. 2023 Jan 27;15:51–89. doi: 10.2147/BCTT.S390296

Table 3.

Surgery Strategies Across Countries

Surgery Strategies
Low- and Middle-Income Countries
Studied Country	Type of Study	Study Period	Number of Subjects (Mean/ Average/Median Age)	Key measurements	Key Findings	Comments/Suggestions
Li et al, China³³	The retrospective multicentre cohort study	1 Apr 2020–15 May 2020	8397 (50 years)	Breast cancer surgeries during COVID-19	The proportion of surgery dropped from 16.4% to 2.6% in Hubei. Despite that, significantly**** more surgery was detected in Hubei compared to other provinces.	Surgeries of early breast cancer were significantly altered due to COVID-19, especially in Hubei.
Sadri et al, Iran⁸⁸	Observational study	7 Mar 2019–18 Apr 2020	35 (48 years)	Application of Tc-99m elute during Mo99-Tc-99m generator shortage	SLNB can be done with excellent results using Tc-99m pertechnetate elute during Mo99-Tc-99m generator shortage.	Using special personal protection, nuclear medicine Departments can perform lymphatic mapping and biopsy.
Sattar et al, Pakistan⁶⁹	Method report	18 Mar 2020–12 May 2020	30 (NR)	Prioritizing surgical patients and proposed workflow	Surgical patients were prioritized into 3 groups. The proposed workflow divided surgical procedures into elective, semi-elective, orange emergency, and red emergency groups.	The institutional workflow can act as a guideline for triaging surgical patients.
Vohra et al, Pakistan⁸⁹	The retrospective comparative cohort study	1 Mar 2019–31 Mar 2021	380 (51 years)	Impact of COVID-19 pandemic on breast cancer surgery	35.5% reduction in breast cancer surgeries during the pandemic compared to the pre-pandemic period.	The decline in breast cancer surgeries is probably caused due to the fear of nosocomial SARS-CoV-2 infection, which lead to decreased breast cancer screening and diagnosis.
Vohra et al, Pakistan⁹⁰	Retrospective observational study	15 Mar 2020–31 Dec 2020	206 (NR)	Surgical prioritization during COVID-19	Surgical procedures were prioritized into 3 groups: urgent, can be delayed for 4–8 weeks, and can be suspended until the pandemic ends. The mean hospital stay was 24 hours. No post-operative complication was recorded.	Implementation of surgical guidelines and multidisciplinary management made successful surgical completions.
Ramdas et al, South Africa⁸³	Retrospective study	Nov 2017–May 2020	107 (60.8 years)	Viability and acceptance of TARGIT–IORT	TARGIT–IORT had low complication and recurrence rates which confirms its viability.	TARGIT–IORT can gain more patient acceptance and reduce hospital patient load during the pandemic.
Güler et al, Turkey³⁹	Survey	11 Mar 2020–31 May 2020	93 (NR)	Effect of COVID-19 on the number of breast cancer surgeries	Though the number of breast cancer surgeries reduced initially, it soon increased.	Breast cancer surgeries were not affected.
Kara et al, Turkey⁹¹	Retrospective study	Dec 2019–Nov 2020	332 (NR)	Impact of COVID-19 pandemic on the surgical volume of breast cancer	The number of breast cancer surgeries decreased by 50–60% during the first wave (Apr 2020-May 2020) of the pandemic than in the pre-pandemic period (Dec 2019-Mar 2020), The number of breast cancer surgeries increased during the inter-pandemic period (Jun 2020- Sep 2020) and rose to a similar level during the pre-pandemic period.	The Covid-19 pandemic affected the surgical volume of breast cancer significantly. Allotting some hospitals for breast cancer surgeries could overcome the breast cancer surgical overload due to undone operations during the pandemic.
Kiziltan et al, Turkey³⁷	The single-centre retrospective observational cohort study	11 Mar 2020–1 Jun 2020	350 (51 years)	Impact of COVID-19 pandemic on breast cancer surgery	The number of patients treated with breast cancer surgery reduced significantly during the pandemic (121 vs 229 during the pre-pandemic period).	Hospitals having no SARS-CoV-2 infected patients can be helpful places for escaping surgical delays.
Koca et al, Turkey³⁸	Retrospective cohort study	11 Mar 2019–11 Mar 2021	148 (51.2 years)	Impact of COVID-19 on breast cancer surgery	47.7% reduction in the number of patients who underwent breast surgery during the first year of the pandemic, the total number of BCS + sentinel lymph node biopsy (SLNB) decreased, while the number of mastectomies and modified radical mastectomy (MRM) increased during the first year of the pandemic (11 Mar 2020–11 Mar 2021) compared to the year before the pandemic (11 Mar 2019–11 Mar 2020).	The reduction in breast cancer screening and diagnosis during the pandemic resulted in a decline in the total number of surgeries. Regular breast cancer screening should be ensured to restore surgical procedures and reduce the decline in the number of breast cancer surgeries.
High-income countries
Cadili et al, Canada¹⁰⁷	Questionnaire survey	13 Oct 2020–31 Dec 2020	123 (54 years)	Patients’ perception of telemedicine	Among the operated patients, 85% enjoyed telemedicine consultation, 93% found there was enough time to talk, and 66% wanted to retake the service.	The patients were delighted with telemedicine.
Isaac et al, Canada¹⁰¹	Expert opinion	Apr 2021–Jun 2021	NR	Guidelines for BR during COVID-19	During resource shortages, multidisciplinary teams are strategically used for patient sorting using coordinated alternative treatment methods. Patient-centred shifting and consolidation of resources are made easier with collaborative decision-making. Perioperative administration strategies and surgical care plans are applied to expand the provision of BR treatments.	These strategies can ensure optimized patient care.
Illmann et al, Canada⁹²	Questionnaire-based cross-sectional survey	Mar 2020–May 2021	49 (NR)	Impact of COVID-19 on breast reconstructive services	First wave of COVID-19: 78% reduction in breast reconstruction cases were reported by the responders, a complete cessation in breast reconstructive services was reported by 27.4% of responders, and all responders reported at least a 5% reduction in breast reconstruction services. The second wave of COVID-19: 31% reduction in breast reconstructive services, complete reconstruction services provided by 8% of the responders, and no report of complete cessation of services. The third wave of COVID-19: An average of 49% reduction in reconstruction services reported by the responders.	Following the local institutional capacity, proper application of best practice standards, guidelines, and strategies may improve breast reconstruction services.
Dorri et al, France⁴³	Observational study	Jan 2020–Jul 2020	581 (NR)	Effect of COVID-19 on the number of breast cancer surgeries	Breast cancer surgeries decreased by 18.05% in 2020 compared to 2019. Ambulatory hospitalization rate decreased significantly* in COVID-19 conditions. The IBR after mastectomy rate was not much affected by COVID-19.	The routine gynecological follow-ups should be restored urgently during the COVID-19 period.
Murris et al, France⁹³	Multicentre retrospective study	16 Mar 2020–21 May 2020	NR	Effect of lockdown on surgical management of breast cancer	50% of centres increased their surgical activity, whereas 33% reduced during COVID-19. 81% of centres postponed IBR. 83% of centres did conservative surgeries on an outpatient basis.	A total reorganization of the healthcare system was required during the COVID-19 pandemic.
Fancellu et al, Italy⁹⁴	Retrospective comparative study	1 Mar 2020–30 Apr 2020	42 (62 years)	Breast cancer surgeries during COVID-19	The number of IBR*, the use of regional nerve blocks, and the length of hospital stay* were significantly reduced.	Breast cancer care level was decreased due to COVID-19.
Lisa et al, Italy¹⁰³	Retrospective observational study	9 Mar 2020–9 Apr 2020	51 (53.4 years)	Guidelines for BR during COVID-19	Patients were double-step screened before surgery, proper anesthesia and pain control protocol was followed, patient and clinician protection was ensured, IBRs adopting implants were performed, patients were discharged quickly, post-operative consultations were lessened, and telemedicine was enforced.	The protocol was safe and effective for immediate implant-based BR after tumour resection.
Fregatti et al, Italy¹⁰²	Observational study	9 Mar 2020–9 Jun 2020b	203 (NR)	Preventive surgery strategies during COVID-19	A patient-tailored program was followed to avoid hospitalization of COVID-19 symptomatic patients and to prioritize surgical procedures. Breast-conserving surgery was mainly preferred. Hospital stay was minimized. Systematic home telemonitoring was introduced after the patient’s discharge.	Breast cancer surgeries can be safely and effectively provided during COVID-19 by following preventive strategies.
Losurdo et al, Italy⁴⁹	The observational monocentric retrospective study	Mar 2019–Apr 2021	549 (64)	Impact of COVID-19 on breast cancer surgeries	4.6% reduction in the number of breast cancer surgeries (281 in pre-COVID era vs 268 in Covid period), conservative surgery increased by 8.5% whereas mastectomies decreased by the same percent in Covid era, changes in types of surgeries increased significantly in Covid period than in pre-Covid period.	Maintaining standards of care and proper guidelines is the most crucial strategy for handling diagnostic and operative procedure delays during the pandemic.
Marcasciano et al, Italy¹⁰⁹	Multicentre collaborative study	Oct 2019–Mar 2020	307 (NR)	Role of online videos in the training of breast surgeons	Trainee and faculty surgeons rely on videos from YouTube and other sources for training and education.	Online videos can be helpful for surgeons if the source is reliable.
Pellini et al, Italy⁹⁷	Case-control study	Jan 2018–Jun 2020	341 (62 years during COVID-19)	Efficacy of interventions by lean thinking	No significant difference was found in lengths of pre-admission and stay between COVID and characteristics-matched pre-COVID groups.	The interventions can optimize preoperative and postoperative times during COVID-19.
Vanni et al, Italy⁵¹	Multicentric retrospective study	11 Mar 2020–30 May 2020	203 (NR)	Breast cancer surgeries during COVID-19	Significant* increase in sentinel lymph node biopsy and axillary lymph node dissection during lockdown compared to before.	N/A
Vanni et al, Italy⁹⁶	Retrospective monocentric study	30 Jan 2020–30 Mar 2020	86 (64.77 years)	Breast cancer surgeries during COVID-19	Awake breast surgery* and awake BCS significantly increased during COVID-19 than before. A significant* decrease in operative room time and length of hospital stay was found	Awake surgery and ERAS protocols can be followed to reduce cross-infection and patient discharge time.
Saeki et al, Japan⁴⁴	Survey study	Jan 2019–Mar 2021	2877 (NR)	Influence of COVID-19 pandemic on breast cancer surgeries	The number of surgeries significantly decreased during the pandemic compared to the pre-pandemic period.	The reduction in breast cancer surgeries during the COVID-19 pandemic was caused due to decreased screening, triage, and postponement of surgeries for stage 0 patients.
Filipe et al, Netherlands⁹⁵	The multicentre retrospective cohort study	9 Mar 2020–17 May 2020	217 (62.2 years)	Effect of COVID-19 on the number of breast cancer surgeries	Breast cancer surgeries were dramatically reduced, especially in T1-T2 and N0 tumours. Having co-morbidities and undergoing mastectomy were significant* risk factors for post-operative complications.	The National breast cancer screening program should be restarted, and patients should visit general practitioners more.
Mok et al, Singapore⁴⁶	Observational study	Feb 2020–May 2020	NR	Surgery strategies during COVID-19	Non-urgent surgeries were deferred. Oncological, therapeutic, intermediate, and diagnostic surgery requiring cases were performed. Oncoplastic and IBR surgeries were also done. The surgical team was subdivided to continue operations if any group was quarantined.	These strategies can help prioritize surgical cases and adapt to evolving COVID-19 situations.
Brenes Sánchez et al, Spain⁷⁷	Retrospective observational study	22 Apr 2020–6 May 2020	28 (57 years)	Surgery strategies and patients’ satisfaction after surgery during COVID-19	Patients were categorized into 3 groups based on priority: high, medium, and low. A pre-operative COVID-19 protocol was maintained. Non-urgent surgeries were deferred. After surgery, patients’ satisfaction was “very good” and “excellent” as per the EORTC IN-PATSAT32 questionnaire.	The prioritization of patients and following the pre-operative COVID-19 protocol led to successful surgeries and gaining patients’ satisfaction.
Kang et al, South Korea⁴⁸	A multi-institutional retrospective cohort study	1 Feb 2019–31 Jul 2020	2398 (53 years)	Impact of COVID-19 pandemic on breast cancer surgery	The number of breast cancer surgeries, ie, lumpectomy, mastectomy, lymph node surgeries, sentinel biopsies, axillary lymph node dissections, and breast reconstruction surgeries, decreased during the pandemic period in 2020 compared to the pre-pandemic period in 2019.	Continuation of routine screenings, COVID vaccination of individuals having risk factors such as the family history of cancer, and immediate medical attention after experiencing breast cancer symptoms are recommended.
Abdalla et al, UK¹⁰⁴	Cohort study	16 Mar 2020–18 May 2020	130 (57.6 years)	Breast cancer surgeries during COVID-19	Patients were prioritized and screened for COVID-19 before surgery. Mostly held surgical procedures were WLE + SLNB (40.77%), mastectomy + SLNB (18.46%), and mastectomy + axillary node clearance (18.46%). About 86% of tumours were grade 2 or 3, similarly prevalent.	Early implementation of modified surgical policies can reduce patient complications, COVID-19 infectivity, and negative impacts of COVID-19.
Batt et al, UK⁹⁸	Observational study	NR	74 (64 years in the DLA group)	Efficacy of dilutional local anesthetic (DLA)	Postoperative pain did not increase significantly in the DLA group, though the pain score was higher during 30 and 60 minutes than in the control group.	DLA can be a safe and effective alternative approach to performing breast cancer surgeries.
Ho et al, UK¹¹²	Retrospective study	03 Jun 2020–31 Dec 2020	46 (50.7 years), 29 (51.7 years)	Breast cancer surgeries during COVID-19	During the pandemic, fewer DIEP flaps were done. Flap weight was found significantly increased. The post-operative length was significantly**** less.	Autologous BR was safely conducted throughout the pandemic.
MacInnes et al, UK⁵²	Multi-centre observational study	16 Mar 2020–24 Apr 2020	202 (57 years)	Surgery strategies during COVID-19	Strict COVID-19 protocols were followed. Patients were instructed to isolate themselves for 2 weeks before surgery. All clinicians wore full PPEs. The number of operations was minimized by 38% compared to 2019 to reduce infection. The patients were released on the surgery day whenever possible.	No mentionable unexpected event occurred. So, surgeries can be safely delivered during COVID-19 by following safety protocols strictly.
Romics et al, UK⁵³	Cohort study	31 Jul 2019–7 May 2020	179 (54 years)	Breast cancer surgeries during COVID-19	Significantly fewer BCS** and increased level II oncoplastic conservation* during COVID-19. No IBR was offered during the lockdown. No perioperative COVID-19-related complication arrived.	More oncoplastic breast conservations should be done as IBR was not offered after mastectomy due to COVID-19 risk. Breast cancer surgeries can be safely done in selected patients in a population where 50% have co-morbidities.
Sud et al, UK⁹⁹	Observational study	2013–2020	NR	Effect of surgical delay due to COVID-19	Surgical delay of 3–6 months had minimal impact on the survival of early-stage breast cancer patients.	Alternative breast cancer management strategies should be evaluated to reduce surgical delay-related mortality.
Kennard et al, USA⁶⁵	Cohort study	1 Mar 2020–15 Jun 2020	73 (60.6 years)	Surgery strategies during COVID-19	44% of patients faced treatment change during COVID-19, and it was significantly* linked to surgical prioritization. Diagnosis to surgery time was significantly *** higher in the change group than in the no-change group.	Surgical prioritization leads to deferring surgical time for many patients.
Ludwigson et al, USA¹⁰⁸	Questionnaire survey and interview	Aug 2020 – Feb 2021	133 (NR)	Patients’ perception of telemedicine	Among the patients presenting for surgical consultation, 63% attended telemedicine appointments, and 67% were satisfied with their experience.	The patients were satisfied with telemedicine.
Murphy et al, USA⁸⁰	Observational study	2008–2019	186 (66 years)	Surgical management of axilla following NET	Selective de-escalation of axillary surgery was done effectively in breast cancer patients treated with NET in the same way as the current way of treating first with surgery.	Breast cancer patients receiving NET can be managed safely by adopting the same way as patients with similar tumours treated with a surgery-first approach.
Mo et al, USA¹⁰⁶	Retrospective, population-based cohort study	1 Mar 2019–1 Dec 2020	2942 (NR)	Follow-up after resection of stage I/II breast cancer during COVID-19 situations	Only 42% of patients attended follow-up during the pandemic. Patients being younger, with lower socio-economic status, and previously taking adjuvant radiotherapy were more likely to participate in the follow-up.	Breast cancer survival rate can decline if in-person follow-up care is not re-established after the pandemic, as telemedicine is not enough.
Specht et al, USA¹⁰⁵	Clinical trial	Feb 2020–Mar 2020	15 (45.38 years)	Same day mastectomy and BR	A protocol consisted of pre-operative, day of surgery, and post-operative sections. Patients’ hospital visits were minimized before and after surgery by emphasizing telehealth services. Surgical oncology and plastic surgery teams operated together. Patients were discharged after a few hours of surgery.	Same-day mastectomy and BR can be successfully performed following the protocol to reduce infection risk and optimize hospital resources during the pandemic.
Worldwide
Curigliano et al, Worldwide⁸⁵	Guidelines	NR	NR	Guidelines for breast cancer surgeries during COVID-19	Based on surgical urgency, patients were grouped into urgent, high, intermediate, and low-priority categories. All non-urgent surgeries were suggested to be deferred. Outpatient surgeries were recommended to be adopted.	N/A
Rocco et al, Worldwide⁸⁶	Questionnaire survey	4 Apr 2020–14 Apr 2020	112 (NR)	Impact of COVID-19 on breast cancer surgical management	Countries adopted the triage system in Phase 2 or 3 of the pandemic. Patients with progressive disease on NAC completed NAC, small TN, HER2+ BC, T2N0 HR+/HER2- breast cancer not eligible for neo-adjuvant treatment were prioritized. Primary systemic treatment was widely accepted by surgeons as an alternative when surgeries got postponed. For T2N1 HR+/HER2- tumours, suspicious malignant biopsies, and malignant recurrence excision, more than 50% of surgeons prioritized NAC over surgery. The pandemic phase and the surgical restriction level were significantly*** associated. Benign cases, re-excision cases, in-situ HR+ cases, autologous BR surgery, and bilateral procedures were mainly deferred.	The physicians were reluctant to shift from conventional guidelines whenever possible. Alternative strategies were followed if not possible.

Notes: ****p≤0.0001, ***p≤0.001, **p≤0.01, *p≤0.05.

Abbreviations: ERAS, Enhanced Recovery after Surgery; ECOG, Eastern Cooperative Oncology Group; NR, not reported; NAF, nipple aspirate fluid; BR, breast reconstruction; IBR, immediate breast reconstruction; GAD-2, Generalized Anxiety Disorder two-item questionnaire; IORT, intraoperative radiation therapy; BCS, breast conservation surgery; DCIS, ductal carcinoma in-situ; ER, the estrogen receptor; HER, human epidermal growth factor receptor; HR, hormone receptor; PgR, progesterone receptor; ST, systematic therapy; TN, triple-negative; NAC, neo-adjuvant chemotherapy; CDK, cyclin-dependent kinase; ET, endocrine therapy; N/A, not available.