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It also equals the product of kinship coefficients of its sire and its dame. In these cases, the spleen was the most frequently involved organ (28 cases, 76%) followed by the lung and mediastinum (27 cases, 67%), the liver (24 cases, 65%), and the lymph nodes (16 cases, 43%). Skin and subcutis involvement was reported in 16 affected dogs (19%), 10 of them presenting multicentric lesions ( Figure 1 ). Among the remaining 206 dogs, 48 individuals were older than 10 years without evidence of HS or other cancers (20 males and 28 females) and were considered to be healthy controls. To test whether a fully recessive model could explain the transmission of the disease, nuclear families with at least 2 phenotyped offspring, one of them being affected, were selected. Oxford University Press is a department of the University of Oxford. (1996) . In the subset of 21 nuclear families, analyzed in detail for the segregation analysis, 12 mast cell tumors (7.5%), 5 lymphomas (frequency 3.1%), and 5 melanocytic tumors (frequency 3.1%) were found (data not shown). Using a subset of 160 BMDs, encompassing 21 complete sibships, we now propose an oligogenic transmission mode of the disease. The second study reported responses to lomustine. Analyses of the US and the European populations reveal common ancestors. At each generation, only 5.5 % ( 0.3%) of sires and 13.2 % ( 0.3%) of dams were used for reproduction, with only 0.78% ( 0.1%) of sires and 3% ( 0.3%) of dams producing more than the half of next generation ( Figure 4 ). Hematological investigations at time of diagnosis revealed anemia, which was listed as severe for 41 dogs (66%), and thrombocytopenia in 56% of the cases (22 dogs). In France, a few champion males born in the 1980s have produced 400 puppies. Of those 121 dogs, 89 with pathological reports had been collected between 2005-01-01 and 2008-11-01. Involvement of multiple organ systems at the time of presentation was present in 55% of the dogs (37 cases). This is also in favor of a major role of the genetic background of the BMD breed in the neoplastic transformation of dendritic cells. In this calculation, we take into account the exact number of offspring in each family. Finally, we were interested in gaining a better insight into diagnosis criteria used in current veterinary practice to define HS and to compare these data with those from human studies. Follow-up and treatment information were available for all dogs. Unit d'Anatomie pathologique, Ecole Nationale Vtrinaire de Nantes, BP40706, 44307 Nantes cedex 3, France (Abadie); Cancer Genetics Branch, National Human Genome Research Institute, National Institutes of Health, 50 South Drive, Bethesda, MD (Cadieu, Parker, and Ostrander); Institut de Gntique et Dveloppement, Une unit mixte de recherche 6061 Centre national de la recherche scientifique/Universit de Rennes1, Facult de Mdecine, Rennes, France (Hdan, Brito, Vaysse, Galibert, Andr); Centre anti-cancereux, Ecole nationale vtrinaire dAlfort 7 avenue du general de Gaulle 94700, Maisons-Alfort, France (Devauchelle); Institut Inserm U535Genetique Epidemiologique et Structure des Populations humaines, Hpital Paul Brousse Btiment Leriche B.P., Villejuif, France (Bourgain and Margaritte-Jeannin). Affected dogs (cases) are defined as less than 7.5 years of age at diagnosis with HS. 2008 ). Diagnosis of HS was made using strong clinical or pathological evidence of the disease and confirmed by histology or cytology in 79 cases (89%). Coughing was recorded in 19% of affected dogs. 1995 ). A Reference Genome Assembly of the Bobcat, Tree of Life: Population structure, phylogeography and phylogenomics, http://www.akc.org/breeds/bernese_mountain_dog/history.cfm, Receive exclusive offers and updates from Oxford Academic, Frequency of the disease among parents of unknown status (, Expected proportion of affected offspring under recessive model, Copyright 2022 American Genetic Association. The oldest dog was born in 1931, the youngest in 2007. Among the 19 therapeutic surgeries, 13 (68%) consisted of splenectomy. Eighty-nine (89) BMDs affected by HS, for which we collected complete clinical information, were included in this study. For permissions, please email: journals.permissions@oxfordjournals.org. The mean age at diagnosis was 6 years and 6 months (range = 211 years). Interestingly, in human, Egeler et al. Lesions included nodules (12, 16%) associated or not with plaques (6, 6%). But the authors reported that anemia, thrombocytopenia, and splenic involvement were all associated with a poor prognosis. The club was founded in 1907 with 6 registered officially used for reproduction. These homogenous features are probably related to common physiopathologic mechanisms of oncogenesis in most if not all the cases. The clinical course of HS was very similar in all affected dogs, but the most common clinical signs were nonspecific and consistent with a general illness (anorexia, weakness, weight loss, , etc.). Histiocytic proliferative disorders are rare in humans, precluding the possibility of an efficient study of the genetic components of these diseases ( Arico and Danesino 2001 ). Skin of the thorax and forelegs was involved in 10 cases, head and neck in 6, and abdomen and hind legs in 6. The mean age of onset was 6.5 years, males and females being equally affected. It is clearly higher than the observed proportion in all cases, although the significance of the t -test comparing them is only strictly achieved ( P value < 0.05) when pk = 0.30. An oligogenic model was likely to be a better description of the genetic model underlying the disease. After availability of an assembled 7.5 sequence of the canine genome ( Lindblad-Toh et al. We thus favor an oligogenic model underlying the disease, rather than an autosomal recessive inheritance with incomplete penetrance. Abnormal pulmonary auscultation has been detected in 31% of the dogs, with polypnea (10 cases, 40%), rattle and abnormal pulmonary sounds (7 cases, 28%), dyspnea (6 cases, 24%), tachypnea (5 cases, 23%), shortness of breath (3 cases, 12%), and discordance (1 case, 4%). Interestingly, predisposing factors that have been suspected in humans, that is, vaccination for juvenile LCH and smoking for adult LCH (Donadieu et al. But most of the HSs were localized, and, as expected, the presence of metastasis was associated with shorter survival times ( Fidel et al. When parental status was unknown, we considered them as affected with a probability pk and unaffected with a probability 1 pk ( pk is the estimation of the prevalence of the disease in the breed). The most frequently observed serum chemistry modifications was alanine-amino transferase and alkaline phosphatase increase (45% of the cases), indicative of liver-related issues. Dogs older than 10 years that have not been diagnosed with any other cancer were considered as healthy; the other unaffected dogs were considered as unknown status. 2006 ). This strategy increases the likelihood of finding significant association. All data were entered into a confidential database. Indeed, information regarding canine exposure to carcinogenic substances is difficult to obtain. 2007 ). 2004 ). To be a powerful model in comparative pathology, the canine disease has to be characterized as precisely as possible and compared with the human counterpart. Since that date, genetic diversity has been restricted by pedigree barrier and reduced by use of popular sires. Right: neoplastic cells expressing the leukocyte CD18 marker (immunoperoxidase reaction, diaminobenzidine as chromogen, hematoxylin counterstaining); bar=30 m. The human equivalents of HS could encompass 2 types of aggressive proliferation of dendritic cells: disseminated LCH, which is an accumulation of tissue histiocytes in multiple organs and is generally associated with extensive multiorgan failure, and/or dendritic cellrelated HS, which is a very rare malignancy featuring cells with a dendritic phenotype ( Schmitz and Favara 1998 ). Survival data were available for 77 affected BMDs. Only 7 dogs received chemotherapy, with lomustine being the most commonly used drug. However, a common feature was the presence of internal masses at time of diagnosis (82% of the cases), commonly in the spleen, lungs, mediastinum, and lymph nodes, with frequent multiple organ involvement (55% of the cases). Histiocytic sarcoma (HS) refers to a highly aggressive and frequently disseminated neoplastic disease belonging to the class of canine histiocytic proliferative disorders. The questionnaire investigated epidemiological, clinical, and pathological features including identification of the dog (identity sex, age, etc.) All dogs for which parental DNA was available were tested for parental compatibility using a set of informative microsatellite markers. With substantial recent progress in veterinary medicine, dogs live longer and are affected by many cancer types. Twenty-one nuclear families (including a total of 160 dogs) with at least 2 phenotyped offspring, one of them being affected, could be identified from the larger pedigree. Among the 327 dogs sampled in France and Europe, 121 BMDs were affected by HS. Although HS is clearly overrepresented in the BMD, its mode of inheritance is not well understood, and the genes likely to be involved are unknown. Diagnosis must be made by a licensed veterinarian or veterinary oncologist. AKC-Canine Health Foundation (grant 936b to B.H., E.C. There were, however, few reports of therapeutic trials and survival rates in dogs with HS. The pedigree derives largely from a few male ancestors who were mated multiple times. We used kinship algorithms programmed using R ( http://cran.r-project.org ) to calculate the inbreeding coefficient for all dogs belonging to the large extensive pedigree. Other cancers observed in the sampled dogs included 13 lymphomas (7 males, 6 females), 18 mast cell tumors (7 males and 11 females), and 6 melanomas (5 males and 1 female). Fourteen dogs (20%) had a history of previous nonneoplastic dermatological disease. 2006 ). The most commonly reported clinical symptoms were anorexia (92% of the cases), asthenia and weakness (90%), weight loss (88%), and hyperthermia (43%). A total of 70.5% of the cases had been diagnosed between 5 and 8 years of age. 2006 ). Strikingly, it has been estimated that 80% of histiocytosis cases reported in France were diagnosed in the BMD breed (Devauchelle P, personal communication). 1986 ). This was the first description of a possible familial presentation or a related disease in dogs. Such characterization is also useful for veterinary medicine in order to improve the diagnosis of the disease, as well as sample collection. Furthermore, 35 dogs (39%) have first- or second-degree relatives affected with malignant neoplastic diseases other than HS. Systemic signs have been recorded in all affected dogs. Blood samples and the accompanying pedigree were collected by licenced veterinarians, and complementary information was obtained directly from the owners and breeders. Unaffected dogs were declared controls if they were older than 10 years and had never been diagnosed with any form of cancer. Most HS cases in BMDs have been reported to be of dendritic antigen-presenting cell origin even though a distinctive neoplastic proliferation of macrophages has been recently described in dogs ( Affolter and Moore 2002 ; Moore et al. Less than 10% of the dogs lived longer than 4 months, and 61 dogs (79%) were euthanazied. Splenomegaly was present in 49% of the dogs (34 cases), hepatomegaly in 34% (24 cases), and lymphadenomegaly in 26% (16 cases). Results are presented in Table 1 . Although reported clinical signs may vary, lethargy, anorexia, weight loss, as well as abnormalities of the respiratory system or liver and central nervous system (CNS) predominate in the initial diagnosis. Clinical signs associated with other organ system involvement were not consistently reported. In 35 cases, a palliative and supportive corticosteroid therapy (prednisone: 0.52 mg/kg) was performed. HS, in our BMD population, displayed reproducible presentation and clinical course. 1986; Affolter and Moore 2000 ; Affolter and Moore 2006). The average time between 2 generations was 3.7 years with a standard deviation of 1.2 years. The BMD population was originally developed from the Berne region of Switzerland. Whole-genome linkage scans as well as association studies using a case/control analysis, in parallel with expression profiling of neoplastic versus normal histiocytes, are all underway. (This figure appears in color in the online version of Journal of Heredity .). Furthermore, the number of affected dogs in siblings with 1 or 2 affected parents is lower than expected for a monogenic transmission mode leading us to rule out a fully autosomal recessive mode of inheritance as proposed by Padgett et al. 1986 ; Ramsey et al. The life span after diagnosis has been estimated to be 49 days. ( Affolter and Moore 2002 ; Fidel 2006). Towards this end, we undertook a collection of probands and their relatives, as well as unrelated cases and controls with rigorous diagnoses. Moreover, as in many dog breeds, the use of popular sires and inbreeding reduces diversity. A subset of 327 was selected to construct a pedigree segregating the disease. Although the expected proportion of affected offspring under a fully recessive model is not very sensitive to the values of HS prevalence, the significance of the t -test is only strictly achieved when the prevalence equals 30%. To better characterize the physiopathology and epidemiology, an in-depth analysis of 89 BMD cases has been performed. Flat coated and golden retrievers, for example, are reported to be less frequently affected, and, in these 2 breeds, the sarcoma is generally localized and not disseminated as is observed in the BMD ( Affolter and Moore 2002 ; Fidel et al. Second, a set of unrelated BMDs, including cases and controls, were collected from throughout the United States. Forty-six offspring were affected, representing 39% of the 118 offspring from the set. Abnormal heart auscultation was observed in 16% of the dogs, with tachycardia (10 cases, 71% of the cardiac abnormalities), arrhythmia (2 cases, 14%), and decreased heart sound (2 cases, 14%). We collected DNA samples and clinical information from 800 BMDs, of which 200 are affected by HS. This was close to values described by Calboli et al. In France, 80% of HS diagnoses occur in BMDs, yet the BMD is only the 13th most popular breed and represents 1.8% of dogs registered in 2007 in France ( http://www.scc.asso.fr ). A portion of 650 dogs of the BMD family segregating HS. Altogether, these complementary approaches are expected to localize the genes for HS in the BMD, leading to advances in our knowledge of histiocyte diseases in dogs and humans. ), therapeutics, and follow-up. Comparison of the expected proportion of affected offspring in the 21 nuclear families under a fully recessive model and the observed proportion ( pk is the estimation of the prevalence of the disease in the breed). 1995 ), and by analyzing the inheritance of histiocytosis in 127 affected BMDs, they reported that the disease was inherited in the BMD ( Padgett et al. In our population, hematologic alterations and splenic involvement were frequent, which may partially explain the poor prognosis and short survival time observed. Poorly specific digestive signs (anorexia, vomiting, diarrhea) were observed in 28% of the dogs. In France, with 50 recorded cases per year, the incidence is estimated to 1/200000 children of less than 15 years per year ( Donadieu et al. A surgical procedure was performed in 39 dogs, either for diagnosis purpose or as a therapeutic procedure. In order to search for predisposing genes to this devastating disease, complementary genetic mapping projects are underway: 1) a genetic linkage study using the large multigenerational European BMD pedigree, 2) a whole-genome association study with matched cases and controls collected in the United States, and 3) a RNA profiling analysis on tumor versus healthy tissue samples. (This figure appears in color in the online version of Journal of Heredity .). (1993) reported associations of LCH and malignant neoplasms including malignant lymphoma or Hodgkins disease, as we observed in our population. Book Review: An Intrepid Ecological Geneticists Pursuit of Industrial Melanism, A chromosome-scale genome assembly of the okapi (. A subset of 21 nuclear families with full sibships (160 dogs) was retained to study the mode of inheritance of HS. Therefore, the BMD breed represents a unique model to study genes involved in neoplastic transformation of histiocytes of the dendritic lineage, as well as genes more generally involved in other cancer types. Furthermore, 10 cases of infectious diseases were recorded: 8 cases of babesiosis (11.5%), 1 case of localized leishmaniosis, and 1 case of positive serology for borreliosis. If any of these males were affected or were carriers, it could easily explain the fact that the disease has spread so rapidly and in so few generations. For full access to this pdf, sign in to an existing account, or purchase an annual subscription. Marked cellular atypias and a high mitotic index were present. Concerning environmental factors, which may have been involved in the neoplastic development, no particular factor has been underlined. The domestic dog has emerged last years as an excellent model for genetic analysis of complex diseases, ( Parker and Ostrander 2005 ; Galibert and Andr 2007 ; Wayne and Ostrander 2007 ; Ostrander et al. Dogs are indeed an exceptional model for studying the genetic bases of cancer ( Cadieu and Ostrander 2007 ). In addition, with the plan of selecting the best population for genetic investigation, we have conducted a prospective study in order to collect an extensive pedigree and to define the epidemiological, clinical, and pathological features of HS in this BMD population. The clinical course of the disease is generally rapidly progressive with a poor prognosis. Thus, the exclusion of a fully recessive model, although probable, is not significant ( P value=6%). anamnestic data and case history, previous illness, diseases, clinical presentation of HS at time of diagnosis, biological evaluations (including hematology, blood chemist, etc. For example, among male dogs born between 2000 and 2002, 3 dogs produced more than 120 puppies. The clinical features, biochemical parameters, and pathological features have been determined. All rights reserved. Among the 89 affected BMDs, 58 (70%) have relatives (first or second degree) with a confirmed diagnosis of HS. Malignant dendritic cellrelated disorders are indeed rare in human beings, and their nosology, etiology, and pathogenesis remain largely undefined ( Arico and Danesino 2001 ). Despite the significant increase in registrations, particularly since the 1970s, BMDs are still regularly imported from Europe to the United States to enhance breeding programs. 2000 ) particularly cancer ( Cadieu and Ostrander 2007 ). Cases are selected so that they do not share common grandparents, thus allowing us to interrogate a large portion of the historical contribution of the breed. Clinical outcome reflected the very aggressive behavior and poor prognosis of this disease. More than 40% of cases displayed related cases of malignant neoplastic diseases other than HS, as close as 2 generations, as lymphoma, mast cell tumor, or melanoma. 2007 ). Moreover, the incidence of other hematopoietic neoplasia in the same families segregating HS could be suggestive of the involvement of several genes acting on general tumorigenic mechanisms. Identifying causative genes in dogs may help to highlight predisposing genes in human and/or at least common pathways and genes. Eleven dogs (16%) were reported to have experienced previous benign neoplastic diseases, including 7 cases of cutaneous histiocytoma, 1 melanocytoma, 1 benign mammary tumor, 1 lipoma, 1 case of multiple oral papillomatosis, and 1 vaginal fibroma. Previous segregation studies suggest a multigenic mode of inheritance ( Moore and Rosin 1986 ; Padgett et al. We calculated inbreeding coefficients within the pedigree, defining the probability that for any locus of an individual both 2 alleles descend from the same ancestral genotype. In 1995, Padgett reported that 25.4% of tumors diagnosed in the BMD were histiocytosis ( Padgett et al. ** P value of the t -test comparing the expected proportion with the observed proportion (0.39). Of informative microsatellite markers biochemical parameters, and 61 dogs ( 37 )... The dogs ( 20 % ) generally rapidly progressive with a poor prognosis this... Account the exact number of offspring in each family moreover, as observed. 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