Jan Weichert

Rafael David Hartge

Obstetrical sonography in obese women: A review

Keywords: obesity, ultrasound, pregnancy, image quality, body mass index

The prevalence of overweight and obese women of childbearing age poses a major challenge to obstetric practice, because increased maternal size is associated with a number of pregnancy complications affecting both mother and the developing fetus. Obstetrical ultrasound imaging in pregnant women is adversely affected by obesity with negative impact on the detection rate of congenital anomalies. This review aims to tabulate relevant data dealing this issue and to discuss clinical as well as technical problems accompanied with ultrasound examination of the obese gravida.

Introduction

The World Health Organization (WHO) stated in 2005 that an estimated number of 1.6 billion adults (aged 15 years and older) were overweighted (body mass index, BMI ≥ 25-29.9) and additional 400 million adults were obese (BMI ≥ 30) by definition. By 2015 it is expected that one third of the world's population (2.3 billion) will be overweighted and more than 700 million people (9 %) will match the criteria of obesity 1,2 . The incidence of obesity among pregnant women in the United States ranges from 18.5 to over 38 % 3,4 . These alarming data constitute a significant public health concern not only for obstetrical care providers and is likely to remain so for the forseeable future. A recently published study of more than 13.000 pregnant women clearly demonstrated that obese parturients increasingly use healthcare resources 5 .

Obese women, especially those who show abdominal adiposity, are at increased risk of adverse pregnancy outcome including gestational diabetes, hypertension, infectious morbidity, postpartum haemorrhage, fetal macrosomia and stillbirth [6][7][8][9][10][11][12][13] . In a large retrospective study Sebire et al. reviewed the database records of 290.000 pregnancies of the North West Thames Region and highlighted the association of obesity and maternal and fetal pregnancy complications in relation to the degree of obesity 14 . Similar data were previously published by Cnattingius et al. and Nohr et al. who analysed records derived from Scandinavian birth registers 15,16 . Furthermore, maternal obesity has been established as a potential risk factor for congenital malformations even in the absence of gestational diabetes. Several population-based studies have reported the likelihood of structural abnormalities of the offspring of obese mothers, such as neural tube defects, congenital heart defects, anorectal atresia, hydrocephaly, hypospadias and limb reduction defects [17][18][19][20][21][22] .

Although considerable technical advances in obstetrical ultrasonography have been achieved over the last 3 decades, ultrasound imaging of obese patients remains challenging due to adverse effects of obesity on propagating sound waves. This review tabulates the available data on these conditions regarding imaging options in obese pregnant women and clinical Obstetrical ultrasound and obesity importance for the detection of fetal abnormalities to provide a framework for a proper parental counseling.

Quantification of obesity

For the estimation of the degree of fat accumulation, assessment of the body mass index (BMIcalculated as weight in kilograms divided by height in meters squared) has been established as the principal standard method to diagnose overweight and obesity. By definition the World Health Organization (WHO) and the National Institutes of Health (NIH) both define normal weight comprising a BMI of 18.5-24.9, overweight as a BMI of 25-29.9, and obesity as a BMI of 30 or greater. Obesity is further categorized by BMI into Class I (30-34.9), Class II (35-39.9), and Class III or morbid obesity (≥ 40) 2,23 . In pregnancy, BMI is calculated using pre-pregnant weight or the weight measured during the initial visit at the prenatal care provider. Due to the fact that BMI is an indirect measure reflecting the overall fatness without distinguishing between fat and fat-free components it is not as useful in predicting the difficulties encountered with ultrasound visualization and putative obesity-related risks during advancing pregnancy. In the past few years, a number of studies have called attention to the importance of abdominal obesity and its measuring modalities. A strong relation between increase in abdominal girth and cardiovascular disease among adults has recently been demonstrated 24 . Other publications stressed the association of abdominal obesity and poor respiratory function or the increased risk of chronic kidney disease in the general population 25,26 . However, from an obstetric perspective Yamamoto et al. in 2001 were the first who reported a higher waist-to-hip ratio (WHR) prior to 9 gestational weeks to be significantly linked to an increased risk for pre-eclampsia 27 . Similar findings were published by Sattar et al., who found a significant correlation of increased waistcircumference prior to 16 weeks' gestation and pregnancy-induced hypertension (Odds Ratio -OR 1.8, 95% confidence intervall -CI 1.1, 2.9) and pre-eclampsia (OR 2.7, 95% CI 1.1, 6.8) 28 . In a prior series an impact of maternal WHR on elevated fetal growth was established 29 . Both waistto-hip ratio (WHR) and waist circumference (WC) have been additionally used as proxy Obstetrical ultrasound and obesity measures for body fat distribution when investigating health concerns evolving from (maternal) obesity [30][31][32] . Bartha and colleagues introduced an ultrasonographic measurement of maternal visceral fat thickness (VFT) during early pregnancy and were able to demonstrate a better correlation of the VFT estimate compared to BMI with metabolic and cardiovascular risk factors such as hyperinsulinaemia, insulin resistance, high blood pressure or dyslipidaemia in pregnancy 33 .

Obstetrical ultrasound

Pre-examination counseling of the obese gravida has to point out the likely impact of adiposity on image clarity and diagnostic accuracy 34 . This should be communicated to the patient in a sensitive but appropriate way, because it allows earlier abandonment of a technically difficult study and enables to set realistic expectations regarding the scan 35 . It seems reasonable to claim an informed consent signed by the gravida in advance of the anatomic survey. Furthermore, the first prenatal visit should focus on dating the pregnancy and confirming viability of the fetus. In fact, obese women are more likely to have anovulatory or irregular cycles, so that the utility of determining the last menstrual period for establishing gestational age may be limited [START_REF] Phillips | For the obese gravida, try strong counselling and close follow-up[END_REF] . To improve the accuracy of pregnancy-dating during the early first trimester, transvaginal assessment of the crown-rump-length should be performed.

Image clarity

In addition to the arithmetic indices, measuring the distance from skin surface to the intrauterine region of interest (e.g. key fetal structures) allows simple documentation of the fat layer, thereby conveying the grade of image clarity impairment (figure 1) 35 . Excess of abdominal (subcutaneous or intraabdominal) fat results in an increased number of interfaces and consecutively in marked attenuation of the signal. Attenuation encompasses absorption, reflection, reverberation and scatter [START_REF] Davidoff | Maternal umbilicus: ultrasound window to the gravid uterus[END_REF] . The overall visualization of fetal organs with respect to Obstetrical ultrasound and obesity increasing maternal size has been previously addressed by several studies [START_REF] Zador | Nomograms for ultrasound visualization of fetal organs[END_REF][START_REF] Wolfe | Trends in sonographic fetal organ visualization[END_REF] . Reduction in successful image generation was most marked for cardiac and cerebrospinal structures as well as the umbilical cord [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF][START_REF] Hendler | The impact of maternal obesity on midtrimester sonographic visualization of fetal cardiac and craniospinal structures[END_REF] . Catanzarite et al. postulated five categories of potential barriers to complete fetal anatomic survey. In addition to maternal body habitus, other confounding variables such as gestational age, fetal spine-up position, resolution/penetration of ultrasound equipment and sonographer skills evidently exert influence on image clarity. The authors also described a strong relation of scanning duration and completion of the anatomical survey in the non-obese population. For each 5-minute time increment up to 30 minutes, the rate of complete morphological assessment improved in their study [START_REF] Catanzarite | Targeted mid-trimester ultrasound examination: how does fetal anatomic visualization depend upon the duration of the scan?[END_REF] .

The impact of sonographer's experience on the rate of suboptimal visualization in the obese gravida is obvious and was previously reported [START_REF] Hendler | Does sonographer's experience impact the rate of suboptimal visualization in the obese gravida [abstract]?[END_REF]44 . Rates of completed anatomic surveys rise with advancing gestational age. The preferred timing of midtrimester ultrasound examination of the obese gravida appears to be between 18-20 weeks' gestation in order to achieve maximum efficiency with respect to the potential duration of the scan and need for repeated scans 45,46 . This is slightly different to the findings of Wolfe et al. who stated an optimal overall organ visualization at 21-23 weeks for a mean maternal BMI of 27.3 of the women enrolled in their study [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF] .

Hendler et al. described an inverse relationship between the severity of maternal obesity and the ability to adequately visualize the fetal heart (37.3 % obese vs. 18.7 % non-obese, p < 0.001) and craniospinal structures (42.8 % obese vs. 29.5 % non-obese, p < 0.001). They found a degradation in image quality by 10 % for every further step in obesity classification [START_REF] Hendler | The impact of maternal obesity on midtrimester sonographic visualization of fetal cardiac and craniospinal structures[END_REF] .

Wolfe et al reported a 14.5 % reduction in visualization rates in the markedly obese patient [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF] .

Similar observations were recently published with respect to suboptimal visualization of facial soft tissue (39.1 % obese vs. 19.3 % non-obese, p < 0.001) and abdominal wall (2.7 % obese vs. 0 % non-obese, p < 0.001) 47 . Series assessing the potential impact of maternal obesity 48 on optimal visualization and completion of anatomic survey 49 Obstetrical ultrasound and obesity Due to this poor transmission of ultrasound waves in adipose tissue there were several attempts to optimize in image quality. A transvaginal approach is beneficial for assessment of fetal structures close to the lower uterine segment and therefore mainly limited to ultrasound examinations throughout the first trimester. Measurement of fetal nuchal translucency between 11-13+6 weeks most often performed transabdominally as this allows a wider range of scanning angles, may substantially be hampered by increasing maternal size 50,51 . In the obese patient therefore, a transvaginal assessment to facilitate a better resolution of the skin line, perispinal tissue or amniotic sheet as separate structures, should be considered 35 . This approach enables proper assessment of fetal limbs and extremities and is feasible to perform early fetal echocardiography as well. Recently, it has been postulated that most of the anomalies detectable during standard 18-week scan can be seen at 12 to 13 weeks with appropriate imaging even in obese women 52 . However, this has been challenged by other authors, which concordantly emphasize that a number of anomalies are not amenable to first trimester detection (regardless recent promising findings, such as intracranial translucency) [53][54][55] . Further studies are needed to systematically investigate the diagnostic capability of a first trimester anatomic sonogram and to establish reliable standards taking into account increased maternal size and limited acoustic window 56 . Beyond 14-15 weeks' gestation ultrasonic scans are preferentially performed by transabdominal imaging, thereby utilizing appropriate anatomic regions (e. g. lower transverse abdominal crease). Morbidly obese women often have an abnormally lowered, ptotic apron. Elevating and retracting the fatty apron (panniculus) towards the patient's head enables optimized access to the fetal areas of interest by placing the probe near the arcus tendineus superior to the pubis 35,[START_REF] Phillips | For the obese gravida, try strong counselling and close follow-up[END_REF] . This is of particular importance with regard to diagnostic procedures such as chorionic villous sampling (CVS), amniocentesis (AC) or cordocentesis (CS). In later gestation it may also be helpful to get access to the gravid uterus from a subcostal approach with the women in a lateral position which shifts the abdomen towards the examination table. In general, the higher the Obstetrical ultrasound and obesity degree of maternal obesity, the higher will be the pressure exerted on the abdominal wall to reduce the depth of insonation thereby trying to achieve an acceptable acoustic window.

Alternative approaches

In obese patients, in whom a successful fetal anatomic survey has apparently failed, the maternal umbilicus, the thinnest section of the abdominal wall potentially affords improved image resolution. A previous series by Davidoff et al. revealed an optimized image clarity in most of the 68 included women, but the relatively large curvilinear transducer may have limited the ultrasonic sector view [START_REF] Davidoff | Maternal umbilicus: ultrasound window to the gravid uterus[END_REF] . Based on these findings Rosenberg et al. and later McCoy and coworkers established a transumbilical use of the endovaginal probe in the obese gravida 57,58 .

Placement of the transvaginal transducer in the umbilicus resulted in improved resolution and satisfactory fetal cardiac survey in 95 % and 87 % respectively. The authors resumed, that transumbilical use of the transvaginal probe is a beneficial, well-tolerated technique, which clearly improves gray-scale imaging. In addition, color and pulsed Doppler interrogation of fetal vessels may also be optimized. Similar observations were made by Paladini, who assumed that improved cardiac visualization (with the fetus in breech presentation) may be achieved when the scan is performed with filled maternal bladder pushing the uterus cephalad, allowing the sonographer to explore the heart via the periumbilical region 59 .

On the contrary, a transrectal approach has been undertaken in those patients undergoing assisted reproduction where difficult embryo transfer was anticipated and transabdominal ultrasound guidance was hampered by increased BMI 60 . However, these procedures have not been regularly implemented in routine obstetrical ultrasound practice.

Tissue harmonic imaging

Tissue harmonic imaging (THI), nowadays commonly implemented into commercially available ultrasound systems, constitutes a real-time imaging technique that relies on the detection of socalled harmonics created by non-linear propagation of the fundamental ultrasonic beam through Obstetrical ultrasound and obesity tissue 61 . The generation of harmonics by tissue itself increases with depth up to a point where attenuation causes them to decrease. Modern ultrasound transducers are able to isolate the second harmonic frequency in the detected echo, enabling image rendering of harmonic reflection. This relatively novel method of echo processing is useful while scanning technically difficult patients to improve image quality and confidence of diagnosis 62,63 . Treadwell and colleagues found that tissue harmonic imaging was able to improve resolution of at least one fetal structure in more than 50 % of patients enrolled in their study 64 . Whether the use of THI may result in improved detection of fetal abnormalities this study was not able to confirm, because the included patients had normal fetuses. Nevertheless, the advantages of THI in fetal cardiac examination were recently addressed by three studies [65][66][67] . The differences in image clarity obtained by using THI in a morbidly obese gravida compared to inconclusive images depicted without technical adjuncts are illustrated in figure 2. Other technical advances facilitating improved ultrasound assessment of fetal morphology in obese mothers include preand postprocessing techniques such as compound imaging, speckle reduction filters and multi-Hertz transducer technology.

Other imaging modalities

In recent years, three-and four-dimensional ultrasound applications have become clinically valuable in obstetrics as well as in gynecology. Comparative studies addressing the beneficial value of 3D ultrasound are contradictory. In a review of 11 studies comparing conventional 2D imaging and 3D ultrasound for the diagnosis of facial anomalies, seven studies reported additional information using 3D while four found similar findings achieved by these two modalities 68 . Many of the studies on the accuracy of 3D ultrasonography in prenatal diagnosis are biased by the availability of information from the initial 2D scan. Nevertheless, a previous study suggests three-dimensional ultrasound as being capable of improving visualization of fetal anatomy even in fetuses in anterior spine position 69 . In spite of the apparent advantages of 3D obstetrical imaging, non-favourable scanning conditions, such as oligohydramnios, severe Although ultrasound is the primary imaging modality for the evaluation of the fetus, because of proven utility, relatively low cost and widespread availability, fetal magnetic resonance imaging (MRI) has grown in popularity over the past two decades as a complementary tool for antenatal assessment of fetal abnormalities [START_REF] Gonçalves | What does 2-dimensional imaging add to 3-and 4dimensional obstetric ultrasonography?[END_REF][START_REF] Wang | Imaging comparison of basic cardiac views between two-and three-dimensional ultrasound in normal fetuses in anterior spine positions[END_REF] . MRI has been useful in confirming abnormalities seen on ultrasound scan or determining the underlying cause of nonspecific sonographic anomalies and may add incremental information that might have influence on prognosis or management at birth [START_REF] Behairy | Magnetic resonance imaging in fetal anomalies: What does it add to 3D and 4D US?[END_REF][START_REF] Frates | Fetal anomalies: comparison of MR imaging and US for diagnosis[END_REF][START_REF] Whitby | Ultrafast magnetic resonance imaging of central nervous system abnormalities in utero in the second and third trimester of pregnancy: comparison with ultrasound[END_REF] . Faster scanning techniques allow studies to be performed without sedation in the second and third trimester with minimal motion artefacts [START_REF] Hubbard | Ultrafast fetal MRI and prenatal diagnosis[END_REF] . Moreover, MRI is not hampered by maternal obesity, fetal position, overlying bones or oligohydramnios, so that fetal MRI has emerged as a clinically valuable diagnostic supplement to ultrasound in case of inconclusive findings or degraded image.

Detection of malformations

Infants of obese parturients are reported to be at elevated risk for congenital malformations (11.1 %) compared with those of mothers of average prepregnancy weight (7.9 %). Queisser-Luft et al. reported significant odds for major malformations (OR 1.3, 95 % CI 1.0-1.7) [START_REF] Queisser-Luft | Malformations in newborn: results based on 30.940 infants and fetuses from the Mainz congenital birth defect monitoring system (1990-1998)[END_REF] . Similar findings were recently published by two meta-analyses in which the authors systematically assessed the attributable risk for anomalies in the offspring of obese mothers 21,22 Obstetrical ultrasound and obesity been described. On the other hand, the relative risk for gastroschisis among obese mothers was significantly lower (OR 0.17, 95 % CI 0.10-0.30) compared with women of recommended BMI [START_REF] Siega-Riz | National Birth Defects Prevention Study. The joint effects of maternal prepregnancy body mass index and age on the risk of gastroschisis[END_REF] .

An opposite effect has been found for offspring with omphalocele, with increased odds (OR 1.63, 95 % CI 1.01-2.47) when the mother was classified as obese. These data emphasize the superior importance of detailed sonographic examination of fetuses of obese pregnant women 78,79 .

According to the findings of the FaSTER (First and Second Trimester Evaluation of Risk) trial in an unselected obstetric population, it has been stated that maternal obesity significantly decreased the likelihood of sonographic detection of common anomalies (adjusted OR 0.7, 95 % CI 0.6-0.9) 80 . In a recent paper Dashe et al. assessed the impact of maternal body habitus on the detection of major structural abnormalities during second-trimester standard and targeted sonographic scan 81 . Detection of anomalous fetuses with standard ultrasound decreased substantially from 66 % in women having a normal BMI to only 25 % in morbidly obese women.

In high risk pregnancies receiving targeted scans detection of malformations ranged from 83 % (lean patients) to 67 % (class III obesity). Within the targeted group the detection rate was significantly lower among women with pre-gestational diabetes than in women with other highrisk indications. These data are consistent with previous findings. In order to facilitate proper counseling, the residual risk of an undetected anomaly was calculated to be 0.4 % among women of normal BMI compared to 1.0 % in obese gravida (p < 0.001). However the authors did not address the issue whether follow up ultrasonography could have improved anomaly detection in obese women. Hendler et al. noted that 64 % of their included study population, who were scheduled for an additional fetal heart examination due to the initial inability to complete morphology assessment of the fetus, were obese 82 . The rate of persistent suboptimal visualization of cardiac structures even after recalled exam increased in a BMI-dependent manner from 1.5 % (non-obese) up to 20 % in morbidly obese women (p < 0.001). In conclusion the authors stated that the rate of initially inadaequate image clarity could be reduced by at least 80 % by repeating sonographic scans, thereby improving the prenatal diagnosis of congenital heart defects in an obstetric setting. In accordance to these observations, which are similar to Obstetrical ultrasound and obesity previous reports, maternal obesity limits the likelihood of adequate ultrasound visualization even when advanced ultrasound systems for assessing fetal structures are used 83 .

Summary

Given the continuing rise in prevalence of overall obesity, and in particular maternal obesity with impact on ultrasound imaging of fetal anatomy, obstetricians have to face new challenges in the antenatal and peripartal management of complications during pregnancy, labor, delivery and beyond. Obtaining adequate sonographic images in obese patients is of particular concern because of the increased rate of congenital anomalies. Considering the findings of sensitivity studies on mixed populations or obese gravid patients, it is reasonable that the anomaly scan at 20 weeks' gestation should be left to experienced sonographers. Moreover, obese mothers will benefit from repeated ultrasonic scans.

The main determinants of signal intensity and consecutive image clarity remain the depth of the part to be depicted as well as the specific tissue characteristics. Thus, future additions to the imaging efforts should include optimized signal processing, further advances in transducer technology or the adjunctive use of complementary image modalities such as fetal MRI to resolve associated shortcomings of obesity in obstetric practice.

An appropriate counseling prior to the commencement of the sonographic exam of overweight and obese patients allowing for the limitations of the study is advisable. The greater potential for delayed or missed diagnoses in obese patients constitutes one of the major medicolegal issues in obstetric care.

Introduction

The World Health Organization (WHO) stated in 2005 that an estimated number of 1.6 billion adults (aged 15 years and older) were overweighted (body mass index, BMI ≥ 25-29.9) and additional 400 million adults were obese (BMI ≥ 30) by definition. By 2015 it is expected that one third of the world's population (2.3 billion) will be overweighted and more than 700 million people (9 %) will match the criteria of obesity 1,2 . The incidence of obesity among pregnant women in the United States ranges from 18.5 to over 38 % 3,4 . These alarming data constitute a significant public health concern not only for obstetrical care providers and is likely to remain so for the forseeable future. A recently published study of more than 13.000 pregnant women clearly demonstrated that obese parturients increasingly use healthcare resources 5 .

Obese women, especially those who show abdominal adiposity, are at increased risk of adverse pregnancy outcome including gestational diabetes, hypertension, infectious morbidity, postpartum haemorrhage, fetal macrosomia and stillbirth [6][7][8][9][10][11][12][13] . In a large retrospective study 15,16 . Furthermore, maternal obesity has been established as a potential risk factor for congenital malformations even in the absence of gestational diabetes. Several population-based studies have reported the likelihood of structural abnormalities of the offspring of obese mothers, such as neural tube defects, congenital heart defects, anorectal atresia, hydrocephaly, hypospadias and limb reduction defects [17][18][19][20][21][22] .

Although considerable technical advances in obstetrical ultrasonography have been achieved

over the last 3 decades, ultrasound imaging of obese patients remains challenging due to adverse effects of obesity on propagating sound waves. This review tabulates the available data on these conditions regarding imaging options in obese pregnant women and clinical Obstetrical ultrasound and obesity importance for the detection of fetal abnormalities to provide a framework for a proper parental counseling.

Quantification of obesity

For the estimation of the degree of fat accumulation, assessment of the body mass index (BMIcalculated as weight in kilograms divided by height in meters squared) has been established as the principal standard method to diagnose overweight and obesity. By definition the World Health Organization (WHO) and the National Institutes of Health (NIH) both define normal weight comprising a BMI of 18.5-24.9, overweight as a BMI of 25-29.9, and obesity as a BMI of 30 or greater. Obesity is further categorized by BMI into Class I (30-34.9), Class II (35-39.9), and

Class III or morbid obesity (≥ 40) 2,23 . In pregnancy, BMI is calculated using pre-pregnant weight or the weight measured during the initial visit at the prenatal care provider. Due to the fact that BMI is an indirect measure reflecting the overall fatness without distinguishing between fat and fat-free components it is not as useful in predicting the difficulties encountered with ultrasound visualization and putative obesity-related risks during advancing pregnancy. In the past few years, a number of studies have called attention to the importance of abdominal obesity and its measuring modalities. A strong relation between increase in abdominal girth and cardiovascular disease among adults has recently been demonstrated 24 . Other publications stressed the association of abdominal obesity and poor respiratory function or the increased risk of chronic kidney disease in the general population 25,26 . However, from an obstetric perspective Yamamoto et al. in 2001 were the first who reported a higher waist-to-hip ratio (WHR) prior to 9 gestational weeks to be significantly linked to an increased risk for pre-eclampsia 27 . Similar findings were published by Sattar et al., who found a significant correlation of increased waistcircumference prior to 16 weeks' gestation and pregnancy-induced hypertension (Odds Ratio -OR 1.8, 95% confidence intervall -CI 1.1, 2.9) and pre-eclampsia (OR 2.7, 95% CI 1.1, 6.8) 28 . In a prior series an impact of maternal WHR on elevated fetal growth was established 29 . Both waistto-hip ratio (WHR) and waist circumference (WC) have been additionally used as proxy Obstetrical ultrasound and obesity measures for body fat distribution when investigating health concerns evolving from (maternal) obesity [30][31][32] . Bartha and colleagues introduced an ultrasonographic measurement of maternal visceral fat thickness (VFT) during early pregnancy and were able to demonstrate a better correlation of the VFT estimate compared to BMI with metabolic and cardiovascular risk factors such as hyperinsulinaemia, insulin resistance, high blood pressure or dyslipidaemia in pregnancy 33 .

Obstetrical ultrasound

Pre-examination counseling of the obese gravida has to point out the likely impact of adiposity on image clarity and diagnostic accuracy 34 . This should be communicated to the patient in a sensitive but appropriate way, because it allows earlier abandonment of a technically difficult study and enables to set realistic expectations regarding the scan 35 . It seems reasonable to claim an informed consent signed by the gravida in advance of the anatomic survey. Furthermore, the first prenatal visit should focus on dating the pregnancy and confirming viability of the fetus. In fact, obese women are more likely to have anovulatory or irregular cycles, so that the utility of determining the last menstrual period for establishing gestational age may be limited [START_REF] Phillips | For the obese gravida, try strong counselling and close follow-up[END_REF] . To improve the accuracy of pregnancy-dating during the early first trimester, transvaginal assessment of the crown-rump-length should be performed.

Image clarity

In addition to the arithmetic indices, measuring the distance from skin surface to the intrauterine region of interest (e.g. key fetal structures) allows simple documentation of the fat layer, thereby conveying the grade of image clarity impairment (figure 1) 35 . Excess of abdominal (subcutaneous or intraabdominal) fat results in an increased number of interfaces and consecutively in marked attenuation of the signal. Attenuation encompasses absorption, reflection, reverberation and scatter [START_REF] Davidoff | Maternal umbilicus: ultrasound window to the gravid uterus[END_REF] . The overall visualization of fetal organs with respect to Obstetrical ultrasound and obesity increasing maternal size has been previously addressed by several studies [START_REF] Zador | Nomograms for ultrasound visualization of fetal organs[END_REF][START_REF] Wolfe | Trends in sonographic fetal organ visualization[END_REF] . Reduction in successful image generation was most marked for cardiac and cerebrospinal structures as well as the umbilical cord [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF][START_REF] Hendler | The impact of maternal obesity on midtrimester sonographic visualization of fetal cardiac and craniospinal structures[END_REF] . Catanzarite et al. postulated five categories of potential barriers to complete fetal anatomic survey. In addition to maternal body habitus, other confounding variables such as gestational age, fetal spine-up position, resolution/penetration of ultrasound equipment and sonographer skills evidently exert influence on image clarity. The authors also described a strong relation of scanning duration and completion of the anatomical survey in the non-obese population. For each 5-minute time increment up to 30 minutes, the rate of complete morphological assessment improved in their study [START_REF] Catanzarite | Targeted mid-trimester ultrasound examination: how does fetal anatomic visualization depend upon the duration of the scan?[END_REF] .

The impact of sonographer's experience on the rate of suboptimal visualization in the obese gravida is obvious and was previously reported [START_REF] Hendler | Does sonographer's experience impact the rate of suboptimal visualization in the obese gravida [abstract]?[END_REF]44 . Rates of completed anatomic surveys rise with advancing gestational age. The preferred timing of midtrimester ultrasound examination of the obese gravida appears to be between 18-20 weeks' gestation in order to achieve maximum efficiency with respect to the potential duration of the scan and need for repeated scans 45,46 . This is slightly different to the findings of Wolfe et al. who stated an optimal overall organ visualization at 21-23 weeks for a mean maternal BMI of 27.3 of the women enrolled in their study [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF] .

Hendler et al. described an inverse relationship between the severity of maternal obesity and the ability to adequately visualize the fetal heart (37.3 % obese vs. 18.7 % non-obese, p < 0.001) and craniospinal structures (42.8 % obese vs. 29.5 % non-obese, p < 0.001). They found a degradation in image quality by 10 % for every further step in obesity classification [START_REF] Hendler | The impact of maternal obesity on midtrimester sonographic visualization of fetal cardiac and craniospinal structures[END_REF] .

Wolfe et al reported a 14.5 % reduction in visualization rates in the markedly obese patient [START_REF] Wolfe | Maternal obesity: a potential source of error in sonographic prenatal diagnosis[END_REF] .

Similar observations were recently published with respect to suboptimal visualization of facial soft tissue (39.1 % obese vs. 19.3 % non-obese, p < 0.001) and abdominal wall (2.7 % obese vs. 0 % non-obese, p < 0.001) 47 . Series assessing the potential impact of maternal obesity 48 on optimal visualization and completion of anatomic survey 49 are summarized in table 1. Obstetrical ultrasound and obesity Due to this poor transmission of ultrasound waves in adipose tissue there were several attempts to optimize in image quality. A transvaginal approach is beneficial for assessment of fetal structures close to the lower uterine segment and therefore mainly limited to ultrasound examinations throughout the first trimester. Measurement of fetal nuchal translucency between 11-13+6 weeks most often performed transabdominally as this allows a wider range of scanning angles, may substantially be hampered by increasing maternal size 50,51 . In the obese patient therefore, a transvaginal assessment to facilitate a better resolution of the skin line, perispinal tissue or amniotic sheet as separate structures, should be considered 35 . This approach enables proper assessment of fetal limbs and extremities and is feasible to perform early fetal echocardiography as well. Recently, it has been postulated that most of the anomalies detectable during standard 18-week scan can be seen at 12 to 13 weeks with appropriate imaging even in obese women 52 . However, this has been challenged by other authors, which concordantly emphasize that a number of anomalies are not amenable to first trimester detection (regardless recent promising findings, such as intracranial translucency) [53][54][55] . Further studies are needed to systematically investigate the diagnostic capability of a first trimester anatomic sonogram and to establish reliable standards taking into account increased maternal size and limited acoustic window 56 .

Beyond 14-15 weeks' gestation ultrasonic scans are preferentially performed by transabdominal imaging, thereby utilizing appropriate anatomic regions (e. g. lower transverse abdominal crease). Morbidly obese women often have an abnormally lowered, ptotic apron. Elevating and retracting the fatty apron (panniculus) towards the patient's head enables optimized access to the fetal areas of interest by placing the probe near the arcus tendineus superior to the pubis 35,[START_REF] Phillips | For the obese gravida, try strong counselling and close follow-up[END_REF] . This is of particular importance with regard to diagnostic procedures such as chorionic villous sampling (CVS), amniocentesis (AC) or cordocentesis (CS). In later gestation it may also be helpful to get access to the gravid uterus from a subcostal approach with the women in a lateral position which shifts the abdomen towards the examination table. In general, the higher the Obstetrical ultrasound and obesity degree of maternal obesity, the higher will be the pressure exerted on the abdominal wall to reduce the depth of insonation thereby trying to achieve an acceptable acoustic window.

Alternative approaches

In obese patients, in whom a successful fetal anatomic survey has apparently failed, the maternal umbilicus, the thinnest section of the abdominal wall potentially affords improved image workers established a transumbilical use of the endovaginal probe in the obese gravida 57,58 .

Placement of the transvaginal transducer in the umbilicus resulted in improved resolution and satisfactory fetal cardiac survey in 95 % and 87 % respectively. The authors resumed, that transumbilical use of the transvaginal probe is a beneficial, well-tolerated technique, which clearly improves gray-scale imaging. In addition, color and pulsed Doppler interrogation of fetal vessels may also be optimized. Similar observations were made by Paladini, who assumed that improved cardiac visualization (with the fetus in breech presentation) may be achieved when the scan is performed with filled maternal bladder pushing the uterus cephalad, allowing the sonographer to explore the heart via the periumbilical region 59 .

On the contrary, a transrectal approach has been undertaken in those patients undergoing assisted reproduction where difficult embryo transfer was anticipated and transabdominal ultrasound guidance was hampered by increased BMI 60 . However, these procedures have not been regularly implemented in routine obstetrical ultrasound practice.

Tissue harmonic imaging

Tissue harmonic imaging (THI), nowadays commonly implemented into commercially available ultrasound systems, constitutes a real-time imaging technique that relies on the detection of socalled harmonics created by non-linear propagation of the fundamental ultrasonic beam through Obstetrical ultrasound and obesity tissue 61 . The generation of harmonics by tissue itself increases with depth up to a point where attenuation causes them to decrease. Modern ultrasound transducers are able to isolate the second harmonic frequency in the detected echo, enabling image rendering of harmonic reflection. This relatively novel method of echo processing is useful while scanning technically difficult patients to improve image quality and confidence of diagnosis 62,63 . Treadwell and colleagues found that tissue harmonic imaging was able to improve resolution of at least one fetal structure in more than 50 % of patients enrolled in their study 64 . Whether the use of THI may result in improved detection of fetal abnormalities this study was not able to confirm, because the included patients had normal fetuses. Nevertheless, the advantages of THI in fetal cardiac examination were recently addressed by three studies [65][66][67] . The differences in image clarity obtained by using THI in a morbidly obese gravida compared to inconclusive images depicted without technical adjuncts are illustrated in figure 2. Other technical advances facilitating improved ultrasound assessment of fetal morphology in obese mothers include preand postprocessing techniques such as compound imaging, speckle reduction filters and multi-Hertz transducer technology.

Other imaging modalities

In recent years, three-and four-dimensional ultrasound applications have become clinically valuable in obstetrics as well as in gynecology. Comparative studies addressing the beneficial value of 3D ultrasound are contradictory. In a review of 11 studies comparing conventional 2D imaging and 3D ultrasound for the diagnosis of facial anomalies, seven studies reported additional information using 3D while four found similar findings achieved by these two modalities 68 . Many of the studies on the accuracy of 3D ultrasonography in prenatal diagnosis are biased by the availability of information from the initial 2D scan. Nevertheless, a previous study suggests three-dimensional ultrasound as being capable of improving visualization of fetal anatomy even in fetuses in anterior spine position 69 . In spite of the apparent advantages of 3D obstetrical imaging, non-favourable scanning conditions, such as oligohydramnios, severe Obstetrical ultrasound and obesity obesity and the absence of tissue borderlines, cause the same problems in 3D as in 2D scanning so far.

Although ultrasound is the primary imaging modality for the evaluation of the fetus, because of proven utility, relatively low cost and widespread availability, fetal magnetic resonance imaging (MRI) has grown in popularity over the past two decades as a complementary tool for antenatal assessment of fetal abnormalities [START_REF] Gonçalves | What does 2-dimensional imaging add to 3-and 4dimensional obstetric ultrasonography?[END_REF][START_REF] Wang | Imaging comparison of basic cardiac views between two-and three-dimensional ultrasound in normal fetuses in anterior spine positions[END_REF] . MRI has been useful in confirming abnormalities seen on ultrasound scan or determining the underlying cause of nonspecific sonographic anomalies and may add incremental information that might have influence on prognosis or management at birth [START_REF] Behairy | Magnetic resonance imaging in fetal anomalies: What does it add to 3D and 4D US?[END_REF][START_REF] Frates | Fetal anomalies: comparison of MR imaging and US for diagnosis[END_REF][START_REF] Whitby | Ultrafast magnetic resonance imaging of central nervous system abnormalities in utero in the second and third trimester of pregnancy: comparison with ultrasound[END_REF] . Faster scanning techniques allow studies to be performed without sedation in the second and third trimester with minimal motion artefacts [START_REF] Hubbard | Ultrafast fetal MRI and prenatal diagnosis[END_REF] . Moreover, MRI is not hampered by maternal obesity, fetal position, overlying bones or oligohydramnios, so that fetal MRI has emerged as a clinically valuable diagnostic supplement to ultrasound in case of inconclusive findings or degraded image.

Detection of malformations

Infants of obese parturients are reported to be at elevated risk for congenital malformations (11.1 %) compared with those of mothers of average prepregnancy weight (7.9 %). Queisser-Luft et al. reported significant odds for major malformations (OR 1.3, 95 % CI 1.0-1.7) [START_REF] Queisser-Luft | Malformations in newborn: results based on 30.940 infants and fetuses from the Mainz congenital birth defect monitoring system (1990-1998)[END_REF] . Similar findings were recently published by two meta-analyses in which the authors systematically assessed the attributable risk for anomalies in the offspring of obese mothers 21,22 Obstetrical ultrasound and obesity been described. On the other hand, the relative risk for gastroschisis among obese mothers was significantly lower (OR 0.17, 95 % CI 0.10-0.30) compared with women of recommended BMI [START_REF] Siega-Riz | National Birth Defects Prevention Study. The joint effects of maternal prepregnancy body mass index and age on the risk of gastroschisis[END_REF] .

An opposite effect has been found for offspring with omphalocele, with increased odds (OR 1.63, 95 % CI 1.01-2.47) when the mother was classified as obese. These data emphasize the superior importance of detailed sonographic examination of fetuses of obese pregnant women 78,79 .

According to the findings of the FaSTER (First and Second Trimester Evaluation of Risk) trial in an unselected obstetric population, it has been stated that maternal obesity significantly decreased the likelihood of sonographic detection of common anomalies (adjusted OR 0.7, 95 % CI 0.6-0.9) 80 . In a recent paper Dashe et al. assessed the impact of maternal body habitus on the detection of major structural abnormalities during second-trimester standard and targeted sonographic scan 81 . Detection of anomalous fetuses with standard ultrasound decreased substantially from 66 % in women having a normal BMI to only 25 % in morbidly obese women.

In high risk pregnancies receiving targeted scans detection of malformations ranged from 83 % (lean patients) to 67 % (class III obesity). Within the targeted group the detection rate was significantly lower among women with pre-gestational diabetes than in women with other highrisk indications. These data are consistent with previous findings. In order to facilitate proper counseling, the residual risk of an undetected anomaly was calculated to be 0.4 % among women of normal BMI compared to 1.0 % in obese gravida (p < 0.001). However the authors did not address the issue whether follow up ultrasonography could have improved anomaly detection in obese women. Hendler et al. noted that 64 % of their included study population, who were scheduled for an additional fetal heart examination due to the initial inability to complete morphology assessment of the fetus, were obese 82 . The rate of persistent suboptimal visualization of cardiac structures even after recalled exam increased in a BMI-dependent manner from 1.5 % (non-obese) up to 20 % in morbidly obese women (p < 0.001). In conclusion the authors stated that the rate of initially inadaequate image clarity could be reduced by at least 80 % by repeating sonographic scans, thereby improving the prenatal diagnosis of congenital heart defects in an obstetric setting. In accordance to these observations, which are similar to Obstetrical ultrasound and obesity previous reports, maternal obesity limits the likelihood of adequate ultrasound visualization even when advanced ultrasound systems for assessing fetal structures are used 83 .

Summary

Given the continuing rise in prevalence of overall obesity, and in particular maternal obesity with impact on ultrasound imaging of fetal anatomy, obstetricians have to face new challenges in the antenatal and peripartal management of complications during pregnancy, labor, delivery and beyond. Obtaining adequate sonographic images in obese patients is of particular concern because of the increased rate of congenital anomalies. Considering the findings of sensitivity studies on mixed populations or obese gravid patients, it is reasonable that the anomaly scan at 20 weeks' gestation should be left to experienced sonographers. Moreover, obese mothers will benefit from repeated ultrasonic scans.

The main determinants of signal intensity and consecutive image clarity remain the depth of the part to be depicted as well as the specific tissue characteristics. Thus, future additions to the imaging efforts should include optimized signal processing, further advances in transducer technology or the adjunctive use of complementary image modalities such as fetal MRI to resolve associated shortcomings of obesity in obstetric practice.

An appropriate counseling prior to the commencement of the sonographic exam of overweight and obese patients allowing for the limitations of the study is advisable. The greater potential for delayed or missed diagnoses in obese patients constitutes one of the major medicolegal issues in obstetric care.

F

  Obstetrical ultrasound and obesity obesity and the absence of tissue borderlines, cause the same problems in 3D as in 2D scanning so far.

  Obstetrical ultrasound and obesity 36. Phillips J, Henderson J. For the obese gravida, try strong counselling and close follow-up. OBG Management 2009;21:42. 37. Davidoff A, Reuter K, Karellas A, et al. Maternal umbilicus: ultrasound window to the gravid uterus. J Clin Ultrasound 1994;22:263. 38. Zador IE, Bottoms SF, Tse GM, et al. Nomograms for ultrasound visualization of fetal organs. J Ultrasound Med 1988;7:197. 39. Wolfe HM, Zador IE, Bottoms SF, et al. Trends in sonographic fetal organ visualization. Ultrasound Obstet Gynecol 1993;3:97.40. Wolfe HM, Sokol RJ, Martier SM, et al. Maternal obesity: a potential source of error in sonographic prenatal diagnosis. Obstet Gynecol 1990;76:339. 41. Hendler I, Blackwell SC, Bujold E, et al. The impact of maternal obesity on midtrimester sonographic visualization of fetal cardiac and craniospinal structures. Int J Obes Relat Metab Disord 2004;28:1607. 42. Catanzarite V, Delaney K, Wolfe S, et al. Targeted mid-trimester ultrasound examination: how does fetal anatomic visualization depend upon the duration of the scan? Ultrasound Obstet Gynecol 2005;26:521. 43. Hendler I, Blackwell SC, Treadwell MC, et al. Does sonographer's experience impact the rate of suboptimal visualization in the obese gravida [abstract]? Am J Obstet Gynecol 2004;189:S239.

  Obstetrical ultrasound and obesity 70. Gonçalves LF, Nien JK, Espinoza J, et al. What does 2-dimensional imaging add to 3-and 4dimensional obstetric ultrasonography? J Ultrasound Med 2006;25:691. 71. Wang PH, Chen GD, Lin LY. Imaging comparison of basic cardiac views between two-and three-dimensional ultrasound in normal fetuses in anterior spine positions. Int J Cardiovasc Imaging 2002;18:17. 72. Behairy NH, Talaat S, Saleem SN, et al. Magnetic resonance imaging in fetal anomalies: What does it add to 3D and 4D US? Eur J Radiol 2010;74:250. 73. Frates MC, Kumar AJ, Benson CB, et al. Fetal anomalies: comparison of MR imaging and US for diagnosis. Radiology 2004;232:398. 74. Whitby E, Paley MN, Davies N, et al. Ultrafast magnetic resonance imaging of central nervous system abnormalities in utero in the second and third trimester of pregnancy: comparison with ultrasound. BJOG 2001;108:519. 75. Hubbard AM. Ultrafast fetal MRI and prenatal diagnosis. Semin Pediatr Surg 2003;12:143. 76. Queisser-Luft A, Stolz G, Wiesel A, et al. Malformations in newborn: results based on 30.940 infants and fetuses from the Mainz congenital birth defect monitoring system (1990-1998). Arch Gynecol Obstet 2002;266:163. 77. Siega-Riz AM, Herring AH, Olshan AF, et al. National Birth Defects Prevention Study. The joint effects of maternal prepregnancy body mass index and age on the risk of gastroschisis. Paediatr Perinat Epidemiol 2009;23:51.

FIGURE 1 .FIGURE 2 :

 12 FIGURE 1. Documentation of the depth of insonation in a lean (BMI 21.8 kg/m2) pregnant woman (A), compared to a gravida with morbid obesity (BMI > 40 kg/m2) at 22 weeks of gestation. 180x91mm (150 x 150 DPI)

  resolution. A previous series by Davidoff et al. revealed an optimized image clarity in most of the 68 included women, but the relatively large curvilinear transducer may have limited the ultrasonic sector view 37 . Based on these findings Rosenberg et al. and later McCoy and co-

  are summarized in table 1.

  . Based on these pooled data, obese women are at significantly increased odds of a pregnancy affected by a neural tube defect (OR 1.87, 95 % CI 1.62-2.15). The statistically strongest correlation was found for

	F o r
	P
	e
	e r
	R
	e
	v i e
	w
	spina bifida (OR 2.24, 95 % CI 1.86-2.69). Moreover, an association of maternal adiposity and
	cardiovascular anomalies (OR 1.30, 95 % CI 1.12-1.51) with significant odds for septal anomalies
	(OR 1.20, 95 % CI 1.09-1.31); orofacial clefts, e.g. cleft palate (OR 1.23, 95 % CI 1.03-1.47) or cleft
	lip and palate (OR 1.20, 95 % CI 1.03-1.40); anorectal atresia (OR 1.48, 95 % CI 1.12-1.97);
	hydrocephaly (OR 1.68, 95 % CI 1.19-2.36) and limb reduction (OR 1.34, 95 % CI 1.03-1.73) has

TABLE 1 .

 1 Published studies investigating the deleterious impact of maternal obesity on optimal visualization and completion of anatomic survey according to BMI classification. SUV, suboptimal ultrasound visualization.

	Non-obese	Obese	p-value

John Wiley & SonsJournal of Clinical Ultrasound


Salvatore Greco

Riccardo Centenaro

Giuseppe Lavecchia

Francesco Rossi

Keywords: Sonographic appearance ultrasound, submandibular glands, iodide mumps

teaching and research institutions in France or abroad, or from public or private research centers.

Discussion

Swelling of the submandibular, sublingual, and parotid is an uncommon complication associated with intravascular administration of contrast agents. This reaction was called "iodide mumps" by Sussman and Miller [1] in 1956, although only few cases had been reported [2,3]. Iodide mumps is syndrome due to excessive intake or injection of iodine and iodine-containing compounds. This is known as iodism and includes inflammatory swelling of the salivary glands, coryza, skin erythema, facial nerve paralysis and other more severe systemic reactions [4].

To our knowledge, this is a rare case of description of sonographic appearance of iodide mumps: enlarged and hyperechoic parenchimal pattern with prominent ducts and hypervascularity of glands are expression of bilateral submandibular swelling.

The cause remains unclear but the reaction seems to be related to toxic accumulation of iodide in the ductal system of the salivary glands. Indeed we know that about 98% of injected iodide is eliminated by the kidneys and only 2% is excreted from other organs, such as salivary, sweat and lacrimal glands. Salivary gland swelling is caused in part by the ability of these glands to store high levels of inorganic iodide, with subsequent inflammatory phenomenon of the glands [5].

The onset of signs and symptoms varies from within a few minutes to up to 5 days after contrast agent administration. The prognosis of iodide mumps is relatively benign.

Current treatment for iodide mumps is supportive therapy and administration of antiinflammatory agents [6]. For patients who do not respond use of hemodialysis to reduce blood levels of contrast agent and iodide may be necessary [2,7]. We performed [ultrasound of the neck] high-resolution sonography of the submandibular space with 7-13 MHz linear probe of Aloka α10. The ultrasound findings were diffuse bilateral swelling of submandibular glands and internal low echoic thick septa that most likely represent prominent ducts (Figure 1). Approximately 48 h after contrast agent administration, after short cycle of oral prednisone, sonography of the submandibular space showed well-capsulated glandular structure with uniform homogeneus parenchimal echopattern and no significant increase of vascular flow [the swelling of his submandibolar glands progressively decreased towards normal aspect].

Discussion

Swelling of the submandibular, sublingual, and parotid is an uncommon complication associated with intravascular administration of contrast agents. This reaction was called "iodide mumps" by Sussman and Miller [1] in 1956, although only few cases had been reported [2,3]. Iodide mumps is syndrome due to excessive intake or injection of iodine and iodine-containing compounds. This is known as iodism and includes inflammatory swelling of the salivary glands, coryza, skin erythema, facial nerve paralysis and other more severe systemic reactions [4].

To our knowledge, this is a rare case of description of sonographic appearance of iodide mumps: enlarged and hyperechoic parenchimal pattern with prominent ducts and hypervascularity of glands are expression of bilateral submandibular swelling.

The cause remains unclear but the reaction seems to be related to toxic accumulation of iodide in the ductal system of the salivary glands. Indeed we know that about 98% of injected iodide is eliminated by the kidneys and only 2% is excreted from other organs, such as salivary, sweat and lacrimal glands. Salivary gland swelling is caused in part by the ability of these glands to store high levels of inorganic iodide, with subsequent inflammatory phenomenon of the glands [5]. The onset of signs and symptoms varies from within a few minutes to up to 5 days after contrast agent administration. The prognosis of iodide mumps is relatively benign.

Current treatment for iodide mumps is supportive therapy and administration of antiinflammatory agents [6]. For patients who do not respond use of hemodialysis to reduce blood levels of contrast agent and iodide may be necessary [2,7].

Although iodide mumps is a rare late adverse reaction to the intravascular administration of iodine containing contrast material, ultrasound findings may be worthwhile to recognize this entity.

Figure 1 2 Axial

 12 Figure 1

  [Colour] Power Doppler sonography [ultrasound] used to examine tissue blood flow showed vascular flow, particularly in middle part of submandibular glands (Figure2). Thyroid and parotid glands were normal.

Figure 1 Figure 2 Figure 1 Figure 2

 1212 Figure 1

John Wiley & SonsJournal of Clinical Ultrasound

John Wiley & Sons

Journal of Clinical Ultrasound


Roxana C Sisu

Guido Lanzillo

Diana C Benea

Gheorghe Cerin

Dragos Vinereanu

A rare association

Keywords: papillary fibroelastoma, myxomatous disease, echocardiography, transesophageal, two avi videos

come

Introduction

Primary cardiac tumours are extremely rare, with an incidence of 0.28% in the necropsy series. Papillary fibroelastomas (PFEs) are the third most frequent benign tumours of the heart (8-10%), after myxoma and lipoma 1 . There are small tumours, with range in diameter from 0.2 to 7 cm 2,3 . A comprehensive analysis of 725 cases showed that valvular endocardium was the predominant location of tumour 3 . The most commonly involved valve is the aortic valve (30%), followed by the mitral valve (20-25%) 3,4,5 . Highest prevalence is in the 8 th decade of life. Males comprise 55% of patients 3 .

No clear risk factor for development of PFE has been reported. Some PFEs are congenital, but most lesions are probably acquired 6 .

Most often diagnosed incidentally, PFEs may embolize, mainly to the cerebral circulation. Clinically, PFEs were associated with transient ischemic attack, stroke, myocardial infarction, sudden death, peripheral embolism and blindness, syncope, pulmonary embolism, and heart failure 3,6,7 . Because of their infrequent occurrence, an appropriate management strategy has been difficult to define. An intraoperative transesophageal echocardiography (TEE), done just before the cardiopulmonary bypass, confirmed the presence, severity, and the mechanism of mitral regurgitation described by TTE (Video1), but also revealed a small, round shape, "phantomathic" image (7x7 mm), with an echo lucent centre, that appeared only in diastole, involving the atrial side of the anterior mitral valve leaflet (A1) (Video2). This image was considered to be either a bulge of the myxomatous anterior leaflet, or a tumoral tissue (Figure 1). We could not exclude completely a vegetant mass suggestive for endocarditis. A commercially available sytem was used (Vingmed Vivid 7, and Vivid i, General Electric). Data were obtained using a 3,5-Mhz transducer, and a multiplane transesophageal probe 6T-RS (2.2-8 Mhz).

Left atriotomy and visual exploration of the mitral valve revealed a small translucide tumoral mass on the atrial side of A1 scallop (Figure 2). Surgical procedure consisted of complete resection of the tumoral mass and partial resection of A1 scallop, associated with mitral annuloplasty with complete ring, and three Gore-Tex chordae on the P1, P2, and P3 scallops and both mitral commissures. Intra operative TEE after cardiopulmonary bypass showed a competent valve repair, with minimal residual regurgitation of the level of A1 scallop. Histopatological exam of the tumour revealed benign papillary fibroelastoma. Patient had an uneventful postoperative recovery and was discharged on the 8 th postoperative day. Warfarin was recommended for 3 months.

Discussion

We reported a rare case of myxomatous mitral valve disease with severe regurgitation, associated with fibroelastoma. PFEs are rare, benign tumours. The incidence is not clear because most patients are asymptomatic. They usually occur in elderly patients (>65 years), and are seen rarely in children 5,8 . PFEs have a valvular predilection, and the mitral valve is the second common location. When the mitral valve is involved, the tumour is most often on the atrial mid portion side of the valve, away from the free edge or the annulus 5 . Particularly, in our patient, we found an uncommon location, on the A1 scallop of the anterior mitral leaflet, closely related to the antero-lateral commissure. PFEs are mostly associated with rheumatic and atherosclerotic lesions, such as fibrosis and calcifications 8 . They also have been described in association with congenital diseases, and hypertrophic obstructive cardiomyopathy. A possible role of radiotherapy or cytomegalic virus infection was described 6,9 .

The chronic trauma of the endocardium appears the most important mechanism in the pathogenesis of PFE 4 . In our case, we speculate that long-standing mitral disease, with turbulent blood flow and mechanical trauma, might be the mechanism for tumour development.

There are no cases reported in which PFEs was considered responsible for valvular dysfunction 4 . Similarly, in our patient, mitral regurgitation was produced by mitral valve prolaps, tumour having no implication.

For their diagnosis TEE has an important role. This is the most reliable and less invasive method of establishing the presence of the tumours. Even so, the TEE may fail to diagnose, because the tumours might be masked by an associated lesion, and have no significant characteristics in order to be differentiated from the degenerative valves or vegetant lesions. In our case, we were unaware of the existence of the tumour until intraoperative TEE was performed.

The echocardiographic image was suggestive for tumoral tissue rather then vegetation. Our patient also did not have any signs of infective endocarditis. This information is critical to the surgeon in planning the operative procedure and the preoperative management.

PFEs are soft and friable, often with adherent thrombus, which explains their propensity to embolize. Tumoral resection should proceed on an emergency basis, because of the potential to embolizate 10 . An aggressive manipulation may result in fragmentation and further embolism 4,5,10 . There are no cases reported of local After operation, it is common practice to put patients on warfarin. However, there are no evidence-based recommendations regarding efficacy and duration of anticoagulation therapy for patients with PFE resection 4,5 .

In conclusion, we have reported a very rare association of PFE and myxomatous mitral valve disease with severe mitral regurgitation. To the best of our knowledge there are no other similar cases reported about this association. We speculate that long-standing mitral disease with turbulent blood flow and mechanical trauma might be the main mechanism for tumour development. We suggest that a preoperative transesophageal echocardiography should be done in order to exclude any associated lesions that might change preoperative management, timing and type of surgical procedure. After the tumoral excision, a 3-month warfarin therapy should be recommended.

Figure 2 legend

Intraoperatory exploration of the mitral valve showed a 10x10 mm translucide yellow tumoral mass on the atrial side of the A1 scallop (arrow), with a large base of implantation.

Video 1 legend

The lower esophageal window at 0º showed severe mitral regurgitation. Color flow Doppler demonstrated two separate jets: a central jet resulting from annular dilation and an anterior directed mitral regurgitant jet generated from posterior mitral valve.

Video 2 legend

The lower esophageal window at 0º revealed bileaflet thickening and prolaps of mitral valve. A round shape image attached to the atrial side of the A1 scallop of mitral valve appeared only in diastole.

Introduction

Primary cardiac tumours are extremely rare, with an incidence of 0.28% in the necropsy series. Papillary fibroelastomas (PFEs) are the third most frequent benign tumours of the heart (8-10%), after myxoma and lipoma 1 . There are small tumours, with range in diameter from 0.2 to 7 cm 2,3 . A comprehensive analysis of 725 cases showed that valvular endocardium was the predominant location of tumour 3 . The most commonly involved valve is the aortic valve (30%), followed by the mitral valve (20-25%) 3,4,5 . Highest prevalence is in the 8 th decade of life. Males comprise 55% of patients 3 .

No clear risk factor for development of PFE has been reported. Some PFEs are congenital, but most lesions are probably acquired 6 .

Most often diagnosed incidentally, PFEs may embolize, mainly to the cerebral circulation. Clinically, PFEs were associated with transient ischemic attack, stroke, myocardial infarction, sudden death, peripheral embolism and blindness, syncope, pulmonary embolism, and heart failure 3,6,7 . Because of their infrequent occurrence, an appropriate management strategy has been difficult to define.

Discussion

We reported a rare case of myxomatous mitral valve disease with severe regurgitation, associated with fibroelastoma. PFEs are rare, benign tumours. The incidence is not clear because most patients are asymptomatic. They usually occur in elderly patients (>65 years), and are seen rarely in children 5,8 . PFEs have a valvular predilection, and the mitral valve is the second common location. When the mitral valve is involved, the tumour is most often on the atrial mid portion side of the valve, away from the free edge or the annulus 5 . Particularly, in our patient, we found an uncommon location, on the A1 scallop of the anterior mitral leaflet, closely related to the antero-lateral commissure.

PFEs are mostly associated with rheumatic and atherosclerotic lesions, such as fibrosis and calcifications 8 . They also have been described in association with congenital diseases, and hypertrophic obstructive cardiomyopathy. A possible role of radiotherapy or cytomegalic virus infection was described 6,9 .

The chronic trauma of the endocardium appears the most important mechanism in the pathogenesis of PFE 4 . In our case, we speculate that long-standing mitral disease, with turbulent blood flow and mechanical trauma, might be the mechanism for tumour development.

There are no cases reported in which PFEs was considered responsible for valvular dysfunction 4 . Similarly, in our patient, mitral regurgitation was produced by mitral valve prolaps, tumour having no implication.

For their diagnosis TEE has an important role. This is the most reliable and less invasive method of establishing the presence of the tumours. Even so, the TEE may fail to diagnose, because the tumours might be masked by an associated lesion, and have no significant characteristics in order to be differentiated from the degenerative valves or vegetant lesions. In our case, we were unaware of the existence of the tumour until intraoperative TEE was performed.

The echocardiographic image was suggestive for tumoral tissue rather then vegetation. Our patient also did not have any signs of infective endocarditis. This information is critical to the surgeon in planning the operative procedure and the preoperative management.

PFEs are soft and friable, often with adherent thrombus, which explains their propensity to embolize. Tumoral resection should proceed on an emergency basis, because of the potential to embolizate 10 . An aggressive manipulation may result in fragmentation and further embolism 4,5,10 . There are no cases reported of local recurrence after the complete resection. Long term postoperative prognosis is excellent 3 .

After operation, it is common practice to put patients on warfarin. However, there are no evidence-based recommendations regarding efficacy and duration of anticoagulation therapy for patients with PFE resection 4,5 .

In conclusion, we have reported a very rare association of PFE and myxomatous mitral valve disease with severe mitral regurgitation. To the best of our knowledge there are no other similar cases reported about this association. We speculate that long-standing mitral disease with turbulent blood flow and mechanical trauma might be the main mechanism for tumour development. We suggest that a preoperative transesophageal echocardiography should be done in order to exclude any associated lesions that might change preoperative management, timing and type of surgical procedure. After the tumoral excision, a 3-month warfarin therapy should be recommended.

Video 1 legend

The lower esophageal window at 0º showed severe mitral regurgitation. Color flow Doppler demonstrated two separate jets: a central jet resulting from annular dilation and an anterior directed mitral regurgitant jet generated from posterior mitral valve.

Video 2 legend

The lower esophageal window at 0º revealed bileaflet thickening and prolaps of mitral valve. A round shape image attached to the atrial side of the A1 scallop of mitral valve appeared only in diastole.

  year old man was admitted to the cardio-surgery department for assessment of the opportunity for surgical correction of a previously known mitral regurgitation due to myxomatous disease. Patient was known to have a 10 years history of asymptomatic myxomatous mitral valve disease, with progressive mitral regurgitation. He was followed annually by transthoracic echocardiography (TTE) in order to establish the correct timing for surgical correction. On admission, he presented with class 2 NYHA symptoms. On examination, he had a grade IV/VI pansystolic apical murmur, without signs of congestion. There were no other pathological findings. Laboratory examination was unremarkable. The electrocardiogram displayed normal sinus rhythm. Lung fields and heart size were normal on chest Xray examination. Repeated TTE examination found severe eccentric mitral regurgitation (regurgitant volume of 100 ml), in a myxomatous valve with prolapse of both leaflets, flail of the P2-P3 scallops, and mitral annular dilation. Left ventricle was dilated (EDD of 60 mm, ESD of 41 mm, EDV of 190 ml, and ESV of 90 ml), with normal ejection fraction (of 55%), without signs of elevated filling pressure (E/E´= 10, E/Vp =1.5). There was no pulmonary hypertension, and good right ventricular systolic function (TAPSE of 27 mm, systolic velocity of the tricuspid annulus of 12 cm/s). He was therefore scheduled for mitral valvuloplasty.

  after the complete resection. Long term postoperative prognosis is excellent3 .

Figure 1 legend

 1 Figure 1 legend

  year old man was admitted to the cardio-surgery department for assessment of the opportunity for surgical correction of a previously known mitral regurgitation due to myxomatous disease. Patient was known to have a 10 years history of asymptomatic myxomatous mitral valve disease, with progressive mitral regurgitation. He was followed annually by transthoracic echocardiography (TTE) in order to establish the correct timing for surgical correction. On admission, he presented with class 2 NYHA symptoms. On examination, he had a grade IV/VI pansystolic apical murmur, without signs of congestion. There were no other pathological findings. Laboratory examination was unremarkable. The electrocardiogram displayed normal sinus rhythm. Lung fields and heart size were normal on chest Xray examination. Repeated TTE examination found severe eccentric mitral regurgitation (regurgitant volume of 100 ml), in a myxomatous valve with prolapse of both leaflets, flail of the P2-P3 scallops, and mitral annular dilation. Left ventricle was dilated (EDD of 60 mm, ESD of 41 mm, EDV of 190 ml, and ESV of 90 ml), with normal ejection fraction (of 55%), without signs of elevated filling pressure (E/E´= 10, E/Vp =1.5). There was no pulmonary hypertension, and good right ventricular systolic function (TAPSE of 27 mm, systolic velocity of the tricuspid annulus of 12 cm/s). He was therefore scheduled for mitral valvuloplasty.An intraoperative transesophageal echocardiography (TEE), done just before the cardiopulmonary bypass, confirmed the presence, severity, and the mechanism of mitral regurgitation described by TTE (Video1), but also revealed a small, round shape, "phantomathic" image (7x7 mm), with an echo lucent centre, that appeared only in diastole, involving the atrial side of the anterior mitral valve leaflet (A1) . This image was considered to be either a bulge of the myxomatous anterior leaflet, or a tumoral tissue (Figure1). We could not exclude completely a vegetant mass suggestive for endocarditis. A commercially available sytem was used (Vingmed Vivid 7, and Vivid i, General Electric). Data were obtained using a 3,5-Mhz transducer, and a multiplane transesophageal probe 6T-RS (2.2-8 Mhz) Left atriotomy and visual exploration of the mitral valve revealed a small translucide tumoral mass on the atrial side of A1 scallop (Figure2). Surgical procedure consisted of complete resection of the tumoral mass and partial resection of A1 scallop, associated with mitral annuloplasty with complete ring, and three Gore-Tex chordae on the P1, P2, and P3 scallops and both mitral commissures. Intra operative TEE after cardiopulmonary bypass showed a competent valve repair, with minimal residual regurgitation of the level of A1 scallop. Histopatological exam of the tumour revealed benign papillary fibroelastoma. Patient had an uneventful postoperative recovery and was discharged on the 8 th postoperative day. Warfarin was recommended for 3 months.

Figure 1 legend

 1 Figure 1 legend

Figure 2 legend

 2 Figure 2 legend

Figure 1 Figure 2

 12 Figure 1 TEE showed a round (7x7 mm), mobile tumour attached to the atrial side of the anterior mitral leaflet (A1 scallop). Image is visible only in diastole, as a camber of the anterior leaflet (arrow). 160x106mm (96 x 96 DPI)


Marek Wronski

Maciej Slodkowski

Wlodzimierz Cebulski

Ireneusz Dominika Karkocha

Wojciech Krasnodebski

Keywords: Necrotizing fasciitis -early sonographic diagnosis necrotizing fasciitis, soft tissue infection, ultrasonography, musculoskeletal Necrotizing fasciitis -early sonographic diagnosis necrotizing fasciitis, ultrasonography, soft tissue infection, musculoskeletal Necrotizing fasciitis -early sonographic diagnosis necrotizing fasciitis, ultrasonography, soft tissue infection, musculoskeletal

Introduction

Necrotizing fasciitis (NF) is a life-threatening infection of the soft tissues. It is an uncommon and often rapidly progressive infection of the deep soft structures. Necrotizing fasciitis and may involve any part of the body, but the extremities and perineum are most frequently affected 1 . At its early stages, NF necrotizing fasciitis is difficult to differentiate from common skin infections such as cellulitis and a high index of clinical suspicion is required.

Delay in establishing the correct diagnosis and surgical exploration results in high morbidity and mortality 2 . Clinical recognition of NF is difficult and imaging studies can prove helpful in suggesting early diagnosis. Computed tompgraphy (CT) and magnetic resonance imaging (MRI) are most frequently used diagnostic tools in patients with suspected necrotizing fasciitis 3,4 . Ultrasonography has rarely been used in the recognition of NF necrotizing fasciitis [5][6][7][8] .

We report a case of necrotizing fasciitis affecting the right upper extremity after a venipuncture that was diagnosed early based on sonographic findings. Case report 62-year-old male was admitted to our surgical department because of a gastrointestinal bleeding. His medical history was significant for a recently diagnosed diabetes mellitus. On admission, he was in poor general condition with severe anemia and hypovolemia. Flexible endoscopy revealed a peptic ulcer located in the duodenum. The patient was treated medically with intravenous fluids and omeprazole. He received 4 units of packed red blood cells. A few days later, the patient complained of a small patchy discoloration on the right forearm approximately 5 cm above the venipuncture site. Within the next 24 hours, the skin induration and erythema progressed to involve the whole internal surface of the right forearm and arm and it became extremely painful. The patient was running fever. Crepitus was absent on palpation.

The sonographic examination was performed using a 8-12 MHz linear-array probe (Famio 8, Toshiba, Japan). Ultrasonography showed increased echogenicity of the subcutaneous fatty tissue with interlacing thin anechoic spaces corresponding to perifascial fluid resulting in the cobblestone appearance. There was a gas layer just above the deep fascia with posterior acoustic shadowing (Fig. 1). The subcutaneous emphysema extended a few centimeters beyond the margins of grossly changed skin, but the fatty tissue still appeared normal at that level (Fig. 2). Oblique scans of the upper extremity showed normal muscles without any detectable gas bubbles or fluid collections within the muscular compartments. The sonographic examination suggested the diagnosis of necrotizing fasciitis and therefore the patient underwent urgent surgical exploration. A generous longitudinal incision was made over the affected area. On inspection, the subcutaneous tissue was edematous with discharge of turbid fluid from the cut edges. The perifascial planes had a foamy appearance with crepitations due to gas bubbles. Only a few small necrotic patches were found within the skin and subcutaneous fat and the deep fascia still appeared normal. The tissues were debrided and

Discussion

Necrotizing fasciitis is a progressive and often rapidly spreading infection of the deep soft tissues. This type of infection was originally reported to affect the genital region and is now known as Fournier's gangrene 9 . Subsequently, Meleney found NF necrotizing fasciitis to involve also other body regions 10 . The term of "necrotizing fasciitis" was introduced by Wilson in 1952 11 . Recently, the term of necrotizing soft-tissue infections was proposed to highlight the same treatment strategy in this group of infections 12 .

Necrotizing fasciitis is an infection that spreads along the superficial and deep fascial planes of the soft tissues. The skin and muscles are usually spared at the early stages of the disease.

The speed with which the infection progresses depends on the virulance of the causative pathogen and the severity of immune suppression of the host. Necrotizing fasciitis is a synergistic bacterial infection usually due to a mixed flora. Most frequently cultured pathogens are streptococci. Clostridial infections, although commonly suspected, are rarely responsible 1 . NF necrotizing fasciitis often occurs in patients predisposed to infection because of the underlying chronic disease, especially diabetes mellitus that is a risk factor found in 21-64% of cases 1 . Patients present with severe pain that is often disproportionate to physical findings.

Initially necrotizing fasciitis has an insidious course and its clinical picture may be similar to Necrotizing fasciitis in US 7 based solely on clinical findings is incorrect in 64% cases 13 . Early recognition is essential because any delay in the surgical management results in worse prognosis 2,14 .

Clinical recognition of NF necrotizing fasciitis is difficult and imaging studies can be helpful in suggesting early diagnosis. Radiographic studies are usually used in doubtful cases without obvious signs of NF necrotizing fasciitis such as overt skin necrosis or tissue crepitus.

Radiographic findings in NF necrotizing fasciitis are similar to those found in cellulitis.

Cellulitis begins and spreads in the superficial layers of the subcutaneous tissues. In contrast, NF necrotizing fasciitis involves deeper structures and the inflammatory changes are more severe 15 . The subcutaneous emphysema is a distinguishing sign of NF necrotizing fasciitis, but crepitus is not always present on palpation. Plain x-rays show subcutaneous emphysema when there is a moderate to large amount of gas within the tissues. Although crepitus is found on physical examination in 12-36% of patients with NF necrotizing fasciitis, soft tissue gas is seen on plain x-ray in 17-57% of patients 1 . Tissue emphysema has been generally regarded a late finding in necrotizing fasciitis. Our case illustrates, however, that in some cases tissue gas might appear early in the course of the disease.

CT and MRI are frequently used diagnostic tools in patients with suspected necrotizing fasciitis. The tomographic findings suggesting NF necrotizing fasciitis include asymetric fascial thickening, fluid collections along the deep fascia and soft tissue gas 4 . Although MRI has a high resolution for soft tissues, its value is limited in necrotizing fasciitis, because the patients are often too ill to undergo a timely study. MRI findings such as fluid collections along the deep fascial sheath and thickening of the deep fascia with contrast enhancement suggest necrotizing fasciitis 3 . Nevertheless, both CT and MRI have high sensitivity and low specifity for NF necrotizing fasciitis 3,4,16 .

The sonographic appearance of necrotizing fasciitis has rarely been reported in the literature 6- 8,17 . The ultrasound findings suggesting NF necrotizing fasciitis included thickening of the The sonographic appearance of NF necrotizing fasciitis may be similar to cellulitis. In both conditions, there is swelling and increased echogenicity of the subcutaneous tissue. In more severe cases, the subcutaneous tissue has a so-called cobblestone appearance due to interlaced anechoic spaces within the fatty tissue corresponding to fluid collections dissecting along the perifascial planes. Nevertheless, fluid spaces tracking along the deep fascia strongly suggest the diagnosis of necrotizing fasciitis and are usually not observed in cellulitis 6 .

In necrotizing fasciitis, the inflammatory changes are usually more severe and located in deeper layers than in cellulitis. In our patient, the sonographic diagnosis of necrotizing fasciitis was based on the recognition of soft tissue gas and fluid collections dissecting along the deep fascia. Soft tissue gas is indicative of necrotizing fasciitis and warrants an urgent surgical exploration and debridement. In our patient, the debridement was performed before the development of overt necrosis of the deep fascia. The infection was controlled early and there was no need for any subsequent debridement procedures.

Our case highlights two essential features of necrotizing fasciitis. Firstly, the subcutaneous emphysema may appear early in the course of the disease due to gas-forming bacteria.

Secondly, the inflammation spreads along the deep fascia and extends beyond the margins of apparent skin infection.

In conclusion, ultrasonography is an attractive tool for early recognition of necrotizing fasciitis, especially due to gas-forming bacteria. The subcutaneous emphysema and fluid collections spreading along the deep fascia favor the diagnosis of necrotizing fasciitis. Liberal Computed tompgraphy (CT) and magnetic resonance imaging (MRI) are most frequently used diagnostic tools in patients with suspected necrotizing fasciitis 3,4 . Ultrasonography has rarely been used in the recognition of necrotizing fasciitis [5][6][7][8] .

We report a case of necrotizing fasciitis affecting the right upper extremity after a venipuncture that was diagnosed early based on sonographic findings. Case report 62-year-old male was admitted to our surgical department because of a gastrointestinal bleeding. His medical history was significant for a recently diagnosed diabetes mellitus. On admission, he was in poor general condition with severe anemia and hypovolemia. Flexible endoscopy revealed a peptic ulcer located in the duodenum. The patient was treated medically with intravenous fluids and omeprazole. He received 4 units of packed red blood cells. A few days later, the patient complained of a small patchy discoloration on the right forearm approximately 5 cm above the venipuncture site. Within the next 24 hours, the skin induration and erythema progressed to involve the whole internal surface of the right forearm and arm and it became extremely painful. The patient was running fever. Crepitus was absent on palpation.

The sonographic examination was performed using a 8-12 MHz linear-array probe (Famio 8, Toshiba, Japan). Ultrasonography showed increased echogenicity of the subcutaneous fatty tissue with interlacing thin anechoic spaces corresponding to perifascial fluid resulting in the cobblestone appearance. There was a gas layer just above the deep fascia with posterior acoustic shadowing (Fig. 1). The subcutaneous emphysema extended a few centimeters beyond the margins of grossly changed skin, but the fatty tissue still appeared normal at that level (Fig. 2). Oblique scans of the upper extremity showed normal muscles without any detectable gas bubbles or fluid collections within the muscular compartments. The sonographic examination suggested the diagnosis of necrotizing fasciitis and therefore the patient underwent urgent surgical exploration. A generous longitudinal incision was made over the affected area. On inspection, the subcutaneous tissue was edematous with discharge of turbid fluid from the cut edges. The perifascial planes had a foamy appearance with crepitations due to gas bubbles. Only a few small necrotic patches were found within the skin and subcutaneous fat and the deep fascia still appeared normal. The tissues were debrided and

Discussion

Necrotizing fasciitis is a progressive and often rapidly spreading infection of the soft tissues. This type of infection was originally reported to affect the genital region and is now known as Fournier's gangrene 9 . Subsequently, Meleney found necrotizing fasciitis to involve also other body regions 10 . The term of "necrotizing fasciitis" was introduced by Wilson in 1952 11 .

Recently, the term of necrotizing soft-tissue infections was proposed to highlight the same treatment strategy in this group of infections 12 .

Necrotizing fasciitis is an infection that spreads along the superficial and deep fascial planes of the soft tissues. The skin and muscles are usually spared at the early stages of the disease.

The speed with which the infection progresses depends on the virulance of the causative pathogen and the severity of immune suppression of the host. Necrotizing fasciitis is a synergistic bacterial infection usually due to a mixed flora. Most frequently cultured pathogens are streptococci. Clostridial infections, although commonly suspected, are rarely responsible 1 . Necrotizing fasciitis often occurs in patients predisposed to infection because of the underlying chronic disease, especially diabetes mellitus that is a risk factor found in 21-64% of cases 1 . Patients present with severe pain that is often disproportionate to physical findings.

Initially necrotizing fasciitis has an insidious course and its clinical picture may be similar to Necrotizing fasciitis in US 7 based solely on clinical findings is incorrect in 64% cases 13 . Early recognition is essential because any delay in the surgical management results in worse prognosis 2,14 .

Clinical recognition of necrotizing fasciitis is difficult and imaging studies can be helpful in suggesting early diagnosis. Radiographic studies are usually used in doubtful cases without obvious signs of necrotizing fasciitis such as overt skin necrosis or tissue crepitus.

Radiographic findings in necrotizing fasciitis are similar to those found in cellulitis. Cellulitis begins and spreads in the superficial layers of the subcutaneous tissues. In contrast, necrotizing fasciitis involves deeper structures and the inflammatory changes are more severe 15 . The subcutaneous emphysema is a distinguishing sign of necrotizing fasciitis, but crepitus is not always present on palpation. Plain x-rays show subcutaneous emphysema when there is a moderate to large amount of gas within the tissues. Although crepitus is found on physical examination in 12-36% of patients with necrotizing fasciitis, soft tissue gas is seen on plain xray in 17-57% of patients 1 . Tissue emphysema has been generally regarded a late finding in necrotizing fasciitis. Our case illustrates, however, that in some cases tissue gas might appear early in the course of the disease.

CT and MRI are frequently used diagnostic tools in patients with suspected necrotizing fasciitis. The tomographic findings suggesting necrotizing fasciitis include asymetric fascial thickening, fluid collections along the deep fascia and soft tissue gas 4 . Although MRI has a high resolution for soft tissues, its value is limited in necrotizing fasciitis, because the patients are often too ill to undergo a timely study. MRI findings such as fluid collections along the deep fascial sheath and thickening of the deep fascia with contrast enhancement suggest necrotizing fasciitis 3 . Nevertheless, both CT and MRI have high sensitivity and low specifity for necrotizing fasciitis 3,4,16 .

The sonographic appearance of necrotizing fasciitis has rarely been reported in the literature 6- 8,17 . The ultrasound findings suggesting necrotizing fasciitis included thickening of the deep The sonographic appearance of necrotizing fasciitis may be similar to cellulitis. In both conditions, there is swelling and increased echogenicity of the subcutaneous tissue. In more severe cases, the subcutaneous tissue has a so-called cobblestone appearance due to interlaced anechoic spaces within the fatty tissue corresponding to fluid collections dissecting along the perifascial planes. Nevertheless, fluid spaces tracking along the deep fascia strongly suggest the diagnosis of necrotizing fasciitis and are usually not observed in cellulitis 6 .

In necrotizing fasciitis, the inflammatory changes are usually more severe and located in deeper layers than in cellulitis. In our patient, the sonographic diagnosis of necrotizing fasciitis was based on the recognition of soft tissue gas and fluid collections dissecting along the deep fascia. Soft tissue gas is indicative of necrotizing fasciitis and warrants an urgent surgical exploration and debridement. In our patient, the debridement was performed before the development of overt necrosis of the deep fascia. The infection was controlled early and there was no need for any subsequent debridement procedures.

Our case highlights two essential features of necrotizing fasciitis. Firstly, the subcutaneous emphysema may appear early in the course of the disease due to gas-forming bacteria.

Secondly, the inflammation spreads along the deep fascia and extends beyond the margins of apparent skin infection.

In conclusion, ultrasonography is an attractive tool for early recognition of necrotizing fasciitis, especially due to gas-forming bacteria. The subcutaneous emphysema and fluid collections spreading along the deep fascia favor the diagnosis of necrotizing fasciitis. Liberal

  cellulitis. A hallmark of NF necrotizing fasciitis is liquefying necrosis of the subcutaneous tissues, fascia, skin and also muscles in severe cases. Purpuric or necrotic areas in the skin indicative of NF necrotizing fasciitis appear late in the course of the disease and a high index of suspicion is required. The diagnosis of necrotizing fasciitis is a clinical one, but it is often delayed, because the infection begins and progresses in the deep layers of the subcutaneous tissues giving initially a false impression of a typical cellulitis. The provisional diagnosis

  Necrotizing fasciitis in US 8 deep fascia, diffuse thickening of the overlying fatty tissue and a fluid layer of at least 4 mm in depth along the deep fascia. Yen et al 8 reported a sensitivity of 88,2% and specificity of 93,3% for ultrasonography in recognition of necrotizing fasciitis using the aforementioned criteria. The diagnosis of NF necrotizing fasciitis is further aided by the detection of gas within the soft tissues which is thought to be pathognomonic to necrotizing fasciitis.

Fig. 1 A

 1 Fig. 1 A transverse ultrasound scan of the forearm shows a hyperechoic layer above the deep

Fig. 2 A

 2 Fig. 2 A transverse sonographic image of the arm taken just above the proximal margin of the

  Necrotizing fasciitis in US 5 copiously irrigated. Gram stain of the excised necrotic tissues revealed multiple cocci. The patient responded well to surgical debridement and parenteral antibiotics. The infection was controlled and there was no need for further explorations. Subsequently, the skin defects were covered by means of flap plasty.

  cellulitis. A hallmark of necrotizing fasciitis is liquefying necrosis of the subcutaneous tissues, fascia, skin and also muscles in severe cases. Purpuric or necrotic areas in the skin indicative of necrotizing fasciitis appear late in the course of the disease and a high index of suspicion is required. The diagnosis of necrotizing fasciitis is a clinical one, but it is often delayed, because the infection begins and progresses in the deep layers of the subcutaneous tissues giving initially a false impression of a typical cellulitis. The provisional diagnosis

  Necrotizing fasciitis in US 8 fascia, diffuse thickening of the overlying fatty tissue and a fluid layer of at least 4 mm in depth along the deep fascia. Yen et al 8 reported a sensitivity of 88,2% and specificity of 93,3% for ultrasonography in recognition of necrotizing fasciitis using the aforementioned criteria. The diagnosis of necrotizing fasciitis is further aided by the detection of gas within the soft tissues which is thought to be pathognomonic to necrotizing fasciitis.

Fig. 1 A

 1 Fig. 1 A transverse ultrasound scan of the forearm shows a hyperechoic layer above the deep

Fig. 2 AFig. 1 AFig. 2 A

 212 Fig. 2 A transverse sonographic image of the arm taken just above the proximal margin of the

Journal of Clinical Ultrasound

John Wiley & SonsJournal of Clinical Ultrasound

John Wiley & Sons

Journal of Clinical Ultrasound