• No results found

Systematic review of sentinel lymph node biopsy in anal squamous cell carcinoma

N/A
N/A
Protected

Academic year: 2021

Share "Systematic review of sentinel lymph node biopsy in anal squamous cell carcinoma"

Copied!
5
0
0

Loading.... (view fulltext now)

Full text

(1)

Review

Systematic review of sentinel lymph node biopsy in anal squamous

cell carcinoma

A. Noorani

a

, N. Rabey

b

, A. Durrani

b

, S.R. Walsh

c

, R.J. Davies

a,*

aCambridge Colorectal Unit, Addenbrookes Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK

bDepartment of Plastic and Reconstructive Surgery, Addenbrookes Hospital, Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK cGraduate Entry Medical School, University of Limerick, Ireland

a r t i c l e i n f o

Article history:

Received 30 November 2012 Received in revised form 7 May 2013

Accepted 11 July 2013 Available online 19 July 2013

Keywords:

Sentinel lymph node biopsy Anal cancer

a b s t r a c t

Background:Anal squamous cell carcinoma with lymph node metastases carries a poor outcome. There remains a need for a better method to diagnose inguinal lymph node metastases which is minimally invasive, accurate and avoids unnecessary irradiation to the groin with its associated significant co-morbidity. The aim of this study was to evaluate the role of sentinel lymph node (SLN) biopsy in anal squamous cell carcinoma.

Methods:The systematic review was conducted in accordance with PRISMA guidelines. The Medline, Central and Embase databases were searched using the terms ‘sentinel lymph node’ and ‘anus neoplasms’.

Results:The systematic review identified 17 studies, containing 270 patients. SLN detection rate varied from 47% to 100%. The presence of nodal metastases varied from 0 to 44%. The complication rate varied from 0 to 59%. The rate of development of subsequent inguinal lymph node metastases in those previ-ously SLN biopsy-negative (a surrogate marker for false negative rate) ranged from 0 to 18.75%. Conclusion:SLN biopsy is a feasible method of assessing lymph node status in patients with anal squa-mous cell carcinoma. Longer follow up is required to evaluate the proportion of patients who are SLN biopsy-negative and subsequently develop nodal metastases. More studies are required to ascertain whether SLN biopsy should be the main method of assessing inguinal lymph node involvement in pa-tients with anal squamous cell carcinoma.

Ó2013 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved.

1. Introduction

Anal squamous cell carcinoma is an uncommon malignancy, accounting for approximately 4% of all gastrointestinal malig-nancies.1Metastases to superficial inguinal lymph nodes occur in 15e25% of cases in T1/T2 carcinoma and up to 50% of T3/T4 carci-noma.2Lymph node involvement has been shown to be a negative prognostic indicator for survival, yet detecting positive lymph nodes remains a challenge.3 In particular there is no consensus regarding the optimal management of patients with anal squamous cell carcinoma and clinically uninvolved inguinal lymph nodes.

Since the work of Nigro and colleagues in 1974, chemo-radiotherapy has replaced abdominoperineal excision of the rectum as thefirst line treatment of anal squamous cell carcinoma.4

Prophylactic radiotherapy to the groin has been shown to reduce the rate of inguinal lymph node metastasis from 4 to 25%.5 How-ever, significant radiotherapy related morbidity occurs in around 15% of all patients; short term complications include erythema and skin burns, with small bowel damage, hip fractures, bladder injury and sexual dysfunction being more problematic in the long term.6,7 The diagnostic dilemma remains in detecting lymph node meta-stastes in these patients in order to tailor treatment to the indi-vidual, and avoid potential over treatment in those with uninvolved nodes.

Wade and colleagues demonstrated that 44% of all lymph node metastases are<5 mm in diameter and not detectable by con-ventional imaging.8Ultrasound remains variable with a sensitivity of 36e87% and specificity of 56e89%.9Ultrasound withfine needle aspiration (FNA) also has a low detection rate at 65%.10Recently, positron emission tomography (PET) imaging has been shown to detect inguinal metastases in up to 20% of patients who have clinically and radiologically uninvolved nodes on conventional imaging.11There remains a clear need for a more accurate method *Corresponding author. Cambridge Colorectal Unit, Addenbrooke’s Hospital, Hills

Road, Cambridge CB2 0QQ, UK.

E-mail address:justin.davies@addenbrookes.nhs.uk(R.J. Davies).

Contents lists available atScienceDirect

International Journal of Surgery

j o u r n a l h o m e p a g e : w w w . j o u rn a l - s u r g e r y . n e t

1743-9191/$esee front matterÓ2013 Surgical Associates Ltd. Published by Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.ijsu.2013.07.005

(2)

to diagnose inguinal lymph node metastases in order to individu-alize treatment of patients with anal squamous cell anal carcinoma, and avoid unnecessary morbidity from prophylactic groin radiotherapy.

The sentinel lymph node (SLN) concept wasfirst described in 1960 in parotid cancer.12It was clinically implemented by Cabanas in 1977 in penile cancer.13Its role in breast cancer and melanoma has been investigated, but its role in gastrointestinal cancers is less clear.14,15Two techniques are most commonly used for SLN biopsy in anal cancer. The first involves lymphoscintigraphy to identify lymphatic drainage and the first node in which the tracer is captured. The radioisotope, commonly a technetium-labelled nanocolloid, is injected around the anal tumour and the node is localised using a gamma camera. During surgery, a hand-held gamma probe is used to detect the presence of the radioisotope. The second technique involves injection of blue dye around the site of the tumour during surgery. This visually aids the detection of the SLN, and the two techniques may be used individually or in com-bination. Excision of the node can be performed under local or general anaesthesia, and the excised node(s) is sent for

histopathological analysis using either frozen section or paraf n-block sections.

The aim of this systematic review was to investigate the role of SLN biopsy in anal squamous cell carcinoma.

2. Methods

A systematic review was conducted in accordance with the PRISMA guidelines.16 The terms‘sentinel lymph node’and‘anus neoplasms’were used to search Embase, Central and Medline databases by two independent researchers (AN and NR). Conference proceedings from major general surgery meetings (Association of Sur-geons of Great Britain and Ireland, American Society of Colon and Rectal SurSur-geons, European Society of Coloproctology, Association of Coloproctology of Great Britain and Ireland and American College of Surgeons Annual Congress) were searched from 2000 to 2011. Any identified abstracts were scrutinised to determine eligibility for inclusion. Reference lists from eligible reports were also searched for potential abstracts.

The quality of studies was assessed using the Down and Black checklist for both randomised and non-randomised studies.17A total of 27 questions assess each paper on quality of reporting, external validity and internal validity (bias and confounding factors). The maximum a study can score is 27 as one point is given to each satisfied criterion of the checklist. This checklist provides a profile of the publication and helps reviewers identify its strengths and weaknesses. Two reviewers (AN and NR) scored studies independently and a kappa statistic was calculated to assess inter-rater variability using Stats Direct (Stats Direct Ltd, Altrincham, UK). Any differ-ence in score was re-assessed by an independent reviewer (SRW).

Studies were eligible for inclusion provided they met the following criteria: subjects aged 18 or over and at least one clinical outcome reported by authors. Studies were excluded if they included anal melanoma or subjects with clinically palpable inguinal lymph nodes.

The primary outcome was SLN detection (positive SLN/total number patients undergoing SLN biopsy). The secondary outcomes were nodal metastases (SLN nodes positive for metastases/total SLNs identified) and nodal metastases in SLN biopsy-negative patients during follow up (false negative rate). Data were entered into an Excel (Microsoft Excel, Redmond, USA) Spreadsheet for analysis.

3. Results

The search results are presented inFig. 1in the format of the PRISMA guidelines. A total of 17 studies were eligible,17e34equating to a sum of 270 patients.Table 1summarises the results. Sentinel lymph node detection and nodal metastases were reported by all studies.

Table 2summarises the Down and Black score for each study, and provides a detailed breakdown of the component of the score. The maximum score for each of the subdivisions was 10 for quality of reporting, 3 for external validity, 7 for internal validity Figure 1.Flow diagram of screening and selection of articles for the systematic review.

Table 1

Results of systematic review.

Author No. patients Year Dye vs isotope

No of patients having SLN biopsy

SLN identified Nodal metastasis (SLNþSLN identified) Nodal metastasis in SLN biopsy-negative patients during follow up (%) Down and black score De Jonga25 50 2011 Both 21 21/21¼100% 7/21¼33% 9.5% 17

Peley19 8 2002 Both 8 8/8¼100% 2/8¼25% No Follow up 16

Bobin18 33 2003 Both 33 33/33¼100% 7/33¼21% 0% 17

Perera20 12 2003 Both 12 8/12¼67% 2/12¼17% No follow up 12

Damin21 14 2003 Both 14 14/14¼100% 1/14¼7% No follow up 19

Ulmer31 12 2003 Isotope 12 10/12¼80% 4/9¼44% No follow up 16

Mistrangelo23 35 2008 Isotope 34 34/35¼97% 7/34¼21% 0% 18

Gretschel22 40 2008 Isotope 20 20/20¼100% 6/20¼30% 10% 18

Rabbit29 4 2002 Both 4 4/4¼100% 0/4¼0% No follow up 8

Ulmer17 17 2004 Isotope 13 13/17¼77% 5/12¼42% Not stated 18

Castro33 2 2005 Both 2 2/2¼100% 0/2¼0% No follow up 7

Francois32 34 2010 Isotope 34 16/34¼47% 5/16¼31% 18.75% Not scored as

abstract only.

De Nardi24 11 2011 Both 9 9/9¼100% 3/9¼33% No follow up 15

Mistrangelo26 27 2010 Both 27 27/27¼100% 3/27¼11% 0% 23

Hirche27 12 2010 Both 12 9/12¼75% 2/9¼22% 0% 18

Mistrangelo30 15 2005 Isotope 15 15/15¼100% 5/14¼27% No Follow up 18

(3)

(confounding factors) and 7 for internal validity (bias). Hence the total maximum score that could be awarded to each manuscript was 27.

The kappa statistic for inter-rater variability was 0.706 (SE 0.125, 95% CI 0.456e0.957) which demonstrated agoodagreement.

Table 3summarises the complication rates for SLN biopsy. Six studies described complications, with the highest rate reported at 59%.22,25e27,31 However, only two cases of the 46 complications reported needed further intervention with the remainder resolving with conservative management within 2 weeks. In terms of long term follow up data, this was only recorded in 7 studies.

3.1. SLN detection

The results of this review demonstrate that the rate of SLN detection varies from 47% to 100%. Damin et al. highlighted in an earlier report that a lower rate of SLN detection was seen in studies which used radioisotope alone, and that the detection rate was much improved in studies which used radioisotope in combination with blue dye.34In this systematic review, the lower rate of SLN detection of 47% was in a study by Francois and colleagues, which used isotope alone.32However other studies using isotope alone had detection rates of 100%, hence superiority of either method cannot be concluded. There is evidence in melanoma and breast cancer, that combining the two methods results in a better overall method of detecting the SLN38,39and it may be that further studies

are required before we can make such deductions in anal squamous cell carcinoma.

3.2. Nodal metastasis

The rate of nodal metastasis varied from 0%28,29,33e44%.17 Studies with nodal metastasis rate of 0% had very small subject numbers, and this is likely to have contributed to their results.28,29,33

3.3. False negative rate

It is not possible to accurately detect the sensitivity and

speci-ficity of SLN biopsy, as to do this a surgical groin dissection would be required in order to assess the true status of nodes which were not detected using the SLN method. However another surrogate marker for a false negative rate is to follow up SLN biopsy-negative patients who did not undergo radiotherapy. This was done by seven studies and the rate of development of subsequent inguinal lymph node metastases ranged from 0 to 18.75%.18,22,23,25e27,32

4. Discussion

The rationale for SLN biopsy is to improve staging for anal squamous cell carcinoma. As described, the most common SLN biopsy techniques involve injection of radioisotope-labelled nano-colloid with or without blue dye injection. More recently, Table 2

Down and Black scores for each study.

Study Year Quality of reporting (Max score¼10)

External validity (Max score¼3)

Internal validity: bias (Max score¼7)

Internal validity: confounding factors (Max score¼7)

Total score (Max score¼27) De Jonga25 2011 7 3 4 3 17 Peley19 2002 7 3 5 1 16 Bobin18 2003 8 3 4 2 17 Perera20 2003 5 3 2 2 12 Damin21 2003 8 3 5 3 19 Ulmer17 2004 7 3 5 1 16 Mistrangelo23 2008 8 3 4 3 18 Gretschel22 2008 8 3 5 2 18 Rabbit29 2002 5 2 1 0 8 Ulmer31 2003 6 3 4 5 18 Castro33 2005 3 2 2 0 7

Francois32 2010 Not scored Not scored Not scored Not scored Not scored

De Nardi24 2011 8 3 3 1 15 Mistrangelo26 2010 10 3 5 5 23 Hirche27 2010 8 3 5 2 18 Mistrangelo30 2005 5 3 4 6 18 Keshtgar28 2001 3 2 2 0 7 Table 3

Complications from sentinel lymph node biopsy. Author Total patients Year Dye vs isotope No of patients having SLN biopsy Number of complications

Types of complications Further intervention required

De Jong25 50 2010 Both 21 5/21¼24% 2 wound infections 2 seromas 1 lymphoedema

No

Mistrangelo23 35 2008 Isotope 34 20/34¼59% 1 lymphocoele requiring surgery 1 monolateral lymphoedema 18 inguinal lymphorrhoea

Yes (n¼1)

Gretschel22 40 2008 Isotope 20 4/20¼20% 2 wound infections 1 lymphaticfistula 1 haematoma

No

Ulmer17 17 2003 Isotope 12 1/12¼8% 1 cutaneous lymphaticstula No Hirche27 12 2010 Both 12 2/12¼17% 1 lymphocoele, 1 lymphorrhoea No Mistrangelo26 27 2010 Isotope 27 14/27¼52% 13¼inguinal lymphorrhoea

1¼lymphocoele requiring evacuation

(4)

indocyanine green has been used in the identification of SLN in breast cancer,35gastric cancer36and anal cancer.27This technique is well established in breast cancer. However, its role in anal and gastrointestinal malignancies requires further development. In breast cancer, it has been shown to have acceptable sensitivity and specificity.37 In addition it allows transcutaneous visualisation of lymphatic vessesls and intraoperative lymph node detection without the use of radioisotope. Regardless of the method, the aim of SLN biopsy is to detect the presence of lymph node metastases in draining lymph nodes, in order to more accurately stage the dis-ease. This would help identify patients who would benefit from radiotherapy, regardless of its associated side effects and enable patients with no evidence of involved inguinal nodes to be spared the signicant morbidity associated with radiotherapy to the groin. Recent studies have concentrated on the role of positron emis-sion tomography (PET) in anal squamous cell carcinoma, either alone or in combination with computer tomography (CT). Nguyen et al. reported an upstaging in up to onefifth of cases with PET-CT.40 Schwarz and colleagues reported improved survival in patients with complete metabolic response on post-treatment PET imag-ing.41The only study to date to compare PET-CT to SLN biopsy is by Mistrangelo et al.26In this study of 27 patients, SLN biopsy was found to be superior in staging squamous cell carcinoma of the anus compared to PET-CT, mainly because of the high false positive rate with PET-CT. Though PET-CT sensitivity was 100%, the false positive rate resulted in a specificity of 83% and positive predictive value was 43% .The SLN biopsy technique in this study resulted in no false positive results. This is extremely relevant as accurate detection of inguinal lymph node involvement is likely to prevent unnecessary groin irradiation and its associated complications. 5. Limitations

There remain limited studies in the current literature. The total number of patients included in this systematic review was 270 and hence we could not perform any conclusive statistical tests to further analyze the data. In particular we could not perform tests of heterogeneity or bias.

In addition, none of the studies compared SLN biopsy to the gold standard of groin dissection. These data would be required in order to perform a quantitative meta-analysis and to calculate pooled sensitivities and specificities of both methods. Until then, the su-periority of one method over the other cannot be accurately ascertained.

One study compared PET versus SLN biopsy.26It was also un-clear whether a similar cohort of patients had been used in a pre-vious study.23 There was insufficient evidence to suggest this. Therefore, all three studies by Mistrangelo et al. were included.

A Down and Black score was calculated for each study. However one study32was an abstract only and hence could not be scored accurately.

Studies were not randomised as the current literature on this topic still needs further development. However, SLN biopsy appears a feasible method for detection of inguinal nodal metastases, and though complications exist, these are generally self limiting and minor when compared to the complications of unnecessary groin radiotherapy. Certainly further studies are required to assess the false negative rate of SLN biopsy.

6. Conclusion

There remains a need for a more selective approach, to indi-vidualize treatment regimens for patients with anal squamous cell carcinoma. Sentinel lymph node biopsy may prove to be a useful technique to help identify patients who will benefit most from

groin radiotherapy. However, further studies are required before SLN biopsy has a proven role in routine daily practice of staging anal cancer. Serious consideration should now be given to a randomized trial of SLN biopsy versus no prophylactic inguinal radiotherapy, with SLN biopsy-negative patients receiving no radiotherapy and a “watch and wait”policy. Those who are SLN-positive should then still receive groin radiotherapy.

Ethical approval None. Funding

None.

Author contribution

NooranieStudy design, collection of data, write up. RabeyeData collection.

Walshewrite up, statistics and study design. Durraniewrite up.

DavieseStudy concept, manuscript writing up.

Conflicts of interest

None.

Acknowledgements

Justin Davies has received funding from the Bowel Disease Research Foundation and Addenbrooke’s Charitable Trust to investigate novel methods of SLN biopsy in anal cancer.

References

1. Clark MA, Hartley A, Geh JI. Cancer of the anal canal.Lancet Oncol2004;5:149e 57.

2. Ryan DP, Compton CC, Mayer RJ. Carcinoma of the anal canal.N Engl J Med 2000;342:792e800.

3. Deans GT, McAleer JJ, Spence RA. Malignant anal tumours.Br J Surg1994;81(4): 500e8.

4. Nigro ND, Vaitkevicious VK, Considine Jr B. Combined therapy for cancer of the anal canal: a preliminary report.Dis Colon Rectum1974;17:354e6.

5. Myerson RJ, Kong F, Birnbaum EH, et al. Radiation therapy for epidermoid carcinoma of the anal canal, clinical and treatment factors associated with outcome.Radiother Oncol2001;61(1):15e22.

6. Wagner J, Mahe MA, Romestaing P, et al. Radiation therapy in the conservative treatment of carcinoma of the anal canal. Int J Radiat Oncol Biol Phys 1994;29(1):17e23.

7. Gerard JP, Chapet O, Samiei F, et al. Management of inguinal lymph node metastases in patients with carcinoma of the anal canal: experience in a series of 270 patients treated in Lyon and review of the literature.Cancer2001;92(1): 77e84.

8. Wade DS, Herrera L, Castillo NB, Petrelli NJ. Metastases to the lymph nodes in epidermoid carcinoma of the anal canal studied by a clearing technique.Surg Gynecol Obstet1989;169:238e42.

9. Makela PJ, Leminen A, Kaariainen M, Lehtovirta P. Pretreatment of sonographic evaluation of inguinal lymph nodes in patients with vulvar malignancy. J Ultrasound Med1993;12(5):255e8.

10. Bonnema J, Van Geel An, Van Ooijen B, et al. Ultrasound guided aspiration biopsy for detection of non palpable axillary node metastases in breast cancer patients: new diagnostic method.World J Surg1997;21:270e4.

11. Trautmann TH, Zuger JH. Positron emission tomography for pre-treatment staging and post treatment evaluation in cancer of the anal canal.Mol Imag-ing Biol2005;7:309e13.

12. Gould EA, Winship T, Philbin PH, Kerr HH. Observations on a‘sentinel node’in cancer of the parotid.Cancer1960;13:77e8.

13. Cabanas RM. An approach for the treatment of penile carcinoma. Cancer 1977;39:456e66.

14. Bonnema J, Van de Velde CJ. Sentinel lymph node biopsy in breast cancer.Ann Oncol2002;13:1531e7.

15. Van der Pas MH, Meijer S, Hoekstra OS, Riphagen II, de Vet HC, Knol DL. Sentinel-lymph-node procedure in colon and rectal cancer: a systematic re-view and meta-analysis.Lancet Oncol2011;12:540e50.

16. Moher D, Liberati A, Tetzlaff J, Altman DG., PRISMA Group. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.BMJ 2009;339:b2535.

(5)

17. Ulmer C, Bembenek A, Gretschel S, et al. Refined staging by sentinel lymph node biopsy to individualize therapy in anal cancer. Ann Surg Oncol 2004;11(Suppl. 3):259Se62S.

18. Bobin Y, Gerard JP, Chapet O, Romestaing P, Isaac S. Lymphatic mapping and inguinal sentinel lymph node biopsy in anal canal cancers to avoid prophylactic inguinal irradiation.Cancer Radiother2003;7(Suppl. 1):85se90s.

19. Peley G, Farkas E, Sinkovics I, et al. Inguinal sentinel lymph node biopsy for staging anal cancer.Scand J Surg2002;91:336e8.

20. Perera D, Pathma-Nathan N, Rabbitt P, Hewett P, Rieger N. Sentinel node bi-opsy for squamous cell carcinoma of the anus and anal margin.Dis Colon Rectum2003;46:1027e9.

21. Damin DC, Rosito MA, Gus P, et al. Sentinel lymph node procedure in patients with epidermoid carcinoma of the anal canal: early experience.Dis Colon Rectum2003;46:1032e7.

22. Gretschel S, Warnick P, Bembenek A, Dresel S. Lymphatic mapping and sentinel lymph node biopsy in epidermoid carcioma of the anal canal.Eur J Surg Oncol 2008;34:890e4.

23. Mistrangelo M, Bello M, Mobiglia A, Beltramo G. Feasibility of the sentinel node biopsy in anal cancer.Q J Nucl Med Mol Imaging2008;52:1e6.

24. De Nardi P, Carvello M, Canaevari C, Passoni P, Staudacher C. Sentinel node biopsy in squamous cell carcinoma of the anal canal.Ann Surg Oncol2011;18:365e70. 25. De Jong JS, Beukema JC, Gooitzen M, Slart R, Lemstra C, Wiggers T. Limited

value of staging squamous cell carcinoma of the anal margin and canal using the sentinel lymph node procedure: prospective study with long term follow up.Ann Surg Oncol2010;17:3656e62.

26. Mistrangelo M, Pelosi E, Bello M, et al. Comparison of positron emission to-mography scanning and sentinel node biopsy in the detection of inguinal node metastases in patients with anal cancer.Int J Radiat Oncol Biol Phys2010;77(1): 73e8.

27. Hirche C, Dresel S, Krempien R, Hunerbein M. Sentinel node biopsy by indocyanine green retentionfluorescence detection for inguinal lymph node staging of anal cancer: preliminary experience.Ann Surg Oncol2010;17(8): 2357e62.

28. Keshtgar MRS, Amin A, Taylor I, Ell PJ. The sentinel lymph node in anal cancer. Eur J Surg Oncol2001;27(1):113e4.

29.Rabbit P, Pathma-Nathan N, Collinson T, Hewett P, Rieer N. Sentinel lymph node biopsy for squamous cell carcinoma of the anal canal.ANZ J Surg2002;72:651e4. 30.Mistrangelo M, Mobiglia A, Bello M, Beltramo G, Cassoni P, Mussa A. The technique of sentinel lymph nodes in patients with anus neoplasm. Supple-menti di Tumori: Off J Societa Italiana di Cancerologia.2005;4(3):S32e3. 31.Ulmer C, Bembenek A, Gretschel S, Markwardt J, Koswig S, Silsow W. Sentinel

node biopsy in anal cancerea promising strategy to individualize therapy. Onkolgie2003;26(5):456e60.

32.Francois E, Ortholan C, Darcourt J, et al. Long follow-up after inguinal sentinel lymph node (SLN) detection for squamous cell carcinoma (SCC) of the anal canal and anal margin. In:Gastrointestinal cancers symposium2010. 33.Castro LS, Junior JM, Neto JFR, et al. Inguinal sentinel node biopsy in epidermoid

carcinoma of the anal canal: a pilot study.Appl Cancer Res2005;25(2):71e4. 34.Damin DC, Rosito MA, Schwartsmann G. Sentinel lymph node in carcinoma of

the anal canal: a review.Eur J Surg Oncol2006;32:247e52.

35.Murawa D, Hirche C, Dresel S, Hunerbein M. Sentinel lymph node biopsy in breast cancer guided by indocyanine greenfluorescence.Br J Surg2009;96(11): 1289e94.

36.Tajima Y, Yamazaki K, Masuda Y, et al. Sentinel node mapping guided by indocyanine green fluorescence imaging in gastric cancer. Ann Surg 2009;249(1):58e62.

37.Hirche C, Murawa D, Mohr Z, Knelf S, Hunerbein M. ICGfluorescence-guided sentinel node biopsy for axillary nodal staging in breast cancer.Breast Cancer Res Treat2010;121(2):373e8.

38.Gershenwald JE, Tseng CH, Thompson W, et al. Improved sentinel lymph node localization in patients with primary melanoma with the use of radiolabelled colloid.Surgery1998;124:203e10.

39.Villa G, Agnese G, Bianchi P, Costa R, Carli F, Peressini A. Mapping the sentinel lymph node in malignant melanoma by blue dye, lymphoscintigraphy and intra operative gamma probe.Tumori2000;86:343e5.

40.Nguyen BT, Joon DL, Khoo V, et al. Assessing the impact of FDG-PET in the management of anal cancer.Radiother Oncol2008;87:376e82.

41.Schwarz JK, Siegel BA, Dehdashti F, Grigsby PW. Tumor response and survival predicted by post therapy FDG-PET/CT in anal cancer.Int J Radioation Oncol Biol Phys2008;71:180e6.

Figure

Table 2 summarises the Down and Black score for each study, and provides a detailed breakdown of the component of the score.
Table 3 summarises the complication rates for SLN biopsy. Six studies described complications, with the highest rate reported at 59%

References

Related documents

ePages Enterprise is a mature and scalable standard software application which enables you to quickly set up a professional business website or an online shop for the

iPhone, Mobile Phones, Netbooks devices that have more and more web access. All of these activities and devices you need to consider and support. Your target audience defines

Pri vývoji IRB  6700 sa dbalo na skutočnosť, aby nová generácia robotov bola význačná svojou tuhosťou tak, ako je len možné, pre zabezpečenie lepšej ochrany a  ich

FEMA for the failure mechanisms of the Murrah Federal Building. In addition, this report concluded that many of the techniques used to upgrade the seismic resistance

Given that higher real wages are likely to reduce the quantity of regular labour demanded, and that casual farm labour will be included under minimum wage legislation from 2006, the

We hereby report the case of 2 successive pregnancies in a context of severe maternal dependence on tianeptine, which led to subsequent neonatal abstinence syndrome in the

Citation Hird SM, Ganz H, Eisen JA, Boyce WM. The cloacal microbiome of five wild duck species varies by species and influenza A virus infection status. This is an open- access

The spirituality is effective on compatibility person to Chronic diseases، and can be affected by various demographic characteristic، so that the results of different