Abstract
Objective:
To compare AmnioQuick Duo+ versus the placental α-microglobulin-1 (PAMG-1) test for diagnosis of prolonged premature rupture of membranes (PROM).
Methods:
A multicenter prospective cohort study included women with suspected PROM at six tertiary institutions in southern Nigeria between January 1 and December 31, 2015. The inclusion criteria were features of PROM lasting at least 24 hours and a pregnancy duration of more than 24 weeks. AmnioQuick Duo+ (Biosynex, Strasbourg, France) and PAMG-1 (AmniSure International, Boston, USA) tests were used to diagnose PROM, which was confirmed after delivery by any two of the following criteria: delivery within 48 hours to 7 days, chorioamnionitis, membranes perceptibly ruptured at delivery, and adverse perinatal outcomes considerably associated with prolonged PROM.
Results:
Of 100 women assessed for eligibility, 99 were included. Sensitivity, specificity, and accuracy were, respectively, 97.3%, 100%, and 95.9% for AmnioQuick Duo+, and 93.2%, 100%, and 90.4% for PAMG-1. The differences were not significant and the diagnostic discordant rate between the two tests was 3.1%. In equivocal cases (i.e., negative pooling test result), AmnioQuick Duo+ and PAMG-1 performed equally (diagnostic accuracy, 100% vs 97.7%; P>0.99).
Conclusion:
For diagnosis of PROM, AmnioQuick Duo+ was found to be non-inferior and comparable in accuracy to the PAMG-1 test, with a diagnostic discordance rate of 3.1%.
Keywords: Accuracy, AmnioQuick Duo+, Equivocal, PAMG-1, Prolonged, PROM
1 ∣. INTRODUCTION
Prolonged premature rupture of membranes (PROM) is defined as rupture of fetal membranes occurring at least 24 hours before the onset of labor (latency period).1-4 This condition can affect both term and pre-term gestations; in the latter case, it is referred to as prolonged preterm PROM (PPROM).5 Prolonged PROM often leads to chorioamnionitis, which causes serious problems for the mother, fetus, and newborn.6,7 The diagnosis is very imprecise at 24 hours or more after PROM; hence, early diagnosis of the rupture is the key to preventing problems.8
Various bedside tests have been developed for diagnosis of PROM, including the placental α-microglobulin-1 (PAMG-1) test (AmniSure International/Qiagen, Boston, MA, USA), and AmnioQuick Duo+ (Biosynex, Strasbourg, France). Both are immune-chromatologic tests for the detection of amniotic fluid in cervico-vaginal discharge. AmnioQuick Duo+ detects a combination of two proteins: insulin-like growth factor binding protein-1 (IGFBP-1) and α-feto protein (AFP). A previous study of IGFBP-1 suggested that further larger studies need to be carried out on the utility of this test, especially for diagnosing cases of prolonged PROM.9
A previous study reported that the PAMG-1 test is highly accurate for diagnosis of prolonged PROM.2 Despite its use in clinical practice, the newer AmnioQuick Duo+ test has not been evaluated for diagnostic performance in comparison with the PAMG-1 among women with prolonged PROM.2 The aim of the present study was therefore to compare the AmnioQuick Duo+ and PAMG-1 tests in diagnosing membrane rupture among women with prolonged PROM.
2 ∣. MATERIALS AND METHODS
The present prospective longitudinal study enrolled the first 100 consecutive women between January 1 and December 31, 2015, at 24–42 weeks of pregnancy presenting with symptoms suggestive of PROM at six tertiary institutions in southern Nigeria (Nnamdi Azikiwe University Teaching Hospital [NAUTH], Nnewi; University of Nigeria Teaching Hospital, Ituku-Ozalla, Enugu; Federal Medical Center, Umuahia; Madonna University Teaching Hospital, Elele; Chukwuemeka Odumegwu Ojukwu University Teaching Hospital, Awka; and ESUT Teaching Hospital, Parklane, Enugu). The study protocol was approved by the ethics committees of NAUTH and the other recruiting hospitals (approval no. NAUTH/cs/66/vol 7/36). All women included provided written informed consent for study participation.
The inclusion criteria were features of PROM lasting at least 24 hours at 24 weeks pregnancy or later. In the study hospitals, a pooling test, with or without a fern test or nitrazine test, was used to assess the status of the fetal membranes of all pregnant women presenting with symptoms of membrane rupture. An ultrasonography of the uterus and fetus was also performed, whereby the presence of oligohydramnios further suggested PROM.
AmnioQuick Duo+ and/or the PAMG-1 test were used exclusively for women enrolled in the present study. The AmnioQuick Duo+ and PAMG-1 samples were collected in parallel, but different physicians read and interpreted the results simultaneously in a masked fashion.
The AmnioQuick Duo+ test detects the presence of AFP and IGFBP-1 in vaginal samples.10 The vaginal specimen was obtained via a swab stick placed in the posterior fornix for 1 minute. A buffer tube was used to rinse the swab for 10 seconds; in some cases, the tip of the swab was broken off into the buffer tube and the contents were shaken. Three drops of the resultant liquid were dropped into the specimen well on the cassette supplied by the manufacturer. The membrane lodged in the cassette contains monoclonal antibodies to AFP and IGFBP-1, resulting in a pink line in the A and B zones on the cassette if the amniotic fluid contains AFP and IGFBP-1, respectively. The cassette also contains a control zone (C). Up to 10 minutes was required to interpret the result in accordance to the manufacturer’s predefined criteria, categorized as negative or positive for membrane rupture. The test result was negative when both the A and the B lines were absent. The test result was positive when the A, B, and C lines were all present, or the B and C lines were both present, or when the A and C lines were both present for patients at 37 weeks of pregnancy or more. Results were valued as positive if a continuous line was observable, irrespective of whether it was weak or not.
The PAMG-1 test was performed in accordance with the manufacturer’s guidelines, as described previously,2,11 by an investigator who was masked to the AmnioQuick Duo+ result. The caregivers or obstetricians were also masked to the AmnioQuick Duo+ and PAMG-1 results, and the data were analyzed by another researcher.
For women at earlier than 34 weeks of pregnancy, expectant management was started and patients received follow-up for symptoms or signs of infection. Women at 34 weeks of pregnancy or later were allowed 12–24 hours for labor to commence spontaneously; otherwise, induction of labor was initiated.
On the basis of other studies,2,10-14 the ultimate determination of whether or not the women had PROM at first presentation was made after delivery. PROM was diagnosed if any two of the following criteria were fulfilled: delivery within 48 hours to 7 days (depending on gestational age); clinical evidence of chorioamnionitis; perceptibly ruptured membranes at time of delivery; and adverse perinatal/neonatal outcomes strongly associated with prolonged PROM.
The study outcome measures were specificity, sensitivity, positive predictive value (PPV), negative predictive value (NPV), and diagnostic accuracy of the AmnioQuick Duo+ and PAMG-1 tests.
Epi Info version 3.5.1 (Centers for Disease Control and Prevention, Atlanta, GA, USA) was used for data entry and analysis. Sensitivity was calculated by using the VassarStats clinical calculator (Vassar College, Poughkeepsie, NY, USA). The accuracy (true positive + true negative)/(true positive + false negative + false positive + true negative) × 100%, of each test was also estimated. Uncertainty was expressed as 95% confidence intervals. The χ2 test was used to compare categoric data, and the Student t test to compare continuous variables. A P value of less than 0.05 was considered to be statistically significant.
3 ∣. RESULTS
Of the 100 women enrolled, one was lost to follow-up. Table 1 summarizes the sociodemographic characteristics of the 99 women included in the analysis. The mean age of the women was 29.7 ± 5.6 years (range 18–45 years), the mean pregnancy length at presentation was 34.6 ± 4.2 weeks (range 28–42 weeks), and the mean duration of PROM at presentation was 90.5 ± 21.4 hours. Fifty-six (56.6%) women had cesarean delivery and 43 (43.4%) had vaginal delivery. Fifty-one (51.5%) women presented between 24 and 48 hours (excluding the first 24 hours) of PROM, whereas 48 (48.5%) women presented after 48 hours of expressing symptoms or signs of membrane rupture.
TABLE 1.
Sociodemographic characteristics of the study women (n=99).
| Characteristics | No. (%) |
|---|---|
| Age, y | |
| 16–20 | 6 (6.1) |
| 21–25 | 14 (14.1) |
| 26–30 | 36 (36.4) |
| 31–35 | 29 (29.3) |
| 36–40 | 12 (12.1) |
| 41–45 | 2 (2.0) |
| Parity | |
| 0 | 27 (27.3) |
| 1 | 41 (41.4) |
| 2 | 9 (9.1) |
| 3 | 10 (10.1) |
| 4 | 3 (3.0) |
| ≥5 | 9 (9.1) |
| Pregnancy duration, wk | |
| 25–27 | 5 (5.1) |
| 28–30 | 11 (11.1) |
| 31–33 | 13 (13.1) |
| 34–36 | 28 (28.3) |
| 37–39 | 29 (29.3) |
| 40–42 | 13 (13.1) |
| Level of education | |
| Primary | 5 (5.1) |
| Secondary | 53 (53.5) |
| Tertiary | 41 (41.4) |
| Marital status | |
| Single | 2 (2.0) |
| Married | 97 (98.0) |
Table 2 summarizes the diagnostic performance of the AmnioQuick Duo+ and PAMG-1 test for the identification of PROM. AmnioQuick Duo+ and PAMG-1 were discordant in 4 (4.0%) patients, and both were wrong in 1 (1.0%) patient, giving a concordance rate of 96.9% for diagnosis of PROM among women with prolonged PROM (Fig. 1).
TABLE 2.
Performance of the AmnioQuick Duo+and PAMG-1 tests for diagnosis of prolonged PROM (n=99).
| Performance evaluator | AmnioQuick Duo+ | PAMG-1 | IGFBP-1 | AFP |
|---|---|---|---|---|
| No. of true negatives | 25 | 25 | 25 | 24 |
| No. of true positives | 72 | 69 | 70 | 72 |
| No. of false negatives | 2 | 5 | 4 | 2 |
| No. of false positives | 0 | 0 | 0 | 1 |
| Total no. | 99 | 99 | 99 | 99 |
| Specificity, % (95% CI) | 100.0 (83.4–100.0) | 100.0 (83.4–100.0) | 100.0 (83.4–100.0) | 96.0 (77.7–99.8) |
| Sensitivity, % (95% CI) | 97.3 (90.0–99.5) | 93.2 (84.3–97.5) | 94.6 (86.0–98.3) | 92.3 (73.4–98.7) |
| NPV, % (95% CI) | 92.6 (74.2–98.7) | 83.3 (64.5–93.7) | 86.2 (67.4–95.5) | 92.3 (73.4–98.7) |
| PPV, % (95% CI) | 100.0 (93.7–100.0) | 100.0 (93.4–100.0) | 100.0 (93.5–100.0) | 96.6 (77.7–99.8) |
| Accuracy, % (95% CI) | 98.0 (91.5–99.9) | 94.9 (88.8–99.1) | 96.0 (89.9–99.3) | 96.7 (89.5–99.8) |
Abbreviations: AFP, α-fetoprotein; CI, confidence interval; IGFBP-1, insulin-like growth factor binding protein-1; NPV, negative predictive value; PAMG-1, placental α-microglobulin 1; PPV, positive predictive value; PROM, premature rupture of membranes.
FIGURE 1.
Flow diagram showing the study analysis and the discordance/concordance between the AmnioQuick Duo+ and PAMG-1 tests. Abbreviations: FN, false negative; FP, false positive; PAMG-1, placental α-microglobulin-1; TN, true negative; TP, true positive.
Table 3 also shows the diagnostic performance of the AmnioQuick Duo+ versus PAMG-1 test for the identification of PROM in women who presented between 24 and 48 hours (excluding the first 24 hours) and after 48 hours. Overall, 43 (43.4%) women had an “equivocal” result by the standard diagnosis method (i.e., negative pooling test result). The AmnioQuick Duo+ and PAMG-1 test results for these women are shown in Table 4.
TABLE 3.
Performance of the AmnioQuick Duo+and PAMG-1 tests for diagnosis of prolonged PROM by duration of PROM before presentation (n=99).
| Performance evaluator | AmnioQuick Duo+ | PAMG-1 |
|---|---|---|
| Presentation with PROM ≤48 h | ||
| No. of true negatives | 10 | 10 |
| No. of true positives | 41 | 41 |
| No. of false negatives | 0 | 0 |
| No. of false positives | 0 | 0 |
| Total no. | 51 | 51 |
| Specificity, % (95% CI) | 100.0 (65.5–100.0) | 100.0 (65.5–100.0) |
| Sensitivity, % (95% CI) | 100.0 (89.3–100.0) | 100.0 (89.3–100.0) |
| NPV, % (95% CI) | 100.0 (65.5–100.0) | 100.0 (65.5–100.0) |
| PPV, % (95% CI) | 100.0 (89.3–100.0) | 100.0 (89.3–100.0) |
| Accuracy, % (95% CI)a | 100.0 (89.4–100.0) | 100.0 (89.4–100.0) |
| Presenting with PROM >48 h | ||
| No. of true negatives | 15 | 15 |
| No. of true positives | 31 | 28 |
| No. of false negatives | 2 | 5 |
| No. of false positives | 0 | 0 |
| Total no. | 48 | 48 |
| Specificity, % (95% CI) | 100.0 (74.7–100.0) | 100.0 (74.7–100.0) |
| Sensitivity, % (95% CI) | 93.9 (78.4–98.9) | 84.8 (67.3–94.3) |
| NPV, % (95% CI) | 88.2 (62.3–97.9) | 75.0 (50.6–90.4) |
| PPV, % (95% CI) | 100.0 (86.3–100.0) | 100.0 (85.0–100.0) |
| Accuracy, % (95% CI)b | 95.8 (80.5–99.2) | 89.6 (68.7–96.4) |
Abbreviations: CI, confidence interval; NPV, negative predictive value; PAMG-1, placental α-microglobulin-1; PPV, positive predictive value; PROM, premature rupture of membranes.
Among women presenting with prolonged PROM within 48 h, the AmnioQuick Duo+ accuracy of 100% was not statistically different to the accuracy of the PAMG-1 test of 100% (Pearson χ2=0.0, P=0.556; relative risk 1.00, 95% CI 0.76–1.32).
Among women presenting with PROM after more than 48 h, the AmnioQuick Duo+ accuracy of 95.8% was not statistically different to the accuracy of the PAMG-1 test of 89.6% (Pearson χ2=0.0067, P=0.4673; relative risk 1.03, 95% CI 0.78–1.37).
TABLE 4.
Performance of the AmnioQuick Duo+test vs PAMG-1 for diagnosis of equivocal cases of prolonged PROM (n=43).a
| Performance evaluator |
AmnioQuick Duo+ | PAMG-1 |
|---|---|---|
| No. of true negatives | 14 | 14 |
| No. of true positives | 29 | 28 |
| No. of false negatives | 0 | 1 |
| No. of false positives | 0 | 0 |
| Total no. | 43 | 43 |
| Specificity, % (95% CI) | 100.0 (78.5–100.0) | 100.0 (73.2–100.0) |
| Sensitivity, % (95% CI) | 100.0 (88.3–100.0) | 96.6 (80.4–99.8) |
| NPV, % (95% CI) | 100.0 (73.2–100.0) | 93.3 (66.0–99.7) |
| PPV, % (95% CI) | 100.0 (85.4–100.0) | 100.0 (85.0–100.0) |
| Accuracy, % (95% CI) | 100.0 (89.5–100.0) | 97.7 (82.8–99.9) |
Abbreviations: CI, confidence interval; NPV, negative predictive value; PAMG-1, placental α-microglobulin-1; PPV, positive predictive value; PROM, premature rupture of membranes.
For equivocal cases, the pooling test was negative. For these, AmnioQuick Duo+ and PAMG-1 performed equally well (diagnostic accuracy 100% vs 97.7%; P>0.99).
Table 5 summarizes the performance of the AmnioQuick Duo+ and PAMG-1 tests for diagnosing women with prolonged PROM in terms of pregnancy length (<34 weeks vs ≥34 weeks) at presentation. Fifty-five (55.6%) women had a cesarean delivery, after either expectant monitoring or induction of labor (Fig. 2). Twenty-four (44%) of the 55 women who had cesarean delivery had a history of cesarean delivery.
TABLE 5.
Performance of the AmnioQuick Duo+and PAMG-1 tests for diagnosis of prolonged PROM by gestational age at presentation.
| Performance evaluator | AmnioQuick Duo+ | PAMG-1 |
|---|---|---|
| Gestational age <34 wk | ||
| No. of true negatives | 11 | 11 |
| No. of true positives | 31 | 28 |
| No. of false negatives | 1 | 4 |
| No. of false positives | 0 | 0 |
| Total no. | 43 | 43 |
| Specificity, % (95% CI) | 100 (67.9–100) | 100 (67.9–100) |
| Sensitivity, % (95% CI) | 96.9 (82.0–99.8) | 87.5 (70.1–95.9) |
| NPV, % (95% CI) | 91.7 (59.8–99.6) | 73.3 (44.8–91.1) |
| PPV, % (95% CI) | 100 (86.3–100) | 100 (85.0–100) |
| Accuracy, % (95% CI)a | 97.7 (82.5–99.9) | 90.7 (72.8–97.9) |
| Gestational age ≥34 wk | ||
| No. of true negatives | 13 | 13 |
| No. of true positives | 42 | 42 |
| No. of false negatives | 1 | 1 |
| No. of false positives | 0 | 0 |
| Total no. | 56 | 56 |
| Specificity, % (95% CI) | 100 (71.7–100) | 100 (71.7–100) |
| Sensitivity, % (95% CI) | 97.7 (86.2–99.9) | 96.6 (86.2–99.9) |
| NPV, % (95% CI) | 92.9 (64.2–99.6) | 92.9 (64.2–99.6) |
| PPV, % (95% CI) | 100 (89.6–100) | 100 (89.6–100) |
| Accuracy, % (95% CI)b | 98.2 (88.4–99.9) | 98.2 (88.4–99.9) |
Abbreviations: CI, confidence interval; NPV, negative predictive value; PAMG-1, placental α-microglobulin-1; PPV, positive predictive value; PROM, premature rupture of membranes.
Among women presenting with prolonged PROM <34 wk, the AmnioQuick Duo+ accuracy of 97.7% was not statistically different to the PAMG-1 test accuracy of 90.7% (Pearson χ2=0.180, P=0.360; relative risk 2.59, 95% CI 0.40–217.09).
Similarly, among women presenting with PROM at ≥34 wk, the AmnioQuick Duo+ accuracy of 98.2% was not statistically different to the PAMG-1 test accuracy of 98.2% (Pearson χ2=0.712, P>0.99; relative risk 1.00, 95% CI 0.25–4.05).
FIGURE 2.
Flow diagram showing management of the participants on the basis of gestational age. Abbreviation: PROM, premature rupture of membranes.
4 ∣. DISCUSSION
The principal finding of the present study was that the accuracy of the AmnioQuick Duo+ and PAMG-1 tests was minimally affected by prolonged drainage of amniotic fluid lasting at least 24 hours. The diagnostic value of the two tests did not differ between women who presented within 48 hours and those who presented after 48 hours of membrane rupture. Similarly, the diagnostic accuracy of the two tests did not differ between women who presented at a pregnancy duration of less than 34 weeks and those presenting at a pregnancy duration of at least 34 weeks (P>0.99). Both tests had a specificity and positive predictive value of 100%, but the sensitivity was 97.3% and 93.2% for the AmnioQuick Duo+ and PAMG-1 tests, respectively.
The present findings suggest that, after the correct diagnosis of prolonged PROM, a protocol of expectant management should be started for women at less than 34 weeks of pregnancy, and these women should receive follow-up for symptoms or signs of infection. Women at 34 weeks of pregnancy or more should be allowed a period of 12–24 hours for labor to commence spontaneously; otherwise, induction of labor should be initiated.1
More than 55% of women in the present study had a cesarean delivery, suggesting that pregnant women who undergo induction of labor after prolonged PROM at term are more likely to need a cesarean delivery than their counterparts whose labor begins spontaneously within 24 hours of PROM.15 However, this finding contrasts with those of two recent Cochrane reviews,16,17 probably because the present study population comprised only women with prolonged PROM who did not go into spontaneous labor or delivery within 24 hours of PROM. One review found that only 15 in 100 women had a cesarean delivery after either expectant monitoring or induction of labor, and 2 in 100 neonates in each group had proven early-onset neonatal sepsis.17 By contrast, 11 in 100 women developed chorioamnionitis (a criterion used as a gold standard for diagnosis of PROM) after expectant monitoring, as compared with only 5 in 100 after induction of labor. Notably, fewer than 1 in 100 neonates died in both groups.
Women with PROM seem to have a high chance of a correct diagnosis if they arrive late before a full admission assessment can be performed. This has relevance for regions in Africa or elsewhere where women might have a long distance to travel to a healthcare facility. In addition, the specificity of the two tests was 100%, which means that they might be used to rule out PPROM or PROM, and thereby prevent unnecessary interventions such as antibiotics or induction of labor. This might help to manage the rising prevalence of PROM, which in turn increases the number of pregnant women presenting at obstetric triage with signs and symptoms of prolonged PROM.
The diagnostic validation of prolonged PROM in ambiguous cases is a foremost challenge in contemporary obstetric practice. In the present study, 43 (43.4%) women presented with an equivocal case of membrane rupture (i.e., negative pooling test result), and both the AmnioQuick Duo+ and the PAMG-1 test were highly accurate in the diagnosis of prolonged PROM with 100% (95% CI 89.5–100) and 97.7% (95% CI 82.8–99.9), respectively. Previous studies have reported the high accuracy of PAMG-1 as compared with IGFBP-1.18-21 It has been proposed that the lower accuracy of IGFBP-1 in previous diagnostic tests is, at least in part, related to the period of time that might have elapsed since the woman presented with symptoms.18,19
Although there has not been a meta-analysis of women with prolonged PROM, Palacio et al.22 carried out a subgroup analysis of three studies, which found no significant differences between the PAMG-1 and IGFBP-1 tests when compared directly for women with PROM.22 By contrast, Ramsauer et al.23 recently compared the performance of IGFBP-1 and PAMG-1 among women with PROM in a meta-analysis across different patient populations, finding the performance matrices of the PAMG-1 test were significantly superior to those of the IGFBP-1 test even for equivocal cases.23 Several factors have been considered to explain these conflicting results, including the detection limit of the IGFBP-1 kit used in the various studies and the study exclusion criteria. Indeed, it remains controversial whether PAMG-1 and IGFBP-1 are the same molecule.22
Although there are no data, including a cost-effectiveness analysis, supporting the use of AmnioQuick Duo+ instead of PAMG-1, a previous study has reported that AmnioQuick Duo+ has a faster response time.14 In the present study, noninvasive assessment by AmnioQuick Duo+ accurately identified genuine PROM regardless of the duration of rupture or gestational age at rupture. AmnioQuick Duo+ also identified women with PROM who did not go on to deliver within the next 7 days. This might help to circumvent the substantial costs associated with unnecessary hospitalization, the maternal risks associated with prolonged antibiotics, and the fetal risks associated with steroid therapy.24,25
The main strengths of the present study are its double-blind design and strictly defined inclusion criteria. To the best of our knowledge, no other study has reported the diagnostic indices of AmnioQuick Duo+ as compared with PAMG-1 for the exclusive diagnosis of prolonged PROM. Its main limitation is the relatively small sample size, which affects its external validity; therefore, the performance indices of AmnioQuick Duo+ and PAMG-1 determined in the study should not be over-interpreted and further studies are needed to corroborate the findings. In addition, there were no data on neonatal and maternal morbidity or mortality in the small cohort because the study focused on the performance indices of the two biomarkers.
In conclusion, the present evaluation of the AmnioQuick Duo+ test for diagnosis of PROM confirms that this test is non-inferior and comparable to the PAMG-1 test with high diagnostic accuracy for women with prolonged PROM. The rate of diagnostic discordance between the two tests was less than 4%; thus, either test might be used with high diagnostic specificity depending on availability.
ACKNOWLEDGMENTS
The study was supported by Biosynex (Strasbourg, France). PAMG-1 test kits were bought from Placeware Nigeria, Lagos, Nigeria, the PAMG-1 distributor in Nigeria, with financial assistance from Biosynex.
Footnotes
CONFLICTS OF INTEREST
The authors have no conflicts of interest.
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