Research Article
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Laparoscopic colorectal surgery for cancer in a regional service hospital: single surgeon experience

Year 2025, Volume: 58 Issue: 1, 16 - 19, 04.05.2025

Serdar Şenol , Mustafa Kuşak

https://doi.org/10.20492/aeahtd.1495422

Abstract

Aim: In spite of the demonstrated advantages, laparoscopic colorectal surgery is not adequately utilised in regional service hospitals. Purpose of the research was to document the findings of patients managed by a gastroenterological surgeon for colorectal neoplasms using laparoscopic surgery at a service hospital of the Central Black Sea Region, Turkey.
Material and Method: Every sequential patient having laparoscopic colorectal surgery was registered prospectively and analysed retrospectively. Recorded parameters consisted of demographic characteristics, diagnostic work-up, surgical events, post-surgical morbidity, mortality and outcomes.
Results: Seventy-five patients each underwent laparoscopic colorectal surgery for colorectal neoplasm within a period of forty months. Average age was 66.4 years and ratio of males to females was 11:4. Rectal cancer rate was 65.3%. Colon cancer rate was 34.6%. One patient had synchronous colorectal cancer. Mean time of surgery was 276 min and mean volume of haemorrhage was 75 ml. Conversion to open resection rate was 6.6%. Median day of hospitalization was six days. Postoperative complication rate (Clavien–Dindo grade ≥ III) was 8.5%. Two systemic recurrences were observed during the surveillance.
Conclusion: Based on our results and those of other studies presented here, a trained surgeon with a high caseload can perform safe and adequate oncological laparoscopic colorectal resections in a regional service hospital of a developing country. The longer operative time is the drawback of the procedure, especially in crowded service hospitals. The results are also valuable in terms of showing the effect of health policies and regional conditions on surgical practices in our city and country. Under the current conditions, surgeons’ dedication and all relevant supports are required.

Keywords

Colorectal cancer Hospital Minimally invasive surgery Surgeon Volume

References

  • 1. Wexner SD, Cohen SM. Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg. 1995; 82(3): 295–298. doi: 10.1002/bjs.1800820305. PMID: 7795990.
  • 2. Clinical Outcomes of Surgical Therapy Study Group; Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Stryker SJ, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004; 350(20): 2050–2059. doi: 10.1056/ NEJMoa032651. PMID: 15141043.
  • 3. Braga M, Vignali A, Gianotti L, Zuliani W, Radaelli G, Gianotti L, C, et al. Metabolic and functional results following laparoscopic colorectal surgery: a randomized study on short-term outcome. Ann Surg. 2002;45(8):1070–1777. doi: 10.1007/s10350-004-6362-2. PMID: 12195192.
  • 4. Guillou PJ, Quirke P, Thorpe H, Thorpe H, Walker J, Jayne DG, Smith AM, et al. CLASICC Trial Group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomized controlled trial. Lancet. 2005; 365(9472): 1718–1726. doi: 10.1016/ S0140-6736(05)66545-2. PMID: 15894098.
  • 5. Kawinski A, Dziki L, Trzcinski R, Dziki A, Mik M. Is there still a place for open surgery in the treatment strategy of rectal cancer? Przeglad Gastroenterol. 2018;13(4):289-292. doi: 10.5114/ pg.2018.79807. PMID: 30581502.
  • 6. Hamidi M, Hanna K, Omesiete P, Cruz A, Ewongwo A, Pandit V, et al. Does it matter where you get your surgery for colorectal cancer? Int J Colorectal Dis. 2019;34(12):2121-2127. doi: 10.1007/ s00384-019-03436-6. PMID: 31720828.
  • 7. Altieri MS, Yang J, Groves D, Yin D, Cagino K, Talamini M, et al. Effect of academic status on outcomes of surgery for rectal cancer. Surg Endosc. 2018; 32(5): 2774-2780. doi: 10.1007/s00464- 017-5931-0. PMID: 29101562.
  • 8. Archampong D, Borowski D, Wille-Jorgensen P, Iversen LH. Workload and surgeon’s specialty for outcome after colorectal cancer surgery. Cochrane Database Syst Rev. 2012;14:CD005391. doi: 10.1002/14651858. PMID: 22419309.
  • 9. Agachan F, Joo JS, Sher M, Weiss EG, Nogueras JJ, Wexner SD. Laparoscopic colorectal surgery. Do we get faster? Surg Endosc. 1997;11(4):331–335. doi: 10.1007/s004649900357. PMID: 9094271.
  • 10. Bennett CL, Stryker SJ, Ferreira MR, Adams J, Beart RW Jr. The learning curve for laparoscopic colorectal surgery. Preliminary results from a prospective analysis of 1194 laparoscopic- assisted colectomies. Arch Surg. 1997;132(1):41–44. doi: 10.1001/archsurg. 1997.01430250043009. PMID: 9006551
  • 11. Simons AJ, Anthone GJ, Ortega AE, Franklin M, Fleshman J, Geis WP, et al. Laparoscopic assisted colectomy learning curve. Dis Colon Rectum. 1995;38(6): 600–603. doi: 10.1007/BF02054118. PMID: 7774470
  • 12. Morche J, Mathes T, Pieper D. Relationship between surgeon volume and outcomes: a systematic review of systematic reviews. Syst Rev 2016;5(1): 204. doi: 10.1186/s13643-016-0376-4.
  • 13. Akenroye OO, Adebona OT, Akenroye AT. Surgical care in the developing world-strategies and framework for improvement. J Publ Health Afr. 2013;4(2):e20. doi: 10.4081/jphia.2013.e20. PMID: 28299109.
  • 14. Favoriti P, Carbone G, Greco M, Pirozzi F, Pirozzi RE, Corcione F, et al. Worldwide burden of colorectal cancer: a review. Updates Surg. 2016;68(1):7-11. doi: 10.1007/s13304-016-0359-y. PMID: 27067591
  • 15. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205-213. doi: 10.1097/01.sla.0000133083.54934.ae. PMID: 15273542.
  • 16. Weiser MR. Colorectal Cancer. Ann Surg Oncol. (AJCC 8th Edition) 2018; 25(6): 454–1455. doi: 10.1245/s10434-018-6462-1. PMID: 29616422
  • 17. Drolet S, MacLean AR, Myers RP, Shaheen AA, Dixon E, Buie WD. Elective resection of colon cancer by high-volume surgeons is associated with decreased morbidity and mortality. J Gastrointest Surg. 2011;15(4): 541–550. doi: 10.1007/s11605-011-1433-x. PMID: 21279550.
  • 18. Borowski DW, Bradburn DM, Mills SJ, Bharathan B, Wilson RG, Ratcliffe AA, et al.; Northern Region. Volume-outcome analysis of colorectal cancer-related out-comes. Br J Surg. 2010;97(9): 1416– 1430. doi: 10.1002/bjs.7111. PMID: 20632311.
  • 19. Tang BQ, Campbell JL. Laparoscopic colon surgery in community practice. Am J Surg. 2007;193(5):575–578. doi: 10.1016/j. amjsurg.2007.01.018. PMID: 17434358.
  • 20. Bader NA, Sweeney M, Zeymo A, Villano AM, Houlihan B, Bayasi M, et al. Defining a minimum hospital volume threshold for minimally invasive colon cancer resections. Surgery 2022;171(2): 293-298. doi: 10.1016/j.surg.2021.06.031. PMID: 34429201.
  • 21. Bickler SN, Weiser TG, Kassebaum N, Higashi H, Chang DC, Barendregt JJ, et al. Global burden of surgical conditions. In: Debas HT, Donkor P, Gawande A, Jamison DT, Kruk ME, Mock CN, eds. Essential Surgery: Disease Control Priorities. 3rd ed. 1. Washington (DC: The International Bank for Reconstruction and Development/ The World Bank; 2015. Apr 2. Chapter 2.
  • 22. Tsai K-Y, Kiu K-T, Huang M-T, Wu C-H, Chang T-C. The learning curve for laparoscopic colectomy in colorectal cancer at a new regional hospital. Asian J Surg. 2016;39(1):34-40. doi: 10.1016/j.asjsur. 2015.03.008. PMID: 25959025.
  • 23. Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, et al.; Colon Cancer Laparoscopic or Open Resection Study Group (COLOR). Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6(7):477-484. doi: 10.1016/S1470-2045(05)70221-7.PMID: 15992696.
  • 24. Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, et al.; Colon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery for colon cancer: long term outcome of a randomised clinical trial. Lancet Oncol. 2009;10(1): 44-52. doi: 10.1016/S1470-2045(08)70310- 3. PMID: 19071061.
  • 25. Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Beart RW, et al; Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350(20): 2050-2059. doi: 10.1056/NEJMoa032651. PMID: 15141043.
  • 26. D’Annibale A, Morpurgo E, Fiscon V, Termini B, Serventi A, Sovernigo G, et al. Minimally invasive resection for colorectal cancer: perioperative and medium-term results in an unselected patient group at a single institution. Tech Coloproctol. 2006;10(4):303–307. doi: 10.1007/s10151-006-0297-7. PMID: 17115319
  • 27. Hewett PJ, Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Rieger NA, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg. 2008;248(5):728-738. doi: 10.1097/SLA.0b013e31818b7595. PMID: 18948799.
  • 28. Biondi A, Grosso G, Mistretta A, Marventano S, Toscano C, Gruttadauria S, et al. Laparoscopic-Assisted Versus Open Surgery for Colorectal Cancer: Short- and Long-Term Outcomes Comparison. J Laparoendosc Adv Surg Tech A. 2013;23(1):1-7. doi: 10.1089/ lap.2012.0276. PMID: 23004676.
  • 29. Yamamoto S, Inomata M, Katayama H, Mizusawa J, Etoh T, Konishi F, et al.; Japan Clinical Oncology Group Colorectal Cancer Study Group. Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg. 2014;260(1):23-30. doi: 10.1097/ SLA.0000000000000499. PMID: 24509190.
  • 30. Huscher CG, Bretagnol F, Corcione F. Laparoscopic Colorectal Cancer Resection in High-Volume Surgical Centers: Long- Term Outcomes from the LAPCOLON Group Trial. World J Surg. 2015;39(8):2045-2051. doi: 10.1007/s00268-015-3050-4. PMID: 25820910.

Bir bölge hizmet hastanesinde laparoskopik kolorektal kanser cerrahisi: Tek cerrah deneyimi

Year 2025, Volume: 58 Issue: 1, 16 - 19, 04.05.2025

Serdar Şenol , Mustafa Kuşak

https://doi.org/10.20492/aeahtd.1495422

Abstract

AMAÇ: Kanıtlanmış avantajlarına rağmen bölge hizmet hastanelerinde laparoskopik kolorektal cerrahi yeterince kullanılmamaktadır. Türkiye'nin Orta Karadeniz Bölgesi'ndeki bir hizmet hastanesinde bir gastroenteroloji cerrahı tarafından laparoskopik cerrahi ile tedavi edilen kolorektal kanserli hastaların sonuçlarının değerlendirilmesi amaçlanmıştır.
GEREÇ ve YÖNTEM: Laparoskopik kolorektal cerrahi uygulanan ardışık her hastanın verileri prospektif olarak kaydedildi ve retrospektif olarak analiz edildi. Kaydedilen parametreler demografik özellikler, teşhis çalışmaları, cerrahi olaylar, ameliyat sonrası morbidite, mortalite ve sonuçları içeriyordu.
BULGULAR: Kırk aylık bir süre içinde 75 hastaya kolorektal kanser nedeniyle laparoskopik cerrahi uygulandı. Ortalama yaş 66,4 olup erkeklerin kadınlara oranı 11:4'tür. Rektum kanseri oranı %65,3, kolon kanseri oranı yüzde 34,6 idi. Bir hastada senkron kolorektal kanser tespit edildi. Ortalama ameliyat süresi 276 dakika ve ortalama kanama hacmi 75 ml idi. Açık rezeksiyona geçiş oranı %6,6 idi. Ortalama hastanede kalış günü altı gündü. Ameliyat sonrası komplikasyon oranı (Clavien-Dindo derecesi ≥ III) %8,5 idi. Takip sırasında iki sistemik nüks gözlendi.
SONUÇ: Sonuçlarımız ve araştırmada sunulan diğer çalışmalar doğrultusunda, yüksek vaka sayısına sahip eğitimli bir cerrah, gelişmekte olan bir ülkenin bölge hizmet hastanesinde güvenli ve yeterli onkolojik laparoskopik kolorektal prosedürü gerçekleştirebilir. Sağlık politikalarının ve bölgesel koşulların ilimizdeki ve ülkemizdeki cerrahi uygulamalar üzerine olan etkisini göstermesi açısından da sonuçlarımız değerlidir. Özellikle kalabalık hizmet hastanelerinde uzun amaliyat süresi uygulamanın dezavantajıdır. Mevcut şartlarda cerrahların özverisi ve ilgili her türlü destek gereklidir.

Keywords

Cerrah Hastane Kapasite Kolorektal kanser Minimal invazif cerrahi

References

  • 1. Wexner SD, Cohen SM. Port site metastases after laparoscopic colorectal surgery for cure of malignancy. Br J Surg. 1995; 82(3): 295–298. doi: 10.1002/bjs.1800820305. PMID: 7795990.
  • 2. Clinical Outcomes of Surgical Therapy Study Group; Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Stryker SJ, et al. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004; 350(20): 2050–2059. doi: 10.1056/ NEJMoa032651. PMID: 15141043.
  • 3. Braga M, Vignali A, Gianotti L, Zuliani W, Radaelli G, Gianotti L, C, et al. Metabolic and functional results following laparoscopic colorectal surgery: a randomized study on short-term outcome. Ann Surg. 2002;45(8):1070–1777. doi: 10.1007/s10350-004-6362-2. PMID: 12195192.
  • 4. Guillou PJ, Quirke P, Thorpe H, Thorpe H, Walker J, Jayne DG, Smith AM, et al. CLASICC Trial Group. Short-term endpoints of conventional versus laparoscopic-assisted surgery in patients with colorectal cancer (MRC CLASICC trial): multicentre, randomized controlled trial. Lancet. 2005; 365(9472): 1718–1726. doi: 10.1016/ S0140-6736(05)66545-2. PMID: 15894098.
  • 5. Kawinski A, Dziki L, Trzcinski R, Dziki A, Mik M. Is there still a place for open surgery in the treatment strategy of rectal cancer? Przeglad Gastroenterol. 2018;13(4):289-292. doi: 10.5114/ pg.2018.79807. PMID: 30581502.
  • 6. Hamidi M, Hanna K, Omesiete P, Cruz A, Ewongwo A, Pandit V, et al. Does it matter where you get your surgery for colorectal cancer? Int J Colorectal Dis. 2019;34(12):2121-2127. doi: 10.1007/ s00384-019-03436-6. PMID: 31720828.
  • 7. Altieri MS, Yang J, Groves D, Yin D, Cagino K, Talamini M, et al. Effect of academic status on outcomes of surgery for rectal cancer. Surg Endosc. 2018; 32(5): 2774-2780. doi: 10.1007/s00464- 017-5931-0. PMID: 29101562.
  • 8. Archampong D, Borowski D, Wille-Jorgensen P, Iversen LH. Workload and surgeon’s specialty for outcome after colorectal cancer surgery. Cochrane Database Syst Rev. 2012;14:CD005391. doi: 10.1002/14651858. PMID: 22419309.
  • 9. Agachan F, Joo JS, Sher M, Weiss EG, Nogueras JJ, Wexner SD. Laparoscopic colorectal surgery. Do we get faster? Surg Endosc. 1997;11(4):331–335. doi: 10.1007/s004649900357. PMID: 9094271.
  • 10. Bennett CL, Stryker SJ, Ferreira MR, Adams J, Beart RW Jr. The learning curve for laparoscopic colorectal surgery. Preliminary results from a prospective analysis of 1194 laparoscopic- assisted colectomies. Arch Surg. 1997;132(1):41–44. doi: 10.1001/archsurg. 1997.01430250043009. PMID: 9006551
  • 11. Simons AJ, Anthone GJ, Ortega AE, Franklin M, Fleshman J, Geis WP, et al. Laparoscopic assisted colectomy learning curve. Dis Colon Rectum. 1995;38(6): 600–603. doi: 10.1007/BF02054118. PMID: 7774470
  • 12. Morche J, Mathes T, Pieper D. Relationship between surgeon volume and outcomes: a systematic review of systematic reviews. Syst Rev 2016;5(1): 204. doi: 10.1186/s13643-016-0376-4.
  • 13. Akenroye OO, Adebona OT, Akenroye AT. Surgical care in the developing world-strategies and framework for improvement. J Publ Health Afr. 2013;4(2):e20. doi: 10.4081/jphia.2013.e20. PMID: 28299109.
  • 14. Favoriti P, Carbone G, Greco M, Pirozzi F, Pirozzi RE, Corcione F, et al. Worldwide burden of colorectal cancer: a review. Updates Surg. 2016;68(1):7-11. doi: 10.1007/s13304-016-0359-y. PMID: 27067591
  • 15. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6336 patients and results of a survey. Ann Surg. 2004;240(2):205-213. doi: 10.1097/01.sla.0000133083.54934.ae. PMID: 15273542.
  • 16. Weiser MR. Colorectal Cancer. Ann Surg Oncol. (AJCC 8th Edition) 2018; 25(6): 454–1455. doi: 10.1245/s10434-018-6462-1. PMID: 29616422
  • 17. Drolet S, MacLean AR, Myers RP, Shaheen AA, Dixon E, Buie WD. Elective resection of colon cancer by high-volume surgeons is associated with decreased morbidity and mortality. J Gastrointest Surg. 2011;15(4): 541–550. doi: 10.1007/s11605-011-1433-x. PMID: 21279550.
  • 18. Borowski DW, Bradburn DM, Mills SJ, Bharathan B, Wilson RG, Ratcliffe AA, et al.; Northern Region. Volume-outcome analysis of colorectal cancer-related out-comes. Br J Surg. 2010;97(9): 1416– 1430. doi: 10.1002/bjs.7111. PMID: 20632311.
  • 19. Tang BQ, Campbell JL. Laparoscopic colon surgery in community practice. Am J Surg. 2007;193(5):575–578. doi: 10.1016/j. amjsurg.2007.01.018. PMID: 17434358.
  • 20. Bader NA, Sweeney M, Zeymo A, Villano AM, Houlihan B, Bayasi M, et al. Defining a minimum hospital volume threshold for minimally invasive colon cancer resections. Surgery 2022;171(2): 293-298. doi: 10.1016/j.surg.2021.06.031. PMID: 34429201.
  • 21. Bickler SN, Weiser TG, Kassebaum N, Higashi H, Chang DC, Barendregt JJ, et al. Global burden of surgical conditions. In: Debas HT, Donkor P, Gawande A, Jamison DT, Kruk ME, Mock CN, eds. Essential Surgery: Disease Control Priorities. 3rd ed. 1. Washington (DC: The International Bank for Reconstruction and Development/ The World Bank; 2015. Apr 2. Chapter 2.
  • 22. Tsai K-Y, Kiu K-T, Huang M-T, Wu C-H, Chang T-C. The learning curve for laparoscopic colectomy in colorectal cancer at a new regional hospital. Asian J Surg. 2016;39(1):34-40. doi: 10.1016/j.asjsur. 2015.03.008. PMID: 25959025.
  • 23. Veldkamp R, Kuhry E, Hop WC, Jeekel J, Kazemier G, Bonjer HJ, et al.; Colon Cancer Laparoscopic or Open Resection Study Group (COLOR). Laparoscopic surgery versus open surgery for colon cancer: short-term outcomes of a randomised trial. Lancet Oncol. 2005;6(7):477-484. doi: 10.1016/S1470-2045(05)70221-7.PMID: 15992696.
  • 24. Buunen M, Veldkamp R, Hop WC, Kuhry E, Jeekel J, Haglind E, et al.; Colon Cancer Laparoscopic or Open Resection Study Group. Survival after laparoscopic surgery versus open surgery for colon cancer: long term outcome of a randomised clinical trial. Lancet Oncol. 2009;10(1): 44-52. doi: 10.1016/S1470-2045(08)70310- 3. PMID: 19071061.
  • 25. Nelson H, Sargent DJ, Wieand HS, Fleshman J, Anvari M, Beart RW, et al; Clinical Outcomes of Surgical Therapy Study Group. A comparison of laparoscopically assisted and open colectomy for colon cancer. N Engl J Med. 2004;350(20): 2050-2059. doi: 10.1056/NEJMoa032651. PMID: 15141043.
  • 26. D’Annibale A, Morpurgo E, Fiscon V, Termini B, Serventi A, Sovernigo G, et al. Minimally invasive resection for colorectal cancer: perioperative and medium-term results in an unselected patient group at a single institution. Tech Coloproctol. 2006;10(4):303–307. doi: 10.1007/s10151-006-0297-7. PMID: 17115319
  • 27. Hewett PJ, Allardyce RA, Bagshaw PF, Frampton CM, Frizelle FA, Rieger NA, et al. Short-term outcomes of the Australasian randomized clinical study comparing laparoscopic and conventional open surgical treatments for colon cancer: the ALCCaS trial. Ann Surg. 2008;248(5):728-738. doi: 10.1097/SLA.0b013e31818b7595. PMID: 18948799.
  • 28. Biondi A, Grosso G, Mistretta A, Marventano S, Toscano C, Gruttadauria S, et al. Laparoscopic-Assisted Versus Open Surgery for Colorectal Cancer: Short- and Long-Term Outcomes Comparison. J Laparoendosc Adv Surg Tech A. 2013;23(1):1-7. doi: 10.1089/ lap.2012.0276. PMID: 23004676.
  • 29. Yamamoto S, Inomata M, Katayama H, Mizusawa J, Etoh T, Konishi F, et al.; Japan Clinical Oncology Group Colorectal Cancer Study Group. Short-term surgical outcomes from a randomized controlled trial to evaluate laparoscopic and open D3 dissection for stage II/III colon cancer: Japan Clinical Oncology Group Study JCOG 0404. Ann Surg. 2014;260(1):23-30. doi: 10.1097/ SLA.0000000000000499. PMID: 24509190.
  • 30. Huscher CG, Bretagnol F, Corcione F. Laparoscopic Colorectal Cancer Resection in High-Volume Surgical Centers: Long- Term Outcomes from the LAPCOLON Group Trial. World J Surg. 2015;39(8):2045-2051. doi: 10.1007/s00268-015-3050-4. PMID: 25820910.
There are 30 citations in total.

Details

Primary Language English
Subjects Gastroenterology Surgery
Journal Section Original research article
Authors

Serdar Şenol 0000-0002-6084-2491

Mustafa Kuşak 0000-0002-5426-2351

Publication Date May 4, 2025
Submission Date June 4, 2024
Acceptance Date April 20, 2025
Published in Issue Year 2025 Volume: 58 Issue: 1

Cite

AMA Şenol S, Kuşak M. Laparoscopic colorectal surgery for cancer in a regional service hospital: single surgeon experience. Ankara Eğitim ve Araştırma Hastanesi Tıp Dergisi. May 2025;58(1):16-19. doi:10.20492/aeahtd.1495422
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