World J Surg (2014) 38:1077–1083 DOI 10.1007/s00268-013-2382-1
Assessing Patterns of Practice of Sentinel Lymph Node Biopsy for Breast Cancer in Latin America Sergio A. Acuna • Fernando A. Angarita Jaime Escallon
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Published online: 5 December 2013 Ó Socie´te´ Internationale de Chirurgie 2013
Abstract Introduction There is a lack information regarding how sentinel lymph node biopsy (SLNB) for breast cancer is carried out today in developing countries and how it was adapted. To rectify this situation we performed a patternof-practice survey amongst practicing surgeons in Latin America (LA). Methods A survey was developed to assess current surgical practice in breast cancer, use of SLNB, limitations to the implementation, training, technique variations, and observed adverse events. A total of 30 surgical associations and breast surgery societies in 18 Latin American countries were invited to participate. Surveys were distributed among member of these associations and 76.7 % of those
Electronic supplementary material The online version of this article (doi:10.1007/s00268-013-2382-1) contains supplementary material, which is available to authorized users. S. A. Acuna F. A. Angarita J. Escallon Department of Surgery, University of Toronto, Toronto, ON, Canada e-mail:
[email protected] Present Address: S. A. Acuna Institute of Health Policy, Management and Education, University of Toronto, Toronto, ON, Canada Present Address: F. A. Angarita Toronto General Research Institute, University Health Network, Toronto, ON, Canada J. Escallon (&) Department of Surgery, Marvelle Koffler Breast Centre, Mount Sinai Hospital, Room 1266, 600 University Avenue, Toronto, ON M5G 1X5, Canada e-mail:
[email protected]
contacted answered the survey. Responses were limited only to those who reported treating breast cancer patients. Results A total of 463 surgeons who manage breast cancer responded. Over 53 % of surgeons do not have sub-specialty training. Only 47.7 % have a high-volume case load, of which 87.8 % routinely perform SLNB. The main limitations perceived to the implementation of SLNB were a lack of resources/equipment (48 %) and training opportunities (33 %). Over 60 % reported that fewer than half of their patients were eligible for SLNB and 67.8 % reported that they were involved in teaching this technique to residents. Conclusions A significant proportion of surgeons that treat breast cancer cases in LA have not had sub-specialty training or manage a low volume of cases. Among those surgeons with a high-volume caseload, SLNB is routinely performed. SLNB training during residency represents an opportunity for improvement in the region.
Introduction Breast cancer is the most commonly diagnosed cancer in women worldwide [1]. Each year approximately 8 % of the world’s new cases of breast cancer are diagnosed in Latin America (LA) and the Caribbean [2]. Latin American countries tend to have intermediate incidence rates (15 per 100,000 people) [1, 3–5], but countries such as Argentina and Uruguay have rates (69.4 per 100,000 people) resembling those of developed nations (68.3–86.3 per 100,000 people) [6–8]. In light of the growing number of Latin American women affected in the last two decades [9, 10], breast cancer has undeniably become an important concern for public health agencies and governments. In general, the clinical presentation and outcomes for patients in developing regions tend to be unfavorable.
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Unfortunately, this is the result of the type of screening programs and level of accessibility to treatment patients have in these regions [11]. Despite the fact that developing countries spend less on healthcare and public health initiatives than their developed counterparts [12, 13], not every patient with cancer presents at an advanced stage. Because developing regions are highly diverse in terms of population and economy, the spectrum of clinical presentation in some cases is the same as that observed in developed countries [14]. Additionally, in recent years, cancer treatment has been optimized to become more patient- and tumor-specific than ever before [14]. It is therefore necessary for surgeons, regardless of where they practice, to be familiar and competent with basic advances in breast surgical oncology [14]. Sentinel lymph node biopsy (SLNB) for breast cancer is possibly the most rapidly adopted surgical technique in the history of surgical oncology [15]. The transition from axillary lymph node dissection (ALND) to SLNB occurred despite the fact that there was a lack of randomized clinical trials and data regarding morbidity, axillary recurrence, and 5-year survival rates [15]. By 2003, over 50 % of women were spared ALND, this taking place only a year after the first randomized trial of SLNB was published, 5 years after the first multicenter trial publication, and only a decade after it had been first described in breast cancer [15–19]. With a 95 % accuracy rate of detecting metastatic lymph nodes [20, 21], and a significantly low rate of postoperative complications [22–25], SLNB is now the standard-of-care technique that determines prognosis in early breast cancer. It is necessary to determine how standard procedures used in developed countries apply in these other nations and what changes are needed to make them both valid and feasible [26]. Few studies have examined SLNB pattern of practice outside of North America and Western Europe. No detailed information exists in terms of how SLNB is being carried out today, let alone how it was adapted; how extensive is its use and what are the barriers and limitations for a broader application. The aim of this study is assess the patterns of practice of SLNB in LA. We provide self-reported information from LA breast surgeons on current SLNB practices, training, technique, education, as well as reported adverse events.
Methods Target audience After obtaining support and approval from the Latin American Federation of Surgery [Spanish: Federacio´n Latinoamericana de Cirugı´a; Portuguese: Federac¸a˜o Latino Americana de Cirurgia (FELAC)], a total of 18 surgical associations and 12 breast surgery societies in 18 countries
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World J Surg (2014) 38:1077–1083 Table 1 Participating countries and associations Argentina Asociacio´n Argentina Cirugı´a Sociedad de Patologı´a Mamaria de Co´rdoba, Argentina Bolivia Sociedad Boliviana de Cirugı´a Sociedad Boliviana de Mastologı´a Brazil Cole´gio Brasileiro de Cirurgio˜es Sociedade Brasileira de Mastologia Colombia Asociacio´n Colombiana Cirugı´a Asociacio´n Colombiana Mastologı´a Cuba Sociedad Cubana de Cirugı´a Dominican Republic Sociedad Dominicana de Mastologı´a Ecuador Sociedad Ecuatoriana de Cirugı´a Sociedad Ecuatoriana de Patologı´a Mamaria Guatemala Asociacio´n Cirugı´a Guatemala Guatemala Mastologı´a Mexico Asociacio´n Mexicana de Cirugı´a General Asociacio´n Mexicana de Mastologı´a Nicaragua Asociacio´n Cirugı´a Nicaragua Panama Asociacio´n Panamen˜a de Cirugı´a Peru Sociedad Peruana de Mastologı´a Uruguay Sociedad Uruguaya de Mastologı´a Sociedad de Cirugı´a del Uruguay Venezuela Sociedad Venezolana de Cirugı´a Sociedad Venezolana de Mastologı´a
were identified. Society presidents and/or boards from each of these countries were contacted and offered the opportunity to participate. Associations in countries that agreed to participate are summarized in Table 1. After multiple efforts, we were unable to confirm the participation of the remaining Latin American countries. Survey structure An original descriptive self-administered practice-of-pattern survey was developed and provided using a
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commercially available Internet-based survey service (http://www.surveymonkey.com). Questions encompassed SLNB training, surgical technique, education, adverse events, and current surgical practices. A secondary survey was provided only for respondents who were identified to be high-volume breast cancer surgeons (defined as those who had more than four breast cancer surgical cases per month) [27, 28]. In addition to the previous questions, this focus group was also asked more in-depth questions on SLNB use, training, technique, instruction, and adverse events. For the purpose of this publication, the questions have been translated to English and are available in Supplementary Table 1. The survey was either applied in Spanish or Portuguese (exclusively for surgeons in Brazil). Questions were multiple choice or open-ended. The survey was arranged so that respondents could modify their answers to previous questions as they went along, but once their answers were submitted they could not be accessed, edited, or resubmitted.
Survey distribution Before distributing the survey, a pilot study was carried out with five breast surgeons who were included in the final data analysis of this study. After obtaining feedback on the internal congruency and clarity of the questions, the survey was adjusted accordingly. Invitations to the web-based survey were then distributed by one of two means: (i) surgical societies that did not provide the contact information of their members proceeded to internally distribute the survey via their electronic-mail database, or (ii) members whose surgical societies offered their contact information were e-mailed by a general study coordinator. In an attempt to increase participation, the general coordinators periodically sent reminders every 3 months to all non-responding surgeons. Surgical societies were reminded every 3 months to send the e-mail again. No incentives were offered for completing this survey. Survey distribution was started in July 2009 and ended in June 2010. Each invitation was kept open for 12 months and the last invitation was closed in June 2011.
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Results A total of 736 surgeons accessed our survey, 11 of whom did not meet the inclusion criteria and were excluded because they declared to be plastic surgeons or non-surgeons, with a final total of 725. Of these, 610 were directly contacted via their email accounts and 115 were reached through a link distributed by their affiliating association/ society. Among those directly contacted (n = 610), 465 agreed to participate and answered the survey (76.2 %). Of the 115 surgeons reached through the link, 91 agreed to participate and answered the survey (79.1 %). However, the total number of surgeons contacted though the link distributed by the associations and societies and who did not open the survey cannot be estimated. A total of 556 surgeons accepted the invitation and completed our survey. From those, only 463 surgeons reported to be involved in the management of breast cancer patients. These participants responded fully to the general part of the survey, with 221 high-volume surgeons responding to the more in-depth part of the survey (focus group).
Demographic characteristics Respondents were primarily male (84.9 %) and lived in cities with[500,000 inhabitants (73.7 %). Figure 1 depicts the distribution according to nationality. When asked about post-graduate training, 90.1 % said they had trained in general surgery, while 9.9 % had trained in gynecology/obstetrics. The latter was particularly common among the participants from Brazil (43.3 %). A total of 51.8 % had not completed any type of fellowship training. With regards to current type of practice, 64.6 % reported to have an academic position while the rest had a community-based practice. The distribution of self-reported breast cancer surgery case load was as follows: 47.7 % high-volume (more than four cases/month) and 52.3 % low-volume case load (less than four cases/month). This subgroup (n = 221) was selected as the center group for the following questions.
High-volume breast surgeon-focused questions Statistical analysis SLNB implementation SPSS (Statistical Package for the Social Sciences) version 20.0 (Chicago, IL, USA, 2011) was used to perform statistical analysis. Results are described as percentages and continuous variables by means ± standard deviation (SD) as well as medians and ranges.
SLNB was reported to be routinely performed by 87.8 % of this subgroup. Those who did not perform SLNB (n = 27) stated that the major reasons why SLNB could not be performed included lack of resources, equipment, or multi-
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Fig. 2 Cumulative adoption of sentinel lymph node biopsy (SLNB) in Latin America (LA) by year. Cumulative number of Latin American surgeons adopting SLNB per year
Fig. 1 Distribution of participants by country. Countries included in the study were colored in grey (number of respondents per country presented in parentheses): Argentina (2), Bolivia (6), Brazil (83), Colombia (95), Costa Rica (1), Cuba (2), Ecuador (4), Dominican Republic (3), El Salvador (4), Guatemala (13), Honduras (1), Mexico (157), Nicaragua (20), Panama (21), Peru (17), Uruguay (16), and Venezuela (18)
disciplinary services (e.g. nuclear medicine or specialized pathology) (n = 18), lack of training opportunities (n = 9), or the high costs associated with this procedure (n = 1). When those performing SLNB were asked about the main limitations perceived to the extended implementation of SLNB in their country, they consistently reported the lack of resources, namely equipment, (48 %) and training opportunities (33 %) as the main limitations. Training and validation Only 12.9 % of respondents learned SLNB during residency and/or fellowship training. In contrast, the vast majority of surgeons learned the technique through clinical workshops (42.8 %), mentorship (35.6 %), self-learning (30.4 %), and observing fellow colleagues (25.8 %). Of those surgeons who actually validated the technique according to standard guidelines at the time, the average number of cases was 28.3 (SD 19.12). The cumulative
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self-reported year in which survey surgeons performed their first SLNB country is presented in Fig. 2. When asked about when SLNB should be taught in training programs, the majority (61.5 %) considered that it should only be taught during breast and/or surgical oncology fellowships. With respect to the way SLNB training should be offered, the majority responded that the best approach was to undergo training in a specialized center (95.5 %) followed by local workshops (31.5 %). Case load On average, the majority of the surgeons (47.8 %) reported to perform five to ten SLNB cases per month, 43.9 % of the surgeons perform five or fewer cases per month, and only 8.2 % carry out more than ten cases per month. When asked about what percentage of their patient population was eligible for SLNB, surgeons reported the following: \25 (33.5 %), 25–50 (30.9 %), 50–75 (22.2 %), and [75 % (7.2 %). SLNB technique Patent blue is the most commonly used dye (61.3 %), followed by methylene blue (16.1 %) and LymphazurinÒ (isosulfan blue) (8.1 %). Only 14.5 % and 13.7 % use radiotracer or dye, respectively, as the sole imaging technique. Periareolar is the preferred site to inject the dye (83.9 %) and the radiotracer (76.6 %). The radiotracer is more frequently injected a few hours before the surgery (49.1 %) and it is most commonly performed by a nuclear medicine specialist (75.8 %). The majority of surgeons (74.2 %) reported to be aware of the existence of a pathology protocol for processing the sentinel node in their institution. Most of the surgeons used
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intra-operative analysis of the node (70.1 %), done by frozen section (41.9 %), and imprint cytology (28.2 %). Differed standard histopathological analysis was used by 29.8 % of the surgeons. SLNB instruction and training Of the surgeons performing SLNB, 67.7 % were involved in the instruction of the technique: 48.8 % reported that they taught the technique to general surgery or gynecology and obstetrics residents, while 71.4 % were involved in the teaching of the technique to fellows; 45.2 % taught fellows exclusively. On average, they stated that their residents were exposed to 65.5 cases (range 2–300), and were allowed to perform 29.4 supervised cases on average (range 1–100). The majority (60.2 %) considered that residents/fellows should perform more than 20 cases during their training. A significant proportion (71 %) of the surgeons reported that they had a database of the cases they had performed and 20.2 % had published their SLNB case data. SLNB adverse reactions The majority (59.4 %) reported that they had not observed any adverse reaction. Of those surgeons who reported having observed adverse reactions, the majority had seen fewer than five cases since starting to perform SLNB. The most frequently observed reaction was the presence of rash (26.6 %), followed by alterations in the pulse-oximeter reading (14.5 %), and anaphylaxis (14.5 %).
Discussion The scientific knowledge about breast cancer available today is unfortunately only applied to a small portion of the world population [29, 30]. Advances such as breast-conserving surgery and SLNB, which are now considered standard-ofcare practices, face economic and educational barriers to their complete adoption in many developed countries [31]. Despite these challenges, our survey reveals that SLNB use is widespread (87.8 %) among surgeons with a high-volume case load of breast cancer patients in LA. Surgeons in this region welcomed this technique. By 2003, the year that SLNB was officially recognized as standard-of-care, 53.5 % of the surgeons in this survey reported that they were already performing the technique. Consequently, only a low percentage (12.9 %) had been instructed during their surgical residency or fellowship. The majority had learnt SLNB by attending clinical workshops, through self-learning, and by observing colleagues. Findings from our survey indicate that breast cancer patients in LA are not only being treated by sub-specialized
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surgeons; 51.8 % of the surgeons who reported treating these cases had not completed any type of fellowship training. Breast cancer surgeries are part of the scope of cases usually treated by general surgeons, and by 2002 SLNB was already being taught in 92 % of surgical residency programs in the USA [32]. Data from our survey reveal that, although 67.7 % of the surgeons performing SLNB were involved in the instruction of the technique, 45.2 % of these were limiting instruction to fellows. Moreover, 61.5 % considered that SLNB should only be taught during sub-specialty training. This is concerning, given that training during residency is currently considered the means of learning SLNB. Self-reported limitations for the implementation of SLNB in LA included both the high cost of resources and the lack of surgery and pathology training programs. SLNB was originally developed with isosulfan blue as dye, which was scarce and expensive in most regions. Several LA groups adopted methylene blue [33] and patent blue [34] as substitute dyes. Patent blue (61.3 %) and methylene blue (16.1 %) were reported as the most commonly used dyes; isosulfan blue was reported by 8.1 % of surgeons as the dye of choice. Although the most common SLNB technique combines lymphoscintigraphy with a dye to identify the sentinel lymph node (SLN), it has been documented that dye alone is reliable and accurate [35–38]. The availability of nuclear medicine facilities, as well as the added cost and logistical issues associated with the use of radiotracers are limiting factors in LA. This represents an opportunity for surgeons who do not currently use the technique because of the lack of nuclear medicine facilities to adopt the dye alone method. Regarding SLNB training, the majority of surgeons responded that the best approach was to receive formal training in a specialized center (95.5 %). By including SLNB in postgraduate training programs, future generations of surgeons will learn in academic centers, avoiding the need to undergo a learning curve with back-up axillary dissection. In agreement with the established quota of 20–30 cases of SLNB needed to achieve optimal performance of the technique [39, 40], the majority of surgeons (60.2 %) considered that residents/fellows should perform at least this number of cases during their training. In this survey, the average reported number of cases performed by trainees was 29.4. Lack of access to a pathology service adequately trained to process SLNB is reported as a limitation. Furthermore, although the majority (74.2 %) reported knowledge of the existence of a pathology protocol for processing the SLN, one-quarter of surgeons are unaware of their institution’s pathology processing protocol. A structured pathology protocol is considered to be a quality indicator of SLNB [41];
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thus, specific quality assurance programs should be established to ensure that the incidence of missed metastasis on pathology examinations is minimized. The existence of an interdisciplinary team approach, including pathology and nuclear medicine specialists, is required for an adequate implementation of SLNB [42]. Moreover, with the recent change in practice brought about by the American College of Surgeons Oncology Group Trial Z0011 [43], frozen sections are no longer needed; therefore pathology can be centralized and referred to specialized centers. The use of SLNB should be universal to all surgeons treating breast cancer cases, independent of case load and subspecialized training. Improvements to healthcare systems in LA increase the number of patients diagnosed in early stages and therefore the need for SLNB. At the same time, this increases the access to resources and decreases the burden of cost of implementing this technique. Incorporation of SLNB training during residency and educational opportunities is needed to contribute to a more widespread use of the technique in LA. Acknowledgments This project was financed by The Marvelle Koffler Breast Centre, Mount Sinai Hospital, Toronto, Canada. Conflict of interest
The authors declare no conflicts of interest.
References 1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D (2011) Global cancer statistics. CA Cancer J Clin 61:69–90 2. Ferlay J, Shin H, Bray F, Forman D, Mathers C, Parkin D, editors (2012) Globocan 2008: cancer incidence and mortality worldwide. IARC CancerBase No. 10 3. Parkin DM, Fernandez LM (2006) Use of statistics to assess the global burden of breast cancer. Breast J 12(Suppl 1):S70–S80 4. Parkin DM, Bray F, Ferlay J, Pisani P (2005) Global cancer statistics, 2002. CA Cancer J Clin 55:74–108 5. Bosetti C, Malvezzi M, Chatenoud L, Negri E, Levi F, La Vecchia C (2005) Trends in cancer mortality in the Americas, 1970–2000. Ann Oncol 16:489–511 6. Key TJ, Verkasalo PK, Banks E (2001) Epidemiology of breast cancer. Lancet Oncol 2:133–140 7. Schwartsmann G (2001) Breast cancer in South America: challenges to improve early detection and medical management of a public health problem. J Clin Oncol 19:118S–124S 8. Lozano-Ascencio R, Gomez-Dantes H, Lewis S, Torres-Sanchez L, Lopez-Carrillo L (2009) Breast cancer trends in Latin America and the Caribbean. Salud Publica Mex 51(Suppl 2):s147–s156 9. Reyes-Ortiz CA, Freeman JL, Pelaez M, Markides KS, Goodwin JS (2006) Mammography use among older women of seven Latin American and Caribbean cities. Prev Med 42:375–380 10. Forouzanfar MH, Foreman KJ, Delossantos AM et al (2011) Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. Lancet 378:1461–1484 11. Pisani P, Bray F, Parkin DM (2002) Estimates of the world-wide prevalence of cancer for 25 sites in the adult population. Int J Cancer 97:72–81 12. Baquet CR, Commiskey P (2000) Socioeconomic factors and breast carcinoma in multicultural women. Cancer 88:1256–1264
123
13. Robles SC, Galanis E (2002) Breast cancer in Latin America and the Caribbean. Rev Panam Salud Publica 11:178–185 14. Buccimazza I (2011) Implementing sentinel lymph node biopsy programs in developing countries: challenges and opportunities. World J Surg 35:1155–1158. doi:10.1007/s00268-011-0956-3 15. Rescigno J, Zampell JC, Axelrod D (2009) Patterns of axillary surgical care for breast cancer in the era of sentinel lymph node biopsy. Ann Surg Oncol 16:687–696 16. Giuliano AE, Kirgan DM, Guenther JM, Morton DL (1994) Lymphatic mapping and sentinel lymphadenectomy for breast cancer. Ann Surg 220:391–398 (discussion 398–401) 17. Veronesi U, Paganelli G, Viale G et al (2003) A randomized comparison of sentinel-node biopsy with routine axillary dissection in breast cancer. N Engl J Med 349:546–553 18. Krag DN, Weaver DL, Alex JC, Fairbank JT (1993) Surgical resection and radiolocalization of the sentinel lymph node in breast cancer using a gamma probe. Surg Oncol 2:335–339 (discussion 340) 19. Krag D, Weaver D, Ashikaga T et al (1998) The sentinel node in breast cancer—a multicenter validation study. N Engl J Med 339:941–946 20. Lyman GH, Giuliano AE, Somerfield MR et al (2005) American Society of Clinical Oncology guideline recommendations for sentinel lymph node biopsy in early-stage breast cancer. J Clin Oncol 23:7703–7720 21. Giuliano AE, Jones RC, Brennan M, Statman R (1997) Sentinel lymphadenectomy in breast cancer. J Clin Oncol 15:2345–2350 22. Bafford A, Gadd M, Gu X, Lipsitz S, Golshan M (2010) Diminishing morbidity with the increased use of sentinel node biopsy in breast carcinoma. Am J Surg 200:374–377 23. Wilke LG, McCall LM, Posther KE et al (2006) Surgical complications associated with sentinel lymph node biopsy: results from a prospective international cooperative group trial. Ann Surg Oncol 13:491–500 24. Mansel RE, Fallowfield L, Kissin M et al (2006) Randomized multicenter trial of sentinel node biopsy versus standard axillary treatment in operable breast cancer: the ALMANAC trial. J Natl Cancer Inst 98:599–609 25. McLaughlin SA, Wright MJ, Morris KT et al (2008) Prevalence of lymphedema in women with breast cancer 5 years after sentinel lymph node biopsy or axillary dissection: objective measurements. J Clin Oncol 26:5213–5219 26. No authors listed (2009) Breast cancer in developing countries. Lancet 374:1567 27. McDermott AM, Wall DM, Waters PS et al (2013) Surgeon and breast unit volume–outcome relationships in breast cancer surgery and treatment. Ann Surg 258(5):808–813 28. Quan ML, Hodgson N, Lovrics P, Porter G, Poirier B, Wright FC (2008) National adoption of sentinel node biopsy for breast cancer: lessons learned from the Canadian experience. Breast J 14:421–427 29. Carlson RW, Anderson BO, Chopra R et al (2003) Treatment of breast cancer in countries with limited resources. Breast J 9(Suppl 2):S67–S74 30. Olopade OI, Schwartsmann G, Saijo N, Thomas CR Jr (2006) Disparities in cancer care: a worldwide perspective and roadmap for change. J Clin Oncol 24:2135–2136 31. Vanderveen KA, Paterniti DA, Kravitz RL, Bold RJ (2007) Diffusion of surgical techniques in early stage breast cancer: variables related to adoption and implementation of sentinel lymph node biopsy. Ann Surg Oncol 14:1662–1669 32. Davis KG, Schriver JP (2002) Prevalence of teaching sentinel lymph node biopsy for breast cancer in general surgery residency programs. Curr Surg 59:420–422 33. Angarita FA, Acuna SA, Cervera S, Torregrosa L, Tawil M (2012) Meeting surgical necessities for sentinel lymph node
World J Surg (2014) 38:1077–1083
34.
35.
36.
37.
38.
biopsy in breast cancer: experience with methylene blue in a Colombian hospital. Breast J 18(6):618–619 Gallegos-Hernandez JF, Chavez-Garcia MA, Najera I, RamirezRamirez L, Duran-Martinez M (2003) Lymphatic mapping and sentinel lymph node biopsy in patients with breast cancer. Gac Med Mex 139:205–208 Chintamani Tandon M, Mishra A, Agarwal U, Saxena S (2011) Sentinel lymph node biopsy using dye alone method is reliable and accurate even after neo-adjuvant chemotherapy in locally advanced breast cancer–a prospective study. World J Surg Oncol 9:19 Golshan M, Nakhlis F (2006) Can methylene blue only be used in sentinel lymph node biopsy for breast cancer? Breast J 12:428–430 Varghese P, Mostafa A, Abdel-Rahman AT et al (2007) Methylene blue dye versus combined dye-radioactive tracer technique for sentinel lymph node localisation in early breast cancer. Eur J Surg Oncol 33:147–152 Krikanova M, Biggar M, Moss D, Poole G (2010) Accuracy of sentinel node biopsy for breast cancer using blue dye alone. Breast J 16:384–388
1083 39. Clarke D, Newcombe RG, Mansel RE, ALMANAC Trialists Group (2004) The learning curve in sentinel node biopsy: the ALMANAC experience. Ann Surg Oncol 11:211S–215S 40. Sanidas EE, de Bree E, Tsiftsis DD (2003) How many cases are enough for accreditation in sentinel lymph node biopsy in breast cancer? Am J Surg 185:202–210 41. Quan ML, Wells BJ, McCready D, Wright FC, Fraser N, Gagliardi AR (2010) Beyond the false negative rate: development of quality indicators for sentinel lymph node biopsy in breast cancer. Ann Surg Oncol 17:579–591 42. Acuna SA, Angarita FA, McCready DR, Escallon J (2013) Quality indicators for sentinel lymph node biopsy: Is there room for improvement? Can J Surg 56:82–88 43. Giuliano AE, Hunt KK, Ballman KV et al (2011) Axillary dissection vs no axillary dissection in women with invasive breast cancer and sentinel node metastasis: a randomized clinical trial. JAMA 305:569–575
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