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doi:10.1111/jog.12273

J. Obstet. Gynaecol. Res. Vol. 40, No. 4: 954–960, April 2014

Value of maternal procalcitonin levels for predicting subclinical intra-amniotic infection in preterm premature rupture of membranes Tülay Oludag, Funda Gode, Erkan Caglayan, Bahadir Saatli, Recep Emre Okyay and Sabahattin Altunyurt Obstetrics and Gynecology Department, Dokuz Eylul University School of Medicine, Izmir, Turkey

Abstract Aim: To determine whether procalcitonin (ProCT) levels can be used to predict subclinical intra-amniotic infection by comparing maternal plasma levels in preterm premature rupture of membranes (PPROM) and premature rupture of membranes (PROM) at term with the levels in healthy pregnant women. Methods: The mean plasma ProCT levels of 32 patients with PPROM, 35 patients with PROM at term, 24 healthy women at preterm gestation and 30 healthy women at term were compared. In the PPROM group, the presence or absence of histological chorioamnionitis and neonatal infection were used as a reference to analyze ProCT levels. Results: The mean ProCT level of patients in the PPROM group was significantly higher than those in the PROM group and healthy controls. Patients in the PPROM group diagnosed with histological chorioamnionitis had significantly higher ProCT levels than those of the remaining patients. At a cut-off of 0.054 ng/mL, the sensitivity and specificity of ProCT to predict histological chorioamnionitis were 92.3% and 68.4%, respectively. Conclusion: ProCT levels were significantly higher in patients with PPROM, and facilitate identification of those who require expectant management. Key words: chorioamnionitis, maternal, membrane rupture, preterm delivery, procalcitonin.

Introduction Preterm premature rupture of the fetal membranes (PPROM) affects 2–4.5% of all pregnancies and is associated with perinatal morbidity and mortality.1 One of the primary causes of perinatal morbidity is intrauterine infection, which complicates 40–70% of PPROM cases.1–4 When the characteristic clinical signs are present, the condition is referred to as clinical chorioamnionitis or clinical intra-amniotic infection.

There is significant overlap between clinical and histological chorioamnionitis; however, the latter is more commonly diagnosed based on the pathological findings from microscopic examination of the placenta in cases of subclinical or clinical chorioamnionitis. In addition, subclinical chorioamnionitis may manifest as preterm labor or PPROM.4 Chorioamnionitis causes a spectrum of complications for the mother and fetus. Septic shock, disseminated intravascular coagulation and maternal death are

Received: November 27 2012. Accepted: August 15 2013. Reprint request to: Dr Funda Gode, MD, Private Sada Hospital, Canakkale Asfaltı, 2/1 Menemen, I˙zmir 35660, Turkey. Email: [email protected] The English in this document has been checked by at least two professional editors, both native speakers of English. For a certificate, please see: http://www.textcheck.com/certificate/SHnyUi Conflict of interest: None declared.

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Procalcitonin levels in PPROM

serious, but extremely rare, for the mother.2,5 Complications for the fetus include direct fetal infection, sepsis and death. The fetal response to infection, termed fetal inflammatory response syndrome (FIRS), may induce cerebral white matter injury and result in cerebral palsy and other short- and long-term neurological deficits.2,6,7 Therefore, early and appropriate management of chorioamnionitis is important to reduce fetal and maternal complications. Maternal markers, including C-reactive protein (CRP), white blood cells (WBC), interleukin (IL)-6, IL-10, tumor necrosis factor (TNF)-α and granulocytecolony stimulating factor (G-CSF) have been used to predict chorioamnionitis and neonatal infection in pregnant women with premature rupture of membranes (PROM).1,8,9 However, none of these markers are used for the management of PROM, and current treatment strategies are based on gestational age.8,10 Procalcitonin (ProCT) is a 116-amino-acid peptide precursor of calcitonin.11 Microbial infections induce a ubiquitous increase in CALC1 gene expression and a subsequent release of calcitonin precursors from all of the tissues and cell types throughout the body.12 The increase in ProCT in bacterial infections often correlates with disease severity and mortality.11 Furthermore, increases in ProCT occur more rapidly than increases in CRP.13 ProCT can be detected in the plasma 2 h after injection of endotoxins, rising within 6–8 h and reaching a plateau after 20–72 h. ProCT and CRP decrease to their normal values after 2–3 days and 3–7 days, respectively.11,13–15 The use of ProCT as an early marker of bacterial infection in neonates and infants results in better sensitivity and specificity than CRP.11 The aim of our study was to evaluate the relationship between maternal plasma ProCT levels and subclinical intra-amniotic infection in cases of PPROM. Additionally, we compared the plasma ProCT levels of women with PPROM and PROM at term with the levels in healthy pregnant women.

Methods This prospective study was conducted at Dokuz Eylül University Hospital from March–December 2008. The institutional review board approved the study and informed consent was obtained from all of the patients. A total of 121 patients with singleton pregnancies admitted to our hospital were included in the study. The patients were divided into four groups according to gestational week and membrane rupture status: group 1 included 32 patients with PPROM between 24

and 34 weeks of pregnancy; group 2 included 35 patients with PROM at term; group 3 included 24 healthy women at preterm gestation between 24 and 34 weeks of pregnancy; and group 4 included 30 healthy women at term. Groups 3 and 4 represented the control groups of patients and were selected at random during the study period. Women with multiple pregnancies, clinical signs of infection, cervical dilatations of 2 cm or more, or other maternal or fetal complications were not included in the study. Rupture of membranes was diagnosed by sterile speculum examination to confirm fluid leakage from the cervical canal. All of the patients in group 1 received prophylactic i.v. antibiotics (sulbactam–ampicillin 1.5 g every 6 h) after membrane rupture until delivery. In addition, steroid therapy with betamethasone (two 12-mg doses at 12-h intervals) was used for pulmonary maturation in all group 1 patients. The induction of labor with i.v. oxytocin was initiated in all group 2 patients after hospital admission. Subclinical infection was detected with laboratory indices (WBC count of ≥15 000 c/mm3, CRP of ≥1 mg/dL and pathological evaluation of placentas) without any symptoms of infection in group 1 patients. A placental pathological evaluation was conducted for the diagnosis of histological chorioamnionitis. The neonatal records of group 1 patients were assessed for a positive blood culture after 72 h and CRP levels measured to diagnose neonatal infection. Procalcitonin, WBC and CRP levels in groups 1 and 2 patients with PROM were measured in venous blood samples collected within 6 h before administration of any drugs. In other groups, samples were taken during routine ambulatory visits. The venous blood samples of all of the patients were centrifuged at 4000 g for 10 s, and plasma stored at −80°C until analysis. ProCT was measured with an ultrasensitive immunoassay using TRACE (Time Resolved Amplified Cryptate Emission) technology (Kryptor; Brahms). This assay measures concentrations between 0.02 and 5000 ng/mL (0.02– 50 ng/mL directly and up to 5000 ng/mL after sample dilution). The detection limit calculated using the imprecision profile was assessed at 0.019 ng/mL with a 95% probability. The functional assay sensitivity, defined as the lowest analyte concentration that can be determined with an interassay coefficient of variation of less than 20, was assessed at 0.06 ng/mL with a 95% probability. The assay allows for measurement of ProCT with a turnaround time (TAT) of approximately 20 min. WBC counts were determined with the Beckman Coulter GLH750 instrument. The CRP levels

© 2013 The Authors Journal of Obstetrics and Gynaecology Research © 2013 Japan Society of Obstetrics and Gynecology

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Table 1 Clinical characteristics of the patients

Age (years) BMI (kg/m2) Primiparous, n (%) Gestational age at PROM (weeks) Cesarean section delivery n (%) Birthweight

Group 1 (n = 32)

Group 2 (n = 35)

Group 3 (n = 24)

Group 4 (n = 30)

29.1 ± 5.8 27.4 ± 2.9 9 (28.1) 28.1 ± 3.3 19 (59.4) 1710 ± 827

28.5 ± 5.4 26.9 ± 2.1 19 (54.2) 38 ± 1.1 17 (48.5) 3203 ± 460

28.7 ± 5.6 26.5 ± 1.8 9 (37.5) 30.7 ± 2.6 11 (45.8) 3166 ± 372

27.2 ± 4.2 27 ± 1.9 19 (63.3) 39.6 ± 1.2 16 (53.3) 3444 ± 392

Group 1 included patients with preterm premature rupture of membranes between the 24th and 34th weeks of pregnancy; group 2 included patients with PROM at term; group 3 included healthy women at preterm gestation between the 24th and 34th weeks of pregnancy; and group 4 included healthy women at term. BMI, body mass index; PROM, premature rupture of membranes.

were measured by immunoturbidimetry using the Abbott Diagnostics Architect c16000 System (Abbott Diagnostics). The critical values for analysis of WBC and CRP were accepted as 15.0 c/mm3 and 1 mg/dL, respectively, based on data from Torbe et al.16

Statistical analysis The Statistical Package for the Social Sciences version 15 was used for statistical analysis. Parametric comparisons between more than two groups were performed with one-way anova. Non-parametric comparisons between more than two groups were performed with the Kruskal–Wallis test. A receiver–operator curve analysis was employed to establish the cut-off value of plasma ProCT for the prediction of neonatal infection and histological chorioamnionitis. The sensitivity, specificity, positive and negative predictive values were calculated. In addition, the predictive values of a WBC count of 15.0 c/mm3 or higher and a CRP level of 1 mg/dL or higher were evaluated. Data are presented as means ± standard deviation and a value of P < 0.05 was taken to indicate statistical significance.

Results The clinical characteristics of the groups are shown in Table 1. No significant differences were detected between the groups, except for birthweight and gestational week. Laboratory values of each group are shown in Table 2. The mean ProCT level was significantly higher in group 1 (0.086 ng/mL) than in groups 2 and 3. No significant differences in mean ProCT levels were detected between groups 2 and 4. The mean CRP levels were significantly higher in group 1 (2.27 ± 0.29 mg/dL) than in group 2 (0.86 ± 0.16 mg/ dL) and group 3 (0.61 ± 0.34 mg/dL). No significant differences in the mean CRP levels were detected between groups 2 and 4. The WBC count was signifi-

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Table 2 Comparison of the ProCT levels between the groups Groups

ProCT (ng/mL) (range)

Group 1 (n = 32) Group 2 (n = 35) Group 3 (n = 24) Group 4 (n = 30)

0.086 ± 0.01 (0.013–0.490) 0.043 ± 0.02 (0.009–0.140) 0.033 ± 0.01 (0.001–0.056) 0.035 ± 0.01 (0.013–0.068)

Groups 1 and 2, P < 0.05, groups 1 and 3, P < 0.05, groups 2 and 4, not significant, groups 3 and 4, not significant. Group 1 included patients with preterm premature rupture of membranes between the 24th and 34th weeks of pregnancy; group 2 included patients with premature rupture of membranes at term; group 3 included healthy women at preterm gestation between the 24th and 34th weeks of pregnancy; and group 4 included healthy women at term. ProCT, procalcitonin.

cantly higher in group 1 (14 287 ± 4367 c/mm3) than in group 3 (10 462 ± 2811 c/mm3). No significant differences in the WBC counts were detected among the other groups. White blood cell and CRP values were re-analyzed in group 1 patients to detect subclinical intrauterine infection; these values were compared to the mean ProCT levels. We did not detect any significant differences in the ProCT levels between patients with a WBC count of 15 000 c/mm3 or more and less than 15 000 c/mm3 (P = 0.58). We also did not detect any significant differences in the ProCT levels between the patients with CRP levels of 1 mg/dL or more and less than 1 mg/dL (P = 0.29). Additionally, the mean ProCT levels of patients who gave birth to newborns with and without neonatal infection were not significantly different (P = 0.07). The sensitivity, specificity, positive predictive value and negative predictive value of the ProCT, WBC counts and CRP levels in predicting histological chorioamnionitis and neonatal infection are shown in Table 3. In group 1 patients, the mean ProCT level of patients diagnosed with histological chorioamnionitis

© 2013 The Authors Journal of Obstetrics and Gynaecology Research © 2013 Japan Society of Obstetrics and Gynecology

Procalcitonin levels in PPROM

Table 3 Prognostic value of maternal ProCT, WBC and CRP levels in the prediction of neonatal infection and histological chorioamnionitis Neonatal infection

Histological chorioamnionitis

PCT ≥0.054 ng/mL

Sensitivity (%) Specificity (%) PPV (%) NPV (%)

71.4 55.6 55.6 71.4

92.3 68.4 66.7 92.9

WBC ≥15 000 c/mm3

Sensitivity (%) Specificity (%) PPV (%) NPV (%)

64.2 83.3 75 75

53.8 73.6 58.3 70

CRP ≥1 mg/dL

Sensitivity (%) Specificity (%) PPV (%) NPV (%)

92.8 44.4 56.5 88.8

92.3 36.8 50 87.5

CRP, C-reactive protein; NPV, negative predictive value; PPV, positive predictive value; ProCT, procalcitonin; WBC, white blood cells.

natal infection (P < 0.05). However, the WBC count was not significantly different between patients with and without histological chorioamnionitis. The mean CRP levels were significantly higher in patients who gave birth to newborns with neonatal infection than in those who gave birth to newborns without neonatal infection (P < 0.05). In addition, CRP levels were significantly higher in patients diagnosed with histological chorioamnionitis (P < 0.05).

1,0

Sensivity

0,8

0,6

0,4

Discussion

0,2

0,0 0,0

0,2

0,4

0,6

0,8

1,0

Specificity Figure 1 Receiver–operator curve analysis of procalcitonin (ProCT), white blood cell (WBC) count and C-reactive protein (CRP) levels for the prediction , ProCT; , WBC of histological chorioamnionitis. , CRP; , reference. count;

(n = 13, 40.7%) was significantly higher than that of the remaining patients in the group (P < 0.05). The cutoff value for ProCT in predicting histological chorioamnionitis showed that the highest sensitivity and specificity corresponded to a concentration of 0.054 ng/mL (Fig. 1). The sensitivity of ProCT to predict histological chorioamnionitis was 92.3%, the specificity was 68.4%, positive predictive value was 66.7% and negative predictive value was 92.9%. In group 1 patients, the WBC count was significantly higher in those who gave birth to newborns with neo-

Preterm premature membrane rupture management remains a challenge for obstetricians. The current management for PROM before 34 weeks of gestation is antibiotic prophylaxis and steroid therapy.2 PROM patients are generally observed with bedrest until active labor or signs of infection develop.17 However, the early diagnosis of chorioamnionitis is important for the management of these patients because clinical signs of intrauterine infection may not be recognized until after fetal neurological development is impacted by subclinical intra-amniotic infection and FIRS.18 The current methods of predicting subclinical intraamniotic infection are limited and unsatisfactory. Inflammatory markers can be evaluated in amniotic fluid and a diagnosis of chorioamnionitis can be based on the results of amniocentesis; however, the risk of complications from this procedure is significant. In addition, the procedure may cause intrauterine infection and cannot be repeated regularly. Another disadvantage of the procedure is decreased amniotic fluid volume in PROM patients. Therefore, easy, safe and

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repeatable methods are required in clinical practice.19 Several mediators in vaginal and cervical fluid may be beneficial; however, their concentrations can change as a result of PROM.19,20 Procalcitonin is a novel marker for the diagnosis of infectious diseases. In bacterial infections, an increase in ProCT often correlates with disease severity and mortality.11 The upper limit of the ProCT in systemic inflammatory response syndrome and sepsis has been accepted as 0.5 ng/mL. However, this value is approximately 10 times greater than the plasma ProCT levels in a healthy population, and there are no direct cut-off levels for localized and subclinical infections. ProCT can be measured by a semiquantitative assay (PCT-Q; Brahms), a quantitative assay, such as the luminometric immunoassay (Lumitest; Brahms) or an ultrasensitive immunoassay using TRACE (Kryptor; Brahms). Lumitest has been the method used most commonly for the detection of ProCT levels; however, Kryptor is the most sensitive and precise quantitative immunoassay21 and was used in our study for the detection of plasma ProCT levels. Data describing normal levels of ProCT during pregnancy are limited. Morgenthaler et al. did not find any differences in ProCT levels between healthy controls and pregnant women,22 while Paccolat et al. reported recently that the median levels of PCT were 0.043 ng/mL at 24–28 weeks of pregnancy and 0.061 ng/mL at 36–40 weeks of pregnancy.23 Additional studies are needed to determine the exact reference values for ProCT in pregnant women. In our study, we did not detect any significant differences in the ProCT levels between 24 and 36 weeks of pregnancy in healthy pregnant women (0.033 ng/mL) and 36–41 weeks of pregnancy in healthy pregnant women (0.035 ng/mL). Procalcitonin was first described during pregnancy by Torbe et al. in the cervicovaginal secretions of preterm delivery patients. However, a relationship between cervicovaginal ProCT concentrations, and the beginning of active delivery and signs of infection was not identified.24 A subsequent study found higher maternal plasma ProCT levels in preterm delivery patients than in healthy control pregnant women.25 The data correlating PROM with ProCT levels are also limited. Torbe et al. did not detect any association between cervicovaginal fluid ProCT levels and subclinical intra-amniotic infection in PROM patients.16 However, they found higher cervicovaginal ProCT levels in PPROM patients than in term PROM patients16 and higher plasma ProCT levels in PPROM patients

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than in term PROM patients and healthy controls,26 which correlates with the results presented here. In the present study, we found higher ProCT levels in PPROM (group 1) patients than in PROM (group 2) patients and in healthy pregnant women at 24–36 weeks of pregnancy (group 3). The mean ProCT level in term PROM (group 2) patients was higher than in term controls (group 4); however, the difference was not statistically significant. These results suggest that infection may play a role in the etiology of PPROM, whereas an inflammatory response may contribute to PROM in patients at term. In this study, we investigated the role of maternal ProCT levels in predicting subclinical intra-amniotic infection. Torbe et al. found a lower sensitivity (75%) and specificity (45%) of ProCT levels in predicting histological chorioamnionitis than our study.26 Kopyra et al. recently evaluated the usefulness of ProCT, IL-6 and CRP measurements in the prediction of intraamniotic infection and newborn status in PPROM patients. They found that ProCT had a higher predictive value than CRP and IL-6 in predicting chorioamnionitis and newborn infection.27 The exact role of CRP levels in the diagnosis of intra-amniotic infection is not clear. In a recent meta-analysis, the sensitivity and specificity of CRP levels for the diagnosis of chorioamnionitis was found to be 72.8% and 76.4%, respectively.28 In our study, the mean CRP and ProCT levels were higher in patients with histological chorioamnionitis. The specificity and positive predictive value of ProCT level for detecting histological chorioamnionitis were higher than those of the CRP levels, whereas the predictive value of the CRP levels for neonatal infection was higher than that of the ProCT levels. Therefore, from a neonatal prognostic standpoint, CRP values seem to be superior to ProCT for predicting neonatal infection. During pregnancy, many inflammatory changes occur, and cortisol and other factors cause the WBC count to normally increase and peak at the end of pregnancy.29 Therefore, WBC counts may not precisely predict the clinical conditions in pregnant women. We did not detect any significant differences between groups 1 and 2, which may be due to the normal physiological increase in the WBC count during pregnancy. Because this study was designed to detect occult intrauterine infections, samples were collected from patients during the first 6 h of membrane rupture. Thus, increases in the ProCT levels, CRP levels and WBC counts due to ascendant infections during follow-up were excluded. The latent phase of labor

© 2013 The Authors Journal of Obstetrics and Gynaecology Research © 2013 Japan Society of Obstetrics and Gynecology

Procalcitonin levels in PPROM

may be shortened by an intrauterine infection; however, this phase may be affected by other factors that influence the decision to initiate labor. Therefore, we did not investigate the relationship between the latent phase of labor and maternal ProCT levels. In conclusion, we found higher ProCT levels in PPROM patients than in healthy controls and term PROM patients, suggesting an infectious etiology in these groups of patients. ProCT may be more beneficial than CRP in the decision to clinically observe preterm PROM patients because of its higher specificity for predicting histological chorioamnionitis. In addition, the kinetics of ProCT are more rapid than CRP, which makes it a better option for treatment monitoring. However, the cost-effectiveness of widespread use of ProCT as a marker has not been investigated. Larger studies are required to detect the cut-off values of ProCT for predicting subclinical intra-amniotic infections, which will facilitate safe observation of PPROM patients.

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9. Murtha AP, Sinclair T, Hauser ER, Swamy GK, Herbert WN, Heine RP. Maternal serum cytokines in preterm premature rupture of membranes. Obstet Gynecol 2007; 109: 121– 127. 10. Royal College of Obstetricians and Gynaecologists (RCOG): Preterm labour rupture of membranes. Royal College of Obstetricians and Gynecologists 2006, Guideline No.44. 11. Van Rossum AM, Wulkan RW, Quedusluys-Murphy AM. Procalcitonin as an early marker of infection in neonates and children. Lancet Infect Dis 2004; 4: 620–630. 12. Muller B, White JC, Nylen ES, Snider RH, Becker KL, Habener JF. Ubiquitous expression of the calcitonin-i gene in multiple tissues in response to sepsis. J Clin Endocrinol Metab 2001; 86: 396–404. 13. Dandona P, Nix D, Wilson MF et al. Procalcitonin increase after endotoxin injection in normal subjects. J Clin Endocrinol Metab 1998; 83: 3296–3301. 14. Brunkhorst FM, Heinz U, Forycki ZF. Kinetics of procalcitonin in iatrogenic sepsis. Intensive Care Med 1998; 24: 888–889. 15. Gabay C, Kushner I. Acute-phase proteins and other systemic responses to inflammation. N Engl J Med 1999; 340: 448– 454. 16. Torbe A, Czajka R. Are vaginal fluid procalcitonin levels useful for the prediction of subclinical infection in patients with preterm premature rupture of membranes? J Obstet Gynecol Res 2005; 31: 464–470. 17. Turhan NO, Karabulut A, Adam B. Maternal serum interleukin 6 levels in preterm labor: Prediction of admission-to delivery interval. J Perinat Med 2000; 28: 133– 139. 18. Wu Y, Colford J. Chorioamnionitis as a risk factor for cerebral palsy: A metaanalysis. JAMA 2000; 284: 1417–1424. 19. Di Naro E, Ghezzi F, Raio L et al. C-reactive protein in vaginal fluid of patients with preterm premature rupture of membranes. Acta Obstet Gynecol Scand 2003; 82: 1072– 1079. 20. Rizzo G, Capponi A, Rinaldo D, Tedeschi D, Arduini D, Romanini C. Interleukin-6 concentrations in cervical secretions identify microbial invasion of the amniotic cavity in patients with preterm labor and intact membranes. Am J Obstet Gynecol 1996; 175: 812–817. 21. Manzano S, Bailey B, Girias JB, Cousineau J, Delvin E, Gervaix A. Comparison of procalcitonin measurement by a semiquantitative method in a pediatric emergency department. Clin Biochem 2009; 42: 1557–1560. 22. Morgenthaler NG, Struck J, Fischer-Schulz C, Seidel-Mueller E, Beier W, Bergmann A. Detection of procalcitonin(PCT) in healthy controls and patients with local infection by a sensitive ILMA. Clin Lab 2002; 48: 263–270. 23. Paccolat C, Harbarth S, Courvoisier D, Irion O, deTejada BM. Procalcitonin levels during pregnancy,delivery and postpartum. J Perinat Med 2011; 39: 679–683. 24. Torbe A, Czajka R. Procalcitonin in cervico-vaginal secretion pregnancies complicated by preterm labor- a preliminary report. Eur J Obstet Gynecol Reprod Biol 2004; 116: 177– 181. 25. Torbe A, Czajka R. Maternal plasma procalcitonin concentrations in patients with preterm labor and intact membranes-prediction of preterm delivery and admission to delivery interval. J Perinat Med 2004; 32: 332–336.

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26. Torbe A. Maternal plasma procalcitonin concentrations in pregnancy complicated by preterm premature rupture of membranes. Mediators Inflamm 2007; 2007: 35782–35787. 27. Kopyra P, Seremak-Mrozikiewicz A, Drews K. Usefulness of PCT, IL-6, CRP measurement in the prediction of intraamniotic infection and newborn status in pregnant women with premature rupture of membranes. Ginekol Pol 2010; 81: 336–341.

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© 2013 The Authors Journal of Obstetrics and Gynaecology Research © 2013 Japan Society of Obstetrics and Gynecology

Value of maternal procalcitonin levels for predicting subclinical intra-amniotic infection in preterm premature rupture of membranes.

To determine whether procalcitonin (ProCT) levels can be used to predict subclinical intra-amniotic infection by comparing maternal plasma levels in p...
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