Is perioperative hypothermia a risk factor for post-Cesarean...

Is perioperative hypothermia a risk factor for post-Cesareaninfection?

Rodney K. Edwards, Kaivou Madani and Patrick Duff

Department of Obstetrics and Gynecology, University of Florida College of Medicine, Gainesville, FL

Objective: To determine whether hypothermia during Cesarean delivery is a risk factor for postoperativeinfection.Methods: An historical cohort investigation was conducted on all women delivered by Cesarean at our centerduring 2001. Initial recovery-room temperature, taken via the oral or axillary route, was used as a surrogatefor intraoperative temperature. Adding 0.5°C to axillary temperatures generated oral temperature equivalents.Women with chorioamnionitis were excluded, as were those with an initial recovery-room temperature thatexceeded 37.9°C or was recorded more than 20 minutes after the end of surgery. Prophylactic antibiotics(cefazolin, 1 g) were given during Cesarean delivery.Results: A total of 42 women (7.6%) were diagnosed with postoperative infections. Infections includedendometritis (n = 25), wound abscess (n = 7), wound cellulitis (n = 7) and urinary tract infection (UTI) (n = 4).No cases of septic pelvic thrombophlebitis or pelvic abscess occurred. One woman had both endometritis and aUTI. Mean temperatures were higher, rather than lower, for women who subsequently had postoperativeinfections compared with those who did not (36.4 ± 0.8°C vs. 35.9 ± 0.7°C; p < 0.001). Mean temperaturesfor the various postoperative infections were as follows: endometritis, 36.5 ± 0.8°C (p < 0.001 vs. uninfectedgroup); wound abscess 36.0 ± 0.8°C (p = 0.63); wound cellulitis, 36.3 ± 0.6°C (p = 0.14); UTI, 36.7 ± 0.9°C(p = 0.04).Conclusions: Women who develop post-Cesarean infections have higher initial recovery-room temperaturesthan those who do not develop such infections. This suggests the presence of subclinical infection at the timeof Cesarean. Evaluating whether intraoperative warming has any role during Cesarean delivery requires arandomized clinical trial.

Key words: PUERPERAL ENDOMETRITIS; WOUND INFECTION; CESAREAN DELIVERY

Cesarean delivery is the most common indicationfor laparotomy in the USA1. In 2001, 24.4% ofall deliveries in this country were by Cesarean2.Therefore more than one million Cesareans arenow performed in the USA each year. The likeli-hood of post-Cesarean infection varies widely,depending on sociodemographic factors andwhether the Cesarean was performed before orafter labor and/or rupture of the membranes. The

incidence of endometritis after Cesarean delivery is5–20%3, and the rate of wound infection is2–16%4. These infections occur despite the use ofprophylactic antibiotics. Therefore, each year tensof thousands of gravidas in this country developpost-Cesarean infections.

Intraoperative hypothermia may increase theincidence of postoperative infections. Thermo-regulatory vasoconstriction occurs as a result of

Infect Dis Obstet Gynecol 2003;11:75–80

Correspondence to: Rodney K. Edwards, MD, MS, Department of Obstetrics and Gynecology, University of Florida College ofMedicine, PO Box 100294, 1600 SW Archer Road, Gainesville, FL 32610-0294, USA. Email: [email protected]

2003 The Parthenon Publishing Group 75

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intraoperative hypothermia5. Vasoconstrictiondecreases the partial pressure of oxygen in tissuesand decreases resistance to infection in animals6,7.The production of free radicals by leukocytesis oxygen dependent over the range of partialpressures of oxygen that are found in wounds8. Inaddition, hypothermia can adversely affect otherfunctions of leukocytes that are involved indestroying microbes, such as chemotaxis, phago-cytosis and antibody production9. In a guinea-pigmodel, mild hypothermia during anesthesia hasbeen shown to decrease resistance to infectionwith Escherichia coli and Staphylococcus aureus10,11.Finally, a randomized controlled trial in humanshas demonstrated a decrease in the rate of woundinfection in patients undergoing colorectal surgeryfrom 19% in the standard care group to 6% inthe group that received additional warmingmeasures (p = 0.009)12.

If intraoperative hypothermia is associatedwith increased rates of post-Cesarean infections,intraoperative warming might result in a substan-tial decrease in morbidity and cost of care, owingto the prevalence of Cesarean delivery and therelatively inexpensive nature of the measures thatare utilized to warm a patient who is undergoinglaparotomy. The objective of this investigation wasto evaluate whether hypothermia during Cesareandelivery is a risk factor for postoperative infection.

SUBJECTS AND METHODS

An historical cohort investigation was conductedon all women delivered by Cesarean at ShandsHospital at the University of Florida from 1January to 31 December 2001. Patients whounderwent Cesarean delivery were identified fromthe obstetric database maintained by the Divisionof Maternal–Fetal Medicine. The medical recordsof these women were obtained and reviewed.The study was approved by the University ofFlorida Health Center Institutional ReviewBoard.

Demographic data and details of the labor,delivery and postpartum course were abstractedfrom these records and entered into a relationaldatabase (Access 2000, Microsoft Corporation,Redmond, WA). SAS Version 8.0 (SAS Institute,Cary, NC) was utilized for statistical analysis. The

unpaired Student’s t-test was used for continuousdata. Categorical variables were analyzed usingChi-square or Fisher’s exact test, as appropriate. Allstatistical tests were two-tailed, and utilized analpha value of 0.05.

The initial recovery-room temperature accu-rately reflects intraoperative temperature status12.We used the initial recovery-room temperature,taken via the oral or axillary route, as a surrogatefor intraoperative temperature. Adding 0.5°C toaxillary temperatures generated oral temperatureequivalents13,14. The mean oral (or equivalent)temperature was the primary outcome variable.

Exclusion criteria were as follows: clinicaldiagnosis of chorioamnionitis at the time ofCesarean; intrapartum temperature over 37.9°Cbut no other diagnostic criteria for chorio-amnionitis; initial recovery-room temperatureover 37.9°C; initial recovery-room temperaturerecorded more than 20 minutes after the end ofsurgery. All women received prophylaxis againstpost-Cesarean infections with cefazolin, 1 gadministered intravenously, after the umbilicalcord was clamped. For women undergoingCesarean delivery after labor or rupture of themembranes, a second dose was given 8 hours later.Women with a history of allergy to β-lactam anti-biotics or cephalosporins received a single injec-tion of gentamicin and clindamycin instead ofcefazolin.

Subjects were considered to have had endo-metritis if they developed an oral temperatureof 38.0°C or higher more than 4 hours post-operatively, had no signs of infection at sitesother than the uterus, and were treated with anti-biotics for this indication. Those women whowere treated with antibiotics during the post-operative period for a ‘wound infection’ wereconsidered to have either a wound abscess orwound cellulitis. The former category was utilizedfor those subjects in whom the wounds wereopened and purulent fluid was encountered. Thelatter category was utilized for those subjects whohad documented induration and warmth at thewound site but no purulent discharge fromthe wound. Subjects who had dysuria and aurine culture showing > 100 000 colonies/ml of asingle uropathogen were classified as havinga urinary tract infection (UTI).

Hypothermia and infection Edwards et al.

76 • INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY



RESULTS

During the study period, a total of 657 womenwere delivered by Cesarean. Women wereexcluded from the cohort because of missingcharts (n = 18), chorioamnionitis (n = 55), intra-partum temperature over 37.9°C but no othercriteria for diagnosing chorioamnionitis (n = 2),initial recovery-room temperature over 37.9°C(n = 8) or initial recovery-room temperaturehaving been obtained more than 20 minutes afterthe end of surgery (n = 25). The cohort consistedof the remaining 555 women. In total, 42 women(7.6%) had postoperative infections. The distribu-tion of these infections was as follows: endo-metritis, n = 25; wound abscess, n = 7; woundcellulitis, n = 7; UTI, n = 4. No cases of septicpelvic thrombophlebitis or pelvic abscessoccurred. One woman had both endometritis anda UTI. The demographic data are shown inTable 1, and the data on labor and intraoperativecourse are presented in Table 2.

Table 3 shows the mean initial recovery-roomtemperatures for the infected and uninfectedgroups. The initial recovery-room temperaturewas taken via the oral route for all but 17 subjects;

the latter subjects had their temperatures taken viathe axillary route. One of the subjects whose initialrecovery-room temperature was taken via theaxillary route later developed endometritis. Theother 16 subjects were in the uninfected group.Mean temperatures were higher, rather thanlower, for women who subsequently had post-operative infections compared with those who didnot. Of the eight women who were excludedbecause their initial recovery-room temperaturewas over 37.9°C, five developed puerperalendometritis and one developed wound cellulitis.

DISCUSSION

Our study design has some limitations. Duringdata collection, all subjects’ medical records werereviewed no less than 60 days after discharge fromthe delivery hospitalization. Therefore subjectswho developed postoperative infections afterhospital discharge and then presented to theemergency department for evaluation were stilldetected as having postoperative infections. How-ever, subjects who presented to another facilityfor treatment of postoperative infections would


INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY • 77

Variable Infected (n = 42) Uninfected (n = 513) p-value

Age (years)Height (inches)Weight (pounds)Gestational age (weeks)NulliparousRace

WhiteNon-white

DiabeticNoGestationalPregestational

HypertensionNoChronicPre-eclampsia/eclampsia

Preoperative hematocrit (%)Neonatal birth weight (g)Male neonate

24.8 ± 6.563.9 ± 3.5200 ± 4937.0 ± 4.4

66.7

59.540.5

85.714.2

0

78.62.4

19.033.8 ± 4.1

3039 ± 89848.7

27.2 ± 6.864.0 ± 2.8195 ± 5136.7 ± 3.8

36.3

57.742.3

84.013.3

2.7

78.42.3

19.434.1 ± 3.7

3024 ± 92555.0

0.030.830.550.64

< 0.0010.68

0.75

0.89

0.650.920.45

Data are presented as mean values ± standard deviation or proportion of n. Due to rounding, some category proportions do not totalexactly 100%

Table 1 Demographic data



not have been detected. In addition, we cannotaccount for the effect of type of anesthesia on theinitial recovery-room temperature. However,almost all of the subjects in this study (n = 524;94.4%) had their Cesarean deliveries performedunder epidural or spinal anesthesia.

Our study failed to show an association betweenintraoperative hypothermia and an increasedlikelihood of post-Cesarean infections. In contrast,the uninfected group on average had lower initialrecovery-room temperatures. One other study hasevaluated the association between intraoperative

hypothermia and post-Cesarean infection, specifi-cally wound infection. Munn et al.13 performed acase–control study that compared mean initialrecovery-room core temperatures (derived byadding 0.5°C to the oral temperature) in womenwho had post-Cesarean wound infections and incontrols matched for age, weight, presence ofgestational hypertension and duration of surgery.In their study, the mean initial recovery-roomcore temperature was 36.3°C in the women whohad wound infections and 36.6°C in the controls(p = 0.8). Munn et al.13 speculated that their results



Variable Infected (n = 42) Uninfected (n = 513) p-value

In laborTotal number of vaginal examinationsVaginal examinations after ROMDuration of ROM (hours)Duration of IM (hours)Meconium-stained fluidGBS prophylaxisDuration of Cesarean (minutes)Emergent CesareanIntraoperative FIO2 (%)Estimated blood loss (ml)Time between end of surgery and initialrecovery-room temperature (minutes)Skin incision

TransverseVertical

Uterine incisionLow transverseClassical

85.75.5 ± 4.24.0 ± 3.6

35.1 ± 97.74.6 ± 5.4

31.021.4

46.0 ± 14.99.5

31.4 ± 11.5812 ± 2209.6 ± 5.1

92.97.1

97.62.4

50.32.2 ± 3.01.2 ± 2.19.9 ± 66.81.5 ± 3.5

11.517.3

48.5 ± 13.89.2

33.5 ± 17.9788 ± 2238.1 ± 4.6

86.313.7

96.53.5

< 0.001< 0.001< 0.001

0.02< 0.001< 0.001

0.440.270.940.450.500.07

0.23

0.70

Data are presented as mean values ± standard deviation or proportion of n. ROM, rupture of membranes; IM, internal monitors;GBS, group B streptococcus; FIO2, fraction of inspired oxygen. The duration of the Cesarean was the difference between the ‘beginsurgery’ and ‘end surgery’ times as recorded on the anesthesia flow record

Table 2 Data on labor and intraoperative course

Group nInitial recovery-room

temperature (°C) Range (°C) p-value

UninfectedTotal infectedEndometritisWound abscessWound cellulitisUrinary tract infection

5134225

774

35.9 ± 0.736.4 ± 0.836.5 ± 0.836.0 ± 0.836.3 ± 0.636.7 ± 0.9

32.5–37.934.9–37.935.0–37.934.9–37.035.3–37.035.4–37.4

Reference< 0.001< 0.001

0.630.140.04

Data are presented as mean values ± standard deviation

Table 3 Initial recovery room temperatures



may have differed from those in the study ofpatients who underwent colorectal surgery12, dueto differences in operating time between Cesareandelivery and colorectal surgery (resulting in lowermean intraoperative temperatures in the controlgroup of colorectal surgery patients) and differ-ences between gravidas and patients undergoingcolorectal surgery.

Although those factors may have contributedto the differences in the results, the findings ofour study suggest a different reason. We founda higher rather than lower mean initialrecovery-room temperature in the group thatdeveloped post-Cesarean infections comparedwith the group that did not. This result leads us toconclude that the women who developed post-operative infections had subclinical chorio-amnionitis at the time of Cesarean delivery,resulting in a relatively higher mean initialrecovery-room temperature. Previous studieshave shown that women who develop postpartumendometritis often have positive amniotic fluidcultures at the time of Cesarean delivery15–17. In

addition, many of the risk factors for chorio-amnionitis (number of vaginal examinationsduring labor, and duration of labor, rupturedmembranes and internal monitoring) have alsobeen shown to be risk factors for post-Cesareanwound infection18.

Because there is no way to adjust for the effectof differences in bacterial contamination ratesbetween patients, evaluation of any possible roleof intraoperative warming during Cesareandelivery will require a randomized clinical trial.This type of design would also provide forbalance between groups with regard to otherpotentially confounding factors, such as anes-thesia type and volume and the temperatureof intravenous fluid administered. Such a trialcould evaluate warming via intravenous fluidsand/or conduction warmers. If intraoperativewarming was found to be effective in decreasingthe rate of postoperative infections (as it is incolorectal surgery patients), this approach may bea cost-effective way to improve outcomes forour patients.

REFERENCES1. Taffel SM, Placek PJ, Moien M, et al. 1989 US

Cesarean section rate steadies: VBAC rate rises tonearly one in five. Birth 1991;18:73–7

2. Martin JA, Park MM, Sutton PD. Births:preliminary data for 2001. Natl Vital Stat Rep2002;50:1–20

3. Duff P. Maternal and perinatal infection. In GabbeSG, Niebyl JR, Simpson JL, eds. Obstetrics: Normaland Problem Pregnancies, 4th edn. New York:Churchill Livingstone, 2002:1293–345

4. Owen J, Andrews WW. Wound complicationsafter Cesarean sections. Clin Obstet Gynecol 1994;37:842–55

5. Ozaki M, Sessler DI, Suzuki H, et al. Nitrous oxidedecreases the threshold for vasoconstriction lessthan sevoflurane or isoflurane. Anesth Analg1995;80:1212–16

6. Chang N, Mathes SJ. Comparison of the effectof bacterial inoculation in musculocutaneous andrandom-pattern flaps. Plast Reconstr Surg 1982;70:1–10

7. Jonsson K, Hunt TK, Mathes SJ. Oxygen as anisolated variable influences resistance to infection.Ann Surg 1988;208:783–7

8. Hohn DC, MacKay RD, Halliday B, et al.The effect of O2 tension on microbicidal functionof leukocytes in wound and in vitro. Surg Forum1976;27:18–20

9. Van Oss CJ, Absolom DR, Moore LL, et al. Effectof temperature on the chemotaxis, phagocyticengulfment, digestion and O2 consumption ofhuman polymorphonuclear leukocytes. J Reticulo-endothelial Soc 1980;27:561–5

10. Sheffield CW, Sessler DI, Hunt TK. Mildhypothermia during isoflurane anesthesia decreasesresistance to E. coli dermal infection in guinea pigs.Acta Anaesthesiol Scand 1994;38:201–5

11. Sheffield CW, Sessler DI, Hunt TK, et al. Mildhypothermia during halothane-induced anesthesiadecreases resistance to Staphylococcus aureus dermalinfection in guinea pigs. Wound Repair Regen1994;2:48–56


INFECTIOUS DISEASES IN OBSTETRICS AND GYNECOLOGY • 79



12. Kurz A, Sessler DI, Lenhardt R. Perioperativenormothermia to reduce the incidence ofsurgical-wound infection and shorten hospitaliza-tion. N Engl J Med 1996;334:1209–15

13. Munn MB, Rouse DJ, Owen J. Intraoperativehypothermia and post-Cesarean wound infection.Obstet Gynecol 1998;91:582–4

14. Marino P. Approaches to nosocomial fever. InMarino P, ed. The ICU Book. Philadelphia, PA:Lea and Febiger, 1991:571–87

15. Gilstrap LC, Cunningham FG. The bacterialpathogenesis of infection following Cesareansection. Obstet Gynecol 1979;53:545–9

16. Blanco JD, Gibbs RS, Castaneda YS, et al. Correla-tion of quantitative amniotic fluid cultures withendometritis after Cesarean section. Am J ObstetGynecol 1982;143:897–901

17. Yancey MK, Clark P, Duff P. The frequency ofglove contamination during Cesarean delivery.Obstet Gynecol 1994;83:538–42

18. Gibbs RS, Blanco JD, St. Clair PJ. A case–controlstudy of wound abscess after Cesarean delivery.Obstet Gynecol 1983;62:498–501

RECEIVED 10/10/02; ACCEPTED 03/17/03





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