A novel stepwise and continuous high-volume irrigation drainage technique for managing cervical anastomotic leaks post-esophagectomy

Introduction

Esophageal cancer is a common malignancy within the digestive tract. According to statistics from the Global Cancer Observatory (GLOBOCAN), in 2020, there were approximately 604,000 new cases of esophageal cancer and 544,000 deaths worldwide, ranking it seventh in incidence and sixth in overall mortality among all cancers (1). In China, the pathological type of esophageal cancer is predominantly squamous cell carcinoma, accounting for over 90% of cases, while in Western countries, adenocarcinoma prevails, constituting about 70% of cases (2). Early-stage esophageal cancer often goes undetected due to non-specific clinical symptoms, resulting in most patients being diagnosed at a locally advanced stage or with distant metastasis (3).

Currently, treatment options for esophageal cancer include surgical resection, radiotherapy, chemotherapy, systemic drug therapy, and endoscopic treatment. Surgery is the only curative option for patients with esophageal carcinoma (4). Surgical approaches for esophageal cancer include: (I) the traditional open or thoracoscopic-assisted approach McKeown esophagectomy, which involves a right thoracic esophageal mobilization, upper abdominal gastric mobilization, and a cervical anastomosis; (II) the Ivor Lewis esophagectomy, consisting of an upper abdominal gastric mobilization followed by right thoracic esophageal mobilization and intrathoracic anastomosis; (III) the Sweet esophagectomy, involving left thoracic esophageal mobilization, diaphragmatic gastric mobilization, and either intrathoracic or cervical anastomosis (5,6). Furthermore, in recent years, Shanghai Changzheng Hospital has continuously performed mediastinoscopic esophagectomy for esophageal cancer. This approach, which involves mediastinoscopic esophageal mobilization through cervical approach without the need for a thoracic incision, is suitable for patients with early-stage esophageal cancer, poor pulmonary function, and pleural adhesion, and it has significantly reduced the incidence of pulmonary complications (7,8).

Anastomotic leak (AL) is one of the most severe complications following esophagectomy. It is reported that the incidence rate of ALs after esophagectomy ranges from 10% to 30%, with a mortality rate as high as 10% (9-11). Fatal bleeding and sepsis are the most common causes of leak-associated mortality (12). Compared to intrathoracic anastomoses, cervical anastomotic leaks (CALs) occur at a higher rate (13). Early diagnosis and appropriate management are crucial for reducing mortality in patients with ALs. However, to date, there is still no consensus on the management approach for CALs following esophagectomy (14). Traditional dressing changes (DC), due to incomplete drainage, lead to chronic local infections and necessitate repeated DC, resulting in slow healing of the leak and long hospital stay. In recent years, we have adopted irrigation drainage treatment (IDT) for some patients with CALs, significantly accelerating the healing of the leaks and reducing the incidence of sepsis and short-term postoperative mortality, as reported herein. We present this article in accordance with the STROBE reporting checklist (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2158/rc).

Methods

Clinical data

The current study was designed as a retrospective study. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by ethics committee board of Naval Medical University (No. 2023SL053) and informed consent was taken from all the patients. The main aim is to study the effect of IDT on patients with CALs. Patients who developed post-operative CALs were consecutively included in this study at Shanghai Changzheng Hospital from January 2020 to November 2023. Inclusion criteria were: (I) pathologically confirmed esophageal cancer, including squamous cell carcinoma, adenocarcinoma, etc.; (II) patients who underwent esophagectomy at Shanghai Changzheng Hospital, including those who received pre-operative neo-adjuvant therapy; (III) esophagectomy with cervical anastomosis, including the McKeown procedure and the inflatable mediastinoscopic and laparoscopic procedure; (IV) postoperative CALs confirmed by clinical manifestation or radiological study. Exclusion criteria were: (I) benign esophageal tumors; (II) procedures with anastomosis completed in the chest, such as the Ivor Lewis procedure; (III) patients with well-healed anastomoses without anastomotic leakage.

According to the international consensus on standardization of data collection for complications associated with esophagectomy proposed by the Esophagectomy Complications Consensus Group (ECCG), AL was defined as full thickness gastrointestinal defect involving esophagus, anastomosis, staple line, or conduit (15). CAL was defined as AL after cervical anastomosis. CAL was diagnosed using the following criteria: (I) clinical manifestation: evident leakage of gastrointestinal contents into the wound; (II) radiological examination: upper gastrointestinal contrast studies or computed tomography (CT) scans indicating leakage of contrast material outside the gastrointestinal tract into the wound, cervical or mediastinal tissue spaces.

The complications that occurred during the patient’s hospitalization (including pneumonia, sepsis, etc.), as well as data on laboratory tests, the frequency of DC, and the length of hospital stay, were all recorded.

Esophagectomy

Thoracolaparoscopic McKeown esophagectomy (TLME)

This procedure has been extensively reported (16,17). Briefly, it comprises three parts: thoracoscopic esophageal mobilization, laparoscopic gastric mobilization, and cervical anastomosis. The thoracoscopic section involves the dissection of lymph nodes around the esophagus, trachea, right recurrent laryngeal nerve, left recurrent laryngeal nerve, and subcarinal lymph nodes. After laparoscopic gastric mobilization, the mid-line upper abdominal incision is extended, and a linear stapler (easyEndo^TM Universal U12M and R60G, EziSurg Medical, Shanghai, China) is used to create the gastric conduit. Cervical anastomosis is performed using a circular stapler (ESC25A, Ethicon, NJ, USA). The stump of the gastric conduit is closed using the linear stapler. A negative pressure drainage tube (DT) (100 mL, MKL^®, Suzhou, China, the negative pressure was produced by a negative pressure drainage bulb) is placed on the left side of the cervical anastomosis (18). If an AL occurs, the drainage can be directly converted to the irrigation or drainage pathway (the negative pressure is then provided by the central medical vacuum system in the hospital). We routinely perform jejunostomy for early nutritional support after esophageal cancer surgery. In the case of an AL, the jejunal conduit plays a crucial role in maintaining the patient’s nutrition supply.

Inflatable mediastinoscopic and laparoscopic esophagectomy (IMLE)

This procedure was innovated by Ikeda et al. (19). Based on the original techniques, we have made a secondary modification by incorporating novel surgical instrument (8). The major differences between IMLE and TLME are that, in IMLE, the mobilization of esophagus and the dissection of mediastinal lymph nodes are conducted through the cervical incision. The remaining steps, which include gastric mobilization, cervical anastomosis, and jejunostomy, are generally similar to those of TLME.

The peri-operative management of esophagectomy

After esophagectomy, patients receive daily supplementation of approximately 2,500–3,500 mL of fluids along with the necessary electrolytes. Regular DC are conducted, with careful observation of the nature of the cervical drainage fluid, paying attention to the presence of neck tenderness and subcutaneous emphysema. The patient’s clinical complaints (neck pain), vital signs, and blood counts are closely monitored. If there is turbid drainage fluid, subcutaneous emphysema, or unexplained fever, elevated blood counts, or tachycardia, the cervical incision sutures are removed without hesitation. The cervical incisions are opened to expose the anastomotic site for exploration of any gastric content leakage, pus accumulation, or conduit necrosis. If the diagnosis is uncertain, the patient can be instructed to drink a small amount of water to test for anastomotic leakage. For confirmed CALs, intensified the DC group or the IDT group are administered.

The methods of IDT

We employ a “Stepwise” tube placement method for IDT. The suction catheter [4.0 mm (F12) * 450 mm, MKL^®] is used as the irrigation tube (IT) and DT. For patients with larger ALs and significant leakage of gastric contents, a gastric feeding tube (CH/FR 15, 100 cm, Freka^® Tube, Fresenius Kabi AG, Hesse, Germany) with a larger diameter can be employed as DT. In some cases, the original cervical negative pressure DT can be kept and utilized as IT after removing the negative pressure drainage bulb. Typically, the suction catheter has two lateral holes, each with a diameter of approximately 5 mm, located about 3 cm from the distal end, which are sufficient for its use as an IT. However, to achieve optimal suction effects, the number of the lateral holes at the end of the suction tube, when used as a DT, can be appropriately increased. Usually, one IT and one DT are sufficient; however, sometimes, to enhance the suction efficiency, an additional DT may be added. The ideal placement for IT and DT is within the defect. Thus, necrotic tissue, pus, and gastric contents can be continuously drained, maintaining the cleanliness of the wound. Generally, the IT can be positioned slightly deeper to prevent the suction from directly affecting adjacent tissues. The IT and DT can be positioned side by side. Gauze can be packed around the DT; this not only maintains the patency of the fistula but also prevents the DT from adhering to the sidewalls of the cervical tissue, which may cause impaired drainage and bleeding. Optionally, a small amount of gauze can be placed on the surface of the wound.

The IT is connected to the infusion set, utilizing 3,000 mL of saline for continuous irrigation, while the DT is connected to the central vacuum system via a negative pressure suction device. Optionally, to avoid iatrogenic injury caused by excessive suction, such as injury to cervical blood vessels, negative pressure can be applied through a closed chest drainage system (YY0583, Kang-Sheng Medical, Taizhou, China) (20). The patency of the irrigation and drainage system (IDS) is tested. Subsequently, the IT and DT are secured to the skin through suturing and air-knotting. The tightness of the knots should be appropriate, allowing for the adjustment of the tubes’ depth by sliding, when necessary.

In the early stages of CALs, due to severe local contamination, we employ a continuous high-volume irrigation drainage strategy with saline solution. The liquid in Murphy’s drip may form a continuous line, when this strategy is used (20,000–30,000 mL/d). During the healing phase, as the leak gradually diminishes, the irrigation flux can be reduced, or the approach can be switched to traditional DC.

The measurement of treatment efficacy

The measurement indicators for evaluating the efficacy of CAL treatment included healing time (HT), calculated as the number of days from the diagnosis to leak resolution; time to oral feeding; frequency of DC (per day); post-operative hospital stay; 90-day mortality rate; incidence of new-onset pneumonia and sepsis following CAL. The evaluation criteria for leak resolution are as follows: the leak is covered by epithelial cells or scar tissue, the DT is removed, and there is no food leakage from the original leak site after resuming a liquid diet. Sepsis is defined by an increase in sepsis-related organ failure (SOFA) score of ≥2 points due to infection (21,22); and laboratory parameters [white blood cell count (WBC), C-reactive protein (CRP), procalcitonin (PCT), interleukin-6 (IL-6)] measured initially upon CAL diagnosis and subsequently on the 1st, 3rd, and 7th days. Additionally, post-operative anastomotic strictures requiring intervention were recorded.

Statistical analysis

Statistical analyses were conducted using Stata 12.0 software (StataCorp LLC, Texas, USA). Continuous data were presented as the median and interquartile range [Q2 (Q1, Q3)], with group comparisons assessed using the Wilcoxon rank-sum test. Categorical data were presented as counts and percentages [n (%)], with group comparisons assessed using the Chi-squared test. For categorical data with any expected cell count less than 5, Fisher’s exact test was used. Statistical significance was defined as P<0.05.

Results

Basic information of patients with CALs

From January 2020 to November 2023, 1,367 patients with esophageal cancer were admitted to Shanghai Changzheng Hospital. Of these, 1,136 underwent surgical operations, including 611 with cervical anastomosis. The case inclusion process is illustrated in Figure 1. Ultimately, 53 patients with CALs were included in the current study. The incidence of CALs was 8.7%. The study group comprised 47 males and 6 females, with a median age of 64 (interquartile range, 56–68) years. Among the participants, 23 underwent TLME, while 30 underwent IMLE. The postoperative pathology was squamous cell carcinoma in 45 cases, adenocarcinoma in 6 cases, and neuroendocrine tumors in 2 cases. The patients were divided into two treatment groups: 26 in the DC group and 27 in the IDT group. A shift in the treatment paradigm occurred after 2022, during which we increasingly favored the use of IDT for the management of CALs (Table S1). The severity of leaks in both patient groups was comparable. Specifically, 2 cases in the DC group and 2 cases in the IDT group were combined with bleeding in the anastomotic site; while 5 cases in the DC group and 4 cases in the IDT group were combined with conduit necrosis. It is noteworthy that there was no significant difference in the surgical approach (trans-thoracic or mediastinoscopic) between patients treated with different management techniques. There were no statistical differences between the groups in terms of gender, age, pathological type, staging, surgical method, lymph node metastasis, location of the AL, concurrent bleeding, conduit necrosis, and pleural empyema, among other aspects (Table 1).

Figure 1 Patient flow chart. CAL, cervical anastomotic leak; DC, dressing changes; IDT, irrigation and drainage treatment.

IDT significantly improved the outcome of patients with CALs

IDT was successfully conducted on 27 patients (Figure 2). IDT significantly expedited the HT of CALs (45.5 vs. 23 days, P<0.01), reduced the frequency of DC (2.6 vs. 1.5 times/day, P<0.01), shortened the length of time to oral feeding (50 vs. 27 days, P<0.01) and post-operative hospital stay (54 vs. 30 days, P<0.01), and decreased the mortality rate of patients (15.4% vs. 0%, P<0.05, Table 2). The causes of death for four patients in the DC group were sepsis (2 cases) and fatal bleeding (2 cases). Notably, there were no death among patients in the IDT group. Additionally, the incidence of sepsis (23.1% vs. 3.7%, P<0.05) and pneumonia (30.8% vs. 7.4%, P<0.05) significantly decreased in the IDT group. Laboratory tests indicated that IDT significantly reduced the CRP and IL-6 levels on the 3rd and 7th days of treatment (Figure 3). Stricture following CALs is a common complication. In terms of stricture requiring intervention, we did not observe significant difference between these two treatment strategies (Table 2). In addition, we did not find a significant impact of operative approach (TLME vs. IMLE) on the treatment outcome of CALs (Table S2).

Figure 2 Treatment of CAL with the IDT. (A) The placement of IT and DT. Red arrow, IT. Green arrow, DT. The IT and DT are placed parallel to each other. (B) The fixation of IT and DT. Red arrow, IT. Green arrow, DT. Adhesive tape is used to fix the IT and DT to the patient’s temple and clavicular area. Care is taken to leave room for movement, ensuring that neck movement does not exert tension on the tubes. (C) A case of CAL with conduit necrosis. The figure shows necrosis of the gastric wall in the anastomotic area (black arrow), with local accumulation of pus and necrotic tissue. (D) Photograph of the wound of the same patient taken 8 days after IDT. The necrotic tissue has been replaced by freshly growing granulation tissue (black arrow), and the size of the fistula has been reduced. (E) CT image of a patient with esophageal cancer on the 5th day post-esophagectomy. The diagnosis of CAL was clear by the evidence of contrast leakage. White arrow, the fistula cavity. (F) CT image of the same patient on the 10th day after IDT. The fistula cavity (white arrow) was significantly reduced. These images are published with the patient’s consent. AL, anastomotic leak; CAL, cervical anastomotic leak; CT, computed tomography; DT, drainage tube; IDT, irrigation and drainage treatment; IT, irrigation tube.

Figure 3 Changes in inflammatory markers in patients with CALs (A, WBC; B, CRP; C, PCT; D, IL-6). Graphs were created using Python 3.12, presenting box plots (with whiskers representing 1.5 IQR) and scatter plots for two groups of data. The comparison between the two groups was conducted using the Wilcoxon rank-sum test. P values with significance were annotated. CALs, cervical anastomotic leaks; CRP, C-reactive protein; DC, dressing changes; IDT, irrigation and drainage treatment; IL, interleukin; IQR, interquartile range; PCT, procalcitonin; WBC, white blood cell count.

Special management of IDT

Due to the high volume of irrigation and drainage received by patients with IDT, imbalances between the irrigation volume and drainage volume frequently occur. Therefore, we recorded the irrigation and drainage volumes of patients with IDT. During IDT treatment, the average daily irrigation volume was 25,171±241 mL/day, and the average daily drainage volume was 25,109±362 mL/day, which are roughly comparable. Since the irrigation fluid is saline solution, we monitored the incidence of hypernatremia or hyponatremia. A review of the laboratory tests indicated that there were no occurrences of hypernatremia or hyponatremia in the IDT group. It is worth noting that three patients in the IDT group had concomitant pleural empyema. In two patients, the chest tube left in place during surgery was used as the DT, while the other patient required reinsertion of the chest DT. In conclusion, the combination of IDT and chest DT is successful in the treatment of CAL combined with pleural empyema.

Discussion

In recent years, minimally invasive surgical modalities have become the mainstream approach for esophageal cancer. However, the incidence rate of AL has not significantly decreased (10,23,24). According to the location of the anastomosis, esophagectomy procedures can be divided into intrathoracic anastomosis and cervical anastomosis. Compared to intrathoracic anastomosis, cervical anastomosis has a higher rate of leakage, with the incidence rate of CALs reported as 10% to 30% (25,26). The main causes of CAL include increased anastomotic tension due to gravity and compromised blood supply or venous return caused by compression at the junction between the thorax and neck (27). Improvements in surgical techniques cannot reduce the incidence rate of AL to zero (24). Therefore, proper management of AL is crucial for reducing the postoperative mortality rate of esophageal cancer. In the past, there were a few reports of successful management of CALs by early surgical interventions. However, due to significant local contamination and poor blood supply, surgical treatment is no longer the first choice for CALs (28,29).

The superficial nature of the cervical wound provides an opportunity for the early diagnosis and treatment of ALs. Generally, the management principles for CALs include early opening of the wound, fasting, gastrointestinal decompression, treatment and prevention of sepsis, and nutritional support. However, there is still no consensus or standard regarding the local management of the leak. Regarding the local treatment of CALs, traditional methods mainly involve repeated DC and gauze packing for drainage. These treatment methods have the following disadvantages: (I) after DC, local pus quickly reforms, hindering the healing of CAL. (II) Since the local infection is not adequately drained, bacteria and toxins may enter the bloodstream, leading to systemic inflammatory response syndrome and even sepsis. (III) Additionally, the local accumulation of corrosive gastric juice, saliva, and other digestive fluids impedes the healing of the anastomotic site. In the early stages, to improve drainage effectiveness, we have attempted a single-tube drainage method. A single DT was placed in the leak area, connected to negative pressure suction, or subjected to intermittent flushing, but these approaches encountered various problems. Negative pressure suction often led to tube blockages, and intermittent flushing did not achieve satisfactory drainage, with flushing fluids overflowing onto the wound surface. To further improve drainage effectiveness, we designed a stepwise continuous large-volume irrigation and drainage method. Through a dual-tube design, the wound surface can be kept clean at all times, reducing the risk of systemic inflammatory response syndrome and promoting the growth of granulation tissue.

The current study indicates that IDT can reduce HT, lower mortality rates, shorten hospital stay, and decrease the incidence of sepsis and pneumonia. The potential mechanisms by which IDT improves clinical efficacy include reducing local accumulation of digestive fluids, pus and necrotic tissue, thereby decreasing the absorption of toxins into the blood, maintaining the freshness of granulation tissue, and promoting wound healing.

The ideal position of the IT and DT is within the defect. Two common scenarios may occur. In some patients, a positive balance is observed, where the irrigation volume exceeds the drainage volume. This situation arises because a portion of the saline solution enters the stomach, and it is possible to observe irrigation fluid being drawn out through the gastric tube. The presence of the gastric tube can prevent patients from experiencing hypervolemia. In another group of patients, a negative balance occurs, where the irrigation volume is less than the drainage volume. This is due to continuous negative pressure suction extracting a portion of the gastric fluid out of the body. Both situations are acceptable, but attention must be paid to the balance of water and electrolytes, with appropriate administration of diuretics or supplementation of electrolytes as needed. A retrospective analysis of our data revealed that none of the patients who received IDT developed hypernatremia. Optionally, it may be prudent to appropriately retract the IT or DT, to correct any excessive positive or negative balance.

During IDT, maintaining patency of the tubes is crucial. The most common reasons for the failure of IDT are the obstruction of the DT caused by detachment of necrotic tissue or the adhesion of the DT to the sidewalls of cervical tissue. The solutions are as follows: stop irrigation and negative pressure suction, inspect the tubes, remove the accumulated necrotic tissue from the tip of the DT, adjust the position of the DT, or increase the side holes of the DT, and pack gauze between the DT and the neck tissue.

IDT is also applicable for patients with conduit necrosis, which is often accompanied by severe local infection. Extensive irrigation and drainage can remove some of the detached necrotic material, preventing the spread of infection to the mediastinum. However, daily debridement until the necrotic tissue is replaced by fresh gastric mucosa remains essential. Moreover, bleeding is not a contraindication for IDT. In such cases, iced epinephrine saline can be infused through the IT to achieve hemostasis (30). Notably, in the DC group, two patients succumbed to fatal bleeding, while in the IDT group, all patients who experienced bleeding survived. This survival benefit may be attributed to IDT’s capacity to attenuate the absorption of toxins into the bloodstream. In addition, some patients may develop pleural empyema due to the spreading of infection into the mediastinum and pleural cavity (31). In this case, adequate drainage can be achieved by extending the cervical tubes to the mediastinum or by reinserting thoracic tubes under CT guidance.

The neck area is rich in blood supply, with cervical vessels running laterally to the anastomosis site. It is important to adjust the suction force appropriately to avoid undue impact on the tissues, preventing vascular rupture and bleeding. Additionally, excessive suction force may cause local noise disturbance, affecting the patient’s rest, and may lead to excessive loss of gastric fluid. The appropriate range of negative suction pressure should be <0.01 mmHg. Adjust the negative pressure suction valve so that the suction force precisely removes all irrigation fluid without spillage.

Furthermore, it is important to note that although IDT and parenteral nutrition support may confine the patient to bed for most of the daytime, patients undergoing IDT should still maintain regular activity and perform coughing exercises to avoid deep vein thrombosis and pneumonia. Additionally, patients with CALs inevitably experience anxiety and pessimism, and it is important to provide reassurance and continuously encourage the patient. Particularly, cervical irrigation and drainage increase the nursing workload, and close communication with nurses, maintaining collaboration and care, is essential.

There are some limitations in this study. First, this study is a retrospective study with a small number of cases. However, the conclusions of the study indicate that the therapeutic significance of IDT in the treatment of CALs is definitive. Second, this study is limited to CALs. Interestingly, Xu et al. have introduced a slow-flow irrigation drainage technique for treating patients with AL and thoracic empyema, significantly accelerating the healing of the leaks and reducing the occurrence of related complications (32). Thus, it can be inferred that the irrigation drainage method is equally effective for thoracic ALs. In fact, Shanghai Changzheng Hospital has also adopted a similar approach for patients with thoracic ALs and has achieved success. Finally, this study lacks mechanistic research analysis. For example, what is the principle behind IDT accelerating the healing of anastomosis? Can fluids stimulate the angiogenesis of local vessels or the growth of gastric mucosa? These questions remain to be confirmed through basic research.

Conclusions

In summary, the incidence of CALs is high clinically, and there is still a lack of unified treatment standards internationally. In recent years, Shanghai Changzheng Hospital has achieved good therapeutic effects in treating CALs with IDT. Practice has proven that the IDT can accelerate the healing of the leaks, shorten the hospital stay, and reduce mortality. We advocate for a global promotion of this experience.

Acknowledgments

None.

Footnote

Reporting Checklist: The authors have completed the STROBE reporting checklist. Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2158/rc

Data Sharing Statement: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2158/dss

Peer Review File: Available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2158/prf

Funding: The current study was supported by the Naval Medical University “Shenlan” Talent Project “Yuanhang” Talent Cultivation Program (SL13), the 2022 Zhangjiang National Independent Innovation Demonstration Zone Special Development Fund Support Project (No. 2022zjgjzzcx-2), the Shanghai Shenkang Hospital Development Center’s “Three-Year Clinical Innovation Action Plan” (No. shdc2022crd029), Military Medicine Projects in “DZX” Hospitals (No. 2024DZXYY-301), and the National Natural Science Foundation of China’s General Program (No. 81470213).

Conflicts of Interest: All authors have completed the ICMJE uniform disclosure form (available at https://jtd.amegroups.com/article/view/10.21037/jtd-2024-2158/coif). The authors have no conflicts of interest to declare.

Ethical Statement: The authors are accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved. The study was conducted in accordance with the Declaration of Helsinki and its subsequent amendments. The study was approved by ethics committee board of Naval Medical University (No. 2023SL053) and informed consent was taken from all the patients.

Open Access Statement: This is an Open Access article distributed in accordance with the Creative Commons Attribution-NonCommercial-NoDerivs 4.0 International License (CC BY-NC-ND 4.0), which permits the non-commercial replication and distribution of the article with the strict proviso that no changes or edits are made and the original work is properly cited (including links to both the formal publication through the relevant DOI and the license). See: https://creativecommons.org/licenses/by-nc-nd/4.0/.

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