetry · doi:10.1093/rpd/ncu223 · Cited by 15 · see citing works
Effects of captopril against radiation injuries in the Göttingen minipig model of hematopoietic-acute radiation syndrome
Rittase, W. B., McCart, E. A., Muir, J. M., Bouten, R. M., Slaven, J. E., Mungunsukh, O., Bylicky, M. A., Wilkins, W. L., Lee, S.-H., Gudmundsson, K. O., et al. (2021) · PLoS ONE · doi:10.1371/journal.pone.0256208 · Cited by 13 · see citing works
Self-citation
Pilot Study of Radiation-induced Gastrointestinal Injury in a Hemi-body Shielded Göttingen Minipig Model
Measey, T., Pouliot, M., Wierzbicki, W., Swanson, C., Brown, D., Authier, S., & Donini, O. (2017) · Health Physics · doi:10.1097/hp.0000000000000751 · Cited by 10 · see citing works
Celebrating 60 Years of Accomplishments of the Armed Forces Radiobiology Research Institute1
Bene, B. J., Blakely, W. F., Burmeister, D. M., Cary, L. H., Chhetri, S. J., Davis, C. M., Ghosh, S. P., Holmes‐Hampton, G. P., Iordanskiy, S., Kalinich, J. F., et al. (2021) · Radiation Research · doi:10.1667/21-00064.1 · Cited by 10 · see citing works
Significance of Bioindicators to Predict Survival in Irradiated Minipigs
Moroni, M., Port, M., Koch, A., Gulani, J., Meineke, V., & Abend, M. (2014) · Health Physics · doi:10.1097/hp.0000000000000109 · Cited by 10 · see citing works
Self-citation
Whole blood gene expression within days after total-body irradiation predicts long term survival in Gottingen minipigs
Chopra, S., Moroni, M., Sanjak, J. S., MacMillan, L., Hritzo, B. A., Martello, S. E., Bylicky, M. A., May, J. M., Coleman, C. N., & Aryankalayil, M. J. (2021) · Scientific Reports · doi:10.1038/s41598-021-95120-5 · Cited by 8 · see citing works
Self-citation
Developing and comparing models of hematopoietic-acute radiation syndrome in Göttingen and Sinclair minipigs
Doyle‐Eisele, M., Brower, J., Aiello, K. D., Ferranti, E. M., Yaeger, M. J., Wu, G., & Weber, W. (2020) · International Journal of Radiation Biology · doi:10.1080/09553002.2020.1820604 · Cited by 7 · see citing works
Early to sustained impacts of lethal radiation on circulating miRNAs in a minipig model
Chakraborty, N., Holmes‐Hampton, G. P., Gautam, A., Kumar, R., Hritzo, B. A., Legesse, B., Dimitrov, G. I., Ghosh, S. P., & Hammamieh, R. (2023) · Scientific Reports · doi:10.1038/s41598-023-45250-9 · Cited by 7 · see citing works
DEVELOPMENT OF PEDIATRIC MODEL OF HEMATOPOIETIC ACUTE RADIATION SYNDROME (H-ARS) AND COUNTERMEASURE TESTING USING THE GÖTTINGEN MINIPIG
Kaur, A., Vemalapally, N., Gulani, J., Bolduc, D. L., & Moroni, M. (2017) · RAD Association Journal · doi:10.21175/radj.2017.02.017 · Cited by 7 · see citing works
Self-citation
Impairment of IGF-1 Signaling and Antioxidant Response Are Associated with Radiation Sensitivity and Mortality
Aghdam, S. Y., Kenchegowda, D., Holmes‐Hampton, G. P., Moroni, M., & Ghosh, S. P. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22010451 · Cited by 7 · see citing works
Self-citation
Characterization of the hemorrhagic syndrome in the New Zealand white rabbit model following total body irradiation
Jackson, I. L., Gurung, G., Ayompe, E., Fown, E.-R., Triesler, S., Mali, B., Casildo, A., Gibbs, A. M., Poirier, Y. P., Cohen, E. P., et al. (2020) · International Journal of Radiation Biology · doi:10.1080/09553002.2020.1820601 · Cited by 6 · see citing works
What are the practical, ethical and pathobiological considerations in the use of minipigs as an animal model in drug discovery for acute radiation syndrome and delayed effects of acute radiation exposure?
Kenchegowda, D., Seed, T. M., & Singh, V. K. (2020) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2020.1811671 · Cited by 6 · see citing works
Retracted
Development of hematopoietic syndrome mice model for localized radiation exposure
Yashavarddhan, M. H., Sharma, A. K., Chaudhary, P., Bajaj, S., Singh, S., & Shukla, S. K. (2021) · Scientific Reports · doi:10.1038/s41598-020-80075-w · Cited by 5 · see citing works
Mitigation of Hematopoietic Syndrome of Acute Radiation Syndrome by 1-Palmitoyl-2-linoleoyl-3-acetyl-rac-glycerol (PLAG) is Associated with Regulation of Systemic Inflammation in a Murine Model of Total-Body Irradiation
Kim, Y., Jeong, J., Park, K., Sohn, K., Yoon, S. Y., & Kim, J. W. (2021) · Radiation Research · doi:10.1667/rade-20-00288.1 · Cited by 5 · see citing works
New opportunities and current challenges using animal models for the discovery of novel countermeasures for acute radiation syndrome
Singh, V. K., & Seed, T. M. (2025) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2025.2528966 · Cited by 5 · see citing works
rBPI21 (opebacan) promotes rapid trilineage hematopoietic recovery in a murine model of high‐dose total body irradiation
Janec, K. J., Yuan, H., Norton, J. E., Jr., Kelner, R. H., Hirt, C., Betensky, R. A., & Guinan, E. C. (2018) · American Journal of Hematology · doi:10.1002/ajh.25136 · Cited by 4 · see citing works
Radiation emergency medical countermeasures: Current formulary, identified gaps, and future approaches
Ma, W., Yin, R., Ren, G., Zhang⋆, Y., Li, L., Liu, W., Chen, T., Zhou, W., Zu, M., Yin, R., et al. (2025) · Animal Models and Experimental Medicine · doi:10.1002/ame2.70109 · Cited by 3 · see citing works
Ferroptosis, Inflammation, and Microbiome Alterations in the Intestine in the Göttingen Minipig Model of Hematopoietic-Acute Radiation Syndrome
Horseman, T. S., Rittase, W. B., Slaven, J. E., Bradfield, D. T., Frank, A. M., Anderson, J. A., Hays, E. C., Ott, A. C., Thomas, A. E., Huppmann, A. R., et al. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25084535 · Cited by 3 · see citing works
Cutting-edge animal models for radiation combined injury drug development
Singh, V. K., & Seed, T. M. (2025) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2025.2584319 · Cited by 2 · see citing works
Investigating the Multifaceted Nature of Radiation-Induced Coagulopathies in a Göttingen Minipig Model of Hematopoietic Acute Radiation Syndrome
Hritzo, B. A., Legesse, B., Ward, J. M., Kaur, A., Aghdam, S. Y., Kenchegowda, D., Holmes‐Hampton, G. P., & Moroni, M. (2021) · Radiation Research · doi:10.1667/rade-20-00073.1 · Cited by 1 · see citing works
Self-citation
Armed Forces Radiobiology Research Institute: R&D, Training, Crisis Response. Accomplishments, Opportunities and Policy Questions
Whitnall, M. H. (2015) · NATO science for peace and security series. B, Physics and biophysics · doi:10.1007/978-94-017-9891-4_6
Self-citation
Immunomodulatory Activity of Granulocyte Colony-Stimulating Factor and its Therapeutic Effect on Liver Failure
Hu, J., Sun, Z., Tong, J., Chen, J., & Liu, Z. (2021) · Infectious Diseases & Immunity · doi:10.1097/id9.0000000000000030
Musculoskeletal tissue-on-a-chip
Aboutalebianaraki, N., Shar, A., Messmore, M., Misiti, K., & Razavi, M. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-823536-2.00010-9
Additional file 8 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716204
Additional file 2 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.25751493
Additional file 1 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.25751451
Additional file 4 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716192
Additional file 7 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716201
Additional file 6 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716198
Additional file 5 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716195
Additional file 3 of Establishment of human hematopoietic organoids for evaluation of hematopoietic injury and regeneration effect
Chen, K., Li, Y., Wu, X., Tang, X., Zhang, B., Fan, T., He, L., Pei, X., & Li, Y. (2024) · Figshare · doi:10.6084/m9.figshare.26716189
Bone Marrow Colony Stimulating Factors (CSF) and Stem Cell Therapy as Medical Countermeasures (MCM) for Treatment of Hematopoietic-Acute Radiation Syndrome: A Systematic Review
Bogis, A., Pulver, S., Charp, P. A., Wills, E., Kazzi, Z., Buzzell, J., Prasher, J. M., & Chang, A. (2026) · Disaster Medicine and Public Health Preparedness · doi:10.1017/dmp.2025.10061

Radiation Carcinogenesis
Law, L. W. (1960) · Advances in biological and medical physics · doi:10.1016/b978-1-4832-3113-6.50010-5 · Cited by 8 · see citing works
Hematopoietic Radiation Syndrome in the Gottingen Minipig
Moroni, M., Coolbaugh, T. V., Lombardini, E., Mitchell, J., Moccia, K. D., Shelton, L. J., Nagy, V., & Whitnall, M. H. (2011) · Radiation Research · doi:10.1667/rr2481.1 · Cited by 70 · see citing works
Self-citation
DEVELOPMENT OF PEDIATRIC MODEL OF HEMATOPOIETIC ACUTE RADIATION SYNDROME (H-ARS) AND COUNTERMEASURE TESTING USING THE GÖTTINGEN MINIPIG
Kaur, A., Vemalapally, N., Gulani, J., Bolduc, D. L., & Moroni, M. (2017) · RAD Association Journal · doi:10.21175/radj.2017.02.017 · Cited by 7 · see citing works
Self-citation
Hematological Changes as Prognostic Indicators of Survival: Similarities Between Gottingen Minipigs, Humans, and Other Large Animal Models
Moroni, M., Lombardini, E., Salber, R. E., Kazemzedeh, M., Nagy, V., Olsen, C. H., & Whitnall, M. H. (2011) · PLoS ONE · doi:10.1371/journal.pone.0025210 · Cited by 75 · see citing works
Self-citation
Hematological changes as prognostic indicators of survival: Similarities between Gottingen minipigs, humans, and other large animal models,‖ PLoS one
Moroni, M., Lombardini, E., Salber, R. E., Kazemzedeh, M., Nagy, V., Olsen, C., & Whitnall, M. H. (2011)
Self-citation

Authors: Moroni, M., Ngudiankama, B. F., Christensen, C., Olsen, C. H., Owens, R., Lombardini, E. D., Holt, R. K., & Whitnall, M. H.
Affiliations: Uniformed Services University of the Health Sciences (US)
National Institute of Allergy and Infectious Diseases (US)
Armed Forces Research Institute of Medical Science (TH)
Corresponding author: Moroni, Maria
ORCID: Olsen, Cara H.
Lombardini, Eric D.
Venue: International Journal of Radiation Oncology*Biology*Physics
Publisher: Elsevier BV
Published: 2013-08
Volume: 86
Issue: 5
Pages: 986-992
ISSN: 0360-3016 (ISSN-L)
DOI: 10.1016/j.ijrobp.2013.04.041
PMC: PMC3710733
OpenAlex: W1974837400
Cited by: 64
References: 20
Citations by year: 2026: 1 · 2025: 3 · 2024: 6 · 2023: 3 · 2022: 2 · 2021: 11 · 2020: 6 · 2019: 3 · 2018: 6 · 2017: 4 · 2016: 4 · 2015: 7 · 2014: 6 · 2013: 1 · 2012: 1
FWCI: 4.66
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
Locations: International Journal of Radiation Oncology*Biology*Physics (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of Allergy and Infectious Diseases (Y1-AI-1759-01, Y01 AI001759, K08AI001759)
Topics: Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Effects of Radiation Exposure
Health Sciences › Medicine › Hematology › Hematopoietic Stem Cell Transplantation
Life Sciences › Immunology and Microbiology › Immunology › Immunotoxicology and immune responses
Keywords: Göttingen minipig, radiation sickness, granulocyte colony-stimulating factor, radiation countermeasures, hematopoiesis, neutropenia recovery, hematopoietic progenitor cell mobilization, survival, large animal model
MeSH terms: Filgrastim, Animals, C-Reactive Protein, Disease Models, Animal, Drug Evaluation, Preclinical, Hematopoiesis, Humans, Macrophages, Male, Monocytes, Neutropenia, Recombinant Proteins, Swine, Swine, Miniature, Whole-Body Irradiation, Reproducibility of Results, Granulocyte Colony-Stimulating Factor, Hematopoietic Stem Cell Mobilization, Acute Radiation Syndrome, Organs at Risk

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.

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

The Gottingen minipig is a model of the hematopoietic acute radiation syndrome: g-colony stimulating factor stimulates hematopoiesis and enhances survival from lethal total-body γ-irradiation

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks