A Routine Urine Test Has Partial Predictive Value in Premature Rupture of The Membranes

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Clinical Research Report

Journal of International Medical Research


2019, Vol. 47(6) 2361–2370
A routine urine test has ! The Author(s) 2019
Article reuse guidelines:
partial predictive value in sagepub.com/journals-permissions
DOI: 10.1177/0300060519841160
premature rupture of journals.sagepub.com/home/imr

the membranes

Haifeng Liang1, Zhiqiang Xie2, Baohong Liu1,


Xiaojie Song3 and Guanghui Zhao4

Abstract
Objective: This study aimed to examine the predictive value of a routine urine test for
premature rupture of the fetal membranes.
Methods: Routine urine test data of 100 patients with preterm premature rupture of the
membranes (PPROM) and 100 patients with full-term premature rupture of the membranes
(PROM) were collected by the case-based method. Additionally, 100 healthy pregnant women
and 100 nonpregnant adult healthy women were selected as the negative control group and blank
control group, respectively. A receiver operating characteristic curve was established after
identifying the different parameters.
Results: We found that occult blood, glucose, ketone bodies, urine specific gravity, red blood cell
count, epithelial cell count, bacteria, yeast, crystals, and electrical conductivity were significantly
different between the PPROM and PROM groups. There were significant differences in occult
blood, protein, glucose, ketone bodies, pH, red blood cell count, bacteria, urine specific gravity,
crystals, and electrical conductivity between the PPROM and full-term groups. Receiver operating
characteristic curve analysis showed that when the cut-off for bacteria was 130.15, it had the
largest area under the curve value of 0.696.
Conclusion: A routine urine test, especially for bacterial counts, has certain predictive value
for PROM.

4
Clinical Laboratory Medicine Center, Qilu Hospital of
1
Hospital Infection Management, Qilu Hospital of Shandong University, Jinan, Shandong Province, China
Shandong University, Qingdao, Shandong Province, China Corresponding author:
2
Department of Stomatology, Qilu Hospital of Shandong Guanghui Zhao, Clinical Laboratory Medicine Center,
University, Qingdao, Shandong Province, China Qilu Hospital of Shandong University, Jinan, Shandong
3
Department of Respiration, Qilu Hospital of Shandong Province 250012, China.
University, Qingdao, Shandong Province, China Email: [email protected]

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2362 Journal of International Medical Research 47(6)

Keywords
Routine urine test, premature rupture of the membranes, receiver operating characteristic curve,
predictive value, preterm, full-term
Date received: 20 December 2018; accepted: 11 March 2019

Introduction trachomatis, Ureaplasma urealyticum,


Neisseria gonorrhoeae, human herpes sim-
The prevalence of premature rupture of the
plex virus, and certain anaerobes.10–14
membranes (PROM) in China is 2.7% to
Proliferation of chorionic cells is stron-
17%.1 Preterm premature rupture of the
ger than that of amnion cells. If interven-
membranes (PPROM) at <37 weeks of
tion can be performed in the early stage of
gestation is the most harmful, with an inci-
chorionic villous infection, there is a possi-
dence of 2.0% to 3.5%.2 A total of 30% to
bility of preventing PROM. Once infection
40% of preterm births are related to
occurs in the amniotic layer, PROM is inev-
PPROM,3 and preterm birth is associated
with 75% of perinatal deaths.4 At present, itable.15 Traditional inflammatory markers,
treatment of PPROM often involves tradi- such as the white blood cell (WBC) count,
tional single conservative treatment, includ- C-reactive protein, and procalcitonin, are
ing suppression of contractions, antibiotics commonly used by clinicians to diagnose
to prevent infection, and glucocorticoids to chorionic amnionitis.16,17 Sensitivity and
promote lung maturation.5 This therapeutic specificity need to be improved for these
effect is not ideal, and approximately 90% indicators. Amniotic fluid culture requires
of pregnant women with PPROM will a long time and the positive rate is not
deliver in 1 week.6 high. Vaginal microecology is an extremely
The pathogenesis of PPROM is unclear, complex system. The resident flora and
but it usually results from interaction of opportunistic pathogens constantly change
many factors. Studies have shown that and maintain a dynamic balance. Genovese
direct invasion of pathogens, damage of et al.18 found that up to 54.2% of pregnant
the inflammatory response, excessive degra- women had a vaginal infection or imbal-
dation of matrix metalloproteinases in the ance of vaginal microflora at the 28th
extracellular matrix of fetal membranes, week of gestation. Paramel et al.19 further
apoptosis, the oxidative stress response, found that during pregnancy, vaginal
tissue acetylation, and microelement defi- microflora widely varied among individu-
ciency are involved.7,8 Reproductive tract als. Lactobacillus vaginalis is still dominant
infection is a major concern of researchers. in only 13/70 of pregnant women.
More than 60% of PPROM is related to A urine test is routine for pregnant
infection and subsequent cascade amplifica- women and it is a noninvasive procedure.
tion of the inflammatory response.9 This test also has the advantage of low cost
Invasion of pathogens is the beginning of and is easily accepted. This study aimed to
occurrence of PPROM, including Group examine the value of the urine test in diag-
B Streptococcus, Candida, Chlamydia nosis and prognosis of PPROM.
Liang et al. 2363

Materials and methods Dry chemical analysis of urine was per-


formed using the Arkray AX-4030
Patients (Arkray Corp., Kyoto, Japan).
We included pregnant women who were Measurements included leukocytes, occult
admitted to the Maternity Department of blood, protein, glucose, ketone bodies
Qilu Hospital of Shandong University from (KET), urobilinogen, urobilirubin, pH
February 2017 to October 2018. All selected values, urine specific gravity (SG), and
patients met the following criteria: (a) no uri- nitrite. Urinary components were analyzed
nary tract infection; (b) singleton pregnancy; using the Sysmex UF1000i (Sysmex Corp.,
and (c) no antibacterials were used in the Kobe, Japan). These components mainly
past 2 weeks. Patients with the following con- included WBC count, red blood cell
ditions were excluded: (a) patients who did (RBC) count, epithelial cell count (EC),
not meet the inclusion criteria; and (b) the cast, pathological cast, bacteria, small
specimen collection time did not meet the round cells, yeast, crystals, and electrical
prescribed time limit. All participants used conductivity. In specimens that could not
disposable sterile urine cups to collect speci- be correctly detected by an instrument, the
mens and prevent cross-infection. numbers of WBCs, RBCs, ECs, cast, and
A total of 100 patients with PPROM crystals were confirmed by a microscopic
whose gestation was <37 weeks were select- examination.
ed and they received routine urine tests
within 7 days before rupture of the fetal
membranes. A total of 100 patients with Data analysis
PROM with a gestational age >37 weeks In statistical analysis, the patient’s personal
were selected and a routine urine routine information was hidden and replaced with a
examination was conducted 7 days before digital code. Before comparison of data,
rupture of the membranes. Additionally, a general description of the data was per-
100 women with full-term gestational age formed. First, the Kolmogorov–Smirnov
>37 weeks and <42 weeks (full-term test was used to test the normality of two
group) were randomly selected and urine samples. The mean and standard deviation
routine specimens were collected within are shown for data that conformed to a
24 hours before delivery. Finally, 100 non- normal distribution. For data that were
pregnant adult healthy women (normal not normally distributed, the median and
group) were randomly selected and clean interquartile range are shown. The Levene
midstream urine specimens were collected. method was used to test the homogeneity of
All of these selected subjects did not have a variance of two samples. A parametric test
history of urinary tract infection. This study was used if variables in the two groups
was approved by the Ethics Committee of satisfied homogeneity of variance. If homo-
Qilu Hospital of Shandong University. All geneity of variance was not present,
patients involved in the study signed a nonparametric test, such as the
informed consent forms. Kolmogorov–Smirnov Z-rank test, was
used. IBM SPSS Statistics 21.0 (SPSS
Urine analysis method Corporation, Chicago, IL, USA) was used
A disposable cup was used to collect for data analysis. Values of P < 0.05 were
the patient’s clean mid-stream urine. considered statistically significant.
2364 Journal of International Medical Research 47(6)

Establishing the receiver operating meaningful indicator of the effectiveness


characteristic curve of diagnostic tests.

The receiver operating characteristic (ROC)


curve is also referred to as a sensitivity Results
curve. The true positive rate (sensitivity)
was plotted on the ordinate and the false Homogeneity of variance and normal
positive rate (1-specificity) was plotted on distribution
the abscissa. We calculated the area under We investigated urine sample data of 628
the ROC curve (AUC) for each test sepa- pregnant women. After screening, a total
rately to determine which test had the larg- of 300 eligible patients were included in
est AUC. This method has the advantages this study. The homogeneity of variance
of simplicity and intuitiveness. When two test showed that the variables of age, days
indicators needed to be detected jointly, of gestation, leukocytes, occult blood, pro-
logistic regression analysis was used to gen- tein, glucose, KET, urobilirubin, RBC
erate the prediction probability, and then count, yeast, and electrical conductivity
the ROC curve was generated with the did not satisfy the homogeneity of variance
probability. test, with a ¼ 0.5 as the test level. Only age
in the PPROM group and electrical conduc-
Cut-off determination and diagnostic tivity in each group showed a normal
value assessment distribution, with a ¼ 0.5 as the test level
(Table 1). Normally distributed data are
The closer to the upper left corner of the
shown in Table 2.
ROC curve, the higher the accuracy of
this test. The best cut-off value was deter-
mined by the Youden index, and then the Comparison of variables
corresponding sensitivity and specificity Pairwise comparisons among the PPROM,
were calculated. Sensitivity has the ability PROM, full-term, and normal groups were
to recognize patients. Specificity has the performed using the Kolmogorov–Smirnov
ability to recognize non-patients. Both of Z-rank test (Table 3). We found that age
these measures can be used to assess the was significantly younger in the full-term
authenticity of the model. The positive pre- group compared with the other three
dictive value (PPV) and the negative predic- groups (all P < 0.05). Occult blood, KET,
tive value (NPV) were further calculated by and the RBC count were significantly
the cut-off value. The PPV was used to eval- higher, and electrical conductivity was
uate the possibility of the target disease in significantly lower in the PPROM group
the positive population in the screening test, compared with the other three groups
and the NPV was the probability that there (all P < 0.05). Bacteria and crystals were
was no target disease in the negative popu- significantly different between the PPROM
lation. The positive likelihood ratio (þLR) group and the PROM and full-term groups
and negative likelihood ratio (LR) were (all P  0.05). SG, EC, and yeast were sig-
further calculated by sensitivity and specif- nificantly different between the PPROM
icity. þLR and LR combine the advan- and PROM groups (all P < 0.05), while
tages of sensitivity, specificity, PPV and protein, pH, and small round cells were sig-
NPV. þLR and LR are relatively inde- nificantly different between the PPROM
pendent, and they are a clinically and full-term groups (all P < 0.05).
Liang et al. 2365

Table 1. Results of normality and homogeneity of variance tests.

Normality test
Homogeneity
of variance PPROM PROM Full-term Nonpregnant

Variable Stat. P Stat. P Stat. P Stat. P Stat. P

Age 6.11 <0.01 0.99 0.43 0.96 0.01 0.88 <0.01 0.10 0.02
Days 75.43 <0.01 0.77 <0.01 0.94 <0.01 0.92 <0.01 – –
LEU 2.48 0.09 0.69 <0.01 0.79 <0.01 0.80 <0.01 – –
BLD 34.02 <0.01 0.70 <0.01 0.44 <0.01 0.43 <0.01 – –
PRO 16.18 <0.01 0.51 <0.01 0.44 <0.01 0.27 <0.01 – –
GLU 38.67 <0.01 0.60 <0.01 0.21 <0.01 0.31 <0.01 – –
KET 37.43 <0.01 0.70 <0.01 0.45 <0.01 0.29 <0.01 – –
UBG 1.15 0.32 0.08 <0.01 0.12 <0.01 0.12 <0.01 – –
BIL 4.08 0.02 – – 0.08 <0.01 – – – –
pH 1.57 0.21 0.94 <0.01 0.94 <0.01 0.92 <0.01 0.19 <0.01
SG 1.46 0.23 0.96 <0.01 0.94 <0.01 0.97 0.02 0.08 0.10
NIT 0.19 0.83 0.08 <0.01 0.08 <0.01 0.08 <0.01 – –
WBCs 1.98 0.14 0.53 <0.01 0.42 <0.01 0.34 <0.01 0.17 <0.01
RBCs 17.71 <0.01 0.29 <0.01 0.27 <0.01 0.12 <0.01 0.18 <0.01
EC 1.19 0.31 0.37 <0.01 0.80 <0.01 0.65 <0.01 0.14 <0.01
Cast 0.73 0.48 0.22 <0.01 0.24 <0.01 0.88 <0.01 0.17 <0.01
P.CAST 1.89 0.15 0.89 <0.01 0.89 <0.01 0.25 <0.01 0.25 <0.01
BAC 0.04 0.96 0.28 <0.01 0.25 <0.01 0.35 <0.01 0.23 <0.01
SRC 2.59 0.08 0.27 <0.01 0.23 <0.01 0.85 <0.01 0.17 <0.01
BYST 4.05 0.02 0.15 <0.01 – – 0.08 <0.01 – –
Crystals 1.33 0.26 0.14 <0.01 0.08 <0.01 0.08 <0.01 0.40 <0.01
Cond. 3.79 0.02 0.97 0.05 0.99 0.50 0.99 0.45 0.05 0.20
PPROM: preterm premature rupture of the membranes; PROM: premature rupture of the membranes; Stat: statistic; days:
days of gestation; LEU: leukocytes; BLD: occult blood; PRO: protein; GLU: glucose; KET: ketone bodies; UBG: urobili-
nogen; BIL: urobilirubin; SG: urine specific gravity; NIT: nitrite; WBCs: white blood cells; RBCs: red blood cells; EC:
epithelial cell count; P.CAST: pathological cast; BAC: bacteria; SRC: small round cells; BYST: yeast; Cond.: electrical
conductivity.

ROC curve and we found that the AUC did not


increase (Figure 1a–f).
Urinary dry chemical indicators, including
leukocytes, occult blood, protein, glucose,
KET, urobilinogen, urobilirubin, and Predicted value of indicators
nitrite are numeration data, and RBCs are
easily altered by vaginal bleeding. After determining the cut-off value of the
Therefore, these indicators are not suitable ROC curve, the sensitivity, specificity,
for establishing an ROC curve. The AUC PPV, NPV, þLR, and LR were calculated
was calculated by establishing the ROC to estimate the predictive value of each indi-
curve. We found that bacteria had the larg- cator. When the variable bacteria had a cut-
est AUC (0.696). The AUC for electrical off of 130.15, the sensitivity was 58%, the
conductivity was 0.596 and that for crystals specificity was 79%, the PPV was 73.4%,
was 0.577. The ROC curve was established the NPV was 65.3%, þLR was 2.76, and
by combining these three indicators in pairs –LR was 0.53 (Table 4).
2366 Journal of International Medical Research 47(6)

Table 2. Distribution of data for each group.

Variable PPROM PROM Full-term Nonpregnant

Age 31.48  0.55 31.75  0.44 30.11  0.40 31.63  5.06


Days 228.12  3.60 267.06  0.44 282.49  0.41 –
LEU 2.13  0.17 2.27  0.15 2.19  0.14 1.00  0.00
BLD 1.96  0.14 1.33  0.09 1.26  0.07 1.00  0.00
PRO 1.36  0.08 1.28  0.07 1.11  0.04 1.00  0.00
GLU 1.84  0.16 1.14  0.07 1.22  0.08 1.00  0.00
KET 1.97  0.15 1.42  0.11 1.16  0.06 1.00  0.00
UBG 1.02  0.02 1.05  0.04 1.04  0.03 1.00  0.00
BIL – 1.02  0.02 – 1.00  0.00
pH 6.43  0.06 6.56  0.06 6.63  0.05 6.04  0.59
SG 1.01  0.00 1.01  0.00 1.01  0.00 1.02  0.01
NIT 1.02  0.02 1.03  0.03 1.03  0.03 1.00  0.00
WBC 80.76  16.83 64.30  14.55 56.58  14.86 6.16  5.15
RBC 191.96  73.38 19.70  5.56 22.45  12.19 11.06  8.19
EC 25.17  5.81 24.90  2.37 26.21  3.25 9.73  8.47
Cast 1.15  0.33 1.14  0.29 0.77  0.07 0.44  0.41
P.CAST 0.38  0.04 0.40  0.04 0.50  0.14 0.21  0.21
BAC 870.87  326.98 1207.75  374.58 1296.69  317.22 300.77  394.63
SRC 6.89  2.05 9.92  3.37 5.47  0.51 1.44  1.06
BYST 0.91  0.61 – 0.46  0.43 0.00  0.00
Crystals 4.10  2.82 6.02  5.79 12.05  11.52 0.48  1.83
Cond. 13.28  0.84 18.69  0.62 15.91  0.72 20.46  5.99
Values are mean  standard deviation. PPROM: preterm premature rupture of the membranes; PROM: premature rupture
of the membranes; days: days of gestation; LEU: leukocytes; BLD: occult blood; PRO: protein; GLU: glucose; KET: ketone
bodies; UBG: urobilinogen; BIL: urobilirubin; SG: urine specific gravity; NIT: nitrite; WBCs: white blood cells; RBCs: red
blood cells; EC: epithelial cell count; P.CAST: pathological cast; BAC: bacteria; SRC: small round cells; BYST: yeast; Cond.:
electrical conductivity.

Discussion groups, we found significant differences in


various variable among the groups. We
The occurrence of PPROM is often the
found that PROM was more likely to
result of multifactorial interactions.
occur with age. Occult blood and the RBC
Among them, retrograde infection of repro-
ductive tract pathogens is the most impor- count were significantly higher in the
tant cause. In women, the urethra and PPROM group compared with the other
reproductive tract are susceptible to groups. This finding is probably because
exchange of bacteria. To some extent, the patients with PPROM were more likely to
amount of bacteria in a routine urine test have vaginal bleeding symptoms. The WBC
can reflect the microecological status of the count was lower in the normal (nonpreg-
female perineum.20 When PPROM occurs, nant) group than in the other three
dominant bacteria, such as Lactobacillus in groups, but no differences were observed
the vagina, are replaced by pathogenic bac- among the pregnant groups. These results
teria, and the diversity of the flora is signif- suggest that women may have mild or
icantly reduced. asymptomatic urethral infection during
By analyzing routine urine data in the pregnancy, but WBCs cannot be used as a
PPROM, PROM, full-term, and normal diagnostic indicator for PROM. The
Liang et al. 2367

Table 3. Pairwise comparisons for each group.

Mann–Whitney U

PPROM PPROM PPROM PROM PROM Full-term


versus versus versus versus versus versus
Variable PROM Full-term Normal Full-term Normal Normal

Age 0.65 0.03* 0.65 <0.01* 0.90 <0.01*


Days <0.01* <0.01* – <0.01* – –
LEU 0.39 0.53 <0.01* 0.84 <0.01* <0.01*
BLD <0.01* <0.01* <0.01* 0.90 <0.01* <0.01*
PRO 0.48 0.01* <0.01* 0.03* <0.01* 0.01*
GLU <0.01* <0.01* <0.01* 0.30 0.01* <0.01*
KET <0.01* <0.01* <0.01* 0.04* <0.01* <0.01*
UBG 0.56 0.56 0.32 0.99 0.16 0.16
BIL 0.32 1.00 1.00 0.32 0.32 1.00
pH 0.12 0.01* <0.01* 0.41 <0.01* <0.01*
SG 0.02* 0.75 <0.01* <0.01* <0.01* <0.01*
NIT 0.99 0.99 0.32 1.00 0.32 0.32
WBC 0.59 0.93 <0.01* 0.56 <0.01* <0.01*
RBC 0.01* <0.01* 0.02* 0.38 0.82 0.21
EC 0.04* 0.10 <0.01* 0.64 <0.01* <0.01*
CAST 0.93 0.16 <0.01* 0.25 <0.01* 0.01*
P.CAST 0.80 0.93 <0.01* 0.90 <0.01* <0.01*
BAC <0.01* <0.01* 0.15 0.64 <0.01* <0.01*
SRC 0.06 0.04* <0.01* 0.84 <0.01* <0.01*
BYST 0.02* 0.25 0.02* 0.16 1.00 0.16
Crystal 0.03* 0.05* 0.10 0.85 0.63 0.78
Cond. <0.01* 0.02* <0.01* 0.01* 0.07 <0.01*
*P < 0.5 was considered statistically significant. PPROM: preterm premature rupture of the membranes; PROM: prema-
ture rupture of the membranes; days: days of gestation; LEU: leukocytes; BLD: occult blood; PRO: protein; GLU: glucose;
KET: ketone bodies; UBG: urobilinogen; BIL: urobilirubin; SG: urine specific gravity; NIT: nitrite; WBCs: white blood cells;
RBCs: red blood cells; EC: epithelial cell count; P.CAST: pathological cast; BAC: bacteria; SRC: small round cells; BYST:
yeast; Cond.: electrical conductivity.

amount of bacteria was significantly lower related to maternal endocrine function and
in the PPROM group than in the PROM an increase in secreted aldosterone, which
and full-term groups, but there was no dif- could lead to an increase in sodium and
ference between the PPROM and normal chloride reabsorption in the kidney.21
groups. This finding suggested that the We first used non-parametric test meth-
amount of bacteria in the urinary tract in ods to screen differential indicators between
PPORM was significantly reduced, the PPROM and normal groups. ROC
although it was still higher than that in curves were then used to further select indi-
the normal group. The decrease in bacteria cators with good sensitivity, specificity,
is a risk factor, indicating a decrease in the PPV, NPV, þLR, and LR. However,
diversity of flora. Crystals and electrical this study has some limitations. The main
conductivity were significantly reduced in limitation is that none of the metrics
the PPROM group. This low electrical con- showed high enough AUC values. This
ductivity in the PPROM group may be also indicates that use of these indicators
2368 Journal of International Medical Research 47(6)

Figure 1. ROC curve of different indicators. (a) BAC; (b) crystals; (c) Cond.; (d) BACþcrystals;
(e) BACþCond.; (f) crystalsþCond. AUC: area under the curve; ROC: receiver operating characteristic;
BAC: bacteria; Cond.: electrical conductivity.
Liang et al. 2369

Table 4. Comparison of the predictive value of different indicators.

Youden
Variable index Cut-off value Sensitivity Specificity PPV NPV þLR LR

BAC 0.37 130.15 58% 79% 73.4% 65.3% 2.76 0.53


Crystal 0.3 73.9 57% 73% 67.9% 62.9% 2.11 0.59
Cond. 0.21 15.15 64% 57% 58.9% 61.4% 1.49 0.63
BACþcrystals 0.32 0.5128 54% 78% 69.2% 62.3% 2.45 0.59
BACþCond. 0.21 0.5097 58% 63% 61.1% 60% 1.57 0.67
CrystalsþCond. 0.21 0.4948 65% 56% 59.6% 61.5% 1.48 0.63
PPV: positive predictive value; NPV: negative predictive value; þLR: positive likelihood ratio; LR: negative likelihood
ratio; BAC: bacteria; Cond.: electrical conductivity.

to predict occurrence of PROM is of limited Declaration of conflicting interest


value and must be combined with other The authors declare that there is no conflict
indicators. Additionally, qualified urine of interest.
specimens are precursors to authenticity of
the data, although all of the urine speci- Funding
mens used in this study underwent prelimi-
This work was supported in part by grants from
nary conformance testing. However,
the National Natural Science Foundation of
because of the special circumstances of
China (Grant No. 81802068) and the Research
pregnant women, especially pregnant
Foundation of Qilu Hospital of Shandong
women with PPROM, obtaining unconta-
University (Grant No. QDKY2016LH02).
minated urine samples again in a short
time is difficult.
ORCID iD
Guanghui Zhao http://orcid.org/0000-0001-
Conclusions 9417-8421
Identifying an indicator with better specif-
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