Scientists studied lung cancers from seven patients - including smokers, ex-smokers and never smokers. They found that after the first genetic mistakes that cause the cancer, it can exist undetected for many years until new, additional, faults trigger rapid growth of the disease.
During this expansion there is a surge of different genetic faults appearing in separate areas of the tumour. Each distinct section evolves down different paths - meaning that every part of the tumour is genetically unique.
Two-thirds of patients are diagnosed with advanced forms of the disease when treatments are less likely to be successful, researchers said.
By revealing that lung cancers can lie dormant for many years the researchers hope this study will help improve early detection of the disease.
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"Survival from lung cancer remains devastatingly low with many new targeted treatments making a limited impact on the disease. By understanding how it develops we've opened up the disease's evolutionary rule book in the hope that we can start to predict its next steps," study author Professor Charles Swanton, at Cancer Research UK's London Research Institute and the University College London (UCL) Cancer Institute, said.
But as the disease evolved these became less important with the majority of faults now caused by a new process generating mutations within the tumour controlled by a protein called APOBEC.
The wide variety of faults found within lung cancers explains why targeted treatments have had limited success.
Attacking a particular genetic mistake identified by a biopsy in lung cancer will only be effective against those parts of the tumour with that fault, leaving other areas to thrive and take over.
"If we can nip the disease in the bud and treat it before it has started travelling down different evolutionary routes we could make a real difference in helping more people survive the disease," Jones said.
The study was published in the journal Science.