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Additional direct medical costs associated with nosocomial infections after head and neck cancer surgery: a hospital-perspective analysis
Int. J. Oral Maxillofac. Surg. 2008; 37: 135–139 doi:10.1016/j.ijom.2007.08.002, available online at http://www.sciencedirect.com
Clinical Paper
Additional direct medical costs associated with nosocomial infections after head and neck cancer surgery: a hospital§ perspective analysis
N. Penel1,2, J.-L. Lefebvre3, J. L. Cazin4, S. Clisant5, J.-C. Neu3,6, B. Dervaux7, Y. Yazdanpanah2,8 1 De´partement de Cance´rologie Ge´ne´rale, Centre Oscar Lambret, Lille, France; 2Equipe d’Accueil 2694: Sante´ Publique, Epide´miologie et Mode´lisation des Maladies Chroniques, Universite´ Lille II, Lille, France; 3 De´partement de Cance´rologie CervicoFaciale, Centre Oscar Lambret, Lille, France; 4 Pharmacie, Centre Oscar Lambret, Lille, France; 5Unite´ de Recherche Clinique, Centre Oscar Lambret, Lille, France; 6Comite´ de Lutte Contre les Infections Nosocomiales, Centre Oscar Lambret, Lille, France; 7 CRESGE, Lille, France; 8Service Universitaire des Maladies Infectieuses et du Voyageur, Hoˆpital de Tourcoing, France
N. Penel, J.-L. Lefebvre, J. L. Cazin, S. Clisant, J.-C. Neu, B. Dervaux, Y. Yazdanpanah: Additional direct medical costs associated with nosocomial infections after head and neck cancer surgery: a hospital-perspective analysis. Int. J. Oral Maxillofac. Surg. 2008; 37: 135–139. # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. The clinical impact of surgical site infections (SSI) and postoperative pneumonia (PP) after head and neck cancer surgery has been assessed in the past, but little is known about their economic impact. The present study was designed to evaluate costs related to SSI and PP after head and neck cancer surgery with opening of mucosa. The incidence of SSI and PP was measured in a prospective cohort of 261 patients who had undergone head and neck cancer surgery. The additional direct medical costs related to these infections from the hospital perspective were determined based on postoperative length of stay. The mean direct hospital costs for patients with and without SSI or PP were compared. Of the 261 patients, 81 (31%), 21 (8%) and 13 (5%) developed SSI, PP or both, respectively. The additional lengths of stay attributable to SSI, PP or both were 16, 17 and 31 days, respectively, and additional direct medical costs related to these conditions were 17,000, 19,000 and 35,000 Euros. Nosocomial infections after head and neck cancer surgery significantly increase patients’ length of stay and therefore generate additional direct medical costs. These results support the application of preventive interventions to reduce nosocomial infections in this setting.
§
Presented in part at the 3rd World Congress of the International Federation of Head and Neck Oncologic Societies, Prague, 27 June–1 July 2006. 0901-5027/020135 + 05 $30.00/0
The costs of cancer treatment are rising continuously. In the USA, the National Institutes of Health estimated the direct medical costs of cancer care for 2004 at US$ 190 billion, and the loss of productiv-
Key words: cost; head and neck cancer; hospital stay; macrocosting; nosocomial infection; surgical site infection. Accepted for publication 13 August 2007 Available online 19 November 2007
ity due to cancer morbidity and mortality at US$ 17 and 103 billion, respectively2. Inhospital expenses constitute one of the major components of the cost of cancer treatment12. The reduction of these costs
# 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
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Penel et al.
without reducing patient’s quality of care is an important goal for decision makers. Major head and neck cancer surgery is the cornerstone of curative-intent treatment, requiring highly sophisticated technology for patients whose general condition is poor, and often leading to severe postoperative complications10,14,16,19,23,27. Despite antibiotic prophylaxis, the incidence of surgical site infection (SSI) in clean contaminated head and neck cancer surgery is over 30%2,12,16,19,27. Postoperative pneumonia (PP) constitutes the second major medical problem that may occur after head and neck cancer surgery7,16,19,23,27. These postoperative nosocomial infections lead to poor cosmetic results, significant morbidity and possibly death15. They also lengthen the patient’s hospital stay and consequently generate additional cost 3,17,21. For example, nosocomial super-infections due to methicillinresistant Staphylococcus aureus cost about US$ 34,000 per patient3,21. There are no data on the costs of SSI or PP in a major head and neck cancer surgery setting. The present study was undertaken to determine the additional direct medical costs for patients with SSI and/or PP after head and neck cancer surgery with opening of mucosa, compared to the costs incurred by patients without these conditions. Patients and methods Patients
This study focused on a previously reported cohort of patients with biopsyproven squamous cell carcinoma of the upper aero-digestive tract who underwent surgery between January 1997 and December 199914,15. Patients of this cohort enrolled in the present study had undergone the following: (i) surgery with curative intent, (ii) procedures involving a neck wound communication with the oral cavity or the oropharynx, and (iii) antibiotic prophylaxis as recommended by the French Consensus Conference on prophylactic antibiotics in surgery. Between January 1997 and December 1998, all included patients received clindamycin (initially 900 i.v., and 600 mg every 8 h for 48 h), and metromycin (3 mg/kg i.v. once). Between January 1999, according to modification of the French recommendations, the patients received amoxicillin and clavulanic acid (initially 1 g i.v., and then 1 g every 8 h for 48 h)23. For all surgical procedures, the general rules of sterility were observed.
Nosocomial infection surveillance and data collection
Direct medical cost estimation
This study was conducted from the hospital perspective. Cost data considered were direct medical costs of care using a macrocosting approach based on patients’ length of stay in the hospital. First, the length of stay was determined for each patient from the first day of admission until discharge. Next, the length of stay was multiplied by the estimation of the per diem cost of hospitalisation (i.e. s1141) in the Oscar Lambret Cancer centre, which is a nonprofit comprehensive cancer centre. The per diem cost includes room/overhead expenditures, laboratory tests, mediations, procedures and the average fees for physicians and nurses. Mean length of stay and costs per patient and the corresponding standard deviation were calculated for patients with SSI or PP, and for those without. Differences between infected and non-infected patients were analysed using Wilcoxon’s rank sum test9,11,12. P < 0.05 was considered statistically significant. A sensitivity analysis was performed by varying the per diem cost of hospitalisation to assess the impact of this variable on the overall costs. Costs were expressed as 2005 s (US$ 1.00 = approximately s0.83).
All patients were examined daily by a physician for the presence of SSI and PP from the day of surgery until the date of discharge or death. For each patient were recorded: sociodemographic characteristics, surgical characteristics, the nature of the surgery undergone, the type of antibiotic prophylaxis administered and the length of stay (LOS). Only early nosocomial infections occurring during the first seven postoperative days were taken into account. Definitions of SSI as superficial incisions and deep incisional organ/space are described elsewhere, and were based on the Centres for Disease Control 1992 definitions7. The definitions for PP were adapted from those of the Centres for Disease Control and Prevention19. PP was defined as: (1) the presence of rales or dullness to percussion on physical examination of the chest, and at least one of the following: (a) new onset of purulent sputum or change in character of sputum, (b) organism cultured from blood, and/or (c) isolation of an etiologic agent from a specimen obtained by trans-tracheal aspirate, bronchial brushing or biopsy; and (2) chest radiograph that shows new or progressive infiltrate, consolidation, cavitation or pleural effusion, and at least one of the following: (a) new onset of purulent sputum or change in character of sputum, (b) organism cultured from blood, (c) isolation of an etiologic agent from a specimen obtained by trans-tracheal aspirate, bronchial brushing or biopsy, and (d) histopathologic evidence of pneumonia.
Results Nosocomial infections
Of the 261 patients enrolled in this study, 94 (36%) developed a SSI and 34 (13%) a PP. The main characteristics of patients with SSI and/or PP and those without were similar (Table 1), but there was a trend
Table 1. Characteristics of patients with or without nosocomial infections after head and neck cancer surgery Variable Age (years)
Patients without infection (145)
Patients with infection (116)
P
57 (21–80)
56 (40–83)
0.97y
Male Female
126 19
109 7
0.78z
ASA 3 ASA 1 or 2
36 109
32 84
0.61z
Laryngeal cancer Hypopharyngeal cancer Oral cavity cancer
32 34 77
21 34 60
0.42z 0.53z 0.78z
T 3–4 T 1–2
85 60
76 40
0.77z
Clinical nodal involvement Absence of nodal involvement
63 82
49 67
Duration of surgical procedure (min) Results are shown as median (range). y Wilcoxon’s rank sum test. z Fisher exact test.
198 (49–450)
232 (36–641)
0.84z 0.07y
Direct medical costs associated with nosocomial infections
137
Table 2. Length of hospital stay and direct medical costs for patients with and without nosocomial infections after head and neck cancer surgery
Without SSI and PP With SSI With PP With PP and SSI
n (%)
Length of stay* (days)
Total cost* (s)
Mean additional cost (s)
Py
145 (55) 83 (31) 21 (8)
19.74 (9.36) 35.02 (26.12) 36.81 (22.13)
22,523 (10,679) 39,957 (29,802) 42,000 (25,250)
Reference 17,434 19,476
– 6.2 108 3.5 106
12 (5)
50.75 (26.54)
57,905 (30,282)
35,382
3.5 108
SSI: surgical site infection; PP: postoperative pneumonia; SD: standard derivation. * Values are means (SD). y Wilcoxon’s rank sum test vs. reference.
towards a longer duration of procedure in patients with infection. Additional direct medical costs attributable to nosocomial infections
The mean LOS and mean direct medical cost per patient for patients with nosocomial infections and those without are shown in Table 2. Compared to non-infected patients, SSI increased the mean LOS per patient by 16 days and the mean direct medical costs of care by about 16,000 Euros (P = 6.2 108). PP increased the mean LOS by 17 days, and the mean direct medical costs of care by about 17,000 Euros (P = 3.5 106). The combination of both SSI and PP increased the mean LOS by 31 days and the mean direct medical costs of care by about 35,000 Euros (P = 3.5 108) compared to non-infected patients (Table 2). Sensitivity analysis
A sensitivity analysis was performed to assess the impact of variation in (i) per diem cost of hospitalisation and (ii) length
of stay on the additional direct medical costs of nosocomial infections. The case of SSI is illustrated in Fig. 1. Additional costs were highly sensitive to the mean per diem cost of hospitalisation, which was varied from s200 to s1500 (regular lines). The thick line represents the base case analysis at s1141 per day. Discussion
Surgery requiring advanced technology remains the gold standard in treatment with curative intent for head and neck cancer, but leads to high postoperative morbidity, due in particular to SSI and PP12,14–16,19,27. In the present study, of a cohort of 261 patients, it was estimated that SSI and PP occurred in 94 (36%) and 34 patients (13%), respectively. These estimates are consistent with those reported in other studies16,19,23,27. Secondly, the mean length of stay for patients with SSI or PP or both was compared with that for patients without these infections. The additional mean direct medical costs of care for a patient with SSI and PP were estimated at s17,000 and s19,000,
Fig. 1. Impact of variation of (i) the per diem cost of hospitalisation and (ii) length of stay on the additional direct medical costs attributable to surgical site infection (SSI). Thick line: s1141 is per diem cost of hospitalisation considered in base case analysis.
respectively, compared to those for noninfected patients. In-patient care is the main expense in the treatment of cancer2,12. Numerous previous studies have shown that SSI5,11,13 and nosocomial pneumonia18,20 are associated with a significant increase in the length of hospital stay. The savings obtained by shortening hospitalisation after initial surgical treatment may be substantial11,25. In the medical literature, additional costs attributable to SSI were estimated at US$ 800–6800, depending on the depth and severity of infection5,6. Nosocomial pneumonia has been shown to be associated with an additional cost of about $2200, including the extra cost of antibiotics which is about $990. Several studies have shown that the extra cost attributable to nosocomial infection is essentially due to the lengthening of hospital stay5,6. There are few studies concerning this issue in cancer surgery, especially for head and neck cancer. WATTERS et al. showed that antibiotic costs per patient rose by about £2400 after head and neck cancer surgery because of methicillin-resistant Staphylococcus aureus carriage26. VOSSING & ECKEL reported that in the case of SSI the length of hospital stay increased from a normal mean of 9.5– 25.5 days25. There are several limitations to the present study. First, the sample population used to estimate the cost of care consisted of patients from a hospital in Northern France, and the results may not be directly applicable to other areas in France or elsewhere. For example, the length of postoperative stay in one hospital may be closely related to that hospital’s policy for postoperative care. Other hospitals may have different approaches to postoperative management even when nosocomial infections occur11. Second, one may hypothesise that differences in length of stay and therefore costs between infected and non-infected patients are related to differences between these populations. The data shown in Table 1 indicate that the general characteristics and cancerrelated characteristics of infected and
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non-infected patients were not different. From this study, it is difficult to demonstrate whether the extra length of stay was a cause or a consequence of occurrence of nosocomial infections, especially for PP. Pneumonia occurrence has been shown to be a consequence of increased length of stay in the past13,20,24,26,27. In this study, only early nosocomial infections occurring in the seven first days were taken into account. As a result, given that the mean length of stay for patients without nosocomial infections was estimated at 19.7 days, it is more likely that infections increased length of stay than the opposite. This study highlights the fact that expenses due to nosocomial infections may have a substantial impact on the hospital budget. In France, a new hospital budget allocation was recently introduced (‘Tarification a` l’activite´’), according to which the Ministry of Health allocates funds on the basis of hospital activities in four sectors of health care: medicine, surgery, obstetrics and odontology4. Allocations are calculated according to national diagnosis-related groups. For example, a hospital may be funded for a particular head and neck cancer surgical procedure with opening of mucosa by about 16,000 Euros1. This only covers the direct medical costs of providing care to less than 50% of the patients without SSI or PP infections (the mean cost is estimated at 22,500 Euros), and to even fewer patients with these infections. In the hospital where this study was performed, approximately 85 head and neck cancer surgical procedures with opening of mucosa are performed yearly. On the basis of incidence of SSI and PP in this hospital, and of the additional direct medical costs of these infections, it may be postulated that these 85 procedures generate an extra cost of about s620,000 that is not covered by the Ministry of Health funds. Therefore, the occurrence of nosocomial infections should be taken into account when classifying procedures such as head and neck cancer surgery according to national diagnosis-related group systems. Lastly, the extra costs of nosocomial infections, which in this study are equivalent to the annual wages of nine hygiene nurses, justify the application of expensive preventive interventions. Considering these costs, further studies are warranted to reduce the occurrence of nosocomial infections and their associated costs. First, risk factors for the occurrence of nosocomial infections and in particular SSI should be better identified in patients
undergoing head and neck cancer surgery. Next, other antibiotic prophylaxis strategies than those currently recommended for SSI should be evaluated. Finally, preventative strategies, such as administration of granulocyte growth factors28 and immuno-enhancing nutritional supplements8,22, need to be better evaluated. References 1. Agence Technique de l’Information sur l’Hospitalisation Echelle Nationale des couˆts ‘2005’ (donne´es 2002–2003) http://www.atih.sante.fr/. 2. American Cancer Society. Cancer Facts and Figures 2005. Atlanta: American Cancer Society 2005. 3. Bonnema J, van Wersch AMEA, van Geel AN, Pruyn JFA, Schmitz PIM, Uyl-de Groot CA, Wiggers T. Cost of care in a randomised trial of early hospital discharge after surgery for breast cancer. Eur J Cancer 1998: 34: 2015– 2020. 4. Circulaire N8DHOS/F3/F1/2005/103 du 23 fe´vrier 2005 relative a` la campagne tarifaire 2005 pour les activite´s de me´dicine, chirurgie, obste´trique et odontologie exerce´es dans les e´tablissements de Sante´ prive´s mentionne´s aux d) et e) de l’article L 162-22-06 du code de se´curite´ sociale. 5. Coello R, Charlett A, Wilson J, Ward V, Pearson A, Borriello P. Adverse impact of surgical site infections in English hospitals. J Hosp Infect 2005: 60: 93–103. 6. Coskun D, Aytac J, Aydinli A, Bayer A. Mortality rate, length of stay and extracosts of sternal surgical infections following coronary bypass grating in a private medical centre in Turkey. J Hosp Infect 2005: 60: 176–179. 7. Culver DH, Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori T. Surgical wound infection rates by wound class, operative procedure, and patient risk index. Am J Med (Suppl. 3B): 1991: 152–157. 8. Gianotti L, Braga M, Frei A, Greiner R, Di Carlo V. Health care resources consumed to treat postoperative infections: cost saving by preoperative immunonutrition. Shock 2000: 14: 325–330. 9. Harper DR. Disease cost in a surgical ward. Br Med J 1979: 1: 647–649. 10. Johnson JT, Wagner R, Schuller D, Gluckman J, Suen J, Snyderman N. Prophylactic antibiotics for head and neck surgery with flap reconstruction. Arch Otolaryngol Head Neck Surg 1992: 118: 488–490. 11. Kambouris A. Physical, psychological, and economic advantages of accelerated discharge after surgical treatment for breast cancer. Am Surg 1996: 62: 123– 127.
12. Koopmanschap MA, Van Roijen L, Bonneux L, Barendergt JJ. Current and future costs of cancer. Eur J Cancer 1994: 30A: 60–65. 13. Morris JA, Gardner MJ. Calculating confidence intervals for relative risks (odds ratios) and standardised ratios and rates. Br Med J 1988: 296: 1313– 1316. 14. Penel N, Fournier C, Lefebvre D, Lefebvre JL. Multivariate analysis of risk factors for wound infection in head and neck squamous cell carcinoma surgery with opening of mucosa. Study of 260 surgical procedures. Oral Oncol 2005: 41: 294–303. 15. Penel N, Lefebvre D, Fournier C, Sarini J, Kara A, Lefebvre JL. Risk factors for wound infection in head and neck cancer surgery: a prospective study. Head Neck 2001: 23: 447–455. 16. Piccart M, Dor P, Klastersky J. Antimicrobial prophylaxis of infections in head and neck cancer surgery. Scand J Infect Dis 1983: 39: 92–96. 17. Plowman R, Graves N, Griffin MA, Roberst JA, Swan AV, Coockson B, Taylor L. The rate and cost of hospitalacquired infections occurring in patients admitted to selected specialities of a district general hospital in England and the national burden imposed. J Hosp Infect 2001: 47: 198–209. 18. Raphael R, Yves D, Giselle C, Magali M, Odile MC. Cancer treatment at home or in the hospital: what are the costs for French public health insurance? Findings of a comprehensive-cancer center. Health Policy 2005: 72: 141–148. 19. Ribeiro KCB, Kowalsky LP, Latorre MRDO. Perioperative complications, comorbidities and survival in oral and oropharyngeal cancer. Arch Otolaryngol Head Neck Surg 2003: 12: 219–228. 20. Rosenthal VD, Guzman S, Migone O, Safdar N. The attributable cost and length of stay because of nosocomial pneumonia in intensive care units in 3 hospitals in Argentina: a prospective, matched analysis. Am J Infect Control 2005: 33: 157–161. 21. Rubin RJ, Harrington CA, Poon A, Dietrich K, Greene JA, Moiduddin A. The economic impact of Staphylococcus aureus infection in New York hospitals. Emerg Infect Dis 1999: 5: 9–17. 22. Snyderman CH, Kachman K, Molseed L, Wagner R, D’Amico F, Bumpous J, Rueger R. Reduced postoperative infections with an immune-enhancing nutritional supplement. Laryngoscope 1999: 109: 915–921. 23. Socie´te´ Franc¸aise d’Anesthe´sie-Re´animation. Recommandations pour la pratique de l’antibioprophylaxie en chirurgie. Actualisation 1999. Coordonateur Pr C Martin Presse Med 2001; 30: 794–802. 24. Tibi-Levy Y, de Pouvourville G, Rozenholc Y, Goursot G, Clergue
Direct medical costs associated with nosocomial infections F, De´le´montey B, Feiss P, Laxenaire MC, Marty J, Be´resniak A. Evaluation of benefits related to reduced length of stays in postanesthesia care units. Int J Technol Assess Health Care 1998: 14: 172–179. 25. Vossing M, Eckel HE. Nosocomial infections in head and neck surgery. HNO 1996: 44: 61–67 [in German]. 26. Watters K, O’Dwyer TP, Rowley J. Cost and morbidity of MRSA in head and neck cancer patients: what are the con-
sequences? J Laryngol Otol 2004: 118: 694–699. 27. Weber RS, Hankins P, Rosenbaum B, Raad I. Nonwound infections following head and neck oncologic surgery. Laryngoscope 1993: 103: 22–27. 28. Wenisch C, Wergartner T, Saisler M, Patruta S. Effect of preoperative prophylaxis with filgrastim in cancer neck dissection (Abstract meeting). J Antimicrob Chemother 1999: 44(Suppl. A):S161.
Address: Penel Nicolas De´partement de Cance´rologie Ge´ne´rale Centre Oscar Lambret 3 rue F Combemale 59020 Lille France Tel: +33 3 20 29 59 20 Fax: +33 3 20 29 59 63 E-mail: [email protected]
139
Clinical Paper
Additional direct medical costs associated with nosocomial infections after head and neck cancer surgery: a hospital§ perspective analysis
N. Penel1,2, J.-L. Lefebvre3, J. L. Cazin4, S. Clisant5, J.-C. Neu3,6, B. Dervaux7, Y. Yazdanpanah2,8 1 De´partement de Cance´rologie Ge´ne´rale, Centre Oscar Lambret, Lille, France; 2Equipe d’Accueil 2694: Sante´ Publique, Epide´miologie et Mode´lisation des Maladies Chroniques, Universite´ Lille II, Lille, France; 3 De´partement de Cance´rologie CervicoFaciale, Centre Oscar Lambret, Lille, France; 4 Pharmacie, Centre Oscar Lambret, Lille, France; 5Unite´ de Recherche Clinique, Centre Oscar Lambret, Lille, France; 6Comite´ de Lutte Contre les Infections Nosocomiales, Centre Oscar Lambret, Lille, France; 7 CRESGE, Lille, France; 8Service Universitaire des Maladies Infectieuses et du Voyageur, Hoˆpital de Tourcoing, France
N. Penel, J.-L. Lefebvre, J. L. Cazin, S. Clisant, J.-C. Neu, B. Dervaux, Y. Yazdanpanah: Additional direct medical costs associated with nosocomial infections after head and neck cancer surgery: a hospital-perspective analysis. Int. J. Oral Maxillofac. Surg. 2008; 37: 135–139. # 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved. Abstract. The clinical impact of surgical site infections (SSI) and postoperative pneumonia (PP) after head and neck cancer surgery has been assessed in the past, but little is known about their economic impact. The present study was designed to evaluate costs related to SSI and PP after head and neck cancer surgery with opening of mucosa. The incidence of SSI and PP was measured in a prospective cohort of 261 patients who had undergone head and neck cancer surgery. The additional direct medical costs related to these infections from the hospital perspective were determined based on postoperative length of stay. The mean direct hospital costs for patients with and without SSI or PP were compared. Of the 261 patients, 81 (31%), 21 (8%) and 13 (5%) developed SSI, PP or both, respectively. The additional lengths of stay attributable to SSI, PP or both were 16, 17 and 31 days, respectively, and additional direct medical costs related to these conditions were 17,000, 19,000 and 35,000 Euros. Nosocomial infections after head and neck cancer surgery significantly increase patients’ length of stay and therefore generate additional direct medical costs. These results support the application of preventive interventions to reduce nosocomial infections in this setting.
§
Presented in part at the 3rd World Congress of the International Federation of Head and Neck Oncologic Societies, Prague, 27 June–1 July 2006. 0901-5027/020135 + 05 $30.00/0
The costs of cancer treatment are rising continuously. In the USA, the National Institutes of Health estimated the direct medical costs of cancer care for 2004 at US$ 190 billion, and the loss of productiv-
Key words: cost; head and neck cancer; hospital stay; macrocosting; nosocomial infection; surgical site infection. Accepted for publication 13 August 2007 Available online 19 November 2007
ity due to cancer morbidity and mortality at US$ 17 and 103 billion, respectively2. Inhospital expenses constitute one of the major components of the cost of cancer treatment12. The reduction of these costs
# 2007 International Association of Oral and Maxillofacial Surgeons. Published by Elsevier Ltd. All rights reserved.
136
Penel et al.
without reducing patient’s quality of care is an important goal for decision makers. Major head and neck cancer surgery is the cornerstone of curative-intent treatment, requiring highly sophisticated technology for patients whose general condition is poor, and often leading to severe postoperative complications10,14,16,19,23,27. Despite antibiotic prophylaxis, the incidence of surgical site infection (SSI) in clean contaminated head and neck cancer surgery is over 30%2,12,16,19,27. Postoperative pneumonia (PP) constitutes the second major medical problem that may occur after head and neck cancer surgery7,16,19,23,27. These postoperative nosocomial infections lead to poor cosmetic results, significant morbidity and possibly death15. They also lengthen the patient’s hospital stay and consequently generate additional cost 3,17,21. For example, nosocomial super-infections due to methicillinresistant Staphylococcus aureus cost about US$ 34,000 per patient3,21. There are no data on the costs of SSI or PP in a major head and neck cancer surgery setting. The present study was undertaken to determine the additional direct medical costs for patients with SSI and/or PP after head and neck cancer surgery with opening of mucosa, compared to the costs incurred by patients without these conditions. Patients and methods Patients
This study focused on a previously reported cohort of patients with biopsyproven squamous cell carcinoma of the upper aero-digestive tract who underwent surgery between January 1997 and December 199914,15. Patients of this cohort enrolled in the present study had undergone the following: (i) surgery with curative intent, (ii) procedures involving a neck wound communication with the oral cavity or the oropharynx, and (iii) antibiotic prophylaxis as recommended by the French Consensus Conference on prophylactic antibiotics in surgery. Between January 1997 and December 1998, all included patients received clindamycin (initially 900 i.v., and 600 mg every 8 h for 48 h), and metromycin (3 mg/kg i.v. once). Between January 1999, according to modification of the French recommendations, the patients received amoxicillin and clavulanic acid (initially 1 g i.v., and then 1 g every 8 h for 48 h)23. For all surgical procedures, the general rules of sterility were observed.
Nosocomial infection surveillance and data collection
Direct medical cost estimation
This study was conducted from the hospital perspective. Cost data considered were direct medical costs of care using a macrocosting approach based on patients’ length of stay in the hospital. First, the length of stay was determined for each patient from the first day of admission until discharge. Next, the length of stay was multiplied by the estimation of the per diem cost of hospitalisation (i.e. s1141) in the Oscar Lambret Cancer centre, which is a nonprofit comprehensive cancer centre. The per diem cost includes room/overhead expenditures, laboratory tests, mediations, procedures and the average fees for physicians and nurses. Mean length of stay and costs per patient and the corresponding standard deviation were calculated for patients with SSI or PP, and for those without. Differences between infected and non-infected patients were analysed using Wilcoxon’s rank sum test9,11,12. P < 0.05 was considered statistically significant. A sensitivity analysis was performed by varying the per diem cost of hospitalisation to assess the impact of this variable on the overall costs. Costs were expressed as 2005 s (US$ 1.00 = approximately s0.83).
All patients were examined daily by a physician for the presence of SSI and PP from the day of surgery until the date of discharge or death. For each patient were recorded: sociodemographic characteristics, surgical characteristics, the nature of the surgery undergone, the type of antibiotic prophylaxis administered and the length of stay (LOS). Only early nosocomial infections occurring during the first seven postoperative days were taken into account. Definitions of SSI as superficial incisions and deep incisional organ/space are described elsewhere, and were based on the Centres for Disease Control 1992 definitions7. The definitions for PP were adapted from those of the Centres for Disease Control and Prevention19. PP was defined as: (1) the presence of rales or dullness to percussion on physical examination of the chest, and at least one of the following: (a) new onset of purulent sputum or change in character of sputum, (b) organism cultured from blood, and/or (c) isolation of an etiologic agent from a specimen obtained by trans-tracheal aspirate, bronchial brushing or biopsy; and (2) chest radiograph that shows new or progressive infiltrate, consolidation, cavitation or pleural effusion, and at least one of the following: (a) new onset of purulent sputum or change in character of sputum, (b) organism cultured from blood, (c) isolation of an etiologic agent from a specimen obtained by trans-tracheal aspirate, bronchial brushing or biopsy, and (d) histopathologic evidence of pneumonia.
Results Nosocomial infections
Of the 261 patients enrolled in this study, 94 (36%) developed a SSI and 34 (13%) a PP. The main characteristics of patients with SSI and/or PP and those without were similar (Table 1), but there was a trend
Table 1. Characteristics of patients with or without nosocomial infections after head and neck cancer surgery Variable Age (years)
Patients without infection (145)
Patients with infection (116)
P
57 (21–80)
56 (40–83)
0.97y
Male Female
126 19
109 7
0.78z
ASA 3 ASA 1 or 2
36 109
32 84
0.61z
Laryngeal cancer Hypopharyngeal cancer Oral cavity cancer
32 34 77
21 34 60
0.42z 0.53z 0.78z
T 3–4 T 1–2
85 60
76 40
0.77z
Clinical nodal involvement Absence of nodal involvement
63 82
49 67
Duration of surgical procedure (min) Results are shown as median (range). y Wilcoxon’s rank sum test. z Fisher exact test.
198 (49–450)
232 (36–641)
0.84z 0.07y
Direct medical costs associated with nosocomial infections
137
Table 2. Length of hospital stay and direct medical costs for patients with and without nosocomial infections after head and neck cancer surgery
Without SSI and PP With SSI With PP With PP and SSI
n (%)
Length of stay* (days)
Total cost* (s)
Mean additional cost (s)
Py
145 (55) 83 (31) 21 (8)
19.74 (9.36) 35.02 (26.12) 36.81 (22.13)
22,523 (10,679) 39,957 (29,802) 42,000 (25,250)
Reference 17,434 19,476
– 6.2 108 3.5 106
12 (5)
50.75 (26.54)
57,905 (30,282)
35,382
3.5 108
SSI: surgical site infection; PP: postoperative pneumonia; SD: standard derivation. * Values are means (SD). y Wilcoxon’s rank sum test vs. reference.
towards a longer duration of procedure in patients with infection. Additional direct medical costs attributable to nosocomial infections
The mean LOS and mean direct medical cost per patient for patients with nosocomial infections and those without are shown in Table 2. Compared to non-infected patients, SSI increased the mean LOS per patient by 16 days and the mean direct medical costs of care by about 16,000 Euros (P = 6.2 108). PP increased the mean LOS by 17 days, and the mean direct medical costs of care by about 17,000 Euros (P = 3.5 106). The combination of both SSI and PP increased the mean LOS by 31 days and the mean direct medical costs of care by about 35,000 Euros (P = 3.5 108) compared to non-infected patients (Table 2). Sensitivity analysis
A sensitivity analysis was performed to assess the impact of variation in (i) per diem cost of hospitalisation and (ii) length
of stay on the additional direct medical costs of nosocomial infections. The case of SSI is illustrated in Fig. 1. Additional costs were highly sensitive to the mean per diem cost of hospitalisation, which was varied from s200 to s1500 (regular lines). The thick line represents the base case analysis at s1141 per day. Discussion
Surgery requiring advanced technology remains the gold standard in treatment with curative intent for head and neck cancer, but leads to high postoperative morbidity, due in particular to SSI and PP12,14–16,19,27. In the present study, of a cohort of 261 patients, it was estimated that SSI and PP occurred in 94 (36%) and 34 patients (13%), respectively. These estimates are consistent with those reported in other studies16,19,23,27. Secondly, the mean length of stay for patients with SSI or PP or both was compared with that for patients without these infections. The additional mean direct medical costs of care for a patient with SSI and PP were estimated at s17,000 and s19,000,
Fig. 1. Impact of variation of (i) the per diem cost of hospitalisation and (ii) length of stay on the additional direct medical costs attributable to surgical site infection (SSI). Thick line: s1141 is per diem cost of hospitalisation considered in base case analysis.
respectively, compared to those for noninfected patients. In-patient care is the main expense in the treatment of cancer2,12. Numerous previous studies have shown that SSI5,11,13 and nosocomial pneumonia18,20 are associated with a significant increase in the length of hospital stay. The savings obtained by shortening hospitalisation after initial surgical treatment may be substantial11,25. In the medical literature, additional costs attributable to SSI were estimated at US$ 800–6800, depending on the depth and severity of infection5,6. Nosocomial pneumonia has been shown to be associated with an additional cost of about $2200, including the extra cost of antibiotics which is about $990. Several studies have shown that the extra cost attributable to nosocomial infection is essentially due to the lengthening of hospital stay5,6. There are few studies concerning this issue in cancer surgery, especially for head and neck cancer. WATTERS et al. showed that antibiotic costs per patient rose by about £2400 after head and neck cancer surgery because of methicillin-resistant Staphylococcus aureus carriage26. VOSSING & ECKEL reported that in the case of SSI the length of hospital stay increased from a normal mean of 9.5– 25.5 days25. There are several limitations to the present study. First, the sample population used to estimate the cost of care consisted of patients from a hospital in Northern France, and the results may not be directly applicable to other areas in France or elsewhere. For example, the length of postoperative stay in one hospital may be closely related to that hospital’s policy for postoperative care. Other hospitals may have different approaches to postoperative management even when nosocomial infections occur11. Second, one may hypothesise that differences in length of stay and therefore costs between infected and non-infected patients are related to differences between these populations. The data shown in Table 1 indicate that the general characteristics and cancerrelated characteristics of infected and
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non-infected patients were not different. From this study, it is difficult to demonstrate whether the extra length of stay was a cause or a consequence of occurrence of nosocomial infections, especially for PP. Pneumonia occurrence has been shown to be a consequence of increased length of stay in the past13,20,24,26,27. In this study, only early nosocomial infections occurring in the seven first days were taken into account. As a result, given that the mean length of stay for patients without nosocomial infections was estimated at 19.7 days, it is more likely that infections increased length of stay than the opposite. This study highlights the fact that expenses due to nosocomial infections may have a substantial impact on the hospital budget. In France, a new hospital budget allocation was recently introduced (‘Tarification a` l’activite´’), according to which the Ministry of Health allocates funds on the basis of hospital activities in four sectors of health care: medicine, surgery, obstetrics and odontology4. Allocations are calculated according to national diagnosis-related groups. For example, a hospital may be funded for a particular head and neck cancer surgical procedure with opening of mucosa by about 16,000 Euros1. This only covers the direct medical costs of providing care to less than 50% of the patients without SSI or PP infections (the mean cost is estimated at 22,500 Euros), and to even fewer patients with these infections. In the hospital where this study was performed, approximately 85 head and neck cancer surgical procedures with opening of mucosa are performed yearly. On the basis of incidence of SSI and PP in this hospital, and of the additional direct medical costs of these infections, it may be postulated that these 85 procedures generate an extra cost of about s620,000 that is not covered by the Ministry of Health funds. Therefore, the occurrence of nosocomial infections should be taken into account when classifying procedures such as head and neck cancer surgery according to national diagnosis-related group systems. Lastly, the extra costs of nosocomial infections, which in this study are equivalent to the annual wages of nine hygiene nurses, justify the application of expensive preventive interventions. Considering these costs, further studies are warranted to reduce the occurrence of nosocomial infections and their associated costs. First, risk factors for the occurrence of nosocomial infections and in particular SSI should be better identified in patients
undergoing head and neck cancer surgery. Next, other antibiotic prophylaxis strategies than those currently recommended for SSI should be evaluated. Finally, preventative strategies, such as administration of granulocyte growth factors28 and immuno-enhancing nutritional supplements8,22, need to be better evaluated. References 1. Agence Technique de l’Information sur l’Hospitalisation Echelle Nationale des couˆts ‘2005’ (donne´es 2002–2003) http://www.atih.sante.fr/. 2. American Cancer Society. Cancer Facts and Figures 2005. Atlanta: American Cancer Society 2005. 3. Bonnema J, van Wersch AMEA, van Geel AN, Pruyn JFA, Schmitz PIM, Uyl-de Groot CA, Wiggers T. Cost of care in a randomised trial of early hospital discharge after surgery for breast cancer. Eur J Cancer 1998: 34: 2015– 2020. 4. Circulaire N8DHOS/F3/F1/2005/103 du 23 fe´vrier 2005 relative a` la campagne tarifaire 2005 pour les activite´s de me´dicine, chirurgie, obste´trique et odontologie exerce´es dans les e´tablissements de Sante´ prive´s mentionne´s aux d) et e) de l’article L 162-22-06 du code de se´curite´ sociale. 5. Coello R, Charlett A, Wilson J, Ward V, Pearson A, Borriello P. Adverse impact of surgical site infections in English hospitals. J Hosp Infect 2005: 60: 93–103. 6. Coskun D, Aytac J, Aydinli A, Bayer A. Mortality rate, length of stay and extracosts of sternal surgical infections following coronary bypass grating in a private medical centre in Turkey. J Hosp Infect 2005: 60: 176–179. 7. Culver DH, Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori T. Surgical wound infection rates by wound class, operative procedure, and patient risk index. Am J Med (Suppl. 3B): 1991: 152–157. 8. Gianotti L, Braga M, Frei A, Greiner R, Di Carlo V. Health care resources consumed to treat postoperative infections: cost saving by preoperative immunonutrition. Shock 2000: 14: 325–330. 9. Harper DR. Disease cost in a surgical ward. Br Med J 1979: 1: 647–649. 10. Johnson JT, Wagner R, Schuller D, Gluckman J, Suen J, Snyderman N. Prophylactic antibiotics for head and neck surgery with flap reconstruction. Arch Otolaryngol Head Neck Surg 1992: 118: 488–490. 11. Kambouris A. Physical, psychological, and economic advantages of accelerated discharge after surgical treatment for breast cancer. Am Surg 1996: 62: 123– 127.
12. Koopmanschap MA, Van Roijen L, Bonneux L, Barendergt JJ. Current and future costs of cancer. Eur J Cancer 1994: 30A: 60–65. 13. Morris JA, Gardner MJ. Calculating confidence intervals for relative risks (odds ratios) and standardised ratios and rates. Br Med J 1988: 296: 1313– 1316. 14. Penel N, Fournier C, Lefebvre D, Lefebvre JL. Multivariate analysis of risk factors for wound infection in head and neck squamous cell carcinoma surgery with opening of mucosa. Study of 260 surgical procedures. Oral Oncol 2005: 41: 294–303. 15. Penel N, Lefebvre D, Fournier C, Sarini J, Kara A, Lefebvre JL. Risk factors for wound infection in head and neck cancer surgery: a prospective study. Head Neck 2001: 23: 447–455. 16. Piccart M, Dor P, Klastersky J. Antimicrobial prophylaxis of infections in head and neck cancer surgery. Scand J Infect Dis 1983: 39: 92–96. 17. Plowman R, Graves N, Griffin MA, Roberst JA, Swan AV, Coockson B, Taylor L. The rate and cost of hospitalacquired infections occurring in patients admitted to selected specialities of a district general hospital in England and the national burden imposed. J Hosp Infect 2001: 47: 198–209. 18. Raphael R, Yves D, Giselle C, Magali M, Odile MC. Cancer treatment at home or in the hospital: what are the costs for French public health insurance? Findings of a comprehensive-cancer center. Health Policy 2005: 72: 141–148. 19. Ribeiro KCB, Kowalsky LP, Latorre MRDO. Perioperative complications, comorbidities and survival in oral and oropharyngeal cancer. Arch Otolaryngol Head Neck Surg 2003: 12: 219–228. 20. Rosenthal VD, Guzman S, Migone O, Safdar N. The attributable cost and length of stay because of nosocomial pneumonia in intensive care units in 3 hospitals in Argentina: a prospective, matched analysis. Am J Infect Control 2005: 33: 157–161. 21. Rubin RJ, Harrington CA, Poon A, Dietrich K, Greene JA, Moiduddin A. The economic impact of Staphylococcus aureus infection in New York hospitals. Emerg Infect Dis 1999: 5: 9–17. 22. Snyderman CH, Kachman K, Molseed L, Wagner R, D’Amico F, Bumpous J, Rueger R. Reduced postoperative infections with an immune-enhancing nutritional supplement. Laryngoscope 1999: 109: 915–921. 23. Socie´te´ Franc¸aise d’Anesthe´sie-Re´animation. Recommandations pour la pratique de l’antibioprophylaxie en chirurgie. Actualisation 1999. Coordonateur Pr C Martin Presse Med 2001; 30: 794–802. 24. Tibi-Levy Y, de Pouvourville G, Rozenholc Y, Goursot G, Clergue
Direct medical costs associated with nosocomial infections F, De´le´montey B, Feiss P, Laxenaire MC, Marty J, Be´resniak A. Evaluation of benefits related to reduced length of stays in postanesthesia care units. Int J Technol Assess Health Care 1998: 14: 172–179. 25. Vossing M, Eckel HE. Nosocomial infections in head and neck surgery. HNO 1996: 44: 61–67 [in German]. 26. Watters K, O’Dwyer TP, Rowley J. Cost and morbidity of MRSA in head and neck cancer patients: what are the con-
sequences? J Laryngol Otol 2004: 118: 694–699. 27. Weber RS, Hankins P, Rosenbaum B, Raad I. Nonwound infections following head and neck oncologic surgery. Laryngoscope 1993: 103: 22–27. 28. Wenisch C, Wergartner T, Saisler M, Patruta S. Effect of preoperative prophylaxis with filgrastim in cancer neck dissection (Abstract meeting). J Antimicrob Chemother 1999: 44(Suppl. A):S161.
Address: Penel Nicolas De´partement de Cance´rologie Ge´ne´rale Centre Oscar Lambret 3 rue F Combemale 59020 Lille France Tel: +33 3 20 29 59 20 Fax: +33 3 20 29 59 63 E-mail: [email protected]
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