Nosocomial infections in pediatric patients: A prevalence study in Spanish hospitals

Nosocomial infections atientse A prevalence Spanish hospitals

in pediatric study in

M. Campins, MDa

I.. Armada~~, MDa EPltdE Working Group Barcelona,

Madrid,

Salamanca,

and Mhlaga,

Spain

Background: The magnitude of the problem of nosocomial infection in children has never been studied in Spain. Methods: In 1990, a nationwide cross-sectional study was conducted to determine the prevalence of nosocomial infection and associated risk factors. Results: Among 38,489 patients surveyed, 4081 were pediatric patients. Three hundred forty-five patients (8.4%) had active nosocomial infection at the time of the survey. units (22%) showed Pediatric intensive care units (29.7%), hematology (23%), and special the highest rates. Infections were most common in patients younger than 1 year (prevalence, 12.3%). Frequencies of nosocomial infection by site were as follows: bloodstream, 22.1%; urinary tract, 13.1%; lower respiratory tract, 12.3%; postoperative wound, 8%; gastrointestinal tract, 7.6%; skin, 6.5%; eye, 5.8%; and others 24.6%. The factors most closely associated with a higher prevalence of nosocomial infection in pediatrics were as follows: age younger than 1 year, surgery, moderate and severe baseline risk, number of diagnoses, and all categories of extrinsic risk factors. The most frequent etiologic agents were gram-positive bacteria (45.8%). Conc2ttsians: Although the overall prevalence is at an acceptable level, future efforts should be focused on developing more effective prevention strategies in specific areas. (AJIC AM J INFECT CONTROL 1993;21:58-63.)

Nosocomial infection (NI) is a major concern in pediatric patients. The Centers for Disease Control identified nosocomial infections as one of several major potentially preventable health problems targeted for special intervention in the 1980s.’ From the Servei de Medicina Preventiva,a and Servei de Pediatria,b Vail d’Hebron Hospital, Universitat Autbnoma de Barcelona, Barceiona, Sant Joan de Deu Hospital,c Barcelona, Ramon y Cajal Hospital,d Madrid, La Paz Hospital,e Madrid, Clinico Universitario Hospital,’ Salamanca, and Carlos Haya Hospital,g Malaga, Spain, Correspondence to M. Campins, MD, Servei de Medicina Preventiva, Ciutat Sanitaria Vail d’Hebron, 08035~Barcelona, Spain. 0 1993 by the Association 0196-6553193

$0.100

for Practitioners + 0.10

17/46/42386

in Infection

Control,

Inc.

In general the magnitude of the pro pediatric hospitals remains poorly defined. Few systematic studies have provided rates in childrenze7 and much information is based on reports of disease outbreaks. Infection In 1984 the National Nssocomial Surveillance Study (NNIS) reported incidence rates ranging from 1.66% at large teaching hospitals to 0.12% at nonteaching hospitals.’ ‘These rates are lower than the 5% to 7% currently observed within university-affiliated pediatric hospitals.2* 5-8 Rates are influenced by the age of the patient, duration of hospitalization, anatomic site, and type of patient care setting.’ Surveillance and knowledge of the risk factors for such

JIQ: Campins et al.

Volljme 21, Number 2

infections are essential for developing control strategies, A nationwide, cross-sectional survey was conpain (EPINE- 1990 study).‘O We report in this article the results obtained in pediatric patients.

The survey was conducted in 126 acute care hospitals during a 2-week period in May 1990. This task was performed at each center by the infection surveillance and control team. One hundred thirteen hospitals contributed pediatric patients and were eligible for overall assessment. The hospitals were divided into three categories: small hospitals (fewer than 200 beds), 50 centers (40.7%); medium-sized hospitals (between 200 and 500 beds), 46 centers (37.4%); and large hospitals (more than 500 beds), 27 centers (2 1.9%). The pediatric services were classified into 10 areas: neonatal units (including only neonatal intensive care areas), hematology units, oncology units, nephrology and kidney transplantation units, infant medicine units (infants and toddlers), general medicine units (preschool children and schoolchildren), pediatric intensive care units (PICUs), general surgical units, surgical specialty units, and special units (burn and isolation areas).

All inpatients of the centers participating in the study were studied. Among the 38,489 patients included, 408 1 were younger than 15 years and thus considered pediatric patients. The patient population included 113 1 neonates ( 5 28 days of age), 895 infants and toddlers (28 days to 2 years), 577 preschoolers (2 to 4 years), 1160 children (5 to 12 years), and 287 teenagers (between 13 and 15 years). Data collection ata collection was based on clinical records and information provided by physicians and nurses in charge of the patients. The study protocol” was widely tested in previous surveys,‘O, ‘* and all its variables were explicitly defined. The Centers for Disease Control criteria13 were used for diagnosing infections. The date of onset of the infection was recorded (the day on which the symptoms appeared or antibiotic therapy was begun). Microbiologic cultures and serologic tests were used to determine the cause of infections. Intrinsic risk factors studied included the follow-

ing: coma, renal failure, diabetes mellitus, neoplasia, immunodeficiency, neutropenia, cirrhosis, hypoalbuminaemia, high-risk neonates, and neonates born to intravenous drug a Extrinsic risk factors, or those a hospitalization, included the following: urinary catheterization, peripheral or central vascular catheterization, parenteral nutrition, tracheostomy, mechanical ventilation, and immunosuppressive therapy. Information was also compiled on the surgical operations performed, including type, contamination degree, and duration. aseline risk in relation to clinical prognosis was classified as severe, moderate, or mild, as follows: severe, survival less than a year; moderate, life expectancy between 1 and 5 rs; and mild, the agnoses was also rest of the cases. The number recorded for each patient to evaluate the complexity of the baseline situation and the multisystemic extension of disease. Statistical

analyses

The prevalence of NI, calculated by obtaining the ratio between the number of clinically active NIs and the total number of patients studied, was expressed as a percentage. The prevalence of infected patients is the percentage of patients with active infections in relation to the total number of patients studied. Confidence intervals (CIs) and hypothesis testing were calculated on the basis of prevalence of infected patients, The crude association between a risk factor an the infection was estimated by the odds ratio (OR) w according to the Cornfield method.14 between patients with or without NI variables were estimated for statistical signincance by the x2 test or when necessary by Fisher’s Exact Test, as well as by analysis of trend. For continuous variables the Man-~~litney l.Jtest was used. In all tests the null hypothesis was rejected at the significance level ofp < 0.05. Joint study of the associated risk factors involved in the development of NI was conducted by means of a multiple logistic regression model RESULTS The number of NIs detected was 409 in 345 patients. The overall prevalences of infected patients were 10.02% and tively. Among patients with NI, 84% had a single infection, 13% had two infections, and 3% had three or more. There were no associations between the prevalence of hospital-acquired infection and hospital size (p = 0.47). The highest

Campins et al. Table

I.

April IQ93

Prevalence

of NI by services Patients Infections (n)

Wardiretvice

n

%

PICU Hematology units Special units Oncology units Neonatal units Nephrology units infant medicine units Surgical specialty units General surgical units General medicine units Other units*

53 6 4 12 184 1 49 5 35 21 39

778 26 18 64 1103 9 591 68 606 862 556

TOTAL

zs

4081100.00

*Pediatric mixed wards specialties. tAverage for all units.

in

small

general

NI prevalence w

4.36 0.64 0.44 1.57 27.03 0.22 14.48 1.67 14.85 21.12 13.62

hospitals

29.78 23.08 22.22 la.75 16.68 11.11 a.29 7.35 5.78 2.44 7.01

Table 2. Age-specific Nls by site

Site Bacteremia Urinary tract Respiratory tract Surgical wound Gastrointestinal tract Skin Others All sites

prevalence

of principal

~1 year W

l-4 fears 6)

4.07 2.04 1.51 0.52 1.34

0.68 0.57 1.24 0.45 0.45

0.55 0.41 0.68 G.55 -

0.84 1.26 0.84 2.09 0.42

0.76 4.94 15.18

0.34 2.04 5.77

0.55 2.33 5.07

0.70 1.39 7.53

years (W

10.02t without

pediatric

prevalences of NI by service occurred in PICUs (29.7%), hematology units (23%), and special units (22%) (Table 1). The average age ( + SD) of infected patients was 2.79 years +- 4.40 and 4.05 years -+ 4.52 for cases without infection, with the difference being statistically significant (p = 0.0001). The highest prevalence of NI occurred in patients younger than 1 year (12.3%), d ecreased in children aged 1 to 4 years (5.4%)‘ and was lowest in those between 5 and 9 years (4.2%). The age-specific prevalences of major NI by site are shown in Table 2. The prevalence of bacteremia was six times higher in ehildren younger than 1 year than in the other age groups. The most frequent type of NI was bacteremia (22.1%), followed by urinary tract infection (13.1%), lower respiratory tract infection (12.3%), surgical wound infection (8%), gastrointestinal tract infection (7.6%), skin infection (6.5%), and eye infection (5.8%); other types accounted for the remaining 24.6%. High prevalences of bacteremia were found in PICUs (7.8%) and in neonatal services (5.7%)‘ accounting for 15.1% and 71.6% of the total, respectively. Urinary tract infections were detected predominantly in hematology units (3.8%).and PICUs (2.2%). Lower respiratory tract infections were the most prevalent NI in PICUs (7.8%) and in oncology units (7.8%). Surgery was performed in 877 patients. One hundred of these (11.4%) acquired NI. Of these, 3 1 patients (3.5%) had surgical wound infection. Abdominal surgery was the most frequently per(308 operations), but the highest prevalence of surgical wound infections (7.6%) was found in patients who underwent thoracic and

thoracoabdominal surgery. Abdominal, extremity, and cranial surgery showed surgical wound infection prevalences of 5.1%, 3. I%, and l%, respectively. The overall surgical wound infections prevalence after clean surgery was 3.4% (405 operations); after dirty surgery it was 6.7% (59 operations). The mean preoperative stay was 7.8 1 24.5 days. The relationship be&veen. the length of preoperative stay and the prevalence of surgical wound infection was not statistically significant (p = 0.50). The baseline risk was strongly associated with the development of NI, showing a significant trend (p < 0.00001). Intrinsic risk factors were present in 1271 patients (3 1%); among these, high-risk neonates (19.3%), hypoalbuminaemia (3.6%), and neoplasia (3.5%) were the most fre associated with higher proportions of patients with NI were neutropenia (25.3%), hypoatbuminemia (22.5%), and immunodeficiency (20.9%); the ORs were 3.82 (95% Cl, 2.09 to 6.90), 3.37 (95% CI, 2.19 to 5.17) and 3.02 (95% CI, 1.92 to 4.75), respectively. The percentage of patients exposed to extrinsic risk factors was 53.1%; 40% had peripheral vascular catheters, 5.6% had urinary catheter, 4.7% had central catheters, 5.3% were receiving mechanical ventilation, 5% were receiving immunosuppressive therapy, 4.4% receiving parenteral nutrition, and 0.5% h tracheostomies. All these extrinsic risk factors were significantly associated with the prevalence of patients with NI, particularly parenteral nutrition (33.1%; OR, 6.27; 95% CI, 4.43 to 8.87), tracheostomy (3 1.8%; OR, 5.14; 95% CI 1.89 to ?13.52), and central catheter (25%; OR, 4.02; 95% CI, 2.79 to 5.79). The prevalence of patients with Nl increases significantly with the number of intrinsic and extrinsic risk factors (p < 0.00001). As shown in Table 3, the following associated

Volume

21,

Number

2

Table

4. Principal cases of NI

Table 3. Association of NI with risk factors studied, multiple logistic regression model Associated factors*

pathogens

identified

Organism OR

95% Cl

Bacteria Gram-positive 2.51 0.76 1.25

Male sex

1.04

Surgery Baseline

2.28

1.67-3.76 0.43-I .32 0.76-2.06 0.79-l .37 1.65-3.14

Moderate Severe Diagnoses (number)

0.0001 0.3339 0.3734 0.7602 0.0001

1.96 2.07

1.38-2.79 1.28-3.35

0.0002 0.0028

2 3 24 Intrinsic 1-2 r3 Extrinsic 1-2 23

3.35 3.72 6.28

2.45-4.58 2.35-5.89 3.74-10.53

0.0001

1.19 2.76

0.87-l .63 I .38-5.49

0.2692 0.0038

1.98 3.12

1.48-2.64

0.0001 0.0003

risk

risk factors

0.0001 0.0001

(number)

risk factors

1.67-5.83

i-3

%

127 42 34 18 15 6 6 4 6

45.8 15.2 12.3 6.5 5.4 2.2 2.2 1.4 0.7

114 44 26 13 12

41 .I 15.9 9.4 4.7 4.4 2.5 I.4 1.1 0.7 1.1

P

Age 21 years 5-9 years 1 O-1 4 years

in

*Comparison categories: Age between 1 and 4 years, female sex, absence of surgical procedures, low baseline risk, only one diagnosis, and absence of intrinsic or extrinsic risk factors.

Coagulase-negative

Staphylococcus aureus Staphylococcus sp. Enterococcus sp. Streptococcus pneumoniae Streptococcus sp. Streptococcus agaiactiae Other streptococci

Gram-negative Escherichia co/i Pseudomonas sp. Klebsiella sp. Enterobacfer sp. Haemophilus sp. Profeus mirabilis Serratia marcescens Acinetobacter calcoaceticus

Other gram-negative Anaerobes Bacillus sp. Bacteroides sp. Clostridium

factors were statistically significant in the overall logistic model for NI: age younger than 1 year, surgical procedure, moderate and severe baseline risk, diagnosis number, three or more intrinsic risk factors, and all categories of extrinsic risk factor. Microbiologic or serologic study was performed in 80.2% of NI cases, with a pathogen isolated in 5 8.4% of cases. The percentage of positive cultures was 77.1% for urinary tract infection, 64.6% for eremia, 57.1% for surgical wound infection, 56.2% for lower respiratory tract infection. The proportional frequencies of pathogens isolated are summarized in Table 4. The most prevalent microorganisms were Escherichia coli for urinary tract infection (54.5%), Staphylococcus epidemidis for bacteremia (22%), Enterococcus for surgical wound infection (15.4%), and Pseudomonas aemginosa for lower respiratory tract infection (16.2%). DISCUSSION ospital surveillance has become an integral part of hospital infection control activities. Between 1980 and 1988, the number of Spanish adult acute care hospitals conducting surveillance for NI increased rapidly. However, only one previous nationwide prevalence study in our country was conducted, in 1986.15 All of the

staphylococci

Fungi Candida Candida

4 2 3 4 3

perfringens

albicans

sp.

15 IO 4

5.4 3.6 1.4 0.4

4 2

7.5 0.7 0.4 0.4

Others Viruses Respiratory syncytial virus Adenovirus Hepatitis B virus

1. 6 a.4 0.8 0.4

1

previous reports involved adult patients. The data from this study represent the largest m~ltic~nter prevalence series of pediatric NI reported to date, and provide an overview of NI by type of hospital, service, site, age-specific rate, and pathogen. The overall prevalence of NI observed (18.03%) could be considered acceptable, bearing in mind the characteristics of cross-sectional surveys. The results of most important multicenter prevalence surveys reported from other countries”6”1 are between 4.1% and 15.6%. NNIS data range from 1.2 to 10.3 infections per 100 discharges.22 Higher rates for patients from a developing community have been reported by Cotton and associates.23 In general the NI rate in children is lower than that reported in adults. However, comparisons among these surveys should be made with caution because methods, definitions used NI, intensity of surveillance, a factors were not equivalent. In Spanish hospitals,

Campins et al.

we have detected no associations between hospital size and prevalences of NI, in contrast to the NNIS, which reports three times higher rates among pediatric patients at large medical schoolaffiliated hospitals (> 500 beds) than among pediatric patients at nonteaching hospitals8 The prevalence of NI varies widely by services. It is highest in PICUs, hematology units, oncology units, special units, and neonatal unit: patients in these areas are severely compromised and undergo prolonged stays and many diagnostic and therapeutic procedures. Our data clearly demonstrate higher frequency of NI than that seen in most U.S. hospitals. In 1984, Welliver and McLaughlin’ reported infection rates in a PICU of I I% at the Children’s Hospital of Buffalo. Wenzel of and coworkers,24 in a statewide investigation infections in different types of intensive care units, demonstrated a mean neonatal intensive care unit infection rate of 8% among the three units surveyed. Infection rates are inversely correlated with age, as most studies demonstrate.5, ’ This is in keeping with our own data; 12% of hospitalized infants younger than 1 year of age acquired NI, whereas only 4% of children 5 years of age or older acquired infection. The most important finding was the high prevalence of bacteremia, the most frequent form of NI detected. Bacteremia was mainly concentrated among neonates, probably because of immunologic deficiency in neonates and because our study only included medium and high-risk neonatal areas and not well-baby nurseries; addition of the latter population would inflate the denominator, lowering the infection rate. Moreover, the most prevalent intrinsic risk factor detected was “high-risk neonate,” with this group represented in excess. Data from the pediatric services included in the NNIS between 1980 and I984 also indicate that the distribution of infections by site is determined by the population studied. Townsend and Wenzelz5 reported a 4% incidence rate of nosocomial bloodstream infections in this type of patient. Our results on surgical wound infections may be considered satisfactory compared with those of other authors,26-28 although efforts must be made to reduce the rates for clean surgery. We found fewer cutaneous and gastrointestinal tract infections than expected in pediatric patients. The organisms identified in this review continue to support the increasing role of coagulasenegative staphylococci as pathogens in hospitalized patients. 2g-31Although viruses are an important cause of NI in pediatric patients, they ac-

April

1993

counted for only 1.5% of the isolated organisms in this survey. Different factors may have contributed to this low level: first, the impact of seasonal variations with an increase in midwinter to early spring, particularly for respiratory syncytial virus, and second, the availability of diagnostic virology laboratories. Prevalence studies are affected by an overrepresentation bias caused by long-term stay patients.32 Although cross-sectional surveys are not adequate for establishing causal inferences, they do provide data of descriptive interest on the dimension of the problem and the risk factors that may contribute to NI. We believe that future efforts should be focused on develaping more effective prevention strategies to reduce the NI level in infants and children in Spanish hospitals. Survey sponsored by the Spanish Association of Hospital Hygiene and Preventive Medicine, with the technical collaboration of Laboratorios Beecham S.A., Madrid, Spain.

EPINE-1990

Working

Group Consultive

Committee:

J. L.

Arribas, A. Asensio, J. Barrio, P. Blasco, F. Calbo, R. Coello, V. Dominguez, R. Galvez, J. Garcia Caballero, A. Gonzalez Toria, A. Hernandez, R. Herruzo, P. Lopez Encinar, 0. Hidalgo, V. Monge, M. C. Saenz, J. R. Saenz, M. Santos, J. Rossellb, J. VaquC, and J. L. Vaquero.

Coordinators

in Hospitals in Autonomous Communities: AnTorres, I. Fernandez, F. Rodriguez, J. M. Bautista, Roman, R. Galvez, R. Rodriguez-Contreras, S. Martin Ruiz, F. Lopez, J. Lorente, P. Alamillos, M. Fernandez, S. Duefias, R. Creagb, and D. Sureda. Muniesa and P. Prieto. Asturias- A. Gonzalez Torga, T. Fernandez, P. Prendes, and A. Torreblanca. Baleares - 0. Hidalgo. Canarias - G. Lopez and 3. Alamo. Castilla-La Mancha-J. Martinez, A. Biurriin, E. Ruiz, and J. Medrano. CastiIla-Lecin-J. de la Lama, N. Coladas, J. Moro, F. Benito, M. Mendo, A. Sacristan, G. Fernandez, A. Hita, P. Vicente, E. Robles, and J. Blanco. Catalunya-IX. Campins, M. Olona, B. Bermejo, J. M. Bayas, M. Gurgui, L. Drobnic, J. M. GarcCs, E. Plass, N. Sanjuan, N. Miserachs, M. Duran, M. Esteve, C. Brotons, F. Rossell, I. Garcia, A. Casagran, M. T. Martinez, L. Moner, R. Priu, A. Verdaguer, L. Gurgui, J. Alijotas, R. Pujol, M. Oliveras, J. M. Sanchez, X. Puig, J. Brau, F. Ribas, A. Anglada, A. Vilamala, J. Baucells, C. Clemente, T. Puig, J. J. Guardiola, F. Ballester, A. Manonelles, V. Romeu, .I. Galvany, and J. Luna, Extremaduva - J. Jimenez and A. Cerrillo. Galicia - J. J. Gestal, M. L. Cal, V. Souto, J. L. Lopez, B. Uriel, A. Blanco, and M. Cueto. Madrid-A. Asensio, R. Hernrzo, J. M. Garcia PQez, P. Gbmez, A. Blanco, B. Perez, S. Sanchez, and V. Vails. Murcia - F. Botia, J. Piqueras, and A. M&s. Comunidad Vale%ciana-L. Ferreres, M. Santos, F. Asensi, S. Cervello, V. C. Zanbn, C. Gonzalez, C. Oltra, and J. F. Navarro. Pais Vasco - I. L. Novales. J. M. Artvalo, and M. E. Elcisegui. daluciaS. Ofia, Oliver, J. de Cueto, Arag&-P.

M. D. L. R.

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AJI Volume

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2

2. Donowitz LG. High risk of nosocomial infection in the pediatric critical care patient. Crit Care Med 1986; 14:26-8. 3. Ford-Jones EL. The special problems of nosocomial infection in the pediatric patients. In: Wenzel RP, ed. Prevention and control of nosocomial infections. Baltimore: Williams and Wilkins, 1987:494-540. 4. Ford-Jones EL, Mindorf CM, Langley JM, Allen U. Epidemiologic study of 4684 hospital acquired infections in pediatric patients. Pediatr Infect Dis J 1989;8:668-75. 5. Gardner P, Carles DG. Infections acquired in a pediatric hospital. J Pediatr 1972;81:1205-10. 6. Polz M, Jablonsky N. Nosocomial infection in a children’s hospital: a retrospective study. J Hyg Epidemiol Microbial Immunol 1986;30:149-53. 7. Welliver RC, McLaughlin S. Unique epidemiology of nosocomial infections in a children’s hospital. Am J Dis Child 1984;138:131-5. 8. Horan TC, White JW, Jarvis WR. Nosocomial infection surveillance 1984. CDC. MMWR Surveillance Summaries 1984;35(supp1):17§s”29s.§. 9. Upton A, Ford-Jones EL. Nosocomial infections in the pediatric patients: an update. AM J INFECT CONTROL 1990;18:176-93. 10. EPINE Working Group. Prevalence of hospital-acquired infections in Spain. J Hosp Infect 1992;20:1-13. 11. Proyecto EPINE. Protocolo de1 estudio EPINE-1990. Madrid: Sociedad Espaiiola de Higiene y Medicina Preventiva Hospitalarias, 1990. 12. VaquC J, Rossello J, Campins M. Prevalencia de las infecciones en un hospital medico-quirmgico de tercer nivel. I. Infecciones y factores de riesgo. Med Clin (Bare) 1987;89:355-61. 13. Garner JS, Jarvis WR, Emori TG. CDC definitions for nosocomial infections, 1988. AM J INFECT CONTROL 1988; 16:128-40. 14. Cornfield 3. A statistical problem arising from retrospective studies. In: Neyman J, ed. Proceedings of the third Berkeley symposium, vol. IV. Berkeley: University of California Press, 1956;135-48. I§. Ministerio de Sanidad y Consumo. Direction General de Planificacmn Sanitaria. Encuesta epidemiol6gica de prevalencia en un punto de la infection hospitalaria y uso clinico de antimicrobianos en Espafia: analisis descriptive de resultados. Madrid: Minisrerio de Sanidad y Consumo, 1986. 16. Hovig B, Lystad A, Opsjon H. A prevalence survey of infections among hospitalized patients in Norway. NIPH Ann 1981;4:49-60.

Campins et al. 17. Meers PD, Ayliffe GAJ, Emmerson AM Report af the national survey of infections in hospitals, 1980. J Hosp Infect 1981;2(Suppl):l-41. 18. Moro ML, Stazi MA, Marasca D. A national prevalence survey of hospital-acquired infections in Italy, I983. J Hosp Infect 1986;8:72-85. 19. Mayon-White RT, Durcel G, Kereselidze T, Tikhomirou E. An international survey of the prevalence of hospitalacquired infection. J Hosp Infect I988;I l(Suppl):43-8. 20. Sramova H, Bartonova A, Bolek S. National prevalence survey of hospital-acquired infections in Czechoslovakia. J Hosp Infect 1988;11:328-34. 21. Danchaivijitr S, Chokloikaew S. A national prevalence study on nosocomial infections 1988. J Med Assoc Thai 1989;72(Suppl):l-6. 22. Jarvis WR. Epidemiology of nosocomial infections in pediatric patients. Pediatr Infect Dis J 1987;6:344-5 1. 23. Cotton MF, Berkowitz FE, Berkowitz Z, Becker PI, Heney C. Nosocomial infections in black South African children. Pediatr Infect Dis J 1989;8:676-83. 24. Wenzel RP, Thompson RI., Landry SM. Hospital-acquired infection in the intensive care unit patient: an overview with emphasis on epidemics. Infect Control i983;4: 371-5. 25. Townsend TR, Wenzel RP. Nosocomial bloodstream infections in a newborn intensive care unit: a case-matched control study of morbidity, mortality and risk. Am J Epidemiol 1981;114:73-80. 26. Redo SF. Pediatric surgery infections. In: Davis JM, Shires GT, eds. Principles and management of surgical infections. Philadelphia: JB Lippincott, 1991;383-93. 27. Cooper RG, Sumner C. Hospital infection data from a children’s hospital. Br J Surg 1976;63:647-50. 28. Davis SD, Sobocinski K, Hoffmann RG, Mohr B, Nelson DB. Postoperative wound infections in a children’s hospital. Pediatr Infect Dis 1984;3: 114-6. 29. Mayer KH, Zinner SH. Bacterial pathogens of increasing significance in hospital acquired infections. Rev Infect Dis 1985;7(Suppl 3):S371-8. 30. McGowan JE. Changing etiology of nosocomial bacteremia and fungemia and other hospital acquired infections. Rev Infect Dis 1985;7(Suppl 3):S357-62. 31. Milliken J, Tait GA, Ford-Jones EL, Mindorff CA, Gold R, Mullins G. Nosocomial infections in a pediatric intensive care unit. Crit Care Med 1988;16:233-7. 32. Freeman J, McGowan JE. Methodologic issues in hospital epidemiology. II. Time and accuracy in estimation, Rev Infect Dis 1981;3:668-77.