{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,29]],"date-time":"2026-10-29T00:49:50Z","timestamp":1793234990292,"version":"4.5.0"},"reference-count":41,"publisher":"MDPI AG","issue":"2","license":[{"start":{"date-parts":[[2020,2,1]],"date-time":"2020-02-01T00:00:00Z","timestamp":1580515200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"PA Poultry Industry Broiler Research Check-Off Program","award":["NA"],"award-info":[{"award-number":["NA"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Microorganisms"],"abstract":"<jats:p>Bacterial chondronecrosis with osteomyelitis (BCO) is a septic necrosis of the skeletal system of unknown origin and an important cause of lameness in broiler chickens. Epithelial inflammation has been proposed as an avenue for bacterial translocation leading to BCO. We evaluated the effect of subclinical necrotic enteritis (SNE), an intestinal inflammatory event, with the development of BCO. In each of two experiments, chickens were divided into three treatments: (1) SNE challenge, including both dietary (wheat- and fish-based diet) and intestinal pathogenic challenges (Eimeria maxima and Clostridium perfringens), (2) dietary challenge only, and (3) control diet (corn-and soy-based diet). Floor ramps were introduced as part of an established method for increasing the frequency of BCO. The efficacy of the SNE challenge was corroborated by necropsy evaluation of a representative sample of the population. At the end of each experiment, all birds were evaluated for BCO. A high incidence of BCO was found, even in birds with no external signs of lameness. However, the incidence of BCO was not correlated with the intestinal challenge. Conclusions: under the conditions used in these studies, a treatment that is associated with severe damage to the intestinal mucosa does not change the incidence of BCO in broiler chickens.<\/jats:p>","DOI":"10.3390\/microorganisms8020205","type":"journal-article","created":{"date-parts":[[2020,2,3]],"date-time":"2020-02-03T11:28:31Z","timestamp":1580729311000},"page":"205","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":8,"title":["Incidence of Bacterial Chondronecrosis with Osteomyelitis (Femoral Head Necrosis) Induced by a Model of Skeletal Stress and its Correlation with Subclinical Necrotic Enteritis"],"prefix":"10.3390","volume":"8","author":[{"given":"Irene","family":"Rojas-N\u00fa\u00f1ez","sequence":"first","affiliation":[{"name":"Animal Science Department, The Pennsylvania State University, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ashli F.","family":"Moore","sequence":"additional","affiliation":[{"name":"Animal Science Department, The Pennsylvania State University, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"A. Gino","family":"Lorenzoni","sequence":"additional","affiliation":[{"name":"Animal Science Department, The Pennsylvania State University, State College, PA 16802, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2020,2,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"45","DOI":"10.3184\/147020602783698421","article-title":"A review of the aetiology and pathology of leg weakness in broilers in relation to their welfare","volume":"13","author":"Bradshaw","year":"2002","journal-title":"Avian Poult. Biol. Rev."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1080\/03079459408418991","article-title":"Skeletal disorders in the fowl: A review","volume":"23","author":"Thorp","year":"1994","journal-title":"Avian Pathol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1371\/journal.pone.0001545","article-title":"Leg disorders in broiler chickens: Prevalence, risk factors and prevention","volume":"3","author":"Knowles","year":"2008","journal-title":"PLoS ONE"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"432","DOI":"10.3382\/japr.2008-00061","article-title":"Impact of lameness on broiler well-being","volume":"18","author":"Paz","year":"2009","journal-title":"J. Appl. Poult. Res."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"253","DOI":"10.1080\/03079450050118386","article-title":"Bacterial chondronecrosis with osteomyelitis (\u2019femoral head necrosis\u2019) of broiler chickens: A review","volume":"29","author":"McNamee","year":"2000","journal-title":"Avian Pathol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"325","DOI":"10.3382\/ps\/pev320","article-title":"Bacterial chondronecrosis with osteomyelitis and lameness in broilers: A review","volume":"95","author":"Wideman","year":"2016","journal-title":"Poult. Sci."},{"key":"ref_7","first-page":"1","article-title":"Bone circulatory disturbances in the development of spontaneous bacterial chondronecrosis with osteomyelitis: A translational model for the pathogenesis of femoral head necrosis","volume":"3","author":"Wideman","year":"2013","journal-title":"Front. Endocrinol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"870","DOI":"10.3382\/ps.2011-01907","article-title":"A wire-flooring model for inducing lameness in broilers: Evaluation of probiotics as a prophylactic treatment","volume":"91","author":"Wideman","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"1354","DOI":"10.3382\/ps.2013-03781","article-title":"Evaluating portable wire-flooring models for inducing bacterial chondronecrosis with osteomyelitis in broilers","volume":"93","author":"Gilley","year":"2014","journal-title":"Poult. Sci."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"25","DOI":"10.3382\/ps\/peu025","article-title":"Prophylactic administration of a combined prebiotic and probiotic, or therapeutic administration of enrofloxacin, to reduce the incidence of bacterial chondronecrosis with osteomyelitis in broilers","volume":"94","author":"Wideman","year":"2015","journal-title":"Poult. Sci."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"185","DOI":"10.1007\/978-3-319-66653-2_9","article-title":"Impact of enteric health and mucosal permeability on skeletal health and lameness in poultry","volume":"1033","author":"Bielke","year":"2017","journal-title":"Adv. Exp. Med.e Biol."},{"key":"ref_12","first-page":"e43","article-title":"Experimental reproduction of enterococcal spondylitis in male broiler breeder chickens","volume":"6","author":"Martin","year":"2011","journal-title":"Avian Dis. Dig."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"332","DOI":"10.3382\/ps\/pew299","article-title":"Chondronecrosis with osteomyelitis in broilers: Further defining a bacterial challenge model using the wire flooring model","volume":"96","author":"Ekesi","year":"2017","journal-title":"Poult. Sci."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"32","DOI":"10.1016\/j.tim.2008.09.005","article-title":"Rethinking our understanding of the pathogenesis of necrotic enteritis in chickens","volume":"17","author":"Rood","year":"2009","journal-title":"Trends Microbiol."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1080\/03079457.2011.590967","article-title":"Necrotic enteritis in broilers: An updated review on the pathogenesis","volume":"40","author":"Timbermont","year":"2011","journal-title":"Avian Pathol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/1297-9716-43-74","article-title":"The successful experimental induction of necrotic enteritis in chickens by Clostridium perfringens: A critical review","volume":"43","author":"Shojadoost","year":"2012","journal-title":"Vet. Res."},{"key":"ref_17","first-page":"16","article-title":"The true cost of necrotic enteritis","volume":"31","author":"Wade","year":"2015","journal-title":"World Poult."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1145","DOI":"10.3382\/ps.0711145","article-title":"Barley inclusion and avoparcin supplementation in broiler diets. 2. Clinical, pathological, and bacteriological findings in a mild form of necrotic enteritis","volume":"71","author":"Kaldhusdal","year":"1992","journal-title":"Poult. Sci."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"375","DOI":"10.1080\/03079450701589118","article-title":"Quantification of gut lesions in a subclinical necrotic enteritis model","volume":"36","author":"Gholamiandehkordi","year":"2007","journal-title":"Avian Pathol."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1080\/03079450903505771","article-title":"The effect of commonly used anticoccidials and antibiotics in a subclinical necrotic enteritis model","volume":"39","author":"Lanckriet","year":"2010","journal-title":"Avian Pathol."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"e23","DOI":"10.1637\/9456-933810-DIGEST.1","article-title":"Optimized necrotic enteritis model producing clinical and subclinical infection of Clostridium perfringens in broiler chickens","volume":"5","author":"Wu","year":"2010","journal-title":"Avian Dis. Dig."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"5297","DOI":"10.3382\/ps\/pez311","article-title":"The netB-positive Clostridium perfringens in the experimental induction of necrotic enteritis with or without predisposing factors","volume":"98","author":"Yang","year":"2019","journal-title":"Poult. Sci."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"34","DOI":"10.1637\/7955-022307-Reg","article-title":"Reproducible infection model for Clostridium perfringens in broiler chickens","volume":"52","author":"Pedersen","year":"2008","journal-title":"Avian Dis."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"1453","DOI":"10.1017\/S0007114509990407","article-title":"The cereal type in feed influences gut wall morphology and intestinal immune cell infiltration in broiler chickens","volume":"102","author":"Teirlynck","year":"2009","journal-title":"Br. J. Nutr."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1080\/03079457.2016.1150587","article-title":"Necrotic enteritis predisposing factors in broiler chickens","volume":"45","author":"Moore","year":"2016","journal-title":"Avian Pathol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"414","DOI":"10.1093\/ps\/83.3.414","article-title":"Effects of dietary protein source and level on intestinal populations of Clostridium perfringens in broiler chickens","volume":"83","author":"Drew","year":"2004","journal-title":"Poult. Sci."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"159","DOI":"10.1080\/03079450500112195","article-title":"Intercurrent coccidiosis and necrotic enteritis of chickens: Rational, integrated disease management by maintenance of gut integrity","volume":"34","author":"Williams","year":"2005","journal-title":"Avian Pathol."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"543","DOI":"10.1016\/j.rvsc.2008.02.007","article-title":"Sub-clinical necrotic enteritis in broiler chickens: Novel etiological consideration based on ultra-structural and molecular changes in the intestinal tissue","volume":"85","author":"Olkowski","year":"2008","journal-title":"Res. Vet. Sci."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"686","DOI":"10.1637\/aviandiseases-D-19-00093","article-title":"Effect of aspirin on the intestinal response to a necrotic enteritis challenge","volume":"63","author":"Lorenzoni","year":"2019","journal-title":"Avian Dis."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1637\/8367-051908-Reg.1","article-title":"Histopathology and serum clinical chemistry evaluation of broilers with femoral head separation disorder","volume":"53","author":"Durairaj","year":"2009","journal-title":"Avian Dis."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"2464","DOI":"10.3382\/ps.2012-02386","article-title":"Dexamethasone triggers lameness associated with necrosis of the proximal tibial head and proximal femoral head in broilers","volume":"91","author":"Wideman","year":"2012","journal-title":"Poult. Sci."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"2311","DOI":"10.3382\/ps.2013-03150","article-title":"Susceptibility of 4 commercial broiler crosses to lameness attributable to bacterial chondronecrosis with osteomyelitis","volume":"92","author":"Wideman","year":"2013","journal-title":"Poult. Sci."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"1675","DOI":"10.3382\/ps.2014-03912","article-title":"Bacterial chondronecrosis with osteomyelitis in broilers: Influence of sires and straight-run versus sex-separate rearing","volume":"93","author":"Wideman","year":"2014","journal-title":"Poult. Sci."},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1016\/j.anifeedsci.2018.09.014","article-title":"Coinfection with Eimeria spp. decreases bacteremia and spinal lesions caused by pathogenic Enterococcus cecorum","volume":"250","author":"Borst","year":"2019","journal-title":"Anim. Feed Sci. Technol."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1016\/S0165-2427(96)05689-9","article-title":"Eimeria tenella infections in chickens: Aspects of host-parasite: Interaction","volume":"54","author":"Jeurissen","year":"1996","journal-title":"Vet. Immunol. Immunopathol."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"303","DOI":"10.1016\/S0145-305X(99)00080-4","article-title":"Intestinal immune responses to coccidiosis","volume":"24","author":"Yun","year":"2000","journal-title":"Dev. Comp. Immunol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"61","DOI":"10.1177\/0300985816658098","article-title":"Pathogenesis of enterococcal spondylitis caused by Enterococcus cecorum in broiler chickens","volume":"54","author":"Borst","year":"2017","journal-title":"Vet. Pathol."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3389\/fvets.2018.00199","article-title":"Evaluation of the epithelial barrier function and ileal microbiome in an established necrotic enteritis challenge model in broiler chickens","volume":"5","author":"Latorre","year":"2018","journal-title":"Front. Vet. Sci."},{"key":"ref_39","first-page":"1","article-title":"Molecular survey of bacterial communities associated with bacterial chondronecrosis with osteomyelitis (BCO) in broilers","volume":"10","author":"Jiang","year":"2015","journal-title":"PLoS ONE"},{"key":"ref_40","doi-asserted-by":"crossref","unstructured":"Simjee, S. (2007). Enterococcus and its association with foodborne illness. Foodborne Diseases, Humana Press.","DOI":"10.1007\/978-1-59745-501-5"},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"1575","DOI":"10.3382\/ps\/pey538","article-title":"The utility of infrared thermography for evaluating lameness attributable to bacterial chondronecrosis with osteomyelitis","volume":"98","author":"Weimer","year":"2019","journal-title":"Poult. Sci."}],"container-title":["Microorganisms"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/2\/205\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,11]],"date-time":"2025-10-11T08:53:50Z","timestamp":1760172830000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2076-2607\/8\/2\/205"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2020,2,1]]},"references-count":41,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2020,2]]}},"alternative-id":["microorganisms8020205"],"URL":"https:\/\/doi.org\/10.3390\/microorganisms8020205","relation":{},"ISSN":["2076-2607"],"issn-type":[{"value":"2076-2607","type":"electronic"}],"subject":[],"published":{"date-parts":[[2020,2,1]]}}}