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Table 1. 
Infection by Other Risk Factors
Infection by Other Risk Factors
Table 2. 
Infection by Tumor Stage*
Infection by Tumor Stage*
Table 3. 
Infection by Node Status*
Infection by Node Status*
Table 4. 
Infection by Tumor Grade*
Infection by Tumor Grade*
Table 5. 
Infection by Type of Laryngeal Surgery*
Infection by Type of Laryngeal Surgery*
Table 6. 
Infection by ND*
Infection by ND*
Table 7. 
Significance of the Contribution of Each Variable, Also Considering the Effect of Others
Significance of the Contribution of Each Variable, Also Considering the Effect of Others
1.
Dominioni  LBianchi  MDionigi  R Factors predisposing to surgical infections and identification of patients at risk. Surg Res Commun 1990;91- 7
2.
Anielski  RBarczynski  M Postoperative wound infections, I: population data and risk factors. Przegl Lek 1998;55101- 108
PubMed
3.
Gonzalez Aguilar  OPardo  HAVannelli  A  et al.  Total laryngectomy: pre- and intrasurgical variables of infection risk. Int Surg 2001;8642- 48
PubMed
4.
Velasco  EMartins  CAGoncalves  VMDias  LMThuler  LC Risk factors for surgical wound infection development in head and neck cancer surgery. Rev Hosp Clin Fac Med Sao Paulo 1995;5058- 62
PubMed
5.
Manceau  ADenis  FGarand  GGaraud  PBeutter  P Infectious complications after surgery for hypopharyngeal and laryngeal carcinomas. Ann Otolaryngol Chir Cervicofac 2003;120207- 215
PubMed
6.
Farwell  DGReilly  DFWeymuller  EA  JrGreenberg  DLStaiger  TOFutran  NA Predictors of perioperative complications in head and neck patients. Arch Otolaryngol Head Neck Surg 2002;128505- 511
PubMedArticle
7.
Girod  DAMcCulloch  TMTsue  TTWeymuller  EA  Jr Risk factors for complications in clean-contaminated head and neck surgical procedures. Head Neck 1995;177- 13
PubMedArticle
8.
Perracchia  ARoncroni  LVidi  V La Chirurgia Nell’Anziano.  Parma, Italy: Atti della Società Italiana di Chirurgia Geriatrica; 1990
9.
Dunne  JRMalone  DTracy  JKGannon  CNapolitano  LM Perioperative anemia: an independent risk factor for infection, mortality and resource utilization in surgery. J Surg Res 2002;102237- 244
PubMedArticle
10.
Brown  BMJohnson  JTWagner  RL Etiologic factors in head and neck wound infections. Laryngoscope 1987;97587- 591
PubMedArticle
11.
Ceschia  TBeorchia  AGuglielmi  R  et al.  Influence of radiotherapy on lymphocyte subpopulations. Radiol Med (Torino) 1991;81532- 536
PubMed
12.
Louagie  HVan Eijkeren  MPhilippe  JThierens  Hde Ridder  L Changes in peripheral blood lymphocyte subsets in patients undergoing radiotherapy. Int J Radiat Biol 1999;75767- 771
PubMedArticle
13.
Haley  RWCulver  DHMorgan  WMWhite  JWEmori  TGHooton  TM Identifying patients at high risk of surgical wound infection: a simple multivariate index of patient susceptibility and wound contamination. Am J Epidemiol 1985;121206- 215
PubMed
14.
Horan  TCGaynes  RPMartone  WJJarvis  WREmori  TG CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Infect Control Hosp Epidemiol 1992;13606- 608
PubMedArticle
15.
Lilienfeld  DEVlahov  DTenney  JHMcLaughlin  JS Obesity and diabetes as risk factors for postoperative wound infections after cardiac surgery. Am J Infect Control 1988;163- 6
PubMedArticle
16.
Johnson  JTMyers  ENThearle  PBSigler  BASchramm  VL  Jr Antimicrobial prophylaxis for contaminated head and neck surgery. Laryngoscope 1984;9446- 51
PubMed
17.
Li  YZhang  QWang  T The relationship between the phenotype of tumor infiltrating cells and the prognosis in laryngeal cancer. Zhonghua Er Bi Yan Hou Ke Za Zhi 1995;30209- 212
PubMed
18.
Bulbuk  GA Immunity indices of patients with locally disseminated malignant neoplasm of the head and neck. Vopr Onkol 1982;2857- 59
PubMed
19.
Dietz  AHeimlich  FDaniel  VPolarz  HWeidauer  HMaier  H Immunomodulating effects of surgical intervention in tumors of head and neck. Otolaryngol Head Neck Surg 2000;123132- 139
PubMedArticle
20.
Schantz  SPPeters  LJ Patterns of recurrence from head and neck cancer: an immunologic prospective. Cancer 1989;641232- 1237
PubMedArticle
21.
Gonzalez  FMVargas  JALopez-Cortijo  C  et al.  Prognostic significance of natural killer cell activity in patients with laryngeal carcinoma. Arch Otolaryngol Head Neck Surg 1998;124852- 856
PubMedArticle
22.
Gonzalez  FMVargas  JALacoma  F  et al.  Natural killer cell activity in laryngeal carcinoma. Arch Otolaryngol Head Neck Surg 1993;11969- 72
PubMedArticle
23.
Jecker  PVogl  KTietze  LWesthofen  M Dendritic cells, T and B lymphocytes and macrophages in supraglottic and glottic squamous epithelial carcinoma: location and correlation with prognosis of the illness. HNO 1999;47466- 471
PubMedArticle
24.
Wanebo  HJJun  MYStrong  EWOettgen  H T-cell deficiency in patients with squamous cell cancer of the head and neck. Am J Surg 1975;130445- 451
PubMedArticle
25.
Strome  MClark  JRFried  MPRodliff  SBlazar  BA T-cell subsets and natural killer cell function with squamous cell carcinoma of the head and neck. Arch Otolaryngol Head Neck Surg 1987;1131090- 1093
PubMedArticle
Original Article
September 2006

Clean-Contaminated Neck SurgeryRisk of Infection by Intrinsic and Extrinsic Factors

Author Affiliations

Author Affiliations: Departments of Otorhinolaryngology “Giorgio Ferreri” (Drs Fusconi, Gallo, Pagliuca, Pulice, and de Vincentiis) and Statistics (Ms Vitiello), “La Sapienza” University of Rome, Rome, Italy.

Arch Otolaryngol Head Neck Surg. 2006;132(9):953-957. doi:10.1001/archotol.132.9.953
Abstract

Objective  To evaluate the risk of surgical wound infection (the most common complication in neoplastic clean-contaminated neck surgery) due to 10 intrinsic risk factors and 5 extrinsic risk factors.

Design  Retrospective clinical study.

Setting  Academic tertiary referral medical center.

Patients  The study group included 115 patients with laryngeal carcinomas referred to our department from January 1, 1996, to August 31, 2002.

Intervention  Fifty-seven patients underwent total laryngectomy and 58 underwent subtotal laryngectomy.

Main Outcome Measures  The association between surgical wound infection due to 10 intrinsic risk factors and 5 extrinsic risk factors was evaluated with multivariate models.

Results  Surgical wound infection occurred in 27 patients (23.5%). There was no significant increase in the incidence of infection in patients with extensive tumors (P>.20) and in patients undergoing total laryngectomy and subtotal laryngectomy (P>.20). The incidence of infection was significantly higher in patients with stage IV disease (P<.01), in patients who underwent neck dissections (P<.05), and in those presenting with lymph node metastases (P<.001). Multivariate analysis showed that the presence of higher tumor stage is the best predictor of infection because it is the only significant factor (P<.03) even when adjusting for others. The association between infection and the other factors considered in this study (age [P>1.0], underweight [P = .26], anemia [P = .84], lymphocytopenia [P = .79 by Fisher exact test], number of preoperative hospitalizations [P<1.0], preoperative radiotherapy [P = .57 by Fisher exact test], diabetes mellitus [P = .70 by Fisher exact test], cirrhosis, resection margins infiltrated by the tumor [P = .57 by Fisher exact test], and myocutaneous flap reconstructions [P = .82]) was not significant.

Conclusion  The risk of surgical wound infection is correlated with a higher tumor stage and lymph node metastases; it is not associated with the extent of surgery or other factors considered.

In neoplastic clean-contaminated neck surgery, antibiotic prophylaxis does not always prevent infection of the surgical wound. This can be attributed to various intrinsic and extrinsic risk factors. The intrinsic risk factors are linked to the patient and, therefore, not all can be modified; the extrinsic factors can be modified because they depend on the hospital environment and procedures adopted preoperatively, intraoperatively, and postoperatively.

Our study considers some intrinsic risk factors for infection: being older than 65 years, being underweight (body mass index [BMI] [calculated as weight in kilograms divided by the square of height in meters], <18.5), preoperative and postoperative anemia (hemoglobin level, <11.0 g/dL), lymphocytopenia (lymphocytes, <1.0 × 103/μL), diabetes mellitus, cirrhosis, preoperative radiotherapy (failure of definitive radiotherapy on tumor, 65 Gy), and index of neoplasm spreading (stage, tumor type, and node involvement). Among the extrinsic risk factors considered were the extent of surgical damage, surgery on the tumor or node, resection margins infiltrated by the tumor, and preparation of myocutaneous flap reconstructions. Preoperative hospitalization (>3 days) was also evaluated in the present study. The duration of preoperative hospitalization increased the probability of infection after surgery. This is likely because of progressive colonization of skin and mucus by nosocomial germs.116

The present study evaluates the risk of surgical wound infection due to 10 intrinsic risk factors and 5 extrinsic risk factors.

METHODS

From January 1, 1996, to August 31, 2002, 115 subjects with laryngeal carcinoma underwent surgery: 57 underwent total laryngectomy (TL) and 58 underwent subtotal laryngectomy, including cricohyoidopexy and cricohyoidoepiglottopexy. This study group was used for a retrospective analysis, taking into account the following intrinsic and extrinsic elements. The intrinsic risk factors for infection in clean-contaminated neck surgery related to the patient's general condition include the following: being older than 65 years, being underweight (BMI, <18.5), preoperative and postoperative anemia (hemoglobin level, <11.0 g/dL), lymphocytopenia (lymphocytes, <1.0 × 103/μL), diabetes mellitus, cirrhosis, preoperative radiotherapy (failure of definitive radiotherapy on the tumor, 65 Gy), tumor progression as defined by stage, tumor extent, and the presence of lymph node metastases (N+). Extrinsic risk factors included type of laryngectomy, number of neck dissections (NDs), resection margins infiltrated by the tumor, the use of myocutaneous flaps when required to repair surgical defects, and time spent in the hospital (>3 days).

Furthermore, all patients underwent antibiotic prophylaxis with 1 of the following protocols: clindamycin, 600 mg every 6 hours, plus amikacin, 1200 mg/d for 4 days (n = 38); amoxicillin plus clavulanic acid, 2200 mg every 8 hours for 4 days (n = 46); or sulbactam plus ampicillin, 3000 mg every 8 hours for 4 days (n = 31).

Surgical wound infection has been defined according to the criteria established by Johnson et al16(p48) as “the wound presents spontaneous or surgically induced drainage of pus or it presents a mucocutaneous fistula of infective origin.”

Cultures and antibiograms were performed in all cases of infection. The relation between the onset of infection and the variables considered was examined via analysis of contingency tables and a logistic model.

RESULTS

Of the 115 patients who underwent surgery, infection was found in 27 (23.5%). There was no significant (P>1.0) difference among the various cases of infection with reference to the type of antibiotic protocol used. The association between infection and the factors considered in this study was not significant (age >65 years, underweight, preoperative and postoperative anemia [hemoglobin level, <11.0 g/dL], lymphocytopenia, diabetes mellitus, cirrhosis, myocutaneous flaps, time spent in the hospital [>3 days], preoperative radiotherapy [only 4 patients in our study underwent previous radiation therapy and in 1 we found surgical wound infection], and positive resection margins) (Table 1).

The association between infection and stage proved statistically significant (P<.01) (Table 2); more specifically, the most infections were found in patients with stage IV disease. A statistically significant association with infections was also shown in those patients who had undergone NDs (P<.05) and in the patients in whom neoplastic metastases were evident (N+) (P<.001) (Table 3).

There was no statistically significant association between infection and tumor extent (P>.20) (Table 4) nor between infection and type of surgery (TL vs subtotal laryngectomy) (Table 5). However, the association between infection and type of surgery in patients who underwent laryngectomy in addition to ND, compared with those who underwent laryngectomy alone, proved to be statistically significant (P<.05). Paradoxically, infection was more frequent in patients who underwent unilateral ND than in those who underwent bilateral ND (Table 6).

The 3 significant variables at the univariate level (stage [P<.01], N+ [P<.001], and ND [P<.05]) were then included in the multivariate analysis. In this analysis, the unilateral and bilateral ND subgroups were considered as a single element. Initially, the following logistic model was applied: logit (probability of infection) = ND + (N+) + stage.

None of the 3 variables proved to be significant when adjusting for the other 2 (Table 7). Considering that the N+ and stage variables give us substantially the same information, the stage variable alone, which expresses a more complete evaluation in relation to the progression of the neoplasia and consequently the deficiency of the immune system, was maintained and considered in the logistic model. Therefore, the model was modified as follows: logit (probability of infection) = ND + stage.

Table 7 shows how ND proves not to be significant when considering the stage, whereas stage proves significant even when taking ND into account. This stresses the importance of stage in determining the onset of infection, excluding damage incurred by surgery as expressed by ND.

Finally, a logistic model with only 1 variable was considered by recoding stage as follows: S0 indicates stages I, II, and III; and S1, stage IV. The model was as follows: logit (probability of infection) = stage.

In fact, although risk of infection can be considered equivalent for stages II and III (Table 2), stage I has been pooled with the other stages because of the few cases.

The results of this model show that the odds of contracting infection in patients belonging to the S0 group (point estimate, 0.22; 95% confidence limit, 0.08, 0.56 by the Wald statistic) are lower than for those in the S1 group; in other words, the odds of contracting infection in the S1 vs S0 group are 4.58.

Then, multivariate analysis was repeated with all 3 variables, applying stage as previously encoded. Therefore, when rendered dichotomous, this variable (stage) was significant (P<.03) even when adjusting for ND and N+.

COMMENT

Results brought to light a statistically significant association between infection of the surgical wound and the presence of neck metastases (N+) and between infection of the surgical wound and stage. Specifically, the odds of contracting infection for patients with stage IV disease are 4½ times greater than for patients with other stages of disease. These findings show that the progression of the tumor (expressed by stage) is a risk factor for the onset of surgical wound infection and that stage is the most valid predictor variable.

By using univariate analysis, a statistically significant association has been demonstrated between ND and infection of the surgical wound. However, multivariate analysis put this finding into perspective by showing how ND was not significant when considering stage. We decided to analyze the relationship between ND and surgical wound infection because ND would inevitably imply more extensive damage during surgery, longer duration of anesthesia, bleeding, and more surgical drainages; all of these factors can be considered to cause increased risk of infection. However, in our study group, these risk factors expressed by ND did not prove to be statistically significant, nor was there any association between infection and other risk factors considered, such as being older than 65 years, preoperative and postoperative anemia (hemoglobin level, <11.0 g/dL), diabetes mellitus, cirrhosis, myocutaneous flaps, time spent in the hospital (>3 days), positive resection margins, and preoperative radiotherapy. Only 4 patients in our study underwent preoperative radiotherapy. These patients were operated on after failure of definitive radiotherapy of the tumor (65 Gy). Among these 4 patients, 1 had infection of the surgical wound. The number of cases was too few, and for this reason there is no significant statistical association between infection and preoperative radiotherapy. Brown et al,10 in agreement with our findings, found no statistically significant correlation between infection of the surgical wound and diabetes mellitus, preoperative radiotherapy, or tracheotomy performed before surgery. Thus, all our findings confirm this interesting relationship between tumor progression and infection, a relationship that does not seem to be influenced by alternative risk factors that proved not to be significant. In the study presented by Brown et al, concerning 245 patients affected by carcinoma of the head and neck, a statistically significant correlation was found between tumor stage and the onset of infection, bringing to light a higher incidence of infection of the surgical wound in patients with stage IV disease. The researchers assert, but did not investigate, that this could be attributed to the dysphagic nutritional deficit caused by the neoplasia or, alternatively, to the more extensive surgical destruction implicit in the complex reconstructive surgical technique. In our study, we calculated the BMI; 25 patients were underweight (BMI, <18.5), 42 were a normal weight (25.0≤BMI≥18.5), and 21 were overweight (BMI, >25.0). The association between infection and being underweight was not significant.

On the other hand, our study also included the analysis of patients who had undergone subtotal laryngectomy, in whom dysphagia was not present and the surgical technique was not destructive. In our opinion, in this subgroup of patients, the percentage of infection was noticeably inferior (19.0%) compared with those who had undergone TL (28.1%) because the percentage of patients with stage IV disease (22.4%) and N+ (13.7%) was lower compared with those who underwent TL (stage IV disease, 63.1%; and N+, 40.3%). Our study, like that of Brown et al,10 was not diriment, because the evaluation of the patient's nutritional status at hospital admission was missing.

However, in our opinion, the link between neoplastic disease and infection could be the deficit of the immune system in patients affected by neoplasia. In the literature, mention has been made—although with conflicting findings—of the qualitative and quantitative disorders of the immune system, which would seem to be the cause of an insufficient response to the tumor.1723 More specifically, some researchers24,25 found a relationship between an insufficient immune response and the degree of progression of the neoplasia. In our study, however, the association between infection and lymphocytopenia was not significant.

In conclusion, based on the findings of this study and in agreement with data present in the literature, we conclude that the progression of neoplasia causes a greater risk of infection of the surgical wound compared with the extent of surgery and other risk factors linked to the patient preoperatively and postoperatively. In conclusion, the most correct evaluation of risk of infection in the presence of neoplasia can be based on the definition of stage. Stage IV increases the odds for infective processes by almost 4½ times compared with the other stages. Despite the fact that the presence of metastases (N+) was also a highly significant variable (P<.001), stage was preferred because more information was offered in relation to the progression of the neoplasia.

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Article Information

Correspondence: Massimo Fusconi, MD, Department of Otorhinolaryngology “Giorgio Ferreri,” “La Sapienza” University of Rome, viale del Policlinico 155, 00165 Roma, Italy (massimo.fusconi@libero.it).

Submitted for Publication: June 23, 2005; final revision received March 21, 2006; accepted April 5, 2006.

Author Contributions:Study concept and design: Fusconi, Gallo, Pagliuca, and de Vincentiis. Acquisition of data: Pulice. Analysis and interpretation of data: Fusconi, Gallo, Vitiello, and Pagliuca. Drafting of the manuscript: Fusconi, Vitiello, and Pulice. Critical revision of the manuscript for important intellectual content: Fusconi, Gallo, Pagliuca, and de Vincentiis. Statistical analysis: Vitiello. Administrative, technical, and material support: Fusconi, Gallo, Pagliuca, and Pulice. Study supervision: Fusconi, Gallo, Pagliuca, and de Vincentiis.

Financial Disclosure: None reported.

Previous Presentation: This study was presented at the International Conference on Head and Neck Cancer; August 8, 2004; Washington, DC.

Acknowledgment: We thank Maria Grazia Saladino for her help in manuscript preparation.

References
1.
Dominioni  LBianchi  MDionigi  R Factors predisposing to surgical infections and identification of patients at risk. Surg Res Commun 1990;91- 7
2.
Anielski  RBarczynski  M Postoperative wound infections, I: population data and risk factors. Przegl Lek 1998;55101- 108
PubMed
3.
Gonzalez Aguilar  OPardo  HAVannelli  A  et al.  Total laryngectomy: pre- and intrasurgical variables of infection risk. Int Surg 2001;8642- 48
PubMed
4.
Velasco  EMartins  CAGoncalves  VMDias  LMThuler  LC Risk factors for surgical wound infection development in head and neck cancer surgery. Rev Hosp Clin Fac Med Sao Paulo 1995;5058- 62
PubMed
5.
Manceau  ADenis  FGarand  GGaraud  PBeutter  P Infectious complications after surgery for hypopharyngeal and laryngeal carcinomas. Ann Otolaryngol Chir Cervicofac 2003;120207- 215
PubMed
6.
Farwell  DGReilly  DFWeymuller  EA  JrGreenberg  DLStaiger  TOFutran  NA Predictors of perioperative complications in head and neck patients. Arch Otolaryngol Head Neck Surg 2002;128505- 511
PubMedArticle
7.
Girod  DAMcCulloch  TMTsue  TTWeymuller  EA  Jr Risk factors for complications in clean-contaminated head and neck surgical procedures. Head Neck 1995;177- 13
PubMedArticle
8.
Perracchia  ARoncroni  LVidi  V La Chirurgia Nell’Anziano.  Parma, Italy: Atti della Società Italiana di Chirurgia Geriatrica; 1990
9.
Dunne  JRMalone  DTracy  JKGannon  CNapolitano  LM Perioperative anemia: an independent risk factor for infection, mortality and resource utilization in surgery. J Surg Res 2002;102237- 244
PubMedArticle
10.
Brown  BMJohnson  JTWagner  RL Etiologic factors in head and neck wound infections. Laryngoscope 1987;97587- 591
PubMedArticle
11.
Ceschia  TBeorchia  AGuglielmi  R  et al.  Influence of radiotherapy on lymphocyte subpopulations. Radiol Med (Torino) 1991;81532- 536
PubMed
12.
Louagie  HVan Eijkeren  MPhilippe  JThierens  Hde Ridder  L Changes in peripheral blood lymphocyte subsets in patients undergoing radiotherapy. Int J Radiat Biol 1999;75767- 771
PubMedArticle
13.
Haley  RWCulver  DHMorgan  WMWhite  JWEmori  TGHooton  TM Identifying patients at high risk of surgical wound infection: a simple multivariate index of patient susceptibility and wound contamination. Am J Epidemiol 1985;121206- 215
PubMed
14.
Horan  TCGaynes  RPMartone  WJJarvis  WREmori  TG CDC definitions of nosocomial surgical site infections, 1992: a modification of CDC definitions of surgical wound infections. Infect Control Hosp Epidemiol 1992;13606- 608
PubMedArticle
15.
Lilienfeld  DEVlahov  DTenney  JHMcLaughlin  JS Obesity and diabetes as risk factors for postoperative wound infections after cardiac surgery. Am J Infect Control 1988;163- 6
PubMedArticle
16.
Johnson  JTMyers  ENThearle  PBSigler  BASchramm  VL  Jr Antimicrobial prophylaxis for contaminated head and neck surgery. Laryngoscope 1984;9446- 51
PubMed
17.
Li  YZhang  QWang  T The relationship between the phenotype of tumor infiltrating cells and the prognosis in laryngeal cancer. Zhonghua Er Bi Yan Hou Ke Za Zhi 1995;30209- 212
PubMed
18.
Bulbuk  GA Immunity indices of patients with locally disseminated malignant neoplasm of the head and neck. Vopr Onkol 1982;2857- 59
PubMed
19.
Dietz  AHeimlich  FDaniel  VPolarz  HWeidauer  HMaier  H Immunomodulating effects of surgical intervention in tumors of head and neck. Otolaryngol Head Neck Surg 2000;123132- 139
PubMedArticle
20.
Schantz  SPPeters  LJ Patterns of recurrence from head and neck cancer: an immunologic prospective. Cancer 1989;641232- 1237
PubMedArticle
21.
Gonzalez  FMVargas  JALopez-Cortijo  C  et al.  Prognostic significance of natural killer cell activity in patients with laryngeal carcinoma. Arch Otolaryngol Head Neck Surg 1998;124852- 856
PubMedArticle
22.
Gonzalez  FMVargas  JALacoma  F  et al.  Natural killer cell activity in laryngeal carcinoma. Arch Otolaryngol Head Neck Surg 1993;11969- 72
PubMedArticle
23.
Jecker  PVogl  KTietze  LWesthofen  M Dendritic cells, T and B lymphocytes and macrophages in supraglottic and glottic squamous epithelial carcinoma: location and correlation with prognosis of the illness. HNO 1999;47466- 471
PubMedArticle
24.
Wanebo  HJJun  MYStrong  EWOettgen  H T-cell deficiency in patients with squamous cell cancer of the head and neck. Am J Surg 1975;130445- 451
PubMedArticle
25.
Strome  MClark  JRFried  MPRodliff  SBlazar  BA T-cell subsets and natural killer cell function with squamous cell carcinoma of the head and neck. Arch Otolaryngol Head Neck Surg 1987;1131090- 1093
PubMedArticle
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