Guidelines for the surveilance and management of familial adenomatous polyposis (FAP):a world survey among 41 registries
(By: Vasen HFA, Bülow S, and The Leeds Castle Polyposis Group, Colorectal Disease 199; 1, 214-221)

Summary

Background: Familial adenomatous polyposis (FAP) is an autosomal dominant disease characterized by numerous adenomas in the colorectum. The majority of patients also develop adenomas in the duodenum. The purpose of the study was to evaluate the management and screening protocols implemented in FAP families at various polyposis registries in the world.
Methods: A questionnaire was mailed to the members of the Leeds Castle Polyposis Group requesting information on: diagnostic evaluation of polyposis, recommendations for screening and surgical management of the colon, surveillance of the upper gastrointestinal tract and the management of duodenal polyposis
Findings: Almost all members agreed that a newly-diagnosed patient should be referred to a polyposis registry and to a clinical genetic centre for genetic counselling and DNA-testing. If the mutation has been detected in the family, DNA-testing should be offered to first-degree relatives of patients from age 10-12 onwards. The surveillance protocol generally advised includes sigmoidoscopy from age 10-12 at two-year-intervals until age 40. There was no agreement on the preferred surgical treatment of colonic polyposis. Almost all members advised follow-up after colonic surgery. Surveillance of the duodenum was recommended by most members; this would start from age 30. There was no agreement on the preferred surgical treatment of duodenal polyposis, or on the indication for operation.
Interpretation: This survey provides insight into the guidelines used at various polyposis registries for the surveillance and management of FAP patients, and this insight may contribute to the appropriate management of these patients.

Introduction

Familial adenomatous polyposis (FAP) is an autosomal dominantly inherited disease caused by inactivating mutations at the APC-gene on chromosome 5.1,2,3 The disease affects about 30 persons per million. Most polyposis patients develop hundreds of colorectal adenomas during their second and third decade of life. Without timely surgical intervention, the patients almost inevitably develop colorectal carcinoma by the age of 40-50 years. A small proportion of the families (<10%) have an attenuated or atypical form of polyposis, which is characterised by the development of a smaller number of polyps and the development of colorectal cancer at a more advanced age.4 The majority of the patients also develop polyps in the upper-GI tract, i.e., fundic gland polyposis (40%), gastric adenomas (5-10%) or adenomas in the duodenum (90%). Other extracolonic lesions observed in FAP are desmoid tumors (10-15%), epidermoid cysts (in 50%), congenital hypertrophy of the retinal pigment epithelium (CHRPE) (75-80%), dental anomalies (17%), and osteomas (75-90%). FAP patients also have an increased risk of developing brain tumours, hepatoblastoma and papillary carcinoma of the thyroid.1.2.3
The management of some aspects of FAP is controversial and lacks a strong scientific basis or the available evidence is contradictory. The aim of the present study was to evaluate the guidelines for the surveillance and management of polyposis patients currently used in centres specialised in the care of such patients.

Methods

In June 1997, a meeting of the Leeds Castle Polyposis Group was held in Noordwijk in the Netherlands. This international group includes specialists with a particular interest in familial adenomatous polyposis. The members, mainly surgeons, gastroenterologists and geneticists, are involved in the care of such families at clinical departments, polyposis registries or clinical genetic centres.
In mid-1997, a questionnaire was mailed to the members of the collaborative group requesting information on the guidelines used in their respective registries for surveillance and management. The questionnaire addressed the following issues:(1) diagnostic evaluation of FAP, (2) the surgical management of colonic polyposis, (3) follow-up after colonic surgery, (4) surveillance protocol in polyposis of the upper GI tract, (5) the management of duodenal adenomatosis, and (6) the management of desmoid tumours.
The questionnaire comprised specific statements formulated by the authors on each subject; participants were asked whether or not they agreed with these statements, and whether they had specific comments on them.

Results:

Completed questionnaires were received from 41 centres in 16 countries: Australia, Canada, Denmark, Finland, Germany, Hong Kong, Italy, Japan, Korea, Norway, Portugal, Switzerland, Singapore, the Netherlands, the United Kingdom, and the USA.

(1) Diagnostic evaluation of FAP:

Statement: A newly-diagnosed polyposis patient and his/her family should be referred to a polyposis registry and to a clinical genetic centre for genealogic study, genetic counselling and DNA-testing in order to identify all the at-risk individuals in the family and to ensure lifelong follow-up.
Reply: 93% of the clinicians agreed with this statement. One specialist suggested replacing “registry and genetic centre" with "registry or genetic centre".
Statement: Children and siblings of FAP-affected individuals should be offered presymptomatic DNA-testing from age 10-12, if the mutation in the family has been detected or linkage analysis has given high lodscores.
Reply: 88% of the respondents agreed with the statement. Two specialists would not accept the results of linkage analysis. One specialist suggested that sigmoidoscopy should start at age 10-12, and that DNA mutation analysis be postponed until age 16. One specialist suggested that the result of a DNA test should be confirmed by a second test. Another specialist emphasised that DNA-testing should be performed after appropriate genetic counselling.
Statement: At the very minimum, clinical examination should include a search for skin lesions, which occur mainly on the head, trunk and arms; it may also include retinal examination (by an ophthalmologist), and orthopantomographic X-ray for jaw and dental abnormalities.
Reply: 71% agreed with this statement. Ten respondents considered X-ray of the jaws and/or retinal examination to be unnecessary, because neither has any clinical implications. Two of these respondents claimed that these examinations would be useful only in the event of an inconclusive DNA-test. One specialist emphasised that if retinal examination is performed, it should be done by a experienced ophthalmologist.
Statement: If the result of DNA-testing is inconclusive (i.e., mutation is not identified in the family, or there are low or negative lodscores, as in about 30% of the families), it is recommended that regular sigmoidoscopy (preferably by a flexible scope) should start from age 10-12, and continue at two-year-intervals until at least age 40. In families in which the disease tends to manifest late, surveillance should continue to a later age.
Reply: 78% agreed; three centres recommended starting from age 14 or 15. Three centres advised a one-year interval instead of a two-year interval. Four specialists recommended that examinations be continued until age 55-60.
Statement: Total colonoscopy should be considered in families with an atypical form of polyposis, as adenomas may only be located in the right colon. In such families the endoscopic examinations may be started at a later age, e.g. from age 18-20, because adenomas often develop at a late age.
Reply: 78% agreed. Two respondents suggested that periodic examinations should start 10 years before the age at diagnosis of the index case.
Statement: If DNA-testing proves the carrier status of the at-risk family member, the endoscopic programme should be continued as described above. If the test reveals that the person does not carry the mutation, the periodic examinations can be discontinued.
Reply: 73% agreed. Five clinicians did not fully trust negative results of the DNA-test (in a family with a known APC-mutation), and therefore continued endoscopic examinations at longer intervals. Two specialists would perform endoscopic examinations every year in gene carriers.

(2) The surgical management of colonic polyposis:

Statement: Colectomy should be performed soon in an adult family member with a newly-diagnosed FAP. The timing of prophylactic colectomy in a child who has been identified during a family surveillance depends on the number, size and degree of dysplasia of the adenomas. In addition, individual social and educational factors concerning the patient may be taken into account. Most patients are operated on between age 15 and 25.
Reply: 97% agreed. There were no specific comments.
Statement: There are two main techniques of reconstruction following colectomy and proctocolectomy:
(1) Colectomy and ileorectal anastomosis (IRA) at about 12 cm from the anal verge. Compared to a restorative proctocolectomy with an ileo-anal pouch (RPC), this has three advantages: it is a one-stage procedure, has a low complication rate, and leads to total continence. The disadvantages are a high cumulative risk of secondary proctectomy (30% after 15 years of follow up), and a 10-15% cumulative 25-year risk of rectal cancer, despite regular follow-up.
(2) Restorative proctocolectomy with an ileo-anal pouch (RPC). The advantages of this compared to IRA are that it involves a more radical removal of rectal mucosa, and thereby a very low risk of rectal cancer. The disadvantages are that it is usually a two-stage procedure, has a higher complication rate, involves a 5-10% risk of suboptimal continence, and that there is a 5% risk of pouch removal due to complications or malfunction. Two techniques are currently used: (1) a double-stapled anastomosis, i.e., a stapled anastomosis between the pouch and the anal canal at the level of the anorectal junction, and (2) a hand-sewn anastomosis, i.e., mucosectomy with a hand-sewn ileo-anal anastomosis at the dentate line. Most surgeons perform a mucosectomy with a hand-sewn pouch-anal anastomosis, but some prefer a double-stapled anastomosis. The former ensures a radical mucosal removal, but may be followed by a longer acclimatisation period before total continence and a final functional result is achieved. The latter involves a risk of leaving 1-2 cm mucosa, but leads to very good functional results shortly after the operation.
Both IRA and RPC result in an average of 3-6 daily bowel movements without urge, and a good quality of life. However, RPC requires a high level of expertise and experience, and should therefore be carried out by a surgeon who is used to performing it. The technique of mucosectomy and hand-sewn pouch-anal anastomosis is recommended.
Reply: 76% of the respondents agreed with the pros and cons of the surgical procedures specified above. Two clinicians did not agree on the level of risk of cancer developing after ileorectal anastomosis. One specialist mentioned impotence and proctalgia as consequences of the surgical procedures. One responded that an additional disadvantage of IRA is that it cannot be converted to RPC if mesenterial fibrosis develops after the operation. One respondent emphasised the possibility of a permanent ileostomy as a disadvantage of an RPC. A possible disadvantage of a mucosectomy and handsewn anastomosis is that mucosa might be left behind extraluminally and, consequently, that adenomas cannot be detected by endoscopy.
Of the respondents who had a clear opinion on the technique of anastomosis, 67% preferred mucosectomy with a hand-sewn anastomosis, and 32% preferred a double-stapled anastomosis procedure.
Statement: The choice of procedure remains controversial among surgeons, and the pros and cons of the two alternatives should be discussed with the patient. Most surgeons agree on the following general guidelines:
IRA is recommended in the following patients: those with few (less than approx. 20) rectal adenomas of less than 5 mm; those from families with attenuated FAP; those with desmoid tumours; and those with a metastatic cancer of the upper rectum or colon.
RPC is preferred in patients with a large number of rectal adenomas, in patients with a non-metastatic cancer of the upper rectum or colon, and in patients in whom a life-long follow-up cannot be assured.
Reply: 67% of the clinicians agreed that the presence of few adenomas is an indication for IRA, whereas 32% also preferred an RPC in such patients. 73% were in favour of an IRA in patients with an attenuated form of FAP, against 27% of the specialists who preferred an RPC. 58% preferred an IRA in patients with a desmoid tumour, against 42% who were in favour of a RPC in such patients. 89% were in favour of IRA for patients with metastatic disease. 100% regarded a large number of adenomas in the rectum and 94% noncompliance as an indication for RPC. Nonmetastatic rectal and colon cancer are regarded as an indication for RPC by 97% and 94% of the respondents, respectively. One specialist stated that a low age might also be considered as an indication for IRA, and another specialist mentioned poor sphincter function (i.e., poor control) as an additional indication for IRA.

(3) Follow-up after colonic surgery.

Statement: After IRA, an endoscopic follow-up of the rectum is indicated at intervals of 3-12 months, the intervals depending on the number, size and degree of dysplasia of new adenomas. While adenomas > 5 mm should be removed at each endoscopy, it is not necessary to remove every adenoma, irrespective of its size, since such a practice may lead to scarring of the rectum, which makes subsequent assessment difficult.
Reply: 87% agreed with the statement. Two specialists preferred one-year intervals between examinations. Another respondent suggested a four-month interval in patients older than age 50.
Statement: After RPC, an annual follow up by digital examination and rectoscopy is indicated to identify adenomas at the site of the ileo-anal anastomosis and in the pouch.
Reply: 78% agreed that annual follow up is indicated, both after the double-stapled procedure and after hand-sewn anastomosis. 17% were of the opinion that follow-up is indicated only after the use of the double-stapled technique. 94% recommended both digital examination and rectoscopy.
Statement: Treatment of a patient with rectal adenomas after IRA with NSAID (e.g. Sulindac) should only take place in the setting of a prospective study. The follow-up should continue even after the adenomas have disappeared.
Reply: 76% agreed with this statement. 24% thought that treatment with NSAID might also be justified outside the setting of a prospective study if the follow-up were appropriate.

(4) The surveillance protocol of polyposis of the upper GI tract,

Statement: Although the value of the screening of the upper GI is unknown, the option of regular gastroduodenoscopy should be discussed with the patient: the pros are early detection, and the surgical treatment of severe duodenal adenomatosis or early carcinoma. The cons are the low risk (probably < 5%) of duodenal cancer; the absence of definite proof of the benefit of prophylactic examinations, the increased risk of carcinophobia, the morbidity associated with periodic endoscopies; and the risk of morbidity and even mortality associated with major surgery, which in this case is carried out for a condition that is most often non-malignant.
Reply: All respondents recommended surveillance of the upper GI tract. 95% agreed with the pros and cons of surveillance specified above.
Statement: If the patient agrees, one should start regular gastroduodenoscopy at the age of 30 years, continuing this at intervals of 1-3 years, depending on the stage of the duodenal adenomatosis. The Spigelman classification 5 should be used, and examinations should preferably be carried out in the setting of a prospective study.
Reply: 79% of the respondents agreed with the proposed protocol. Among the other respondents, five recommended that surveillance should start at an earlier age, e.g., at the age at diagnosis of FAP, or an age between 20-25. Two participants reported problems with defining the interval of the examinations on the basis of the Spigelman classification, because a small adenoma with high degree of dysplasia together with a low Spigelman score is also an indication for shortening the interval.
Statement: A pancreas-sparing duodenectomy or a partial pancreatico-duodenectomy should be considered in patients older than 35-40 years with a continued finding of duodenal adenomatosis Spigelman stage IV after one year.
Reply: 65% agreed with this statement, while 24% did not, and 11% did not know what would be the best policy. Among the 24% who did not agree, three were of the opinion that Whipple’s operation should be reserved for patients with malignant disease. Three other respondents would prefer a less radical operation. One participant stressed that ‘we really don’t know what would be the best approach.’
The various surgical procedures were recommended as follows: pancreas sparing duodenectomy (11 respondents), partial pancreaticoduodenectomy (12 respondents), duodenectomy with mucosectomy (4 respondents), and ampullectomy (2 respondents).

(5) The management of desmoid tumours

Statement: Examination should include evaluation by CT-scanning and, if possible, MRI.
Reply: 82% agreed. There were no specific comments.
Statement: Surgical treatment is indicated in extra-abdominal and abdominal wall desmoids. Surgical treatment of intra-abdominal desmoids may be considered, as a palliative treatment, only in severely symptomatic cases.
Reply: 85% agreed. Two respondents stressed that intestinal by-pass is the sole intervention indicated in severe cases of intra-abdominal desmoids.
Statement: Medical treatment with Sulindac and Tamoxifen (or Toremifene) may be of benefit, and chemotherapy with Doxorubicin and Dacarbazine may be considered in severe cases for which there are no other therapeutic options. Treatment of desmoids should preferably take place in the setting of an international study.
Reply: 97% agreed. One respondent would prefer radiotherapy to chemotherapy.

Discussion

FAP is a rare dominantly inherited disorder with a high penetrance but a variable expression. In order to improve the care of affected patients, its management is often centralised or co-ordinated by a polyposis registry.1,2,3 To enhance research in FAP, an international collaborative group of specialists and scientists – The Leeds Castle Polyposis Group – was established more than a decade ago.6 The data presented in this manuscript are the result of a survey conducted among the members of this group. The aim of the survey was to outline current ideas on the management of FAP at the various polyposis registries.

Diagnostic evaluation

All respondents agreed that a newly-identified polyposis family should be referred both to a polyposis registry and to a clinical genetic centre. The original aims of polyposis registries are to promote the identification of relatives at risk, and to ensure their lifelong participation in the surveillance programme. The clinical genetic centres that became interested in FAP after the identification of the polyposis gene are specialised in genetic counselling and the DNA-testing of families. The tasks of both types of institute might therefore be considered to be complementary.
A recent study in the USA7 revealed that few of the individuals who had been tested for mutations in the APC-gene had received appropriate genetic counselling. The fact that all respondents in the present survey considered the involvement of a genetic centre to be mandatory, indicates that all polyposis families will receive the appropriate counselling.
The study showed that specialists involved in the care of polyposis families have more trust in the outcome of the results of the DNA-test than they had a number of years ago. Very few specialists would continue periodic examinations after a negative test in the case of a known mutation in the family. If mutation analysis did not lead to the identification of the mutation, it might be useful to use linkage analysis, especially in large families. Two respondents reported that they would not use the results of linkage analysis for the detection of carriers of FAP. Although mutation analysis is the method of choice because of its absolute reliability, the linkage approach becomes almost as reliable as mutation analysis in families with sufficient support for linkage between the disease and the APC locus (lodscore > 0.9).8
It should be emphasised that genetic testing led to identification of the mutation in only 67-82% of the families.9,10 In the remaining families it is possible to estimate the risk of being a carrier on the basis of age of the last negative (i.e., polyp-free) sigmoidoscopy, or of the absence or presence of retinal lesions and osteomas. The most important indications for retina examination and orthopantographic examination of the jaws are in families where DNA-testing did not lead to the identification of the mutation.
Most respondents agreed that the surveillance programme (sigmoidoscopy at two-year intervals from age 10-12) is appropriate, both for at-risk relatives and for proven gene carriers.

Surgical management of colonic polyposis

Experience has shown that most polyposis patients identified through family screening have colonic surgery at an age between 15 and 25. There was general agreement that the exact timing of the operation depends both on the severity of the polyposis and on personal social factors.
The well-known disadvantages of IRA are the high cumulative risk of secondary proctectomy and the risk of developing rectal cancer.11 The disadvantages of RPC are the higher complication rate, and the less satisfactory functional outcome. One respondent indicated that an additional disadvantage of IRA is that the development of an intra-abdominal desmoid tumor after the operation can make a secondary proctectomy impossible.
There was no agreement about the preferred surgical procedure. Although the majority of the respondents considered both the finding of a few polyps in the rectum and an attenuated form of polyposis to be appropriate indications for an IRA, a substantial proportion of the respondents (one third) would also perform an RPC for these indications. For some respondents, the presence of an intra-abdominal desmoid is a reason to perform an IRA; however, for an equal number of respondents, it is an indication for a RPC. The most important argument for choosing an RPC as the preferred primary option is the fact that conversion into RPC might be impossible in the event of the further growth of the desmoid. On the other hand, it might be argued that the most extensive surgical procedure that may lead to growth of the desmoid (i.e., RPC) should be avoided. One respondent suggested that a poor sphincter is a contraindication for IRA. In the opinion of the authors, this would represent a relative contraindication for both procedures. There was no doubt among the respondents about the indications for RPC, i.e., patients with a large number of polyps in the rectum, and patients who do not wish to comply with the follow-up examinations. Most members agreed that patients with a mild form of polyposis are good candidates for an IRA. A recent study revealed that patients with mutations known to be associated with a less aggressive form of polyposis had a lower risk of a secondary proctectomy due to uncontrollable polyps, than patients with mutations known to be associated with an aggressive form of polyposis.12 If larger studies confirm these findings, the result of mutation analysis in combination with the clinical phenotype of a specific family might be helpful in the surgical decision-making.
One respondent suggested that IRA should be performed in young patients, and RPC in those whose age was more advanced. The background for this suggestion lay in the results of a St Mark’s study13 that showed that the risk of rectal cancer increases sharply between age 50 and 60. On the basis of these findings it was proposed to convert an IRA into an RPC in patients reaching this high-risk age. If a patient had already reached an advanced age, it might be argued that RPC should be performed as the primary procedure in order to avoid a second operation a little later. However, there are as yet no published results of such a policy, and the potential reduction of the incidence of metachronous rectal cancer must be outweighed by the morbidity of the conversion procedure. More studies are needed to find out whether the reported increase of risk between age 50-60 applies to all patients.
There was no agreement pertaining to the technique for performing the anastomosis. Two techniques are currently used: i.e., a stapled anastomosis between the pouch and the anal canal at the level of the anorectal junction (double-stapled anastomosis), or a mucosectomy with a conventional ileoanal anastomsis at the dentate line (hand-sewn anastomosis). Two thirds of the respondents preferred a hand-sewn anastomosis, while one third advised a double-stapled anastomosis in polyposis patients. A well-known disadvantage of the double-stapled anastomosis is the fact that it may leave 1-2 cm mucosa which is at risk for adenoma/carcinoma development. A disadvantage of the hand-sewn anastomosis is that there might be a risk of leaving mucosa extraluminally, which might make early detection by endoscopy impossible. The few studies that are available suggest that functional outcome is better after a double-stapled technique than after the hand-sewn technique.14
Most respondents recommend follow-up after IRA (at a three to twelve-month interval), and after RPC, regardless of the technique that has been used (i.e., follow-up annually both by digital examination and endoscopy).

Surveillance of the upper GI tract

Several reports indicated that at least two thirds of polyposis patients have duodenal polyposis. There is ample evidence that the duodenal adenoma also follow the adenoma-carcinoma sequence observed in the colorectum.15 A recent retrospective registry-based study suggested that the lifetime risk of developing duodenal cancer is less than 5%.16 The present study showed that, despite the fact that the effectiveness of surveillance is unknown, all participants discussed the possibility of surveillance with their patients. There was also general agreement about the surveillance programme, i.e., gastroduodenoscopy at 1-3 year intervals starting from age 30.
In contrast, there was no agreement about the indication for and the timing of surgery. Criteria regarding size, rapid growth, polyp induration, or consistently severe dysplasia or villous change suggest that intervention is necessary. In view of the morbidity of major pancreatic surgery, some respondents would consider surgery only in patients with histologically proven carcinoma. Hopefully, ongoing studies17,18 on the natural history of duodenal polyposis will lead to the identification of patients at high risk of developing cancer. Treatment could be more focused if it were possible to predict the natural history of the disease, such that those individuals destined to develop duodenal cancer would be treated in a premalignant stage. Five respondents recommended a duodenoscopy at an earlier age, e.g., at the time of colonic surgery. Although this might be appropriate, especially to reassure relatives of patients with duodenal disease, it not strictly necessary, as the natural history of the disease indicates that duodenal cancer is extremely rare before age 30.
There was no consensus on the preferred surgical procedure. However, as recent studies indicate that mortality due to pancreatic surgery is significantly higher in hospitals with limited experience (i.e., those carrying out fewer than five procedures per year), we would therefore like to emphasise that such procedures should be performed at highly specialised centres.

The management of desmoids

Desmoids are benign fibromatous lesions that arise most often in the abdominal wall and mesentery, but also occasionally in the extremities and trunk.19 These lesions are observed in 7-11% of polyposis patients. The mean age at diagnosis is 30 years. Complications from desmoids have been reported to be second only to metastatic cancer as a cause of death in FAP patients. The cause of desmoids is unclear. In FAP patients, desmoid development has been associated with abdominal surgery, pregnancy and exposure to oral contraceptives. The family history of desmoids may also be an important risk factor. A recent study20 showed that the desmoid risk in FAP family members of a desmoid patient was 25% in first degree relatives. The treatment of desmoids is controversial, and is based largely on anecdotal reports and on studies of small series of patients. The extremely variable natural history of desmoids hampers the evaluation of a specific treatment. The present survey indicated that there is agreement that surgery should be avoided for mesenteric desmoids because of the risk of accelerated growth and the high risk of recurrence. The problem with radiotherapy suggested by one of the respondents is that its use is limited by the radiosensitivity of the surrounding intra-abdominal structures. Most respondents recommended Sulindac as the initial treatment. If growth continues, Tamoxifen or Toremifene is added. If the desmoid is still growing or is giving rise to significant symptoms, Doxorubicin and Dacarbazine chemotherapy is considered. As emphasized by several respondents, operation on intra-abdominal desmoids may be needed to bypass bowel obstruction or to relieve ureteric obstruction.

Conclusion

The survey demonstrates agreement on most parts of the protocol, but also conspicuous differences of opinion on some other parts. It should be emphasised that not all these recommendations have a strong scientific basis. Careful education and counselling of patients and their relatives about all details of the disease are therefore essential. Ideally, the outcome of the protocols should be collected in a uniform manner at a polyposis registry. Hopefully, this information will help to extend effective care to all carriers of the disease.

References

1. Bussey HJR. Familial polyposis coli. Baltimore: John Hopkins University Press, 1975
2. Philips RKS, Spigelman AD, Thomson JPS. Familial adenomatous polyposis and other polyposis syndromes. Edward Arnold 1994, Great Britain
3. Campbell WJ, Spence RA, Parks TG. Familial adenomatous polyposis. Br J Surg 1994; 81:1722-1733
4. Spirio L, Olschwang S, Groden J, et al. Alleles of the APC gene: an attenuated form of familial polyposis. Cell 1993;75:951-957
5. Spigelman AD, Williams CB, Talbot IC, et al. Upper gastrointestinal cancer in patients with familial adenomatous polyposis. Lancet 1989; 2: 783-785
6. Northover JMA. Activities of the Leeds Castle Polyposis Group. Semin Surg Oncol 1987;3:118-119
7. Giardello FM. Brensinger JD, Petersen GM, et al. The use and interpretation of commercial APC gene testing for familial adenomatous polyposis. N Engl J Med 1997; 336:823-827
8. Tops CMJ. Presymptomatic DNA-diagnosis of familial adenomatous polyposis. Ph.D. Thesis, Leiden University
9. Nagase H, Miyoshi Y, Horii A, et al. Screening for germ-line mutations in familial adenomatous polyposis patients: 61 new patients and a summary of 150 unrelated patients. Hum Mutat 1992b;1:467-473
10. Van der Luijt RB, Khan PM, Vasen HF et al. Molecular analysis of the APC gene in 105 Dutch kindreds with familial adenomatous polyposis: 67 germline mutations identified by DGGE, PTT and southern analysis. Human mutation 1997;9:7-16
11. Decosse J, Bulow S, Neale K, et al. Rectal cancer risk in patients treated for familial adenomatous polyposis. Br J Surg 1992; 79:1372-75
12. Vasen HFA, van der Luijt RB, Slors JFM, et al. Molecular genetic tests a guide to surgical management of familial adenomatous polyposis. Lancet 1996; 348:433-435
13. Nugent KP, Phillips RKS. Rectal cancer risk in older patients with familial adenomatous polyposis and an ileorectal anastomosis: a cause for concern. Br J Surg 1992;79:1204-1206
14. Thompson-Fawcett MW and Mortensen NJMcC. Anal transitional zone and columnar cuff in restorative proctocolectomy. Br J Surg 1996;83:1047-1055
15. Spigelman AD, Talbot IC, Penna C, et al. Evidence for adenoma-carcinoma sequence in the duodenum of patients with familial adenomatous polyposis. J Clin Pathol 1994;47:709-710
16. Vasen H.F.A., Bülow S, Myrrhoj T, et al. Decision analysis in the management of duodenal adenomatosis in familial adenomatous polyposis. Gut 1997;6:716-719
17. Bulow S, Alm T, Fausa O, et al. Duodenal adenomatosis in familial adenomatous polyposis. Int J Colorect Dis 1995; 10: 43-46
18. Debinski HS, Spigelman HS, Hatfield A, Williams C, Phillips RKS. Upper intestinal surveillance in familial adenomatous polyposis. Eur J cancer 1995;31A:1149-1153
19. Clark S, Phillips RKS. Desmoids in familial adenomatous polyposis. Br J Surg 1996;83:1494-1504
20. Gurbuz AK, Giardiello FM, Petersen GM, et al. Desmoid tumours in familial adenomatous polyposis. Gut 1994;35:377-381

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