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A general framework for object detection. Computer Vision, 1998 Sixth International Conference on; 1998 4\u20137 Jan 1998."},{"key":"ref14","unstructured":"Viola P, Jones M, editors. Rapid object detection using a boosted cascade of simple features. Computer Vision and Pattern Recognition, 2001 CVPR 2001 Proceedings of the 2001 IEEE Computer Society Conference on; 2001 2001."},{"key":"ref15","first-page":"297","article-title":"Pattern Recognition","author":"R Lienhart","year":"2003"},{"issue":"4","key":"ref16","doi-asserted-by":"crossref","first-page":"349","DOI":"10.1109\/34.917571","article-title":"Example-based object detection in images by components","volume":"23","author":"A Mohan","year":"2001","journal-title":"Pattern Analysis and Machine Intelligence, IEEE Transactions on"},{"issue":"1","key":"ref17","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1023\/A:1008162616689","article-title":"A Trainable System for Object Detection","volume":"38","author":"C Papageorgiou","year":"2000","journal-title":"Int J Comput Vis"},{"issue":"3","key":"ref18","doi-asserted-by":"crossref","first-page":"366","DOI":"10.1002\/(SICI)1097-0320(19981101)33:3<366::AID-CYTO12>3.0.CO;2-R","article-title":"Automated recognition of patterns 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