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Risk factors for cesarean surgical site infections at a Thai-Myanmar border hospital
ARTICLE IN PRESS American Journal of Infection Control ■■ (2016) ■■-■■
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American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Major articles
Risk factors for cesarean surgical site infections at a Thai-Myanmar border hospital Srisuda Assawapalanggool MNS a, Nongyao Kasatpibal PhD b,*, Supatra Sirichotiyakul MD c, Rajin Arora MD d,e, Watcharin Suntornlimsiri MD f a
Infection Control Section, Maesot Hospital, Tak, Thailand Division of Nursing Science, Faculty of Nursing, Chiang Mai University, Chiang Mai, Thailand c Department of Obstetrics and Gynecology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand d Department of Obstetrics and Gynecology, Lampang Hospital, Lampang, Thailand e Collaborative Project to Increase Rural Doctors, Ministry of Public Health, Thailand f Department of Obstetrics and Gynecology, Nakornping Hospital, Chiang Mai, Thailand b
Key Words: Risk factors caesarean section surgical site infections caesarean infections cohort study
Background: Cesarean surgical site infections (SSIs) are a major challenge in Thai-Myanmar border hospital settings. This study aimed to examine risk factors for SSIs after cesarean section. Methods: This was a prospective cohort study conducted in a Thai-Myanmar border hospital between January 2007 and December 2012. Data were collected from the medical record database by trained infection control nurses. Stepwise multivariable logistic regression was used for risk factor analysis and expressed as a risk ratio (RR). Results: The cesarean SSI rate was 5.9% (293 SSIs in 4,988 cases). Of these, 17.1% were incisional SSIs (10.9% superficial and 6.2% deep incisional SSIs), and 82.9% were organ or space SSIs. Risk factors for cesarean organ-space SSIs included a wound class ≥3 (RR, 4.82; 95% confidence interval [CI], 3.41-6.83), ethnic minority (RR, 2.51; 95% CI, 1.61-3.92), hemoglobin <11 g/dL (RR, 2.19; 95% CI, 1.57-3.04), pelvic examination before delivery on ≥5 occasions (RR, 4.16; 95% CI, 2.89-5.99), preterm (RR, 1.98; 95% CI, 1.33-2.95), being a local referral (RR, 3.37; 95% CI, 2.29-4.97), and foul-smelling amniotic fluid (RR, 21.08; 95% CI, 10.23-43.41). Conclusions: Most cesarean SSIs in this study seem to have a high severity. Their risk factors reflected delayed appropriate perinatal maternal care that resulted in late cesarean delivery. Early prenatal care may help reduce cesarean SSIs among this population. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Cesarean section is a major surgery and has increasing prevalence yearly in most countries.1 Cesarean surgical site infections (SSIs), especially organ-space SSIs, are serious complications2 that can result in reoperation, increased medical cost and length of stay, rehospitalization, maternal prolongation of returning to normal function, or mortality. Incidence of cesarean SSI varies depending on the methodology of study, case definition, case identification ability of observers,3 and socioeconomic status. Among developed countries, total cesarean SSIs were approximately 1.5%-7.0%.4,5 Cesarean incisional SSI incidence was approximately 0.18%,6 and endometritis ranged from
* Address correspondence to Nongyao Kasatpibal, PhD, Division of Nursing Science, Faculty of Nursing, Chiang Mai University, Chiang Mai 50200, Thailand. E-mail address: [email protected] (N. Kasatpibal). Conflicts of Interest: None to report.
3%-6%,7,8 The cesarean SSI rates are approximately 6% in underdeveloped countries.9 In Thailand, the incidences of cesarean SSI and cesarean endometritis are 0.9% and 2.0%, respectively.1,10 Various risk factors of cesarean SSIs have been identified. An important risk of cesarean endomyometritis is the cesarean section per se.11 Other identified risk factors are classified in patientrelated conditions (eg, maternal age, socioeconomic status, 12 obesity13) and underlying medical problems. These include anemia (hemoglobin level: <11 g/dL)12; obstetric-related factors; including parity,13 zygosity,14 presence and duration of rupture of amniotic membrane (ROM),15 number of pelvic examinations (PVs),16 and presence of meconium-stained amniotic fluid (MSAF)13; gestational age <37 weeks (preterm labor)7; vaginal procedures performed before cesarean section16; associated gynecologic infections12; and surgical risk factors. Potential surgical risks of SSI include a high American Society of Anesthesiology (ASA) score, 13 high wound class, and long
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2016.01.031
ARTICLE IN PRESS S. Assawapalanggool et al. / American Journal of Infection Control ■■ (2016) ■■-■■
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operation time.17 According to the National Nosocomial Infections Study (NNIS), these are included in the risk index category.18 In addition, emergency surgery,12 type of skin incision and urethrotomy,19 blood volume lost,13 and hematoma12 are identified as potential risks. Our center is adjacent to the Thai-Myanmar border and serves up to 5 districts, including 4 refugee camps in the service area. Patients attending our center vary considerably in tribes and also conceal a variety of health and environmental problems that are overloaded in the clinic. Health care–associated infections are strongly influenced by an overcrowded setting.20 Cesarean SSIs in our center comprised at least 3.0% in 2005. The situation is predicted to worsen after the ASEAN Economic Community (AEC) establishment in 2016, which will be characterized by economic immigration. Based on epidemiologic knowledge, risk factors of cesarean SSI in our setting may differ from other regions both in types and strength of association. Exploration of such risk factors is essential for preparedness of forthcoming changes after the AEC launch.
gynecologic problem was referred to our center for consultation. Patients from camps were referred for such purposes by medics or volunteers in the camps. Patients who did not attend any followup appointments in our network were classified as lost to follow-up. Statistical analysis A statistical software package was used for sample size estimation. Based on the wound class reported in a previous study,22 the sample size was calculated using a 2-sample comparison of proportions where α = 0.05 and β = 0.80. This resulted in the minimum study size of 2,277 patients. Baseline characteristics were descriptively analyzed. Continuous data were tested between comparison groups using t test, Wilcoxon rank-sum test, analysis of variance, or Kruskal-Wallis equality of populations rank test depending on the number of comparison groups and their distribution function. Categorical variables were compared using Fisher exact test and Pearson χ2 test. Subgroup analysis was estimated in patients with cesarean SSIs for the comparison of risk factors between 2 age groups: <20 and ≥20 years. Cesarean SSIs were treated under the assumption of being a multinomial variable. Potential risk factors included age group, ethnic minority status, education level, antenatal care (ANC) status, body weight ≥80 kg, anemia, HIV infection, being referred, primigravida, preterm, PVs ≥5 times before surgery, amniotic characteristic, rupture of membrane ≥12 hours, fetal death in utero, ASA score ≥3, wound class ≥3, operation time >55 minutes, emergency operation, blood loss during operation ≥500 mL, presence of urinary tract infection before surgery, midline skin incision, and additional procedure performed during cesarean section. Each variable was univariably analyzed by using multinomial logistic regression. All significant risk factors were then included in the multivariable regression model where cesarean incisional and cesarean organspace SSIs were treated as separate dependent variables. The backward stepwise multivariable logistic regression model using a significance level for removal from the model of 0.001 was calculated, and collinearity of the independent variables in the final model was checked.
METHODS Setting The study was conducted in a crowded and limited-resource tertiary care hospital with 365 beds on the Northwestern ThaiMyanmar border, with an annual average of 800 caesarean cases. Study design and data collection The study was approved by the institute’s Research Ethical Board, Faculty of Medicine, Chiang Mai University. Data were prospectively collected from January 1, 2007-December 31, 2012, by 2 infection control nurses who had obtained Master’s degrees in infection control. Cesarean SSI cases were defined according to the Centers for Disease Control and Prevention’s (CDC’s) National Healthcare Safety Network criteria.21 Clinical signs and symptoms and medical records were reviewed through the surveillance system. These included patients demographics, background medical problems, obstetric progression with intervention or operative data, antibiotics administration, vital signs, diagnosis throughout admission, documents of their treatment and any complications, follow-up days, and follow-up method. Wounds were inspected among all patients using aseptic techniques on the third postoperative day and whenever necessary or before discharge. All patients made appointments approximately 1 week and 1 month postoperative at a convenient health center in their community in our network. The 1-week follow-up appointment focused on wound checking, and stitches were removed when necessary. When any wound complications occurred, the patient was referred for consultation. The 1-month follow-up appointment aimed at family planning and gynecologic problem screening. Again, any patient who had a
RESULTS In total, 5,122 patients underwent cesarean sections. There were 4,988 patients recruited, and 134 patients (2.6%) were lost to followup from our postdischarge surveillance system (PDS). These patients were excluded. All patients received antibiotic prophylaxis according to their obstetrician’s preference. We identified 293 of 4,988 patients (5.9%) that encountered cesarean SSIs. Of these, 17.1% were classified as incisional SSI (10.9% superficial and 6.2% deep incisional SSIs), and 82.9% were classified as organ-space SSI. Most SSI cases (88.7%) were diagnosed before discharge. The other 11.3% were detected in our PDS (Table 1). The
Table 1 Caesarean SSI classification and surveillance method (N = 4,988) Superficial incisional SSIs (n = 32)
Deep incisional SSIs (n = 18)
Organ-space SSIs (n = 243)
Characteristics
n
%
n
%
Caesarean SSI rate Surveillance method In-hospital surveillance Postdischarge surveillance Hospital OPD Other health care service centers
32
0.6
18
0.4
243
4.9
293
5.9
24 8 1 7
75.0 25.0 12.5 87.5
12 6 1 5
66.7 33.3 16.7 83.3
224 19 13 6
92.2 7.8 68.4 31.6
260 33 15 18
88.7 11.3 45.5 54.5
OPD, obstetrics and gynecology outpatient department; SSI, surgical site infection.
n
Total (n = 293) %
n
%
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Table 2 Characteristics of caesarean section patients among non-SSIs and SSIs (N = 4,988) Characteristics Age (y) <20 20-34 ≥35 Mean ± SD Ethnic minority Education level No Primary Intermediate College or higher Antenatal care No Camp Hospital Body weight (kg) ≥80 Mean ± SD Hb (g/dL) <11 Mean ± SD HIV positive Referral Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD PVs ≥5 occasions before surgery Amniotic fluid Clear MSAF Foul smelling ROM duration (h) ≥12 Median (IQR) Fetal death ASA score ≥3 Wound class ≥3 Operation time (min) >55 Mean ± SD Emergency operation EBL (mL) ≥500 Median (IQR) UTI Skin incision type Midline Pfannelstein Addition procedures Appendectomy/TR
Non-SSIs (n = 4,695)
SSIs (n = 293)
P value <.001
278 (5.9) 3,473 (74.0) 944 (20.1) 29.2 ± 6.1 2,266 (48.3)
21 (7.2) 216 (73.7) 56 (19.1) 27.8 ± 6.2 241 (82.3)
1,930 (41.1) 768 (16.4) 983 (20.9) 1,014 (21.6)
206 (70.3) 40 (13.7) 30 (10.2) 17 (5.8)
<.001
90 (1.9) 1,109 (23.6) 3,496 (74.5)
7 (2.4) 184 (62.8) 102 (34.8)
<.001
617 (13.1) 66.0 ± 12.1
44 (15.0) 64.8 ± 14.2
.010
860 (18.3) 11.4 ± 1.1 133 (2.8) 1,389 (29.6)
107 (36.5) 10.9 ± 1.7 6 (2.1) 203 (69.3)
<.001
1,716 (36.5) 2 (1-3)
149 (50.8) 1 (1-2)
<.001
531 (11.3) 38.5 ± 2.3 599 (12.8)
56 (19.1) 38.5 ± 2.8 103 (35.2)
.144
4,073 (86.7) 609 (13.0) 13 (0.3)
157 (53.6) 95 (32.4) 41 (14.0)
<.001
122 (42.7) 8.8 (0-23.3) 13 (4.4) 17 (5.8) 199 (67.9)
<.001
1,478 (31.5) 48.7 ± 13.4 3,226 (68.7)
122 (41.6) 52.5 ± 15.8 283 (96.6)
<.001
2,390 (50.9) 500 (300-500) 20 (0.4)
190 (64.9) 500 (400-600) 2 (0.7)
<.001
1,883 (40.1) 2,812 (59.9)
196 (66.9) 97 (33.1)
<.001
2,135 (45.5)
83 (28.3)
<.001
560 (12.1) 0 (0-4.2) 45 (1.0) 237 (5.1) 907 (19.3)
<.001
.582 <.001
<.001
<.001 .582 <.001
<.001
.374
NOTE. Values are n (%) or as otherwise indicated. ASA, American Society of Anesthesiology; EBL, estimated blood loss; GA, gestational age; Hb, hemoglobin; IQR, interquartile range; MSAF, meconium-stained amniotic fluid; PV, pelvic examination; ROM, rupture of amniotic membrane; SSI, surgical site infection; TR, tubal resection; UTI, urinary tract infection.
median length of hospital stay was 4 days (interquartile range, 3-5 days), and the median incubation period of the total cesarean SSIs was 4 days (interquartile range, 3-5 days). Patient characteristics included nationality, education level, place of ANC, hemoglobin level, referral status, gravidity, number of PVs prior to surgery, duration of ROM, fetal death, wound class, operation time, emergence of operation, amount of blood loss, type of skin incision, and any additional procedures that differed among patients in the organ-space SSI, incisional SSI, and non-SSI groups (Tables 2-3).
3
Risk factors of incisional SSI obtained by univariable multinomial risk ratio regression included age ≥35 years, being referred (by local setting or refugee camp), MSAF, ANC in camp, ASA score ≥3, wound class ≥3, operation time >55 minutes, and emergency operation (results not shown), but only emergency operation was demonstrated to be a risk factor of incisional SSI by backward stepwise multivariable logistic regression (Table 4). Risk factors of organ-space SSI obtained by univariable multinomial risk ratio regression included ethnic minority status, anemia, being referred, primigravida, preterm, PVs ≥5 times, MSAF, foulsmelling amniotic fluid, ROM >12 hours, ANC in camp or no ANC, fetal death, wound class ≥3, operation time >55 minutes, emergency operation, midline skin incision, and blood loss volume ≥500 mL (results not shown). However, only 7 risk factors were identified, including ethnic minority, anemia, being referred, preterm, PVs ≥5 times, foul-smelling amniotic fluid, and wound class ≥3, and remained in the model after backward stepwise multivariable logistic regression (Table 4). Subgroup analysis demonstrated ethnic minority status, education level, gravidity, gestation age, and operation time differed between the <20 and ≥20 year old age groups (Table 5). DISCUSSION Incidence of cesarean SSIs in this study (5.9%) was relatively higher than a multicenter study in Thailand (0.9%).10 This may be explained by the fact that patients in our study had a higher risk for SSI. However, the SSI rate in our study was lower than a study in Cambodia (6.3%).9 This could be because of higher standards of hygiene practiced and quality of care in Thailand compared with Cambodia. Furthermore, it might be because of the difference in the surveillance methods used to identify infections, antibiotic prophylaxis, and the patient population.23 Deep organ-space cesarean SSIs were predominant in our study. This may partly be because the major cesarean SSIs cases were referred from the local refugee camp in our area. All of the referred cases underwent vaginal delivery assistance (ie, vacuum extraction), resulting in delayed cesarean operations. Incisional SSIs, in contrast, had lesser incidence. This might be because of low health care provider experience in the PDS or out of date knowledge of some personnel because this network system was launched in 2006 and requires continuous quality improvement. Most caesarean SSI cases in this study were organ-space SSIs. Organ-space SSIs were most likely to lead to severe constitutional symptoms, most likely to lead to morbidity, and may be contributed by high virulence microbes. As a result, their detections were mostly found early, before discharge. According to the CDC and the National Healthcare Safety Network, postcesarean endometritis has been categorized as organ-space SSI. Etiologic bacteria originates mostly from the colonization of the lower genital tract and ascends and infects amnion and adjacent areas during the operation.2 Incisional SSIs, on the other hand, frequently result by inoculation of resident skin flora, bacteria from the environment, or contaminated amniotic fluid into the incision.16 Based on various etiologies of SSIs, we assumed that each type of SSI in patients admitted to our setting had different risk factors and also differed in strength of association. Several studies have demonstrated different sets of risk factors for various terms of SSIs with substantial variation in measurements used and their strengths from study to study. Organ-space SSIs encompassed the vast majority of cesarean SSIs in our study, with the 7 risk factors previously stated. Most of the non-Thai patients in our setting were either Burmese, hill tribe, political refugees, economic migrants, or of low socioeconomic and education status. As a consequence, they were malnourished and even anemic and
ARTICLE IN PRESS S. Assawapalanggool et al. / American Journal of Infection Control ■■ (2016) ■■-■■
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Table 3 Characteristics of caesarean section patients among types of SSIs (N = 4,988) Characteristics Age (y) <20 20-34 ≥35 Mean ± SD Ethnic minority Education level No Primary Intermediate College or higher Antenatal care No Camp Hospital Body weight (kg) ≥80 Mean ± SD Hb (g/dL) <11 Mean ± SD HIV positive Referral Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD PVs ≥5 Amniotic fluid Clear MSAF Foul smelling ROM duration (h) ≥12 Median (IQR) Fetal death ASA score ≥3 Wound class ≥3 Operation time (min) >55 Mean ± SD Emergency EBL (mL) ≥500 Median (IQR) UTI Skin incision type Midline Pfannelstein Addition procedures Appendectomy/TR
Non-SSIs (n = 4,695)
Incisional SSIs (n = 50)
Organ-space SSIs (n = 243)
P value <.001
278 (5.9) 3,473 (74.0) 944 (20.1) 29.2 ± 6.1 2,266 (48.3)
4 (8.0) 29 (58.0) 17 (34.0) 29.8 ± 7.0 33 (66.0)
17 (7.0) 187 (76.9) 39 (16.1) 27.4 ± 6.0 208 (85.6)
1,930 (41.1) 768 (16.4) 983 (20.9) 1,014 (21.6)
28 (56.0) 7 (14.0) 10 (20.0) 5 (10.0)
178 (73.3) 33 (13.6) 20 (8.2) 12 (4.9)
<.001
90 (1.9) 1,109 (23.6) 3,496 (74.5)
2 (4.0) 19 (38.0) 29 (58.0)
5 (2.1) 165 (67.9) 73 (30.0)
<.001
617 (13.1) 66.0 ± 12.1
8 (16.0) 67.4 ± 16.9
36 (14.8) 64.3 ± 13.5
.013
860 (18.3) 11.4 ± 1.1 133 (2.8) 1,389 (29.6)
9 (18.0) 11.3 ± 1.7 0 (0) 25 (50.0)
98 (40.3) 10.8 ± 1.8 6 (2.5) 178 (73.3)
<.001
1,716 (36.5) 2 (1-3)
22 (44.0) 2 (1-3)
127 (52.3) 1 (1-2)
<.001
531 (11.3) 38.5 ± 2.3 599 (12.8)
9 (18.0) 38.0 ± 2.8 8 (16.0)
47 (19.3) 38.6 ± 2.8 95 (39.1)
.058
4,073 (86.7) 609 (13.0) 13 (0.3)
37 (74.0) 12 (24.0) 1 (2.0)
120 (49.4) 83 (34.2) 40 (16.5)
<.001
8 (16.0) 0 (0-8) 0 (0) 7 (14.0) 17 (34.0)
114 (48.3) 11.1 (2-24.5) 13 (5.4) 10 (4.1) 182 (74.9)
<.001
560 (12.1) 0 (0-4.2) 45 (1.0) 237 (5.1) 907 (19.3)
<.001
.720 <.001
<.001
<.001 .026 <.001 <.001
1,478 (31.5) 48.7 ± 13.4 3,226 (68.7)
23 (46.0) 54.6 ± 17.0 47 (94.0)
99 (40.7) 52.1 ± 15.6) 236 (97.1)
2,390 (50.9) 500 (300-500) 20 (0.4)
30 (60.0) 500 (400-500) 0 (0.0)
160 (65.8) 500 (400-600) 2 (0.8)
<.001
<.001
.436
1,883 (40.1) 2,812 (59.9)
25 (50.0) 25 (50.0)
171 (70.4) 72 (29.6)
<.001
2,135 (45.5)
16 (32.0)
67 (27.6)
<.001
NOTE. Values are n (%) or as otherwise indicated. ASA, American Society of Anesthesiology; EBL, estimated blood loss; GA, gestational age; Hb, hemoglobin; IQR, interquartile range; MSAF, meconium-stained amniotic fluid; PV, pelvic examination; ROM, rupture of amniotic membrane; SSI, surgical site infection; TR, tubal resection; UTI, urinary tract infection.
therefore prone to SSIs.2,7,12 Patients referred from local settings were put at increased risk of an SSI because of overcrowding, limited resources, and conservative treatment until the conditions of referral for further consultation were met. Obstetric and surgical risk factors in this study included PVs on ≥5 occasions before delivery, foulsmelling amniotic fluid, preterm labor, and a wound class of 3 or 4. These findings were similar to the results from previous studies.7,12,15 Anemia was reported as a risk factor of cesarean SSIs, but no clear reason has been established for this association.12 Anemic patients in our setting were anemic because of iron deficiency and hemoglobinopathy. Iron deficiency always coincides with other nu-
trient deficiencies24 as a result of the low socioeconomic status of the patient. Protein malnutrition will result in malfunctioning of the immune system, delayed wound healing, and infection.12,24 Moreover, low socioeconomic status always hinders the patient from accessing the health care service system, and patients with low socioeconomic status also have poor personal hygiene care. These pose some risk of SSI to the patient. To prevent SSI, improving the care system accessibility is essential. In addition, the attitude, knowledge of pregnant women about prenatal care, and nutritional status should also be improved. Multiple PVs were proven to be a risk factor of SSIs. It increases the risk of ascending infection in the amniotic cavity by
ARTICLE IN PRESS S. Assawapalanggool et al. / American Journal of Infection Control ■■ (2016) ■■-■■
Table 4 Multivariable risk ratios of the caesarean SSIs risk factors Characteristics Total SSIs Ethnic minority Hemoglobin <11 g/dL PVs ≥5 (occasions before surgery) Gestation age <37 wk Primigravida Referral Foul-smelling amniotic fluid Wound class ≥3 Operation time >55 min Emergency operation Incisional SSIs Emergency operation Organ-space SSIs Wound class ≥3 Ethnic minority Hemoglobin <11 g/dL PVs ≥5 Gestational age <37 wk Referral Foul-smelling amniotic fluid
RR
95% CI
P value
1.98 1.83 3.01 1.74 1.50 2.75 18.11 3.29 1.50 2.74
1.37-2.87 1.36-2.48 2.16-4.19 1.21-2.48 1.13-2.00 1.95-3.86 9.07-36.18 2.44-4.45 1.13-1.98 1.40-5.37
<.001 <.001 <.001 .003 .005 <.001 <.001 <.001 .005 .003
7.38
2.29-23.76
.001
4.82 2.51 2.19 4.16 1.98 3.37 21.08
3.41-6.83 1.61-3.92 1.57-3.04 2.89-5.99 1.33-2.95 2.29-4.97 10.23-43.41
<.001 <.001 <.001 <.001 .001 <.001 <.001
CI, confidence interval; PV, pelvic examination; RR, risk ratio; SSI, surgical site infection.
Table 5 Subgroup analysis of caesarean SSI cases between age group Caesarean SSIs Characteristics
Age <20 y
Age ≥20 y
P value
Ethnic minority Education level No Primary Intermediate College or higher Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD Operation time (min) >55 Median (IQR)
13 (61.9)
228 (83.8)
.018
12 (57.1) 3 (14.3) 6 (28.6) 0 (0.0)
194 (71.3) 37 (13.6) 24 (8.8) 17 (6.3)
.026
17 (81.0) 1 (1-1)
132 (48.5) 2 (1-2)
.002
6 (28.6) 37.4 ± 3.0
50 (18.4) 38.6 ± 2.8
.032
118 (43.4) 50 (40-60)
.042
4 (19.1) 45 (40-50)
NOTE. Values are n (%) or as otherwise indicated. GA, Gestational age; IQR, interquartile range; SSI, surgical site infection.
inoculation of microbes from external genitalia and hence increases the risk of caesarean SSIs. 16 The probability of intraamniotic infection depends on the duration of the ROM and degree of contamination. The procedure being performed using limited resources by unskilled personnel in those settings may also increase the chance of infection. To prevent infection, PVs should be done only to monitor labor progression and strictly following sterile techniques. Preterm labor has been shown to be a risk factor for SSI in a previous study.7 This may be because some cases of preterm labor were the result of chorioamnionitis or expectant management of preterm premature ROM and leading to postpartum endometritis. Therefore, in preterm premature ROM with expectant management, delivery should be considered as soon as fetal lung maturation to shorten ROM duration and reduce the chance of infection. Foul-smelling amniotic fluid was demonstrated as a considerable risk factor for cesarean organ-space SSIs in this study. It was included in the clinical signs of chorioamnionitis, which is an important risk factor of cesarean organ-space SSIs.13 Wound classification ≥3 is a contaminated or dirty wound and puts the patient at approximately 7% risk of SSI.18 It has been dem-
5
onstrated as a significant cesarean organ-space SSI risk factor, similar to another study.17 Cesarean wounds among pregnant women with ROM duration >12 hours were classified as dirty wounds. Some patients without obvious history of ROM and fever may intraoperatively present with only foul-smelling amniotic fluid. These 2 entities are not identical, and no statistically significant correlation was detected in our model. Health care centers in the refugee camp have limited resources. Pregnant women who go into labor will be monitored for parturition progression using the World Health Organization’s partogram. If the progression of labor extends beyond the action line, the patient will be referred to our center. The referral process takes time to register, contact, and transfer; therefore, ROM duration is prolonged. Cases at high risk for abnormal delivery should be closely monitored and should be intervened earlier. Patient transfer should be convenient to proceed, and further vaginal delivery trial should be avoided when contraindication exists to prevent delay. Our data revealed an increased risk of SSI if the operative time was >55 minutes. This finding was consistent with a previous study in Thailand that operation time lasted longer >75th percentile (55 minutes for cesarean section), increasing the risk of cesarean SSI.17 The longer operation time may reflect the difficulty of the operation, which substantially increases the degree of contamination and also the risk of cesarean organ-space SSI. Emergency operation was at risk for unsterile technique and SSI, but it was only a risk factor of incisional SSI in our study. Similarly, previous studies revealed that elective caesarean operation was a protective factor of caesarean SSIs.10,12 The obstetrician in our setting tended to perform tubal resection or appendectomy in the elective case; therefore, these procedures showed a protective effect in the univariable regression model (unadjusted risk ratio, 0.47; 95% confidence interval, 0.370.61; P < .001; data not shown in the tables). Additionally, subgroup analysis of baseline characteristics demonstrated ethnic minority status was higher in the ≥20 years old age group. This might be because 94% of patients in our study were older than 20 years. Primigravida was more predominant among the <20 years old age group. This reflected directly with teenage marriage or pregnancy and vice versa. Longer operation time in the ≥20 years old age group might partly be because of repeated operations in the group or other causes that need further study in our setting. The strengths of this study include that it is a long-term prospective cohort study conducted in a large population and trained personnel used the CDC’s definitions to diagnose SSIs. This reduced misclassification bias, and we could infer our study domain precisely. In addition, all patients included in this study were under complete 30-day follow-up. However, 2.6% of patients who underwent cesarean section in our setting were lost from our PDS network and were excluded from this study. This may result in a lower incidence rate of cesarean SSI, and because lost to follow-up bias existed, risk factors and their strength of association were possibly imprecise. A comprehensive PDS, such as home health care and telephone follow-up, should be developed in our PDS to track the patients who were lost to follow-up. The limitation of this study was the populations in our area might differ from others; therefore, the results may not be applicable to other settings. In addition, the change in socioeconomic characteristics and populations after the forthcoming AEC may alter some risk factors. Future research should be conducted to monitor and compare risk factors of cesarean SSIs because new risk factors may occur and some existing risk factors may change in their prevalence. Meetings with personnel working in our PDS network should be conducted at least once a year to update the personnel’s knowledge and gain their opinions on PDS improvement. This may lead to complete 30-day follow-up for all patients.
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CONCLUSIONS This study reflected a high incidence of cesarean SSIs in a crowded setting with limited resources. Most cesarean SSIs were organspace SSIs and may have resulted in significant complications after surgery. Two separate degrees of cesarean SSI risk factors were demonstrated. Emergency operation was the only risk factor for cesarean incisional SSI, whereas ethnic minority status, anemia, referral, preterm labor, frequent PVs, foul-smelling amniotic fluid, and contaminated or dirty wound were found to increase the risk of cesarean organ-space SSI and reflected the delayed appropriate treatment. These findings may guide health care workers in earlier identification and increase monitoring of the cases. It may help create a surgical quality improvement program leading to reduced cesarean SSI in this setting. Acknowledgments We thank Dr Jayanton Patumanond, Clinical Research Center, Faculty of Medicine, Thammasat University, for statistical analysis assistance. References 1. Festin MR, Laopaiboon M, Pattanittum P, Ewens MR, Henderson-Smart DJ, Crowther CA. Caesarean section in four South East Asian countries: reasons for, rates, associated care practices and health outcomes. BMC Pregnancy Childbirth 2009;9:17. 2. Cunningham FG. Postoperative complication. In: Gilstrap LC, Cunningham FG, VanDorsten JP, editors. Operative obstetrics. 2nd ed. New York (NY): McGraw-Hill; 2002. p. 293-309. 3. Bruce J, Russell EM, Mollison J, Krukowski ZH. The measurement and monitoring of surgical adverse events. Health Technol Assess 2001;5:1-194. 4. Edwards JR, Peterson KD, Mu Y, Banerjee S, Allen-Bridson K, Morrell G, et al. National Healthcare Safety Network (NHSN) report: data summary for 2006 through 2008, issued December 2009. Am J Infect Control 2009;37:783-805. 5. Yokoe DS, Christiansen CL, Johnson R, Sands KE, Livingston J, Shtatland ES, et al. Epidemiology of and surveillance for postpartum infections. Emerg Infect Dis 2001;7:837-41. 6. Goepfert AR, Guinn DA, Andrews WW, Hauth JC. Necrotizing fasciitis after cesarean delivery. Obstet Gynecol 1997;89:409-12. 7. Chaim W, Bashiri A, Bar-David J, Shoham-Vardi I, Mazor M. Prevalence and clinical significance of postpartum endometritis and wound infection. Infect Dis Obstet Gynecol 2000;8:77-82.
8. Henderson E, Love EJ. Incidence of hospital-acquired infections associated with caesarean section. J Hosp Infect 1995;29:245-55. 9. Srun S, Sinath Y, Seng AT, Chea M, Borin M, Nhem S, et al. Surveillance of post-caesarean surgical site infections in a hospital with limited resources, Cambodia. J Infect Dev Ctries 2013;7:579-85. 10. Kasatpibal N, Jamulitrat S, Chongsuvivatwong V. Standardized incidence rates of surgical site infection: a multicenter study in Thailand. Am J Infect Control 2005;33:587-94. 11. Bodner K, Wierrani F, Grunberger W, Bodner-Adler B. Influence of the mode of delivery on maternal and neonatal outcomes: a comparison between elective cesarean section and planned vaginal delivery in a low-risk obstetric population. Arch Gynecol Obstet 2011;283:1193-8. 12. Olsen MA, Butler AM, Willers DM, Gross GA, Devkota P, Fraser VJ. Risk factors for endometritis after low transverse cesarean delivery. Infect Control Hosp Epidemiol 2010;31:69-77. 13. Tran TS, Jamulitrat S, Chongsuvivatwong V, Geater A. Risk factors for postcesarean surgical site infection. Obstet Gynecol 2000;95:367-71. 14. Suonio S, Huttunen M. Puerperal endometritis after abdominal twin delivery. Acta Obstet Gynecol Scand 1994;73:313-5. 15. Farret TC, Dalle J, da Silva Monteiro V, Riche CV, Antonello VS. Risk factors for surgical site infection following cesarean section in a Brazilian Women’s Hospital: a case-control study. Braz J Infect Dis 2015;19:113-7. 16. Soper DE, Mayhall CG, Dalton HP. Risk factors for intraamniotic infection: a prospective epidemiologic study. Am J Obstet Gynecol 1989;161:562-6, discussion 6-8. 17. Kasatpibal N, Norgaard M, Jamulitrat S. Improving surveillance system and surgical site infection rates through a network: a pilot study from Thailand. Clin Epidemiol 2009;1:67-74. 18. Culver DH, Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG, et al. Surgical wound infection rates by wound class, operative procedure, and patient risk index. National Nosocomial Infections Surveillance System. Am J Med 1991;91:152S-7S. 19. Franchi M, Ghezzi F, Balestreri D, Beretta P, Maymon E, Miglierina M, et al. A randomized clinical trial of two surgical techniques for cesarean section. Am J Perinatol 1998;15:589-94. 20. Borg MA, Suda D, Scicluna E. Time-series analysis of the impact of bed occupancy rates on the incidence of methicillin-resistant Staphylococcus aureus infection in overcrowded general wards. Infect Control Hosp Epidemiol 2008;29:496502. 21. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309-32. 22. Killian CA, Graffunder EM, Vinciguerra TJ, Venezia RA. Risk factors for surgical-site infections following cesarean section. Infect Control Hosp Epidemiol 2001;22:613-7. 23. Mpogoro FJ, Mshana SE, Mirambo MM, Kidenya BR, Gumodoka B, Imirzalioglu C. Incidence and predictors of surgical site infections following caesarean sections at Bugando Medical Centre, Mwanza, Tanzania. Antimicrob Resist Infect Control 2014;3:25. 24. Hassanein E-SA, Assem HM, Rezk MM, el-Maghraby RM. Study of plasma albumin, transferrin, and fibronectin in children with mild to moderate proteinenergy malnutrition. J Trop Pediatr 1998;44:362-5.
Contents lists available at ScienceDirect
American Journal of Infection Control
American Journal of Infection Control
j o u r n a l h o m e p a g e : w w w. a j i c j o u r n a l . o r g
Major articles
Risk factors for cesarean surgical site infections at a Thai-Myanmar border hospital Srisuda Assawapalanggool MNS a, Nongyao Kasatpibal PhD b,*, Supatra Sirichotiyakul MD c, Rajin Arora MD d,e, Watcharin Suntornlimsiri MD f a
Infection Control Section, Maesot Hospital, Tak, Thailand Division of Nursing Science, Faculty of Nursing, Chiang Mai University, Chiang Mai, Thailand c Department of Obstetrics and Gynecology, Faculty of Medicine, Chiang Mai University, Chiang Mai, Thailand d Department of Obstetrics and Gynecology, Lampang Hospital, Lampang, Thailand e Collaborative Project to Increase Rural Doctors, Ministry of Public Health, Thailand f Department of Obstetrics and Gynecology, Nakornping Hospital, Chiang Mai, Thailand b
Key Words: Risk factors caesarean section surgical site infections caesarean infections cohort study
Background: Cesarean surgical site infections (SSIs) are a major challenge in Thai-Myanmar border hospital settings. This study aimed to examine risk factors for SSIs after cesarean section. Methods: This was a prospective cohort study conducted in a Thai-Myanmar border hospital between January 2007 and December 2012. Data were collected from the medical record database by trained infection control nurses. Stepwise multivariable logistic regression was used for risk factor analysis and expressed as a risk ratio (RR). Results: The cesarean SSI rate was 5.9% (293 SSIs in 4,988 cases). Of these, 17.1% were incisional SSIs (10.9% superficial and 6.2% deep incisional SSIs), and 82.9% were organ or space SSIs. Risk factors for cesarean organ-space SSIs included a wound class ≥3 (RR, 4.82; 95% confidence interval [CI], 3.41-6.83), ethnic minority (RR, 2.51; 95% CI, 1.61-3.92), hemoglobin <11 g/dL (RR, 2.19; 95% CI, 1.57-3.04), pelvic examination before delivery on ≥5 occasions (RR, 4.16; 95% CI, 2.89-5.99), preterm (RR, 1.98; 95% CI, 1.33-2.95), being a local referral (RR, 3.37; 95% CI, 2.29-4.97), and foul-smelling amniotic fluid (RR, 21.08; 95% CI, 10.23-43.41). Conclusions: Most cesarean SSIs in this study seem to have a high severity. Their risk factors reflected delayed appropriate perinatal maternal care that resulted in late cesarean delivery. Early prenatal care may help reduce cesarean SSIs among this population. © 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved.
Cesarean section is a major surgery and has increasing prevalence yearly in most countries.1 Cesarean surgical site infections (SSIs), especially organ-space SSIs, are serious complications2 that can result in reoperation, increased medical cost and length of stay, rehospitalization, maternal prolongation of returning to normal function, or mortality. Incidence of cesarean SSI varies depending on the methodology of study, case definition, case identification ability of observers,3 and socioeconomic status. Among developed countries, total cesarean SSIs were approximately 1.5%-7.0%.4,5 Cesarean incisional SSI incidence was approximately 0.18%,6 and endometritis ranged from
* Address correspondence to Nongyao Kasatpibal, PhD, Division of Nursing Science, Faculty of Nursing, Chiang Mai University, Chiang Mai 50200, Thailand. E-mail address: [email protected] (N. Kasatpibal). Conflicts of Interest: None to report.
3%-6%,7,8 The cesarean SSI rates are approximately 6% in underdeveloped countries.9 In Thailand, the incidences of cesarean SSI and cesarean endometritis are 0.9% and 2.0%, respectively.1,10 Various risk factors of cesarean SSIs have been identified. An important risk of cesarean endomyometritis is the cesarean section per se.11 Other identified risk factors are classified in patientrelated conditions (eg, maternal age, socioeconomic status, 12 obesity13) and underlying medical problems. These include anemia (hemoglobin level: <11 g/dL)12; obstetric-related factors; including parity,13 zygosity,14 presence and duration of rupture of amniotic membrane (ROM),15 number of pelvic examinations (PVs),16 and presence of meconium-stained amniotic fluid (MSAF)13; gestational age <37 weeks (preterm labor)7; vaginal procedures performed before cesarean section16; associated gynecologic infections12; and surgical risk factors. Potential surgical risks of SSI include a high American Society of Anesthesiology (ASA) score, 13 high wound class, and long
0196-6553/© 2016 Association for Professionals in Infection Control and Epidemiology, Inc. Published by Elsevier Inc. All rights reserved. http://dx.doi.org/10.1016/j.ajic.2016.01.031
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operation time.17 According to the National Nosocomial Infections Study (NNIS), these are included in the risk index category.18 In addition, emergency surgery,12 type of skin incision and urethrotomy,19 blood volume lost,13 and hematoma12 are identified as potential risks. Our center is adjacent to the Thai-Myanmar border and serves up to 5 districts, including 4 refugee camps in the service area. Patients attending our center vary considerably in tribes and also conceal a variety of health and environmental problems that are overloaded in the clinic. Health care–associated infections are strongly influenced by an overcrowded setting.20 Cesarean SSIs in our center comprised at least 3.0% in 2005. The situation is predicted to worsen after the ASEAN Economic Community (AEC) establishment in 2016, which will be characterized by economic immigration. Based on epidemiologic knowledge, risk factors of cesarean SSI in our setting may differ from other regions both in types and strength of association. Exploration of such risk factors is essential for preparedness of forthcoming changes after the AEC launch.
gynecologic problem was referred to our center for consultation. Patients from camps were referred for such purposes by medics or volunteers in the camps. Patients who did not attend any followup appointments in our network were classified as lost to follow-up. Statistical analysis A statistical software package was used for sample size estimation. Based on the wound class reported in a previous study,22 the sample size was calculated using a 2-sample comparison of proportions where α = 0.05 and β = 0.80. This resulted in the minimum study size of 2,277 patients. Baseline characteristics were descriptively analyzed. Continuous data were tested between comparison groups using t test, Wilcoxon rank-sum test, analysis of variance, or Kruskal-Wallis equality of populations rank test depending on the number of comparison groups and their distribution function. Categorical variables were compared using Fisher exact test and Pearson χ2 test. Subgroup analysis was estimated in patients with cesarean SSIs for the comparison of risk factors between 2 age groups: <20 and ≥20 years. Cesarean SSIs were treated under the assumption of being a multinomial variable. Potential risk factors included age group, ethnic minority status, education level, antenatal care (ANC) status, body weight ≥80 kg, anemia, HIV infection, being referred, primigravida, preterm, PVs ≥5 times before surgery, amniotic characteristic, rupture of membrane ≥12 hours, fetal death in utero, ASA score ≥3, wound class ≥3, operation time >55 minutes, emergency operation, blood loss during operation ≥500 mL, presence of urinary tract infection before surgery, midline skin incision, and additional procedure performed during cesarean section. Each variable was univariably analyzed by using multinomial logistic regression. All significant risk factors were then included in the multivariable regression model where cesarean incisional and cesarean organspace SSIs were treated as separate dependent variables. The backward stepwise multivariable logistic regression model using a significance level for removal from the model of 0.001 was calculated, and collinearity of the independent variables in the final model was checked.
METHODS Setting The study was conducted in a crowded and limited-resource tertiary care hospital with 365 beds on the Northwestern ThaiMyanmar border, with an annual average of 800 caesarean cases. Study design and data collection The study was approved by the institute’s Research Ethical Board, Faculty of Medicine, Chiang Mai University. Data were prospectively collected from January 1, 2007-December 31, 2012, by 2 infection control nurses who had obtained Master’s degrees in infection control. Cesarean SSI cases were defined according to the Centers for Disease Control and Prevention’s (CDC’s) National Healthcare Safety Network criteria.21 Clinical signs and symptoms and medical records were reviewed through the surveillance system. These included patients demographics, background medical problems, obstetric progression with intervention or operative data, antibiotics administration, vital signs, diagnosis throughout admission, documents of their treatment and any complications, follow-up days, and follow-up method. Wounds were inspected among all patients using aseptic techniques on the third postoperative day and whenever necessary or before discharge. All patients made appointments approximately 1 week and 1 month postoperative at a convenient health center in their community in our network. The 1-week follow-up appointment focused on wound checking, and stitches were removed when necessary. When any wound complications occurred, the patient was referred for consultation. The 1-month follow-up appointment aimed at family planning and gynecologic problem screening. Again, any patient who had a
RESULTS In total, 5,122 patients underwent cesarean sections. There were 4,988 patients recruited, and 134 patients (2.6%) were lost to followup from our postdischarge surveillance system (PDS). These patients were excluded. All patients received antibiotic prophylaxis according to their obstetrician’s preference. We identified 293 of 4,988 patients (5.9%) that encountered cesarean SSIs. Of these, 17.1% were classified as incisional SSI (10.9% superficial and 6.2% deep incisional SSIs), and 82.9% were classified as organ-space SSI. Most SSI cases (88.7%) were diagnosed before discharge. The other 11.3% were detected in our PDS (Table 1). The
Table 1 Caesarean SSI classification and surveillance method (N = 4,988) Superficial incisional SSIs (n = 32)
Deep incisional SSIs (n = 18)
Organ-space SSIs (n = 243)
Characteristics
n
%
n
%
Caesarean SSI rate Surveillance method In-hospital surveillance Postdischarge surveillance Hospital OPD Other health care service centers
32
0.6
18
0.4
243
4.9
293
5.9
24 8 1 7
75.0 25.0 12.5 87.5
12 6 1 5
66.7 33.3 16.7 83.3
224 19 13 6
92.2 7.8 68.4 31.6
260 33 15 18
88.7 11.3 45.5 54.5
OPD, obstetrics and gynecology outpatient department; SSI, surgical site infection.
n
Total (n = 293) %
n
%
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Table 2 Characteristics of caesarean section patients among non-SSIs and SSIs (N = 4,988) Characteristics Age (y) <20 20-34 ≥35 Mean ± SD Ethnic minority Education level No Primary Intermediate College or higher Antenatal care No Camp Hospital Body weight (kg) ≥80 Mean ± SD Hb (g/dL) <11 Mean ± SD HIV positive Referral Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD PVs ≥5 occasions before surgery Amniotic fluid Clear MSAF Foul smelling ROM duration (h) ≥12 Median (IQR) Fetal death ASA score ≥3 Wound class ≥3 Operation time (min) >55 Mean ± SD Emergency operation EBL (mL) ≥500 Median (IQR) UTI Skin incision type Midline Pfannelstein Addition procedures Appendectomy/TR
Non-SSIs (n = 4,695)
SSIs (n = 293)
P value <.001
278 (5.9) 3,473 (74.0) 944 (20.1) 29.2 ± 6.1 2,266 (48.3)
21 (7.2) 216 (73.7) 56 (19.1) 27.8 ± 6.2 241 (82.3)
1,930 (41.1) 768 (16.4) 983 (20.9) 1,014 (21.6)
206 (70.3) 40 (13.7) 30 (10.2) 17 (5.8)
<.001
90 (1.9) 1,109 (23.6) 3,496 (74.5)
7 (2.4) 184 (62.8) 102 (34.8)
<.001
617 (13.1) 66.0 ± 12.1
44 (15.0) 64.8 ± 14.2
.010
860 (18.3) 11.4 ± 1.1 133 (2.8) 1,389 (29.6)
107 (36.5) 10.9 ± 1.7 6 (2.1) 203 (69.3)
<.001
1,716 (36.5) 2 (1-3)
149 (50.8) 1 (1-2)
<.001
531 (11.3) 38.5 ± 2.3 599 (12.8)
56 (19.1) 38.5 ± 2.8 103 (35.2)
.144
4,073 (86.7) 609 (13.0) 13 (0.3)
157 (53.6) 95 (32.4) 41 (14.0)
<.001
122 (42.7) 8.8 (0-23.3) 13 (4.4) 17 (5.8) 199 (67.9)
<.001
1,478 (31.5) 48.7 ± 13.4 3,226 (68.7)
122 (41.6) 52.5 ± 15.8 283 (96.6)
<.001
2,390 (50.9) 500 (300-500) 20 (0.4)
190 (64.9) 500 (400-600) 2 (0.7)
<.001
1,883 (40.1) 2,812 (59.9)
196 (66.9) 97 (33.1)
<.001
2,135 (45.5)
83 (28.3)
<.001
560 (12.1) 0 (0-4.2) 45 (1.0) 237 (5.1) 907 (19.3)
<.001
.582 <.001
<.001
<.001 .582 <.001
<.001
.374
NOTE. Values are n (%) or as otherwise indicated. ASA, American Society of Anesthesiology; EBL, estimated blood loss; GA, gestational age; Hb, hemoglobin; IQR, interquartile range; MSAF, meconium-stained amniotic fluid; PV, pelvic examination; ROM, rupture of amniotic membrane; SSI, surgical site infection; TR, tubal resection; UTI, urinary tract infection.
median length of hospital stay was 4 days (interquartile range, 3-5 days), and the median incubation period of the total cesarean SSIs was 4 days (interquartile range, 3-5 days). Patient characteristics included nationality, education level, place of ANC, hemoglobin level, referral status, gravidity, number of PVs prior to surgery, duration of ROM, fetal death, wound class, operation time, emergence of operation, amount of blood loss, type of skin incision, and any additional procedures that differed among patients in the organ-space SSI, incisional SSI, and non-SSI groups (Tables 2-3).
3
Risk factors of incisional SSI obtained by univariable multinomial risk ratio regression included age ≥35 years, being referred (by local setting or refugee camp), MSAF, ANC in camp, ASA score ≥3, wound class ≥3, operation time >55 minutes, and emergency operation (results not shown), but only emergency operation was demonstrated to be a risk factor of incisional SSI by backward stepwise multivariable logistic regression (Table 4). Risk factors of organ-space SSI obtained by univariable multinomial risk ratio regression included ethnic minority status, anemia, being referred, primigravida, preterm, PVs ≥5 times, MSAF, foulsmelling amniotic fluid, ROM >12 hours, ANC in camp or no ANC, fetal death, wound class ≥3, operation time >55 minutes, emergency operation, midline skin incision, and blood loss volume ≥500 mL (results not shown). However, only 7 risk factors were identified, including ethnic minority, anemia, being referred, preterm, PVs ≥5 times, foul-smelling amniotic fluid, and wound class ≥3, and remained in the model after backward stepwise multivariable logistic regression (Table 4). Subgroup analysis demonstrated ethnic minority status, education level, gravidity, gestation age, and operation time differed between the <20 and ≥20 year old age groups (Table 5). DISCUSSION Incidence of cesarean SSIs in this study (5.9%) was relatively higher than a multicenter study in Thailand (0.9%).10 This may be explained by the fact that patients in our study had a higher risk for SSI. However, the SSI rate in our study was lower than a study in Cambodia (6.3%).9 This could be because of higher standards of hygiene practiced and quality of care in Thailand compared with Cambodia. Furthermore, it might be because of the difference in the surveillance methods used to identify infections, antibiotic prophylaxis, and the patient population.23 Deep organ-space cesarean SSIs were predominant in our study. This may partly be because the major cesarean SSIs cases were referred from the local refugee camp in our area. All of the referred cases underwent vaginal delivery assistance (ie, vacuum extraction), resulting in delayed cesarean operations. Incisional SSIs, in contrast, had lesser incidence. This might be because of low health care provider experience in the PDS or out of date knowledge of some personnel because this network system was launched in 2006 and requires continuous quality improvement. Most caesarean SSI cases in this study were organ-space SSIs. Organ-space SSIs were most likely to lead to severe constitutional symptoms, most likely to lead to morbidity, and may be contributed by high virulence microbes. As a result, their detections were mostly found early, before discharge. According to the CDC and the National Healthcare Safety Network, postcesarean endometritis has been categorized as organ-space SSI. Etiologic bacteria originates mostly from the colonization of the lower genital tract and ascends and infects amnion and adjacent areas during the operation.2 Incisional SSIs, on the other hand, frequently result by inoculation of resident skin flora, bacteria from the environment, or contaminated amniotic fluid into the incision.16 Based on various etiologies of SSIs, we assumed that each type of SSI in patients admitted to our setting had different risk factors and also differed in strength of association. Several studies have demonstrated different sets of risk factors for various terms of SSIs with substantial variation in measurements used and their strengths from study to study. Organ-space SSIs encompassed the vast majority of cesarean SSIs in our study, with the 7 risk factors previously stated. Most of the non-Thai patients in our setting were either Burmese, hill tribe, political refugees, economic migrants, or of low socioeconomic and education status. As a consequence, they were malnourished and even anemic and
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Table 3 Characteristics of caesarean section patients among types of SSIs (N = 4,988) Characteristics Age (y) <20 20-34 ≥35 Mean ± SD Ethnic minority Education level No Primary Intermediate College or higher Antenatal care No Camp Hospital Body weight (kg) ≥80 Mean ± SD Hb (g/dL) <11 Mean ± SD HIV positive Referral Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD PVs ≥5 Amniotic fluid Clear MSAF Foul smelling ROM duration (h) ≥12 Median (IQR) Fetal death ASA score ≥3 Wound class ≥3 Operation time (min) >55 Mean ± SD Emergency EBL (mL) ≥500 Median (IQR) UTI Skin incision type Midline Pfannelstein Addition procedures Appendectomy/TR
Non-SSIs (n = 4,695)
Incisional SSIs (n = 50)
Organ-space SSIs (n = 243)
P value <.001
278 (5.9) 3,473 (74.0) 944 (20.1) 29.2 ± 6.1 2,266 (48.3)
4 (8.0) 29 (58.0) 17 (34.0) 29.8 ± 7.0 33 (66.0)
17 (7.0) 187 (76.9) 39 (16.1) 27.4 ± 6.0 208 (85.6)
1,930 (41.1) 768 (16.4) 983 (20.9) 1,014 (21.6)
28 (56.0) 7 (14.0) 10 (20.0) 5 (10.0)
178 (73.3) 33 (13.6) 20 (8.2) 12 (4.9)
<.001
90 (1.9) 1,109 (23.6) 3,496 (74.5)
2 (4.0) 19 (38.0) 29 (58.0)
5 (2.1) 165 (67.9) 73 (30.0)
<.001
617 (13.1) 66.0 ± 12.1
8 (16.0) 67.4 ± 16.9
36 (14.8) 64.3 ± 13.5
.013
860 (18.3) 11.4 ± 1.1 133 (2.8) 1,389 (29.6)
9 (18.0) 11.3 ± 1.7 0 (0) 25 (50.0)
98 (40.3) 10.8 ± 1.8 6 (2.5) 178 (73.3)
<.001
1,716 (36.5) 2 (1-3)
22 (44.0) 2 (1-3)
127 (52.3) 1 (1-2)
<.001
531 (11.3) 38.5 ± 2.3 599 (12.8)
9 (18.0) 38.0 ± 2.8 8 (16.0)
47 (19.3) 38.6 ± 2.8 95 (39.1)
.058
4,073 (86.7) 609 (13.0) 13 (0.3)
37 (74.0) 12 (24.0) 1 (2.0)
120 (49.4) 83 (34.2) 40 (16.5)
<.001
8 (16.0) 0 (0-8) 0 (0) 7 (14.0) 17 (34.0)
114 (48.3) 11.1 (2-24.5) 13 (5.4) 10 (4.1) 182 (74.9)
<.001
560 (12.1) 0 (0-4.2) 45 (1.0) 237 (5.1) 907 (19.3)
<.001
.720 <.001
<.001
<.001 .026 <.001 <.001
1,478 (31.5) 48.7 ± 13.4 3,226 (68.7)
23 (46.0) 54.6 ± 17.0 47 (94.0)
99 (40.7) 52.1 ± 15.6) 236 (97.1)
2,390 (50.9) 500 (300-500) 20 (0.4)
30 (60.0) 500 (400-500) 0 (0.0)
160 (65.8) 500 (400-600) 2 (0.8)
<.001
<.001
.436
1,883 (40.1) 2,812 (59.9)
25 (50.0) 25 (50.0)
171 (70.4) 72 (29.6)
<.001
2,135 (45.5)
16 (32.0)
67 (27.6)
<.001
NOTE. Values are n (%) or as otherwise indicated. ASA, American Society of Anesthesiology; EBL, estimated blood loss; GA, gestational age; Hb, hemoglobin; IQR, interquartile range; MSAF, meconium-stained amniotic fluid; PV, pelvic examination; ROM, rupture of amniotic membrane; SSI, surgical site infection; TR, tubal resection; UTI, urinary tract infection.
therefore prone to SSIs.2,7,12 Patients referred from local settings were put at increased risk of an SSI because of overcrowding, limited resources, and conservative treatment until the conditions of referral for further consultation were met. Obstetric and surgical risk factors in this study included PVs on ≥5 occasions before delivery, foulsmelling amniotic fluid, preterm labor, and a wound class of 3 or 4. These findings were similar to the results from previous studies.7,12,15 Anemia was reported as a risk factor of cesarean SSIs, but no clear reason has been established for this association.12 Anemic patients in our setting were anemic because of iron deficiency and hemoglobinopathy. Iron deficiency always coincides with other nu-
trient deficiencies24 as a result of the low socioeconomic status of the patient. Protein malnutrition will result in malfunctioning of the immune system, delayed wound healing, and infection.12,24 Moreover, low socioeconomic status always hinders the patient from accessing the health care service system, and patients with low socioeconomic status also have poor personal hygiene care. These pose some risk of SSI to the patient. To prevent SSI, improving the care system accessibility is essential. In addition, the attitude, knowledge of pregnant women about prenatal care, and nutritional status should also be improved. Multiple PVs were proven to be a risk factor of SSIs. It increases the risk of ascending infection in the amniotic cavity by
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Table 4 Multivariable risk ratios of the caesarean SSIs risk factors Characteristics Total SSIs Ethnic minority Hemoglobin <11 g/dL PVs ≥5 (occasions before surgery) Gestation age <37 wk Primigravida Referral Foul-smelling amniotic fluid Wound class ≥3 Operation time >55 min Emergency operation Incisional SSIs Emergency operation Organ-space SSIs Wound class ≥3 Ethnic minority Hemoglobin <11 g/dL PVs ≥5 Gestational age <37 wk Referral Foul-smelling amniotic fluid
RR
95% CI
P value
1.98 1.83 3.01 1.74 1.50 2.75 18.11 3.29 1.50 2.74
1.37-2.87 1.36-2.48 2.16-4.19 1.21-2.48 1.13-2.00 1.95-3.86 9.07-36.18 2.44-4.45 1.13-1.98 1.40-5.37
<.001 <.001 <.001 .003 .005 <.001 <.001 <.001 .005 .003
7.38
2.29-23.76
.001
4.82 2.51 2.19 4.16 1.98 3.37 21.08
3.41-6.83 1.61-3.92 1.57-3.04 2.89-5.99 1.33-2.95 2.29-4.97 10.23-43.41
<.001 <.001 <.001 <.001 .001 <.001 <.001
CI, confidence interval; PV, pelvic examination; RR, risk ratio; SSI, surgical site infection.
Table 5 Subgroup analysis of caesarean SSI cases between age group Caesarean SSIs Characteristics
Age <20 y
Age ≥20 y
P value
Ethnic minority Education level No Primary Intermediate College or higher Gravida Primigravida Median (IQR) GA (wk) <37 Mean ± SD Operation time (min) >55 Median (IQR)
13 (61.9)
228 (83.8)
.018
12 (57.1) 3 (14.3) 6 (28.6) 0 (0.0)
194 (71.3) 37 (13.6) 24 (8.8) 17 (6.3)
.026
17 (81.0) 1 (1-1)
132 (48.5) 2 (1-2)
.002
6 (28.6) 37.4 ± 3.0
50 (18.4) 38.6 ± 2.8
.032
118 (43.4) 50 (40-60)
.042
4 (19.1) 45 (40-50)
NOTE. Values are n (%) or as otherwise indicated. GA, Gestational age; IQR, interquartile range; SSI, surgical site infection.
inoculation of microbes from external genitalia and hence increases the risk of caesarean SSIs. 16 The probability of intraamniotic infection depends on the duration of the ROM and degree of contamination. The procedure being performed using limited resources by unskilled personnel in those settings may also increase the chance of infection. To prevent infection, PVs should be done only to monitor labor progression and strictly following sterile techniques. Preterm labor has been shown to be a risk factor for SSI in a previous study.7 This may be because some cases of preterm labor were the result of chorioamnionitis or expectant management of preterm premature ROM and leading to postpartum endometritis. Therefore, in preterm premature ROM with expectant management, delivery should be considered as soon as fetal lung maturation to shorten ROM duration and reduce the chance of infection. Foul-smelling amniotic fluid was demonstrated as a considerable risk factor for cesarean organ-space SSIs in this study. It was included in the clinical signs of chorioamnionitis, which is an important risk factor of cesarean organ-space SSIs.13 Wound classification ≥3 is a contaminated or dirty wound and puts the patient at approximately 7% risk of SSI.18 It has been dem-
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onstrated as a significant cesarean organ-space SSI risk factor, similar to another study.17 Cesarean wounds among pregnant women with ROM duration >12 hours were classified as dirty wounds. Some patients without obvious history of ROM and fever may intraoperatively present with only foul-smelling amniotic fluid. These 2 entities are not identical, and no statistically significant correlation was detected in our model. Health care centers in the refugee camp have limited resources. Pregnant women who go into labor will be monitored for parturition progression using the World Health Organization’s partogram. If the progression of labor extends beyond the action line, the patient will be referred to our center. The referral process takes time to register, contact, and transfer; therefore, ROM duration is prolonged. Cases at high risk for abnormal delivery should be closely monitored and should be intervened earlier. Patient transfer should be convenient to proceed, and further vaginal delivery trial should be avoided when contraindication exists to prevent delay. Our data revealed an increased risk of SSI if the operative time was >55 minutes. This finding was consistent with a previous study in Thailand that operation time lasted longer >75th percentile (55 minutes for cesarean section), increasing the risk of cesarean SSI.17 The longer operation time may reflect the difficulty of the operation, which substantially increases the degree of contamination and also the risk of cesarean organ-space SSI. Emergency operation was at risk for unsterile technique and SSI, but it was only a risk factor of incisional SSI in our study. Similarly, previous studies revealed that elective caesarean operation was a protective factor of caesarean SSIs.10,12 The obstetrician in our setting tended to perform tubal resection or appendectomy in the elective case; therefore, these procedures showed a protective effect in the univariable regression model (unadjusted risk ratio, 0.47; 95% confidence interval, 0.370.61; P < .001; data not shown in the tables). Additionally, subgroup analysis of baseline characteristics demonstrated ethnic minority status was higher in the ≥20 years old age group. This might be because 94% of patients in our study were older than 20 years. Primigravida was more predominant among the <20 years old age group. This reflected directly with teenage marriage or pregnancy and vice versa. Longer operation time in the ≥20 years old age group might partly be because of repeated operations in the group or other causes that need further study in our setting. The strengths of this study include that it is a long-term prospective cohort study conducted in a large population and trained personnel used the CDC’s definitions to diagnose SSIs. This reduced misclassification bias, and we could infer our study domain precisely. In addition, all patients included in this study were under complete 30-day follow-up. However, 2.6% of patients who underwent cesarean section in our setting were lost from our PDS network and were excluded from this study. This may result in a lower incidence rate of cesarean SSI, and because lost to follow-up bias existed, risk factors and their strength of association were possibly imprecise. A comprehensive PDS, such as home health care and telephone follow-up, should be developed in our PDS to track the patients who were lost to follow-up. The limitation of this study was the populations in our area might differ from others; therefore, the results may not be applicable to other settings. In addition, the change in socioeconomic characteristics and populations after the forthcoming AEC may alter some risk factors. Future research should be conducted to monitor and compare risk factors of cesarean SSIs because new risk factors may occur and some existing risk factors may change in their prevalence. Meetings with personnel working in our PDS network should be conducted at least once a year to update the personnel’s knowledge and gain their opinions on PDS improvement. This may lead to complete 30-day follow-up for all patients.
ARTICLE IN PRESS S. Assawapalanggool et al. / American Journal of Infection Control ■■ (2016) ■■-■■
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CONCLUSIONS This study reflected a high incidence of cesarean SSIs in a crowded setting with limited resources. Most cesarean SSIs were organspace SSIs and may have resulted in significant complications after surgery. Two separate degrees of cesarean SSI risk factors were demonstrated. Emergency operation was the only risk factor for cesarean incisional SSI, whereas ethnic minority status, anemia, referral, preterm labor, frequent PVs, foul-smelling amniotic fluid, and contaminated or dirty wound were found to increase the risk of cesarean organ-space SSI and reflected the delayed appropriate treatment. These findings may guide health care workers in earlier identification and increase monitoring of the cases. It may help create a surgical quality improvement program leading to reduced cesarean SSI in this setting. Acknowledgments We thank Dr Jayanton Patumanond, Clinical Research Center, Faculty of Medicine, Thammasat University, for statistical analysis assistance. References 1. Festin MR, Laopaiboon M, Pattanittum P, Ewens MR, Henderson-Smart DJ, Crowther CA. Caesarean section in four South East Asian countries: reasons for, rates, associated care practices and health outcomes. BMC Pregnancy Childbirth 2009;9:17. 2. Cunningham FG. Postoperative complication. In: Gilstrap LC, Cunningham FG, VanDorsten JP, editors. Operative obstetrics. 2nd ed. New York (NY): McGraw-Hill; 2002. p. 293-309. 3. Bruce J, Russell EM, Mollison J, Krukowski ZH. The measurement and monitoring of surgical adverse events. Health Technol Assess 2001;5:1-194. 4. Edwards JR, Peterson KD, Mu Y, Banerjee S, Allen-Bridson K, Morrell G, et al. National Healthcare Safety Network (NHSN) report: data summary for 2006 through 2008, issued December 2009. Am J Infect Control 2009;37:783-805. 5. Yokoe DS, Christiansen CL, Johnson R, Sands KE, Livingston J, Shtatland ES, et al. Epidemiology of and surveillance for postpartum infections. Emerg Infect Dis 2001;7:837-41. 6. Goepfert AR, Guinn DA, Andrews WW, Hauth JC. Necrotizing fasciitis after cesarean delivery. Obstet Gynecol 1997;89:409-12. 7. Chaim W, Bashiri A, Bar-David J, Shoham-Vardi I, Mazor M. Prevalence and clinical significance of postpartum endometritis and wound infection. Infect Dis Obstet Gynecol 2000;8:77-82.
8. Henderson E, Love EJ. Incidence of hospital-acquired infections associated with caesarean section. J Hosp Infect 1995;29:245-55. 9. Srun S, Sinath Y, Seng AT, Chea M, Borin M, Nhem S, et al. Surveillance of post-caesarean surgical site infections in a hospital with limited resources, Cambodia. J Infect Dev Ctries 2013;7:579-85. 10. Kasatpibal N, Jamulitrat S, Chongsuvivatwong V. Standardized incidence rates of surgical site infection: a multicenter study in Thailand. Am J Infect Control 2005;33:587-94. 11. Bodner K, Wierrani F, Grunberger W, Bodner-Adler B. Influence of the mode of delivery on maternal and neonatal outcomes: a comparison between elective cesarean section and planned vaginal delivery in a low-risk obstetric population. Arch Gynecol Obstet 2011;283:1193-8. 12. Olsen MA, Butler AM, Willers DM, Gross GA, Devkota P, Fraser VJ. Risk factors for endometritis after low transverse cesarean delivery. Infect Control Hosp Epidemiol 2010;31:69-77. 13. Tran TS, Jamulitrat S, Chongsuvivatwong V, Geater A. Risk factors for postcesarean surgical site infection. Obstet Gynecol 2000;95:367-71. 14. Suonio S, Huttunen M. Puerperal endometritis after abdominal twin delivery. Acta Obstet Gynecol Scand 1994;73:313-5. 15. Farret TC, Dalle J, da Silva Monteiro V, Riche CV, Antonello VS. Risk factors for surgical site infection following cesarean section in a Brazilian Women’s Hospital: a case-control study. Braz J Infect Dis 2015;19:113-7. 16. Soper DE, Mayhall CG, Dalton HP. Risk factors for intraamniotic infection: a prospective epidemiologic study. Am J Obstet Gynecol 1989;161:562-6, discussion 6-8. 17. Kasatpibal N, Norgaard M, Jamulitrat S. Improving surveillance system and surgical site infection rates through a network: a pilot study from Thailand. Clin Epidemiol 2009;1:67-74. 18. Culver DH, Horan TC, Gaynes RP, Martone WJ, Jarvis WR, Emori TG, et al. Surgical wound infection rates by wound class, operative procedure, and patient risk index. National Nosocomial Infections Surveillance System. Am J Med 1991;91:152S-7S. 19. Franchi M, Ghezzi F, Balestreri D, Beretta P, Maymon E, Miglierina M, et al. A randomized clinical trial of two surgical techniques for cesarean section. Am J Perinatol 1998;15:589-94. 20. Borg MA, Suda D, Scicluna E. Time-series analysis of the impact of bed occupancy rates on the incidence of methicillin-resistant Staphylococcus aureus infection in overcrowded general wards. Infect Control Hosp Epidemiol 2008;29:496502. 21. Horan TC, Andrus M, Dudeck MA. CDC/NHSN surveillance definition of health care-associated infection and criteria for specific types of infections in the acute care setting. Am J Infect Control 2008;36:309-32. 22. Killian CA, Graffunder EM, Vinciguerra TJ, Venezia RA. Risk factors for surgical-site infections following cesarean section. Infect Control Hosp Epidemiol 2001;22:613-7. 23. Mpogoro FJ, Mshana SE, Mirambo MM, Kidenya BR, Gumodoka B, Imirzalioglu C. Incidence and predictors of surgical site infections following caesarean sections at Bugando Medical Centre, Mwanza, Tanzania. Antimicrob Resist Infect Control 2014;3:25. 24. Hassanein E-SA, Assem HM, Rezk MM, el-Maghraby RM. Study of plasma albumin, transferrin, and fibronectin in children with mild to moderate proteinenergy malnutrition. J Trop Pediatr 1998;44:362-5.