The Journal of Maternal-Fetal & Neonatal Medicine

ISSN: 1476-7058 (Print) 1476-4954 (Online) Journal homepage: http://www.tandfonline.com/loi/ijmf20

To Ignore or Not To Ignore Placental Calcifications

on Prenatal Ultrasound: A Systematic Review and
Meta-analysis

Fadi G. Mirza, Labib M. Ghulmiyyah, Hani M. Tamim, Maha Makki, Dima Jeha
& Anwar H. Nassar

To cite this article: Fadi G. Mirza, Labib M. Ghulmiyyah, Hani M. Tamim, Maha Makki, Dima
Jeha & Anwar H. Nassar (2017): To Ignore or Not To Ignore Placental Calcifications on Prenatal
Ultrasound: A Systematic Review and Meta-analysis, The Journal of Maternal-Fetal & Neonatal
Medicine, DOI: 10.1080/14767058.2017.1295443

To link to this article: http://dx.doi.org/10.1080/14767058.2017.1295443

Accepted author version posted online: 14

Feb 2017.

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To Ignore or Not To Ignore Placental Calcifications on Prenatal Ultrasound:

A Systematic Review and Meta-analysis

Fadi G. Mirza,1,2 Labib M. Ghulmiyyah,1 Hani M. Tamim,3 Maha Makki,3 Dima Jeha,1 Anwar

H. Nassar1

1
Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, American

University of Beirut Medical Center, Beirut, Lebanon

2

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Division of Maternal Fetal Medicine, Department of Obstetrics and Gynecology, Columbia

University Medical Center, New York, NY, USA

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3
Biostatistics Unit, Clinical Research Institute, American University of Beirut Medical Center,
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Beirut, Lebanon

Running Title: Placental calcifications

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Corresponding Author: Anwar H. Nassar, MD

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American University of Beirut

Faculty of Medicine and Medical Center
7 Dag Hammarskjold Plaza
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New York, NY, USA 10017

Phone Number: 961 1 370829
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Fax Number: 961 1 370829

Email: an21@aub.edu.lb
ABSTRACT

Objective: The human placenta is known to calcify with advancing gestational age, and, in fact,

the presence of significant calcifications is one of the components of grade III placenta, typical

of late gestation. As such, the presence of significant placental calcifications often prompts

obstetric providers to expedite delivery. This practice has been attributed, in part, to the

presumed association between grade III placenta and adverse pregnancy outcomes. Such

approach, however, can be the source of major anxiety and may lead to unnecessary induction of

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labor, with its associated predisposition to cesarean delivery as well as a myriad of maternal and

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neonatal morbidities. The objective of this study was to examine the association between grade

III placental calcifications and pregnancy outcomes.

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Materials and Methods: A systematic review of the literature was performed for studies

evaluating the association between grade III placenta and a number of pregnancy outcomes,
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including labor induction, fetal distress (abnormal fetal heart tracing), low Apgar score (less than
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7 at 5 minutes), need for neonatal resuscitation, admission to the Neonatal Intensive Care Unit,

perinatal death, meconium liquor, and low birth weight.

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Results: There was a five-fold increase in risk of labor induction with the presence of grade III

placenta (OR 5.41; 95% CI 2.98-9.82). There was no association between grade III placenta and
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the incidence of abnormal fetal heart tracing (OR 1.62; 95% CI 0.94-2.78), low Apgar score of

less than 7 at 5 minutes (OR 1.68; 95% CI 0.84-3.36), need for neonatal resuscitation (OR 1.08;

95% CI 0.67-1.75), admission to the Neonatal Intensive Care Unit (OR 0.90; 95% CI 0.21-3.74),

and perinatal death (OR 7.41; 95% CI 4.94-11.09). In turn, the incidence of meconium liquor

was higher in the setting of grade III placentae (OR 1.68; 95% CI 1.17 to 2.39). Similarly, a
positive association between grade III placental calcifications and low birth weight (OR 1.63;

95% CI 1.19-2.22) was identified.

Conclusion: The study alerts us to a significant association between grade 3 placental

calcifications and labor induction, although it demonstrates that these sonographic findings do

not appear to predispose to perinatal death or fetal distress, low Apgar score, need for neonatal

resuscitation, or admission to the NICU.

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KEYWORDS

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Calcifications, fetal growth restriction, outcome, placenta, pregnancy.
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INTRODUCTION

Placental calcifications, which result from calcium deposition within the placenta, have intrigued

investigators for decades [1] . In a study published 50 years ago, Tindall and Scott evaluated over

3,000 singleton pregnancies and identified placental calcifications in over 75% of postpartum

placentae [2] . Spirt et al subsequently examined the presence and extent of placental

calcifications using prenatal ultrasound and reported calcifications in over 75% of pregnancies

beyond 33 weeks of gestation [3]. In another study, extensive calcifications were identified in

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nearly 40% of parturients at term [4]. In fact, the Grannum classification, a well-established

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ultrasound grading system for assessment of placental maturity, depends on the presence and

extent of calcifications [5, 6].

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The human placenta is known to calcify with advancing gestational age, and placental changes

identified on ultrasound have been correlated with fetal maturity. In fact, the presence of
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significant basal calcifications is one of the characteristics of a grade III placenta, typical of late
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term and post term gestations. Because of this, placental calcifications have traditionally become

synonymous with “post-term”, and their presence often prompts obstetric providers to expedite
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delivery. This practice has been attributed, in part, to the presumed association between

significant placental calcifications, which characterize a grade III placenta, and adverse
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pregnancy outcomes. As such, these sonographic findings can be the source of major anxiety to

the parturient and her family. More importantly, this mindset can result in unnecessary induction

of labor with its associated predisposition to cesarean delivery in addition to various maternal

and neonatal morbidities. The objective of this study was to examine the association between

grade III placental calcifications and a number of pregnancy outcomes in order to better

understand their clinical significance and importance in clinical practice.

MATERIALS AND METHODS

Study design

This study was carried out as a systematic review and meta-analysis at the Department of

Obstetrics and Gynecology at American University of Beirut Medical Center, Beirut, Lebanon

during the period between January and June 2016.

Literature search

We searched the following engines (PubMed, Embase, and Web of Science…) for articles

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addressing placental calcifications, using a search strategy that included both text word and

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medical subject heading (MeSH) terms. MeSH headings included “(calcification and placenta)

OR (calcifications AND placenta) OR (calcification AND placental) OR (calcifications AND

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placental) OR (placental calcification) OR (placental calcifications)”, “grade III placental

calcifications”, “grade III placenta versus control group”, “pregnancy outcomes”, “fetal growth
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restriction”, “meconium”, “neonatal outcome”, “’Grannum”, “IUGR”, “LBW”, “birth weight”

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and their variants. We also reviewed the references from the extracted articles and we screened

the titles and abstracts to identify the relevant articles related to the objective.
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Study selection
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Eligible studies were restricted to those published in English language between January 1, 1985

and December 31, 2015, and those that examined the effects of placental calcifications and that

included a control group. Moreover, to be eligible for this study, one of the following pregnancy

outcomes should be reported: induction for suspected fetal compromise, abnormal

cardiotocography (CTG), meconium liquor, Apgar score at 5 minutes less than 7, neonatal

resuscitation, low birth weight, admission to the Neonatal Intensive Care Unit (NICU) and
perinatal death. Excluded from this study were those that provided insufficient information to

construct a 2 x 2 contingency table for the calculation of the odds ratio (OR). Our initial search

yielded 183 articles, of which we excluded 149 for the language. Of the remaining articles, 13

reported on perinatal outcomes of interest. We excluded 7 for the following reasons: other grade

of placenta than grade III placenta or no 2 x 2 contingency table between the interaction and the

outcomes. Finally, 6 articles fulfilled our inclusion criteria.

Review process

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We extracted from the eligible articles the following information and included them in the meta-

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analysis: lead author, year of publication, sample size, as well as the number of placental

calcifications, and the pregnancy outcomes as shown in table 1. Two investigators reviewed the
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articles and extracted the relevant information. Disagreement was resolved by communication

and consensus. The quality of the studies included in the systematic review was measured by the
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number of participants, comparability of control group, completeness and duration of follow up,
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and the quality of adjustment for potential confounders.

Statistical analysis
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We used Review Manger (version 5.3) to analyze the data. Data were presented as frequency and

percentage. The Odds Ratio (ORs) with 95% confidence intervals (CI) for each individual study
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was calculated by the Mantel-Haenszel and then an overall OR was calculated between all

studies. We also performed test of heterogeneity between studies using χ 2 and I2 tests for

significance and a p-value ≤ 0.05 was considered for statistical significance.

RESULTS

The association between presence of grade III placenta and labor induction was reported by two

studies [4, 7]. The meta-analyses carried out provided an OR of 5.41 (95% CI 2.98-9.82) with

non-significant heterogeneity test (I2=0%; P=0.98) as illustrated in Figure 1. The same

references [4, 7] were used to analyze the association between grade III placenta and the

incidence of abnormal fetal heart tracing (cardiotocography; CTG). Using Mantel-Haenszel

method, we found that, among parturient with a grade III placenta, the incidence was not

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increased compared to the controls (OR 1.62; 95% CI 0.94-2.78), and the heterogeneity test was

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not significant (I2=0%; P=0.85), as demonstrated in Figure 2.

The relationship between a low Apgar score (less than 7) and grade III placenta was explored by
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the three studies [7-9]. There was no statistically significant association between low Apgar

score (less than 7) and grade III placenta (OR 1.68; 95% CI 0.84-3.36; I2=0%; P=0.48), as shown
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in Figures 3.
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Additionally, for the included studies [4, 7], the analysis demonstrated that there was no

association between grade III placenta and the need for neonatal resuscitation (OR 1.08; 95% CI
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0.67-1.75) and admission to the Neonatal Intensive Care Unit (OR 0.90; 95% CI 0.21-3.74), and

the heterogeneity test was not significant as illustrated in Figures 4, and 5, respectively.
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Three studies [8-10] were combined in a meta-analysis and this result indicated a non-

statistically significant reduction in perinatal death with placenta grade III group compared to

control group (OR 7.41; 95% CI 4.94-11.09; I2=7%; P=0.34), as illustrated in Figures 6.

Moreover, the incidence of meconium liquor (amniotic fluid meconium) that was reported by

three studies [4, 7, 9] was higher in the placenta grade III group compared to control group (OR
1.68; 95% CI 1.17 to 2.39) and the heterogeneity test was considered not significant (I2=24%;

P=0.27), as shown in Figure 7.

Finally, as illustrated in Figure 8, a positive association between grade III placental calcifications

and low birth weight (OR 1.63; 95% CI 1.19-2.22) was identified by five studies [4, 7-9, 11]

with significant heterogeneity test (I2=73%; P=0.005).

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DISCUSSION

This study has showed a number of important findings that pertains to the practice of all

obstetrics health care providers. The study alerts us to a significant association between grade 3

placental calcifications and labor induction (more than five-fold increase), although it

demonstrates that these sonographic findings do not appear to predispose to perinatal death or

fetal distress as evidenced by abnormal fetal heart tracing, low Apgar score, need for neonatal

resuscitation, or admission to the Neonatal Intensive Care Unit. It is noteworthy that grade 3

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placental calcifications were associated with low birth weight and meconium-stained amniotic

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fluid level in this study.

The well-established ultrasound grading system for the placenta, referred to as the Grannum
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classification, is based on the maturity of the placenta and depends on the presence as well as

extent of calcifications [5, 6]. According to this system, a placenta can be classified into one of
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four grades. A grade 0 placenta, typically seen before 18 weeks, is characterized by uniform
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echogenicity and a smooth chorionic plate. In a grade I placenta, typical of 18-29 weeks,

occasional parenchymal calcification/hyperechoic areas are seen, along with subtle indentations
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of the chorionic plate. In turn, a grade II placenta, typically seen beyond 30 weeks, has

occasional basal calcification areas with deeper indentations of the chorionic plate yet not
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reaching up to the basal plate. Finally, a grade III placenta, generally seen during late term and

post term, is marked by significant basal calcifications and chorionic plate interruption by

indentations that reach up to the basal plate. Although ultrasonically detectable placental changes

have been correlated with fetal maturity, the relative incidence of each placental grade at various

gestational ages has not been well established. In the above-mentioned study by Spirt et al [3],

only 18% of term placentae met the criteria for grade III. These results were reproduced by
another study by Hill et al [12] that evaluated placental grading in 1709 third-trimester

sonograms. In this study, even at 40 weeks or beyond, fewer than 20% of placentas showed

sonographic evidence of calcifications consistent with grade III. Hence, the authors concluded

that the latter findings could not be used to predict post-maturity. It is not surprising then that

reporting placental grading does not represent standard obstetric care at the time of prenatal

visits, even during the third trimester.

Because grade III placentae are marked by extensive placental calcifications, the latter have

gradually become synonymous with “post-term”. Thus, the presence of placental calcifications

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has often prompted obstetric providers to expedite delivery, regardless of gestational age. The

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rationale for this approach stems from concerns for underlying placental insufficiency and
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predisposition to adverse pregnancy outcomes. This potential link between placental

calcifications and placental insufficiency derives from the observation that calcifications are
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more commonly seen in the setting of tobacco smoking, hypertensive disorders of pregnancy,
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diabetes, and vasculopathies [13-15]. One of the earliest studies that pertain to this topic has

demonstrated that pregnancies complicated by preeclampsia or intrauterine growth retardation

are characterized by faster placental maturation than normal [16]. This study recommended that
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pregnancies, in which grade III changes are seen prior to 34 weeks, be followed closely for

possible complications. However, the association between grade III placental changes and/or
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placental calcifications per se and adverse perinatal outcome in low risk pregnancies with none

of the above-mentioned risk factors is less clear. The association between adverse pregnancy

outcomes and premature appearance of placental calcifications has been examined in low risk

populations, although most of the pertinent studies were limited by the small sample size and the

presence of multiple confounding factors. These outcomes included intrapartum fetal distress
(non-reassuring fetal heart rate), low Apgar score, fetal growth restriction, low birth weight,

abruptio placenta, and hypertensive disorders of pregnancy [9, 17-22].

In a study by Quinlan et al, these complications were encountered in up to 78% of pregnancies

characterized by premature appearance of grade III placental changes, suggesting that these

sonographic findings reflect placental senescence and dysfunction [22]. In the study by Hill et al

[12], the incidence of intrapartum fetal distress was noted to be higher in the setting of post-

maturity and other conditions that give rise to premature placental senescence yet not with the

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presence of a grade III placenta per se. In other pioneering prospective study, Vosmar et al [16]

examined the usefulness of placental grading in predicting fetal growth restriction. A total of 137

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parturients who had an ultrasound scan within one week of delivery were enrolled, and grade III
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was reached in 42% of placentae. The author did not find any association between grade III

placenta and fetal growth restriction. However, when a grade III placenta was first seen before
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36 weeks, a growth-restricted neonate was born in 3 out of 5 cases. Research interest in placental
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calcifications and their clinical significance was resumed during the last decade. In 2005,

McKenna et al prospectively examined 1,802 low risk patients [4]. Ultrasound scans were

performed at 36 weeks and grade III placental calcifications were reported in only 4% of patients
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at that time. These subjects were at increased risk of induction of labor for fetal compromise (RR

4.7; 95% CI 2.6-8.4), low birth weight (RR 3.1; 95% CI 1.8-5.4), and preeclampsia (RR 4.7;
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95% CI 1.9, 11.8). In turn, the finding of grade III placenta was not associated with adverse fetal

and neonatal outcomes. More recently, Chen et al [8] also examined the significance of grade III

placental calcifications in low risk patients. Subjects were classified into 1 of 3 groups: patients

with placental calcifications diagnosed before 32 weeks; patients with placental calcifications

diagnosed between 32 and 36 weeks; and a control group at 28 to 36 weeks with no evidence of
placental calcifications. The authors reported a statistically significant difference in maternal

outcomes, including postpartum hemorrhage (OR, 3.4; 95% CI, 1.3–9.4), placental abruption

(OR, 6.5; 95% CI, 1.4–31.4) and maternal transfer to the intensive care unit (OR, 9.8; 95% CI,

1.8–52.2). They also reported a statistically significant difference in fetal outcomes, namely

preterm birth (OR, 4.2; 95% CI, 1.8–9.9), low birth weight (OR, 4.6; 95% CI, 2.2–9.5), low

Apgar score (OR, 6.5; 95% CI, 2.1–20.1) and neonatal death (OR, 9.0; 95% CI, 1.7–47.4). The

differences persisted even after adjusting for potential confounders. Finally, a study by Cooley et

al [23] reported that placental calcification was associated a 40-fold increase in the incidence of

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fetal growth restriction.

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While there appears to be a correlation between Grannum grade III placentas and increased
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perinatal risk, it is mandatory to discuss the grading system itself. Although the classification is

well established and grades zero to III are well defined, it is a rather subjective and operator-
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dependent grading system. A study by Sau et al [24] took six participants, all of which well
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experienced in Grannum grading and gave each 55 placental images to grade; and four to six

weeks later gave the six participants the same 55 images to grade again. Only one image

received the same grade by all the participants. Not only was complete agreement difficult to
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come by, but there was also a wide variation among the grades. For example out of 55 images,

participant C labeled 15 images as grade III, while participant A only found two out of 55 images
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to be considered grade III. Another study by Moran et al [25] reported similar findings. In this

study, five experienced ultrasound operators were exposed to 90 placental images, of which

complete agreement among all operators was found for only nine images. Both studies

demonstrate the subjectivity of Grannum grading and suggest that this field might require further

training and possible involvement of digital analysis. The inconsistency among the graders not
just with each other but also among their own grades (after having re-graded the same images

four to six weeks later) does question the reliability of Grannum grading and should always be

considered when discussing this subject.

In conclusion, grade III placenta and significant placental calcifications are typical of the late

term and post term periods, and hence their identification often raises concern for placental

dysmaturity. Previous reports have linked these findings to a myriad of maternal and fetal

adverse outcomes that include intrapartum fetal distress, low Apgar score, fetal growth

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restriction, low birth weight, hypertensive disorders of pregnancy, abruptio placenta, and

postpartum hemorrhage. However, this association has not been established with certainty and it

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is thus not surprising that the reporting of placental grading does not represent standard obstetric
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care during prenatal visits, even during the third trimester. In fact, serious concerns have been

raised regarding the subjectivity of reporting placental calcification and the Grannum
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classification per se. According to our study, the presence of grade III placental calcifications
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appears to be a risk factor for labor induction for concern for fetal well being, although these

sonographic findings did not appear to be associated with abnormal fetal heart tracing, low

Apgar score, need for resuscitation, admission to the Neonatal Intensive Care Unit, and perinatal
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death. Based on the available evidence, the practice of expediting delivery solely on the basis of

significant placental calcifications does not appear to be indicted at this time. Instead, close
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monitoring of pregnancies, including serial assessment of fetal growth, with premature

appearance of such calcifications seems reasonable.

ACKNOWLEDGEMENTS

The authors would like to acknowledge Dr. Ahmad Abdul Wahed for inspiring this study.

DISCLOSURE STATEMENT

The authors declare no conflict of interest pertinent to this manuscript.

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2. Tindall, V.R. and J.S. Scott, Placental Calcification a Study of 3,025 Singleton and

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3. Spirt, B.A., W.N. Cohen, and H.M. Weinstein, The incidence of placental calcification in

normal pregnancies. Radiology, 1982. 142(3): p. 707-11.

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assessing risks of stillbirth. Placenta, 2015. 36(9): p. 1039-44.

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13. Carroll, B., Ultrasonic features of preeclampsia. J Clin Ultrasound, 1980. 8(6): p. 483-8.
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14. Brown, H.L., et al., Premature placental calcification in maternal cigarette smokers.

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15. Moran, M., et al., Novel placental ultrasound assessment: potential role in pre-gestational

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16. Vosmar, M.B., H.W. Jongsma, and P.W. van Dongen, The value of ultrasonic placental

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17. Patterson, R.M., R.H. Hayashi, and D. Cavazos, Ultrasonographically observed early

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18. Hills, D., et al., Distribution of placental grade in high-risk gravidas. AJR Am J

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TABLES

Table 1: Study Characteristics

n of placental
Author Year calcifications / Outcomes
n of study
Miller et al.[11] 1988 97 / 246 Low birth weight

Meconium liquor
Apgar Score at 5 minutes Less than 7
Proud et al.[9] 1987 223 / 1468 Low birth weight
Perinatal death

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Induction for suspected fetal compromise
Abnormal Cardiotocography (CTG)

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Meconium liquor
McKenna et Neonatal resuscitation
2005 68 / 1802
al.[4] Low birth weight
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Admission to the Neonatal Intensive Care
Unit (NICU)

Induction for suspected fetal compromise

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Abnormal Cardiotocography (CTG)

Meconium liquor
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Apgar Score at 5 minutes Less than 7

Sersam et al.[7] 2011 23 / 591 Neonatal resuscitation
Low birth weight
Admission to the Neonatal Intensive Care
Unit (NICU)
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Apgar Score at 5 minutes Less than 7

Low birth weight
Chen et al.[8] 2011 192 / 713
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Perinatal death

Chen et al.[10] 2015 974 / 15122 Perinatal death

FIGURES

Figure 1. Labor induction for suspected fetal compromise

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Figure 2. Abnormal Cardiotocography (CTG)
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Figure 3. Apgar Score at 5 minutes Less than 7

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Figure 4. Need for neonatal resuscitation

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Figure 5. Admission to the Neonatal Intensive Care Unit (NICU)

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Figure 6. Perinatal Death

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Figure 7. Meconium liquor

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Figure 8. Low birth weight

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