The end of chromosomes are characterised by a repetitive sequence known as the telomere. Normal somatic cell division results in telomere erosion, ultimately triggering senescence. Cancer cells bypass senescence via activation of a telomere lengthening mechanism (TLM), either telomerase or Alternative Lengthening of Telomeres (ALT). Identification of ALT relies on the observation of unique phenotypic characteristics including long and heterogeneous telomere lengths, presence of ALT associated PML bodies, and abundant c-circles (extrachromosomal telomeric circular DNA). A cohort of 149 high-risk neuroblastoma tumours was screened for ALT by assessing the amount of telomeric DNA and c-circles. Evidence of ALT (high telomere content and c-circles) was found in 24% of the tumours while another subset (11%) had high telomere content but were c-circle negative. This unique group had a similarly poor 5-year overall survival compared to c-circle positive and MYCN-amplified tumours (47 vs 31 vs 28%; P=0.83). Testing 35 neuroblastoma cell lines identified two neuroblastoma cell lines (unique by STF) with a similar phenotype to the unique tumours, specifically they were negative for telomerase and c-circles. The two cell lines have exceptionally long and heterogeneous telomere length (35kb) (demonstrated by telomere FISH and terminal restriction fragment analysis) and when cultured for >300 population doublings, telomere length shortened by 50 to 80 base pairs per population doubling, consistent with the lack of a TLM. Gene mutations associated with ALT (TP53, ATRX, DAXX, IDH1/2, H3.3) were not present in the two cell lines. All continuously growing cell lines to date have a TLM so this is an unprecedented finding. This is the first report of sustained proliferation of aggressive human cancer despite continuous telomere shortening; patients with tumours of the same phenotype have a poor outcome even though they lack a TLM. These discoveries have implications for the use of telomere maintenance inhibitors in the clinic and in understanding mechanisms of immortalization during carcinogenesis.