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Acoustic radiation force impulse elastosonography of placenta in maternal red blood cell alloimmunization: a preliminary and descriptive study

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Original papers

DOI: 10.11152/mu-924

Acoustic radiation force impulse elastosonography of placenta in maternal red blood cell alloimmunization: a preliminary and descriptive study

Orkun Cetin

1

, Erbil Karaman

1

, Harun Arslan

2

, Ibrahim Akbudak

2

, Recep Yıldızhan

1

, Ali Kolusarı

1

1Department of Obstetrics and Gynecology, 2Department of Radiology, Yuzuncu Yil University, Faculty of Medicine, Van, Turkey

Received 29.08.06.2016 Accepted 30.10.2016 Med Ultrason

2017, Vol. 19, No 1, 73-78

Corresponding author: Orkun Cetin, MD,

Yuzuncu Yil Universitesi Tip Fakultesi, Kadin Hastaliklari ve Dogum Anabilim Dali, Dursun Odabas Tip Merkezi, Kampus, 65080 Van, Turkey.

Phone: +90 432 215 0471, Fax: +90 432 216 8352 E-mail: [email protected]

Introduction

Maternal red blood cell alloimmunization is an impor- tant cause of morbidity and mortality in the antepartum and neonatal periods with the frequency found to range from 0.4% to 2.7% worldwide [1-5]. Maternal red blood cell alloimmunization causes fetal-neonatal anemia with

the mechanism of transplacental passage of maternal hemolytic antibodies that produce fetal red blood cell destruction. This eventually leads to anemia, hyperbiliru- binemia, extra-medullary hematopoiesis and generalized body edema which is called hydrops fetalis [6]. There are three main types of red blood cell alloimmunization, based on the antigen(s) involved: Rhesus (Rh), minor red cell antigens (i.e. Kell, Duffy, Kidd antigens), and ABO [5]. The rate of alloimmunization has been found to be decreased sharply from 16% to ~2% in the past few years with the routine use of postpartum anti-D Immunoglobu- lin (Ig) for Rh D-negative women [7].

The ancient measurements such as placental thick- ness and abdominal circumference could not predict the development of fetal anemia [8]. Currently, the main di- agnostic tool for prediction of fetal anemia is middle cer- Abstract

Aims: Maternal red blood cell alloimmunization is an important cause of fetal morbidity and mortality in the perinatal period, despite well-organized prophylaxis programs. The objective of the study was to evaluate placental elasticity by using Acoustic Radiation Force Impulse (ARFI) in Rhesus (Rh) alloimmunized pregnant women with hydropic and nonhydropic fetuses and to compare those with healthy pregnant women. Material and methods: This case-control and descriptive study comprised twenty-eight healthy pregnant women, 14 Rh alloimmunized pregnant women with nonhydropic fetuses, and 16 Rh alloimmunized pregnant women with hydropic fetuses in the third trimester of pregnancy. Placental elasticity measurements were performed by ARFI elastosonography at the day of delivery. The maternal characteristics and neonatal outcomes of the patients were also noted. Results: The highest mean placental ARFI scores were observed in Rh alloimmunized pregnant women with hydropic fetuses (1.13 m/s) (p=0.001). Healthy controls and Rh alloimmunized pregnant women with nonhy- dropic fetuses had similar mean placenta ARFI scores (0.84 m/s, 0.88 m/s, respectively) (p<0.05). Conclusions: Based on the present findings, the placenta becomes stiffer in Rh alloimmunized pregnancies complicated with hydrops fetalis. The increased placental ARFI scores may be a supplemental marker for adverse pregnancy outcomes, additional to Doppler evalu- ation of middle cerebral artery. This data should be confirmed with a large sample size and prospective studies by using serial measurements of ARFI elastosonography in maternal red blood cell alloimmunization.

Keywords: maternal red blood cell alloimmunization, placental elasticity, ARFI.

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ebral artery Doppler evaluation. This is a non-invasive and feasible technique without any potential risks to the mother and fetus. It is accepted as worldwide in the de- cision of fetal anemia and intrauterine transfusion treat- ment [5].

Human placenta has crucial functions in fetal oxy- genation, endocrinological contributions and nutrition [9]. The placental thickening has been linked with vari- ous pathologies such as congenital infections, maternal diabetes and fetal hydrops [9]. Also, fetal anemia, fetal heart failure and chromosomal abnormalities such as trisomies have been reported to be associated with pla- cental thickening [10,11]. Placental features may have important clues for maternal and fetal risks because the placenta is usually the first organ of manifestation of pregnancy complications [12]. The placental changes that are seen in maternal red blood cell alloimmunization result from edema and compensatory hypertrophy [12].

However, there is a limited number of studies that have evaluated the placental tissue in maternal red blood cell alloimmunization.

Elastosonography is a non-invasive diagnostic tool that evaluates tissue stiffness. It has been used for vari- ous diseases as well as in placenta pathology [13-19].

Acoustic radiation force impulse (ARFI) elastography is relatively a new method which uses a short acoustic push pulse in the target tissue, which causes a tissue displace- ment of approximately 1-20 um. Placental evaluation with ARFI elastosonography has been studied in hyper- tensive disorders and fetal growth restricted pregnancies and a stiffer placenta in both groups was reported [13].

To date, no study has been found which has evaluated the placental tissue stiffness in maternal red blood cell alloimmunization.

Placental structural abnormalities may occur in ma- ternal red blood cell alloimmunization. This condition may affect placental elasticity. Therefore, we aimed to evaluate placental elasticity by using ARFI in Rh alloim- munized pregnant women with hydropic and nonhydrop- ic fetuses and to compare those with healthy pregnant Women.

Materials and methods

This case-control and descriptive study was carried out at Yuzuncu Yil University Medical Faculty, Depart- ment of Obstetrics & Gynecology and Department of Radiology from January 2015 till July 2016. The Uni- versity’s Local Ethics Committee approved the study and informed consent was obtained from all participants.

We identified 39 singleton pregnancies with maternal red cell anti-D alloimmunization referred to our hospi-

tal. The gestational age was determined according to the last menstrual period or to the crown-rump length on the first trimester ultrasonographic examination. The ma- ternal antibody titers of alloimmunized patients ranged from 1:16 to 1:256. Patients were managed exclusively through noninvasive assessment (Doppler evaluation of the middle cerebral artery) and/or rising antibodies.

Intrauterine transfusion was decided in immature (<34 weeks) fetuses when the measurement of middle cerebral artery peak systolic velocity was up to 1.55 multiples of the median (MoM) and in case of sonographic signs (as hydrops). The hydrops were described as the excess liq- uid in two or more fetal spaces [20]. The target of our management strategy was to deliver the fetuses at 34th week of gestation in adequate fetal well-being. Five pa- tients who underwent intrauterine transfusion and four patients with posterior placental location were excluded from the study. Patients with accompanying diseases, multiple gestations and congenital abnormalities were also excluded. The study population consisted of 28 healthy pregnant women (Group 1), 14 Rh alloimmun- ized pregnant women with nonhydropic fetuses (Group 2) and 16 Rh alloimmunized pregnant women with hy- dropic fetuses (Group 3) in the third trimester of preg- nancy. The healthy pregnant women (Group 1) consisted of clinically normal pregnancies with normal fetal so- nography and normal perinatal outcomes. Group 3 com- prised of Rh alloimmunized pregnant women who had not received any antenatal care visits. They were all in lower socioeconomic status and located in a rural part of Eastern Turkey. They were referred to our clinic in a se- vere state of hydrops fetalis. and intrauterine transfusion was recommended. But, no one gave the informed con- sent for the invasive procedure and they were followed with conservative management. The timing of delivery was decided on a case-by-case basis. The clinical charac- teristics of the patients, as maternal age, gravidity, parity and body mass index (BMI) were noted. Data concerning obstetric and neonatal outcomes as, gestational age at de- livery, birthweight, and Apgar scores were also collected.

We used 4-9 MHz 9L4 linear transducer with the Virtual Touch IQ option (Siemens ACUSON S2000™, Siemens Healthcare, Erlangen, Germany) for ARFI elas- tosonography measurements. The standardization of the ARFI elastosonography technique was obtained by ex- amining 5 healthy pregnant women before starting the study. The radiologist who performed the ARFI had at least 10-year experience in gray-scale ultrasound and 5 years in r elastosonography. The measurements of pla- centa were performed in the supine position while the pa- tients held their breath. The placenta was evaluated and divided into three equal parts as fetal edge (inner 1/3 of

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placenta) (ARFI-fetal), maternal edge (outer 1/3 of pla- centa) (ARFI- maternal) and the central part (central 1/3 of placenta) (ARFI-central). Three measurements were taken in each of the three regions of the placenta and the mean of these three measurements were obtained as the value of shear wave velocity in m/s for each region (fig 1, fig 2). The mean of these 9 measurements were also calculated and accepted as the mean placental elasticity

value (ARFI- mean). All ARFI measurements of the pa- tients were performed at the day of delivery.

Statistical analysis

Descriptive statistics for studied variables (char- acteristics) were presented as Median, Minimum and Maximum values. The Kruskal-Wallis Test was used to compare continuous variables among the three groups.

The Mann-Whitney U test was used to compare continu- ous variables between the two groups. The Duncan’s test was performed to determine which group differed sig- nificantly from the other groups. A Chi-Square test was used to examine the association between the categorical variables. The Spearman’s correlation analysis was used to define the relationship between the variables. Statisti- cal significance levels were considered as 5%. The SPSS (Version 20.0 – IBM Corp. Released 2011. IBM SPSS Statistics for Windows. Armonk, NY: IBM Corp.) statis- tical program was used for all statistical computations.

Results

The clinical characteristics and perinatal outcomes of the patients are presented in Table I.

The placental ARFI elastosonography scores of the patients are detailed in Table II. The highest placental ARFI-maternal, ARFI-central and ARFI-fetal elasto- sonography scores were measured in Group 3 (p=0.001, p=0.002, and p=0.004, respectively). The highest placen- tal ARFI-mean elastosonography scores were measured in Group 3 (p=0.001). Group 1 and Group 2 had similar placental ARFI- mean elastosonography scores (p>0.05).

The middle cerebral artery peak systolic velocity mean- MoM values were 0.95±0.31 and 1.54±0.26 in Group 2 and Group 3, respectively. There was a significant dif- ference between the groups (p=0.001). Also, we found a significant positive correlation between the placental ARFI-mean elastosonography scores and the middle Fig 1. a) Rh alloimmunized pregnant women with hydrops fe-

talis at 27 weeks of gestation; b) The ARFI elastosonography measurement of the maternal edge of placenta (ARFI-maternal) at 34 weeks of gestation.

Fig 2. a) The ARFI elastosonography measurement of the cen- tral part of placenta (ARFI-central) at 34 weeks of gestation and b) of the fetal edge of placenta (ARFI-fetal) at 34 weeks of gestation.

Table I. Comparison of the clinical characteristics and perinatal outcomes in the separate groups of patients

Group 1 (n: 28) Group 2 (n: 14) Group 3 (n: 16) p

Maternal age 25.5 (18-39)b 29.5 (18-40)a 30.5 (23-39)a 0.023*

Gravidity 2 (1-9)b 3 (1-8)a 5 (1-10)a 0.001*

Parity 1 (0-8)b 2 (0-7)a 3 (0-9)a 0.002*

BMI 27.8 (23.5-37.5) 28.2 (24.0-36.9) 27.7 (21.7-32.3) 0.542*

Gestational age at delivery 39 (37-40)a 36 (34-38)b 31 (24-36)c 0.001*

Birthweight 3150 (2750-4000)a 2400 (1400-3500)b 1775 (450-3000)c 0.001*

Apgar 1. minute 7 (6-8)a 6 (3-7)b 1 (1-7)c 0.001*

Apgar 5. minutes 9 (7-10)a 8 (5-9)b 5 (2-9)c 0.001*

NICU admission 0 5/14 (35.7%) 16/16 (100%) 0.001#

Early neonatal death 0 0 14/16 (87.5%) 0.001#

*Kruskal-Wallis test was used to compare continuous variables; # Chi-Square test was used to compare categorical variables; a, b, c→ Defined significance between each groups (a>b>c); BMI – body mass index; NICU – neonatal intensive care unit.

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cerebral artery peak systolic velocity mean-MoM values (r=0.486; p=0.006).

Discussions

The current study is the first descriptive, case-control study that has examined the placental elasticity by ARFI elastosonography in Rh alloimmunized pregnancies. The results of our study demonstrated that there was a positive correlation between placental elasticity and development of hydrops fetalis in Rh alloimmunized pregnancies. In- creased placental stiffness may be a useful predictor for the worse perinatal outcomes, additionally to other non- invasive procedures, such as middle cerebral artery peak systolic velocity in this condition.

The diagnosis and management of maternal red cell alloimmunization has been broadly identified in several studies around the world. During the past decades, Rh hemolytic disease has decreased with the widespread adoption of guidelines for antenatal and postpartum use of anti-D Ig prophylaxis [21]. However, there are lim- ited data available on placental changes in maternal red cell alloimmunization [12]. It is known that placento- megaly is a possible finding of erythroblastosis fetalis.

In early studies, increased placental thickness was used as an early predictor for fetal anemia in maternal red cell alloimmunization [8]. However, increased thickness is non-specific and can be found with other adverse preg- nancy complications such as perinatal infections [22].

The thick, heterogeneous (jellylike) appearance of the placenta is also associated with perinatal death, hyperten- sive diseases, fetal growth restriction and preterm deliv- ery [23]. Three-dimensional Power Doppler analysis in fetal growth restricted pregnancies have evidenced that decreased placental vascularity and impaired budding of the villous circulation contribute to the thick and hetero- geneous (jellylike) placenta [24].

Sonography has recently been used to measure tissue elasticity [14]. ARFI is a new technique of elastography which can be applied without any manual compression and also allows detecting histological changes in tissues [13]. It is an ultrasound-based elastography which de-

pends on the usage of a short acoustic push in the target tissue. It induces a tissue displacement of nearly 1-20 μm. This displacement generates a lateral shear wave that propagates through the tissue during recoil, the ve- locity of which is described as Vs (m/s). The Vs level reflects tissue elasticity. Tissue stiffness increases in fast shear wave speeds and small displacements. Oppositely, slow shear wave speeds and large displacements are seen in softer tissues [13]. ARFI technique was firstly used for the evaluation of liver fibrosis, liver cirrhosis, and inflammatory pancreatic diseases [15,16]. Mateen et al [16] stated that increased Vs values occur as a re- sult of inflammatory cell infiltration and cellular swell- ing with increased fluid content in the target tissues. In recent studies, elevated Vs values were also detected in acute hepatitis and pancreatitis. However, the reasons of increased elasticity in these parenchymal organs are still unknown [15,16].

There have been limited studies concerning ARFI in- vestigating placental elasticity [17-19]. Sugitani et al [13]

measured the placental elasticity by using ARFI in an ex vivo study and they found higher ARFI scores in intrau- terine growth restricted and hypertensive pregnancies.

Recent in vivo studies demonstrated that the placenta be- comes stiffer in preeclamptic pregnancies [17-19]. Pla- cental infarction, inflammation of trophoblastic villi and vasculitis are major findings which occur in intrauterine growth restricted and hypertensive pregnancies [25]. Vil- lous congestion and inefficient oxygen delivery are also seen in these pregnancies [13]. The authors stated that as a result of these placental histological changes, the pla- centa may become stiffer in these pregnancies [13].

Elastosonography techniques have similar safety considerations to conventional ultrasonography imaging modes. Although the ARFI technique is based on tissue displacement with generating pulse bursts, Herman et al reported that any temperature increase generated by the ARFI with pulse bursts might still be within the safe lim- it determined by the US Food and Drug Administration [26]. In a recent study Sugitani et al showed that ARFI elastosonography poses no potential thermal or chemical risk to placenta and fetus [13]. In our study the fetus was Table II. A comparison of placental ARFI elastosonography scores in the patients’ groups.

Group 1 (n: 28) Group 2 (n: 14) Group3 (n: 16) p*

ARFI- maternal (m/s) 0.81 (0.61-1.19)b 0.90 (0.62-1.49)b 1.17 (0.71-1.98)a 0.001 ARFI- central (m/s) 0.80 (0.62-1.2)b 0.81 (0.58-1.28)b 1.05 (0.65-2.32)a 0.002 ARFI- fetal (m/s) 0.88 (0.60-1.16)b 0.78 (0.53-1.14)b 1.1 (0.69-1.86)a 0.004 ARFI- mean (m/s) 0.84 (0.63-0.98)b 0.88 (0.62-1.16)b 1.13 (0.58-1.87)a 0.001

*Kruskal-Wallis test was used to compare continuous variables; a, b, c→ Defined significance between each groups (a>b>c); ARFI, acoustic radiation force impulse.

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not within the direction of waveform paths of the ARFI elastosonography.

It is well known that the placental thickening in ma- ternal red blood cell alloimmunization is a result of pla- cental oedema and compensatory hypertrophy [12]. We hypothesized that this placental oedema, which is an early predictor for fetal anemia, may affect placental elasticity.

If we could demonstrate this placental change by ARFI elastosonography measurements, we could use this tech- nique as a novel marker for adverse perinatal outcomes, additional to middle cerebral artery peak systolic velocity in maternal red blood cell alloimmunization. The current study found that there was a positive correlation between placental stiffness and the development of fetal hydrops.

All placental ARFI scores were higher in Rh alloimmun- ized pregnancies with hydropic fetuses than those in non- hydropic fetuses. We also found that there were similar ARFI scores in Rh alloimmunized pregnancies with non- hydropic fetuses and healthy controls.

Currently, the Doppler evaluation of the middle cere- bral artery peak systolic velocity is the referent technique for antenatal detection of fetal anemia in maternal red blood cell alloimmunization [5]. As a result of this study, we can state that increased placental ARFI scores may be a supplemental, useful, and non-invasive marker for ad- verse pregnancy outcomes, additional to middle cerebral artery peak systolic velocity. This data should be con- firmed with a large sample size and prospective studies by using serial measurements of ARFI elastosonography in maternal red blood cell alloimmunization. We hope that future advances in non-invasive techniques for man- aging fetuses at risk of maternal red blood cell alloim- munization would make a beneficial impact on perinatal morbidity and mortality.

The strength of our study was that all patients were in their third trimester in order to eliminate the possible bias related to the changes in placental growth through second trimester to third trimester. On the other hand, our study has several limitations, namely our sample size was small. Another limitation may the non-homogeneity of patients with regards to the maternal age, gravidity, parity, and gestational week at birth as confounding vari- ables. There is limited data regarding ARFI scores chang- es during different gestational weeks. The studies involv- ing ARFI examinations included the third trimester of gestation in the literature [13,19]. We did not evaluate the histopathologic findings of the placentas. All of the ARFI examinations were performed at the day of delivery as a single measurement; we did not examine placental elas- ticity by serial ARFI evaluations which might give more comprehensive data. We only focused on placental mor- phological changes in this study.

Conclusions

To the best of our knowledge, this is the first study that has evaluated the placental ARFI measurements in maternal red cell alloimmunization. Our study showed that the placenta becomes stiffer in Rh alloimmunized pregnancies complicated with hydrops fetalis, evaluated by the ARFI elastosonography technique. Further studies are required in order to apply this measurement in the fol- low up examinations of Rh alloimmunized pregnancies.

Furthermore, the serial measurements of placental ARFI elastosonography may give additional data regarding the prognosis of maternal red blood cell alloimmunization.

Conflict of interest: none

References

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13. Sugitani M, Fujita Y, Yumoto Y, et al. A new method for measurement of placental elasticity: acoustic radiation force impulse imaging. Placenta 2013;34:1009-1013.

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