Journal of Hepatology
Volume 44, Issue 1 , Pages 32-38, January 2006

Should we screen for colorectal cancer in liver transplantation?

Division of Gastroenterology and Hepatology, Department of Internal Medicine, University Hospital of Zürich, Rämistrasse 100, CH-8091 Zürich, Switzerland

published online 08 November 2005.

Article Outline

Abbreviations: CRC, colorectal cancer, ESRD, end-stage renal disease, IBD, inflammatory bowel disease, LT, liver transplantation, PSC, primary sclerosing cholangitis, RR, relative risk, SIR, standardized incidence ratio, UC, ulcerative colitis

 

Liver transplantation (LT) is being performed in a steadily increasing number of patients with more than 70,000 procedures carried out in both the United States and Europe as yet (Fig. 1) [1]. Better patient selection, technical expertise and advances in post-transplantation patient management resulted in a significant improvement in survival, leading to a raising cohort of LT recipients being alive and thus at risk for malignancies.

Malignant tumors of the skin, lymphoproliferative disorders and Kaposi's sarcoma have been shown to frequently occur after LT, even very early in time [2], [3], [4], [5]. Contrary to this knowledge, it is controversial whether the LT population is at increased risk for developing otherwise commonly occurring malignancies, such as cervix, breast, prostate and colorectal cancer (CRC) [6], [7], [8], [9], [10]. Whereas screening for skin and cervix cancer is widely implemented, there is no consensus as to whether we should screen for CRC. With the present review, the authors aim to answer this question basing on demographic issues, the epidemiology of CRC in the population of LT recipients, and the analogies with the patient population for which screening for CRC is currently a widely accepted practice.

Back to Article Outline

1. What is the occurrence of CRC in the LT population? 

1.1. Direct evidence, average risk LT recipients 

Published literature on the occurrence of CRC among LT recipients is scant. Most recent series including at least 100 LT patients are summarized in Table 1. None assessed prospectively the incidence of CRC after LT. Results are presented as incident CRC cases (sometimes as percents of the transplant population) over a mean/median period of follow-up. Because of the imprecise denominator with respect to observation time, it is extremely difficult to draw conclusions on true incidence rates based on these data. The task is even more difficult when considering the large number of reports for which the follow-up time is not stated. A further factor hampering the calculation of incidence rates is the missing information on the population at risk for developing CRC. Indeed, a relevant portion of LT recipients will die during observation and drop out of the population at risk for CRC. As a consequence, reference to the initial number of transplant recipients, thus assuming a constant number of person at risk over years, will result in risk underestimation. A bias in the same direction may occur due to the overall relatively short periods of follow-up. Any conclusions regarding tumors possibly occurring later after transplantation is likely to represent an underestimation of the true incidence and should be interpreted with caution in this setting.

Table 1. Studies on incidence of CRC in the LT population at average risk
First authorLocationLT yearFollow-up, mo., m/m (r)LT pts, nCRC totalCRC in PSC/IBDAge at LT, yrs, m/m (SD/r)Age at CRC, yrs, m/m (SD)Time from LT, mo., m/m (r)Notes
JainPittsburgh, US1989–9278 (56–96)10004143 (20)52 (5)38/25 (12–75)T; pLTC>40 or sy.
KellyNew York, US1988–9652 (16–85)85931NRNR for CRCNRC, T
CatenaBologna, ITo 199773 (NR)3532NRNRNR for CRCNRC2, C3
XiolBarcelona, Sp1990–9569 (43–104)137a2NR49f (15–65)NRNRC4, 1. LT only
HaagsmaGroningen, NL1979–9661 (18–225)174a3043 (20–61)55–6871–200A, C, (T)
JonasBerlin, D1988–9450 (0–97)4580046NANAC4, T
LevyDallas, US1985–9135 (1–85)55611NRNR66NR, with CRC: C
FrezzaPittsburgh, US1982–92NR16574NRbNRNR28–70C, T
VeraBirmingham, UK1986–00NR118470cNRNR52 (6–108)C (87%), T (13%)
FabiaDallas, US1984–95NR97010d47 (12)NR46C, (T); all pLTC
SafadiJerusalem, IlNRNR10121NRNR4eNR

m/m, mean or median; r, range; LT, liver transplantation; NR, not reported; NA, not applicable; PSC, primary sclerosing cholangitis; IBD, inflammatory bowel disease; A, azathioprin; T, tacrolimus; C, cyclosporin; C2, C-based bi-therapy; C3, C-based tri-therapy; C4, C-based quadruple therapy; pLTC, pre-LT colonoscopy; Sy, symptoms.

aOnly those alive >1 year.

bTwo patients had a positive familiy history for CRC.

cOnly patients without PSC.

dOnly patients without PSC or IBD.

eReported only for one patient.

fNot reported whether mean or median.

The longest follow-up periods are those reported by Jain, Kelly, Catena, Haagsma, Xiol et al., varying between 52 and 78 months of mean/median observation time, 16 months representing the shortest time period [8], [10], [11], [12], [13]. In the Pittsburgh series, four CRC cases were identified among 1000 consecutive patients who underwent LT around 1990 and were studied for an average of 78 months [10]. One of these CRC patients suffered from primary sclerosing cholangitis (PSC), a disease associated with a highly increased risk for CRC. The next largest study included 859 recipients transplanted between 1988 and 1996 [8]. One of the three patients who developed CRC was likewise affected by PSC. Out of 353 recipients of LT at a single center in Italy, two CRCs were recorded during a mean observation time of 6.1 years [11]. The analyses from Spain and Netherlands despite having surveyed patients for a median of over 5 years, only included a small cohort of 137 and 174 LT recipients, respectively [12], [13]. In the first study, two patients were reported with CRC without mentioning the primary liver disease leading to transplantation [13]. In the second study, no association with the presence of PSC was noted [12]. Frezza et al. registered as few as four CRC cases among a cohort of 1657 LT recipients observed for an unknown period of time [9].

In all but two studies, transplantation was performed for a wide array of liver disorders and the proportion of patients at baseline increased risk for CRC, such as those with inflammatory bowel disease (IBD)/PSC, is not specified. As an exception, the groups from Birmingham and Dallas provide specific figures for recipients not affected by PSC or ulcerative colitis (UC) [14], [15]. Moreover, often unknown portions of the study population underwent colonoscopic evaluation prior to LT. This aspect should be considered when evaluating the potential benefits of screening post-LT. LT candidates found with neoplasia and undergoing polypectomy will contribute to falsely low CRC incidences shortly after transplantation, thus within the follow-up time of available literature. Lastly, part of the published reports relies on retrospective analyses from large transplantation registries. Their results are limited by a potential for incomplete tumor ascertainment. In single-center analyses, CRC reporting is expected to be more accurate. However, these on small numbers based studies are often characterized by an insufficient statistical power, especially considering the overall low annual incidence rates of CRC in the general population. Over 2000 patients need to be followed over 5 years, for instance, in order to achieve a statistical power of 80% when attempting to show an incidence increase from 0.2 to 0.4% per year [16].

1.2. Direct evidence, high-risk LT recipients 

Patients with PSC are at high risk for developing CRC. This increased risk is explained by the association with IBD in about 75% of cases (particularly with UC) [17]. In UC, development of CRC largely depends on disease extent and duration [18], [19], [20]. Whereas incidence is low during the first 10 years after diagnosis, it steeply raises thereafter at estimated rates of 0.5% annually in the second, 1% annually in the third, and 1.5% annually in the fourth decade of disease persistence [18], [20]. Accordingly, after 40 years of extensive ulcerative colitis, about 30% of the patients will be diagnosed with CRC, as opposed to a lifetime risk of 6% in the general population. The risk for CRC in UC/IBD most likely arises from the chronic inflammation of the colonic mucosa which is not expected to decrease after transplantation, although it can be argued that therapy with immunomodulatory drugs following transplantation may induce disease remission.

With the exception of the study by Loftus et al., available literature does not assess risk for CRC in PSC patients after LT compared to a control population with similar IBD disease duration [21]. Among 57 patients suffering from PSC and UC with an intact colon, the Mayo clinic group found three patients with CRC during a median follow-up of 4.7 years [21]. Almost the entire study cohort underwent surveillance colonoscopy prior to transplantation and in 28% neoplasia was detected at this point in time. Eighteen percent underwent colectomy after LT, and 18% died during follow-up for causes unrelated to CRC. The cumulative risk for CRC was 4 and 8% 5 and 8 years after LT, respectively. The calculated RR compared to a control population was increased by a factor of 4.4 but this difference was not statistically significant.

Vera et al. followed PSC patients with IBD who underwent LT between 1986 and 2000 and reported the outcomes regarding CRC for different risk groups [15]. Of 83 patients with PSC and UC with an intact colon, eight developed CRC, for a cumulative risk of 10 and 16% at 5 and 10 years, respectively. When UC history lasted more then 10 years at LT, 30% of patients had developed CRC 6 years after transplantation. Pancolitis was associated with a CRC risk of 35% 5 years after LT versus 7% when UC involved less than the total colon. The authors identified three important predictors for the development of CRC: age over 45, time interval between UC diagnosis and LT of over 10 years, and the presence of polyps at colonoscopy. The risk for CRC was 0, 20, and 38% at 1, 5, and 10 years, respectively, in case of concurrence of two predictive factors. If three factors concurred, patients had a risk of 100% to be diagnosed with CRC within 5 years from transplantation. Interestingly, none of the 52 patients with PSC but no IBD was found with CRC at follow-up. This finding was reproduced by Fabia et al. among 35 LT recipients [14]. The same study reported five patients with CRC in the group of patients with intact colon and both PSC and UC (n=50). All LT candidates underwent screening colonoscopy prior to colonoscopy.

1.3. Indirect evidence, renal and other solid organ transplantation 

The number of patients followed-up after renal transplantation far exceeds the cohort of LT recipients. Observation data are collected in large registries, sometimes together with data on transplantation of other organs.

Kasiske et al. observed for a length of 3 years 35,765 Medicare patients who underwent renal transplantation in 1995–2001 [22]. They represented 47% of the entire cohort of renal transplant recipients in the United States transplanted during this time period. Cumulative incidences of colon cancer were 0.18, 0.33, and 0.51% at 1, 2, and 3 years, respectively. The authors calculated the relative risk for cancer with transplantation versus comparable end-stage renal disease (ESRD) patients on Medicare without transplantation. After adjusting for age, gender, race, primary diagnosis and prior duration of ESRD, risk for colon cancer was not significantly increased in the transplantation population (RR 0.75, 95% CI 0.54–1.04). In the Collaborative Transplant Study, Steward et al. analyzed the outcome of over 73,000 renal and heart transplant recipients in Europe and North America for transplantations carried out before 1993 [23]. Patients were observed for a minimum of 1 year, in some cases beyond 10 years. A total of 75 colon and 15 rectal cancers were diagnosed during this period. An analysis of data collected in the Nordic Renal Transplant Registry for patients who underwent transplantation between 1964 and 1982 (azathioprin-based immunosuppressive therapy only) resulted in 32,392 persons-years follow-up and identified 22 CRCs. [24] This is a risk of 0.68% per person over 10 years. Among 6596 renal transplant recipients included in the Australian and New Zealand registry, 90 digestive tumors were reported, half of which involved the large intestine (follow-up not stated) [25]. Adami et al. studied 5004 renal transplant and 927 non-renal, solid organ transplant recipients in Sweden between 1970 and 1997 [26]. In the group of non-renal transplants, 394 were LTs. As a whole, the cohort was observed from 0 to 26.8 years with a mean of 6.8 years, and its median age was 46 years. In the group of renal transplant recipients, 37 CRC were recorded whereas only two rectal cancers were diagnosed among the remaining transplant population. Due to small sample sizes and missing follow-up times, other published data do not provide additional useful information.

Although these figures rely on observation of large numbers of patients, extrapolation from the respective findings to the population of LT recipients may be only partially appropriate. As the analysis of the Cincinnati Transplant Tumor Registry showed, the distribution of tumors after renal as compared to liver transplantation is strikingly different [7]. Among 6707 tumor patients after renal transplantation, 42% had skin, 12% lymphoproliferative, and 4.0% colorectal cancer. In contrast, 58% of the tumors occurring after LT were lymphomas, only 15% were skin cancers and 5.6% CRCs. After deducting the number of lymphoma and skin tumors from the total number of malignancies, CRC accounts for 8.7 and 20.7% of the remaining tumors, respectively. It has been speculated that these differences might be related to the more intense immunosuppression after LT and its link to lymphoproliferative disorders [7], [23]. The different length of follow-up between renal and liver transplantation patients may also explain these diversities. With respect to CRC, it has to be noted that one-third of patients who developed the tumor also had a history of ulcerative colitis [7]. It is therefore likely that these results are biased. Since PSC with UC is itself a reason leading to LT, UC is expected to be much more frequent in the population of LT recipients compared to renal transplant recipients. The association of UC with CRC may therefore largely explain the difference in CRC incidence between the two groups. In light of these considerations, extrapolations from one to the other transplant population should be interpreted with caution.

Back to Article Outline

2. How does CRC incidence in LT recipients compare to the general population? 

Only few studies compared the risk for CRC among LT recipients with that of an age- and gender-matched general population. Crude incidence rates do not provide information on excess risk. Due to the different distributions of demographic characteristics and other factors associated with outcome in different populations, direct comparison of crude rates is not meaningful. Computation of the standardized incidence ratio (SIR) is one way to appropriately collapse information on risk in different strata of the populations in one overall relative risk (RR) measure [27]. Observed incident CRC cases in the study population are divided by the expected CRC cases in the general population based on age-, gender- and calendar year-adjusted data. This method allows to adjust for inequalities in the distribution of demographic characteristics in the two populations. A SIR value of 1 indicates a similar risk, SIRs greater than 1 indicate excess risk and less than 1 decreased risk.

Jain et al. used incidence rates from the Surveillance Epidemiologic and End Results (SEERs) as a standard to compute the SIR for CRC after LT [10]. This rate was not significantly different from 1, indicating that the risk for developing CRC after LT was not increased compared with the general population. A divergent result was obtained by Haagsma et al. who used for comparison specific cancer rates from a regional cancer registry [12]. The adjusted risk for CRC was 12.5 times higher than in the general population. As indicated by the wide range of the confidence intervals (2.5–36.6), however, the study was insufficiently powered.

Pertinent additional data have been published for renal and other solid organ transplant recipients. The Collaborative Transplant Study Group retrieved general CRC occurrence data from the published literature and compared them with the occurrence in their renal and heart transplant population [23]. A not significantly increased age-adjusted relative risk for colon cancer (RR 1.2, 95% CI 0.93–1.48) and a significantly decreased risk for rectal cancer (RR 0.36, 95% CI 0.18–0.54) were found. In the Medicare collective of renal transplant patients, age-adjusted CRC rates were increased roughly twofold over 3 years of observation [22]. These results are in accordance with those obtained from the Nordic Renal Transplant Registry with SIRs of 3.2 (95% CI 1.6–5.8) and 3.9 (95% CI 2.0–7.0) for men and women, respectively [24]. In the analyses of Adami et al., there was an excess risk in the renal transplant population for both colon (SIR=2.4) and rectal cancer (SIR=1.7) but results achieved statistical significance only for colon cancer [26].

Although computation of a single overall standardized incidence ratio is generally a welcome epidemiological measure, this approach does not allow to predict the relative risk in different age and gender categories, thus hampering risk stratification and quantification for subgroups of recipients. This specific information is relevant when establishing recommendations for subgroups of the LT population whose demographic characteristics do not overlay with those of the general target population for CRC screening.

Back to Article Outline

3. What is the occurrence of colorectal pre-malignant lesions at LT? 

CRC is known to arise from adenomatous polyps. In a study of 71 asymptomatic patients with cirrhosis undergoing pre-transplantation sigmoidoscopy (followed by colonoscopy in the presence of polyps), 21% were diagnosed with adenomatous and 9% with hyperplastic polyps [28]. In 27% of those with adenoma, the lesions were larger than 1cm in diameter. Weller et al. identified 24 patients with adenoma at a mean age of 48 years among 56 cirrhotic candidates for LT [29]. Thirty percent were below 50 years at the time of diagnosis and over 40% of lesions measured over 1cm. Polyps were present in 5 of 16 patients who underwent colonoscopy in a screening intent only (asymptomatic over 50 years). Contrasting lower prevalences were noted in a study of 412 cirrhotic patients undergoing LT with mean ages varying from 27 to 49 years depending on diagnosis [30]. Colonic polyps were identified in 8.5% of patients and adenomatous lesions in 4.9%.

Reports on pre-transplant colonoscopy among candidates of other solid organ transplantations suggest, again, a high prevalence of adenoma in this patient population. In a series of 31 lung transplant candidates between 49 and 61 years of age, 19% were found with adenomas and 35% with non-adenomatous polyps or polyps with unknown pathology [31]. Parikshak et al. studied 229 patients who underwent pre-transplant colonoscopy, the majority of whom was asymptomatic (71%). They represented 23% of all transplantations (638 renal, 176 liver, 140 heart, 38 heart) carried out at a single center between 1989 and 1999. Of the 74 patients with polyps, 45 had adenomas [32].

Back to Article Outline

4. Screening recommendations in the liver transplant population 

From the data presented above, it is improbable that CRC occurrence among elderly LT recipients will be lower compared to the general population. We could therefore argue, that LT recipients over 50 years should undergo CRC screening as endorsed for the general population. If we do so, we have to assume that the survival benefit is similar. Otherwise no direct translation of recommendations that were based on specific target benefits and cost-effectiveness thresholds can be made. Unfortunately, sparse published evidence is available to verify the correctness of this assumption. In the EDTA–ERA (European Dialysis and Transplantation Association–European Renal Association) Registry, 5-year survival for CRC patients on dialysis or after renal transplantation was 30–35% and differed widely from an overall survival after CRC of about 60% as reported by the National Cancer Institute for the general population [33]. Moreover, life expectancy is possibly shorter in the group of LT recipients compared to the elderly general population [34], [35]. These figures would suggest a lower benefit of screening among LT patients over the age of 50 years. However, CRC occurrence data point generally to an increased incidence in the LT population. In particular, Birkeland et al. reported a statistically significantly increased relative risk of 3.8 for LT recipients over 45 years compared with the general population of the same age group [24]. With higher incidence rates, more patients will profit from survival benefits through screening and this may compensate for the possibly lower individual life-years saved. As a whole, we can conclude that it is reasonable to offer CRC screening to LT recipients above the age of 50 years.

The next question to be answered is whether LT recipients under 50 years of age should be equally screened. Assuming a similar life expectancy of the transplant population under 50 and the general population over 50 years, an equal or greater number of CRC incident cases is required in order to justify screening among younger LT recipients (Fig. 2). Unfortunately, only the Nordic Transplant Registry study provides data regarding the CRC risk for different age groups [24]. The authors found an increased relative risk of 6.4 among women and 7.4 among men under 45 years of age. Such relative risks would barely bring incidence in the younger LT population to values comparable with the older general population. Evidence supporting CRC screening for LT recipients below age 50 is therefore relatively weak and, in our opinion, not to be proposed routinely.

  • View full-size image.
  • Fig. 2. 

    Age-specific incidence of CRC in the general population according to the Surveillance Epidemiologic and End Results (SEERs) cancer statistics 1998–2002, and hypothesized age-specific incidence in the LT population. A, incidence in the LT population <50 years; B, incidence in the general population >50 years. If A≥B, then screening in the LT population <50 years would be justified [37].

Nevertheless, it has to be considered that a relevant portion if this population will anyway undergo screening. Some will have a positive family history for CRC and therefore be candidates for screening. Others will undergo colonoscopy before or after LT because of symptomatic disease and subsequently be enrolled in surveillance protocols in the presence of polyps. In addition, according to OPTN data, about 5% of LT recipients below 50 are transplanted for PSC [36]. The majority of these patients suffer from UC and screening is recommended independently from transplantation. In PSC patients with UC surveillance colonoscopy after liver transplantation is recommend on a yearly basis [37].

As pointed out above, pre-LT colonoscopy provides a good means to identify high-risk patients at relatively low marginal costs.

When offering CRC screening it has also to be kept in mind that, when due to liver disease, comorbid conditions or advanced age, life expectancy does not exceed 5–10 years, CRC disease will not result in life limitation. In such a situation it has to be discouraged from CRC screening.

In conclusion, the present screening strategy is proposed in the awareness that strong evidence is lacking and relies on the best possible use of current knowledge (Table 2). More has to be known on CRC occurrence after LT, especially in the long-run and in the pediatric population, on extent and rapidity of progression of adenomatous lesions into CRC, and on the effects of new immunosuppressive drugs on the incidence of CRC. Only then can targets, times and intervals be optimized for the specific population of LT patients.

Table 2. Recommendations for CRC screening in the LT population
AllPre-LT colonoscopy
Surveillance after polypectomy
Presence of UC in PSCYearly surveillance colonoscopy
Over 50 yearsScreening as recommended for the general population
Under 50 yearsScreening if symptomatic disease

Do not screen in case of life expectancy <5–10 years.

Back to Article Outline

References 

  1. Organ Procurement and Transplantation Network (OPTN). US transplantations 1988–2004: http://www.optn.org/latestData/rptData.asp, accessed 07/19/2005.
  2. Sanchez W, Talwalkar JA, Gores GJ. “Will all liver transplant patients eventually die from cancer?”. J Hepatol 2006;44:13–18.
  3. Aucejo F, Rofaiel G, Miller C. Who is at risk for post-transplant lymphoproliferative disorders (PTLD) after liver transplantation? J Hepatol 2006;44:19–23.
  4. Dufour JF, Fey MF. What is the current treatment of PTLD after liver transplantation? J Hepatol 2006;44:23–26.
  5. Euvrard S, Kanitakis J. Skin cancers after liver transplantation: What to do? J Hepatol 2006;44:27–32.
  6. Fung JJ, Jain A, Kwak EJ, Kusne S, Dvorchik I, Eghtesad B. De novo malignancies after liver transplantation: a major cause of late death. Liver Transpl. 2001;7:S109–S118
  7. Penn I. Posttransplantation de novo tumors in liver allograft recipients. Liver Transpl Surg. 1996;2:52–59
  8. Kelly DM, Emre S, Guy SR, Miller CM, Schwartz ME, Sheiner PA. Liver transplant recipients are not at increased risk for nonlymphoid solid organ tumors. Cancer. 1998;83:1237–1243
  9. Frezza EE, Fung JJ, van Thiel DH. Non-lymphoid cancer after liver transplantation. Hepatogastroenterology. 1997;44:1172–1181
  10. Jain AB, Yee LD, Nalesnik MA, Youk A, Marsh G, Reyes J, et al. Comparative incidence of de novo nonlymphoid malignancies after liver transplantation under tacrolimus using surveillance epidemiologic end result data. Transplantation. 1998;66:1193–1200
  11. Catena F, Nardo B. De novo malignancies after organ transplantation. Transplant Proc. 2001;33:1858–1859
  12. Haagsma EB, Hagens VE, Schaapveld M, van den Berg AP, de Vries EG, Klompmaker IJ, et al. Increased cancer risk after liver transplantation: a population-based study. J Hepatol. 2001;34:84–91
  13. Xiol X, Guardiola J, Menendez S, Lama C, Figueras J, Marcoval J, et al. Risk factors for development of de novo neoplasia after liver transplantation. Liver Transpl. 2001;7:971–975
  14. Fabia R, Levy MF, Testa G, Obiekwe S, Goldstein RM, Husberg BS, et al. Colon carcinoma in patients undergoing liver transplantation. Am J Surg. 1998;176:265–269
  15. Vera A, Gunson BK, Ussatoff V, Nightingale P, Candinas D, Radley S, et al. Colorectal cancer in patients with inflammatory bowel disease after liver transplantation for primary sclerosing cholangitis. Transplantation. 2003;75:1983–1988
  16. Fleiss J. Statistical methods for rates and proportions. New York: Wiley; 1981;p. 33, see also p. 260–80
  17. Lee YM, Kaplan MM. Primary sclerosing cholangitis. N Engl J Med. 1995;332:924–933
  18. Lennard-Jones JE, Melville DM, Morson BC, Ritchie JK, Williams CB. Precancer and cancer in extensive ulcerative colitis: findings among 401 patients over 22 years. Gut. 1990;31:800–806
  19. Sugita A, Sachar DB, Bodian C, Ribeiro MB, Aufses AH, Greenstein AJ. Colorectal cancer in ulcerative colitis. Influence of anatomical extent and age at onset on colitis-cancer interval. Gut. 1991;32:167–169
  20. Ekbom A, Helmick C, Zack M, Adami HO. Ulcerative colitis and colorectal cancer. A population-based study. N Engl J Med. 1990;323:1228–1233
  21. Loftus EV, Aguilar HI, Sandborn WJ, Tremaine WJ, Krom RA, Zinsmeister AR, et al. Risk of colorectal neoplasia in patients with primary sclerosing cholangitis and ulcerative colitis following orthotopic liver transplantation. Hepatology. 1998;27:685–690
  22. Kasiske BL, Snyder JJ, Gilbertson DT, Wang C. Cancer after kidney transplantation in the United States. Am J Transplant. 2004;4:905–913
  23. Stewart T, Henderson R, Grayson H, Opelz G. Reduced incidence of rectal cancer, compared to gastric and colonic cancer, in a population of 73,076 men and women chronically immunosuppressed. Clin Cancer Res. 1997;3:51–55
  24. Birkeland SA, Storm HH, Lamm LU, Barlow L, Blohme I, Forsberg B, et al. Cancer risk after renal transplantation in the Nordic countries, 1964–1986. Int J Cancer. 1995;60:183–189
  25. Sheil AG, Disney AP, Mathew TH, Amiss N. De novo malignancy emerges as a major cause of morbidity and late failure in renal transplantation. Transplant Proc. 1993;25:1383–1384
  26. Adami J, Gabel H, Lindelof B, Ekstrom K, Rydh B, Glimelius B, et al. Cancer risk following organ transplantation: a nationwide cohort study in Sweden. Br J Cancer. 2003;89:1221–1227
  27. Hennekens CHBJ. Epidemiology in medicine. In:  SL M editors. Boston/Toronto: Little, Brown and Company; 1987;p. 82–85
  28. Zaman A, Hapke R, Flora K, Rosen H, Benner K. Prevalence of upper and lower gastrointestinal tract findings in liver transplant candidates undergoing screening endoscopic evaluation. Am J Gastroenterol. 1999;94:895–899
  29. Weller DA, DeGuide JJ, Riegler JL. Utility of endoscopic evaluations in liver transplant candidates. Am J Gastroenterol. 1998;93:1346–1350
  30. Rabinovitz M, Schade RR, Dindzans VJ, Belle SH, Van Thiel DH, Gavaler JS. Colonic disease in cirrhosis. An endoscopic evaluation in 412 patients. Gastroenterology. 1990;99:195–199
  31. Singer LG, Weinacker AB, Levin L, Doyle RL, Theodore J. Diagnostic yield of screening colonoscopies in lung transplant candidates. Transplantation. 2001;72:530–532
  32. Parikshak M, Pawlak SE, Eggenberger JC, Lee CS, Szilagy EJ, Margolin DA. The role of endoscopic colon surveillance in the transplant population. Dis Colon Rectum. 2002;45:1655–1660
  33. Brunner FP, Landais P, Selwood NH. Malignancies after renal transplantation: the EDTA-ERA registry experience. European dialysis and transplantation association-european renal association. Nephrol Dial Transpl. 1995;10(suppl 1):74–80
  34. US Vital Statistics. US age-specific mortality statistics: http://www.cdc.gov/nchs/data/dvs/mortfinal2002_work23r.pdf; 08/22/2005.
  35. Organ Procurement and Transplantation Network (OPTN). Survival after liver transplantation: http://www.optn.org/latestData/rptStrat.asp; 08/22/05.
  36. Organ Procurement and Transplantation Network (OPTN). Liver transplantations by cause: http://www.optn.org/latestData/rptData.asp; 08/25/2005.
  37. Itzkowitz SH, Daniel H, for the Crohn's Colitis Foundation of America Colon Cancer in IBD Study Group. Consensus conference: colorectal cancer screening and surveillance in inflammatory bowel disease. Inflamm Bowel Dis 2005;11:314–321.

PII: S0168-8278(05)00677-X

doi:10.1016/j.jhep.2005.10.011

Journal of Hepatology
Volume 44, Issue 1 , Pages 32-38, January 2006

Article Tools

* Image Usage & Resolution