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  Table of Contents    
ORIGINAL ARTICLE  
Year : 2015  |  Volume : 58  |  Issue : 3  |  Page : 285-291
Risk factors, organ weight deviation and associated anomalies in neural tube defects: A prospective fetal and perinatal autopsy series


1 Department of Pathology, S. C. B. Medical College, Cuttack, Odisha, India
2 Department of Obstetrics and Gynecology, S. C. B. Medical College, Cuttack, Odisha, India
3 Department of Pathology, KIMS, Bhubaneswar, Odisha, India

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Date of Web Publication14-Aug-2015
 

   Abstract 

Introduction: Neural tube defects (NTD) are a group of serious birth defects occurring due to defective closure of neural tube during embryonic development. It comprises of anencephaly, encephalocele and spina bifida. We conducted this prospective fetal autopsy series to study the rate and distribution of NTD, analyze the reproductive factors and risk factors, note any associated anomalies and evaluate the organ weights and their deviation from normal. Materials and Methods: This was a prospective study done over a period of 6 years from August, 2007 to July, 2013. All cases of NTDs delivered as abortion, still born and live born were included. The reproductive and risk factors like age, parity, multiple births, previous miscarriage, obesity, diabetes mellitus, socioeconomic status and use of folic acid during pregnancy were collected.Autopsy was performed according to Virchow's technique. Detail external and internal examination were carried out to detect any associated anomalies. Gross and microscopic examination of organs were done. Results: Out of 210 cases of fetal and perinatal autopsy done, 72 (34.28%) had NTD constituting 49 cases of anencephaly, 16 spina bifida and 7 cases of encephalocele. The mothers in these cases predominantly were within 25-29 years (P = 0.02) and primy (P = 0.01). Female sex was more commonly affected than males (M:F = 25:47, P = 0.0005) There was no history of folate use in majority of cases. Organ weight deviations were >2 standard deviation low in most of the cases. Most common associated anomalies were adrenal hypoplasia and thymic hyperplasia. Conclusion: The authors have made an attempt to study NTD cases in respect to maternal reproductive and risk factors and their association with NTD along with the organ weight deviation and associated anomalies. This so far in our knowledge is an innovative study which was not found in literature even after extensive search.

Keywords: Autopsy, congenital malformation, neural tube defect, organ weight

How to cite this article:
Kar A, Kar T, Kanungo S, Guru L, Rath J, Dehuri P. Risk factors, organ weight deviation and associated anomalies in neural tube defects: A prospective fetal and perinatal autopsy series. Indian J Pathol Microbiol 2015;58:285-91

How to cite this URL:
Kar A, Kar T, Kanungo S, Guru L, Rath J, Dehuri P. Risk factors, organ weight deviation and associated anomalies in neural tube defects: A prospective fetal and perinatal autopsy series. Indian J Pathol Microbiol [serial online] 2015 [cited 2019 Jul 24];58:285-91. Available from: http://www.ijpmonline.org/text.asp?2015/58/3/285/162832



   Introduction Top


Failure of neural tube to develop properly during 3 rd -4 th weeks of gestation gives rise to neural tube defect (NTD) and is incompatible with life. It is classified into cranial type (cranioschisis-anencephaly and encephalocele) and spinal type (spina bifida) respectively. [1] Anencephaly occurs when the cephalic end of the neural tube fails to close. This results in absence of forebrain mainly the cerebral hemisphere including the neocortex. The remaining parts of the brain are often not covered by bone or skin. Another related condition is encephalocele which is herniation of brain through an opening in the skull. Spins bifida, the spinal NTD, is caused due to nonclosure of lower part of the neural tube. Each of these can occur singly or simultaneously which can again be separate or continuous when it is known as craniorachischisis.

Despite the considerable progress in the field of NTDs, they still cause lot of morbiidty and mortality and the cause is still unknown. It is believed that there is an interaction of multiple environmental and genetic factors responsible for the causation of NTDs. [2],[3] Various studies have suggested that the incidence of NTDs is more among mothers <20 or more than 35, low and high parity, previous miscarriage, multiple births, low socioeconomic status and with no periconceptional use of folic acid. Most of these cases are associated with hydrocephalus and adrenal hypoplasia.Extensive literature can be obtained relating NTD, but few describe in detail demographic factors which include the rate, distribution, location, maternal factors like reproductive and risk factors, associated anomalies, organ weight deviation from normal infants and more so the histological findings in each of these organs. Therefore we conducted this study to find out:

  1. The rate, location and type with gestational age and gender of NTD.
  2. Maternal reproductive and risk factors.
  3. Macroscopic and microscopic examination of the organs and the organ weight deviations.
  4. Any associated external or internal anomalies.



   Materials and Methods Top


The study was done prospectively during a period of 6 years from August, 2007 to July, 2013. This includes spontaneous and therapeutic abortion, still born and perinatal death cases referred from Department of Obstetric and Gynecology for autopsy and detail pathological examination. Clinical details of each case including gestational age, maternal risk factors, ultrasonographic findings were recorded. Data base including age, parity, previous miscarriage/infant deaths/NTD, multiple births, socioeconomic status, obesity, H/O diabetes mellitus, folic acid use by the mother were collected. Statistical analysis of these data was done by using Chi-square analysis. Detail external examination was conducted to find out any anomalies. The location and type of NTD was noted. These defects were classified according to methods described previously in literature. [4],[5],[6] Anthropometric measurements like crown heel length (CHL), crown rump length (CRL), chest circumference (CC), foot length (FL) were noted. The head circumference could not be recorded in anencephalic babies because of absence of scalp. The gestational age was estimated. The weight of baby, placental weight and also the length of umbilical cord were recorded. Umbilical cord was examined for presence of stricture, blood clot and/or coiling Autopsy was done according to Virchow's technique by giving an inverted "Y" ' shaped incision encircling the umbilicus on left side. [7] After opening the thoracic and abdominal cavity the organs were removed one by one from body and observed for presence of any anomaly. The weights were recorded and sections were taken from each organ for histopathological examination after hematoxylene and eosin stain. The organ weights were evaluated according to new fetal autopsy standards. [8] Organ weight deviations were grouped as low or normal according to more than or within two standard deviations (SDs) than normal respectively. The organ weight was considered high if it was higher than the standard weight by two SDs. In 2 cases (one spina bifida and one anencephalic fetus), samples were collected for chromosomal analysis. It was not possible in all cases due to noncooperation of parents, lack of facilities in our institution and difficulty in collecting the samples.


   Results Top


Out of 210 autopsies conducted, congenital malformation was observed in 103 or 49.04% cases. The most frequently observed congenital malformation was of central nervous system or NTD constituting 72 out of 210 of all autopsy cases (34.28%) and 69.90% (72 out of 103 cases) of congenital anomalies. Out of NTD cases anencephaly (49 of 72 cases - 68.05%) was the commonest [Table 1]. We did not get any spina bifida occulta case in our series. All were cystic which had ruptured due to trauma during delivery and majority of them were meningomyelocele. The common location of spina bifida in our series was lumbosacral [Figure 1]a. Encephalocele cases had brain tissue in the herniated material [Figure 2]a and b. Out of anencephalic fetuses, 22 (30.5%) were a combined presentation of both anencephaly and continuous spina bifida [Figure 1]b. In one case, there was an intracranial teratoma which was proved histopathologically. Majority of fetuses (15 of 36 cases) were in the gestational age between 29 and 32 weeks and predominantly females (47 of 72-65.27% cases-) [Table 2]. Reproductive factors like maternal age, parity, number of previous births/miscarriages, multiple births were analyzed in [Table 3]. NTDs are found to be more common in age group 25-29 years (40 cases-55.55%), primigravida (65.27%) and most of them had live intrauterine single fetuses with therapeutic termination of pregnancy (51.38% cases). Number of multiple births and previous births and miscarriages are not common among these cases in this study. Analysis of risk factors [Table 4] revealed that obesity and diabetes mellitus are not associated in majority of mothers but association was found with low socioeconomic status, polyhydramnios and lack of folate use. Out of the different risk factors, we got significant P value in maternal age <29 years (P = 0.02), primigravida (P = 0.01), female sex of NTD afffected fetuses (P = 0.0005), nonassociation with multiple births (P = 0.0005), gestational age between 29 and 32 weeks (P = 0.05) and use of folic acid use (P = 0.05). But there was no significant difference in polyhydramnios, socioeconomic status, obesity and diabetes mellitus.
Figure 1: Lumbosacral spina bifida. (b) Anencephalic fetus with continuous spina bifida or craniorachiscisis. (c) Autopsy of anencephalic fetus. (d) Gross photograph of organs removed from anencephalic fetus


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Figure 2: (a) Photograph of encephalocele. (b) Photomicrograph showing brain material in encephalocele (H and E, ×100)


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Table 1: Classification of neural tube defect cases according to location


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Table 2: Gestational age and sex distribution of NTD


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Table 3: Distribution of reproductive factors for women with NTD pregnancies


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Table 4: Analysis of maternal risk factors


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Anthropometric measurements [Table 5] revealed that CHL, CRL and CC were more than one SD low in majority of cases. But the FL was more than normal in 50% of cases. The organs were visualized inside the body for interrelationship with other organs [Figure 1]c. The organ weights including the birth weight after adjustment of brain weight are given in [Table 6] where the data has been tabulated according to the defect encountered. The weights have been taken and compared with the reference value laid by Archie et al. as per the postmenstrual gestational age and afterwards grouped on the basis of the type of defect. 69.4% had low birth weight and 77.2% showed adrenal hypoplasia which includes two cases where adrenals were absent. Pulmonary hypoplasia was seen in 36.1% cases but 55.2% had normal weight of lungs. The weight of heart, liver and kidneys were within normal in most of the fetuses [Figure 1]d. Associated external abnormalities [Figure 3]a and [Figure 3]b were found in few cases [Table 7]. Urogenital anomalies were found in 13 of 72 cases which includes 2 cases of multicystic kidneys [Figure 4]. The histological examination of all the organs were normal as per the gestational age [Figure 5]a-d with the residual and disorganised zona reticularis of adrenal cortex displayed in set in [Figure 5]a. The chromosomal analysis in anencephaly was a complex type involving chromosome 3 and trisomy 18 in spina bifida.
Figure 3: (a) Encephalocele with cleft lip and cleft palate, (b) autopsy findings


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Figure 4: C/S of multicystic kidney showing small cystic spaces present throughout


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Figure 5a-d: Photomicrograph showing histology of lungs, kidney, ear lobule and testis. Inset (a) Disorganised zona reticularis of residual adrenal cortex


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Table 5: Linear measurements in neural tube defect cases


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Table 6: Organ weights in neural tube defect cases


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Table 7: Associated anomalies and neural tube defect


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   Discussion Top


Abnormal closure of neural tube during embryonic development gives rise to congenital malformations of central nervous system together known as NTD. [1] Broadly it is of two types spinal and cranial. Cranial NTDs, otherwise known as cranioschisis are again subclassified into-cephalocele or encephalocele (occipital or parietal) and anencephaly (cranium, cranium and separate spina bifida, craniorachischisis, that is, anencephaly with continuous spina biifda). This is a very rare occurrence in obstetrics practice with anencephaly accounting for 1 out of every 10,000 births. [9] Spina bifida is encountered in.7 out of 1000 births in United States. The pathologists and clinicians have a fascination to study these cases in detail. The associated wide variety of central nervous system and other system anomalies with these cases are a source of great fascination to embryologists, pathologists and clinicians. The fact that it is important to know which conditions require special attention during performance of autopsy still increases the value of autopsy in these cases. And even though literatures are voluminous on NTDs few describe these cases in detail like incidence, gestational age and gender, location, maternal risk factors, reproductive factors, examination of placenta and umbilical cord, associated anomalies and organ studies both grossly and microscopically. Also most of these studies are retrospective analysis of records. Therefore we undertook this work prospectively and tried to study the NTD cases thoroughly with special emphasis on demographic factors, associated anomalies and organ weights and their histological examination.

In the present prospective series of fetal and perinatal autopsy, we have 72 cases of NTDs accounting for 34.28% of total cases. The incidence is higher in comparison to the American study reporting a rate of 3.9% and also to that of Nielsen et al. who found a rate of 4.9%. [1],[10] The reason may be that the obstetricians are more inclined to do an autopsy in a congenital anomalous fetus to know other associated defects and also the cause for this anomaly. Among different types of NTDs, anencephaly constitutes 66.6% of NTD. This is in comparison with that of Pinar's study who got 53% of anencephaly. [10]

Among these cases 2 were live born both being anencephaly-cranium type. One lived for 15 min and other for 2 h. From the rest, 29 came from therapeutic abortions. Two cases (2.77%) of anencephaly and one case (1.38%) of spina bifida were twin and term deliveries. The other babies of twin pregnancy were normal and alive at the time of delivery. 68% of females had undergone regular antenatal check up and ultrasonography [Figure 2] and therefore had chosen for therapeutic abortion. The gestational age varied from 17 weeks to 36 weeks, majority being seen in the range of 29-32 weeks (27 of 72 cases or 37.5%). Nielsen et al. found preponderance of NTD in 13-20 weeks which may be due to awareness among females and also routine ultrasonography in first antenatal check up which was not so in our set up. The mean gestational age according to Myrianthopoulos and Melnick was 39.21 ± 2.24 weeks in a randomly selected control group. [11] However our findings tally with that of Khaskheli et al. who found majority of congenital anomalies in the gestational age group of 29-32 weeks. [12] Females were predominantly affected in our series accounting for 47 out of 72 cases (65.27%). This goes with the research findings of Timson J who also found females to be more affected by anencephaly. [13] But literature analysis has not revealed any significant association between type of sex and occurrence of NTD.

Analysis of maternal age and parity in NTD has shown 'Ü' trend, risk being more in very young <20 years and older females. However other studies have found it to decrease with increasing age. [14] In the present series the incidence of NTD after 30 years of age is only 9.72% but 90.28% of cases occurred to mothers within 20-29 years and no case in age group <20 years. Similarly, 65.27% are primigravida and only 8.32% are multigravida with ≥2 previous pregnancies. Number of previous miscarriage and multiple births in index pregnancy are not statistically significant unlike the studies done by Owen et al., Whiteman et al., Mastroiacovo et al. [14],[15],[16] History of NTD in previous pregnancies also is not significant in our study since most of our cases are delivered to primigravida mothers.

Maternal obesity and body mass index have been consistently associated with increased risk of NTD. Maternal diabetes is also considered as a risk factor. But not proved by multivariate analysis. And in a study done after control of other profounding factors, the risk associated with diabetes did not increase. Present study also failed to prove obesity and diabetes as risk factors. However the number of NTDs are more with low socioeconomic status and in absence of periconceptional use of folic acid. The females in this study (68%) have regular antenatal check ups and have taken folic acid but not in 1-month around the conception period.

The commonly associated maternal risk factor in present study was polyhydramnios encountered in 50% of cases. Myrianthopoulos and Melnick also found polyhydramnios as a common maternal risk factor but there was no difference between live born and still born cases. We also examined placenta and umbilical cord in each case. Only in a few cases (9 out of 72 i.e., 12.5%), there was retroplacental blood clot. The umbilical cord was of normal length and without coiling or stricture. The number of vessels were normal unlike that of Myrianthopoulos and Melnick who found single umbilical artery in 16% of cases.

We have taken the linear measurements like CHL, CRL, CC and FL in each case to confirm the gestational age and also to determine the deviations from standard measurements. We didn't take head circumference because it can be fallacious in encephalocele and anencephalic cases due to protrusion of brain material [Table 5]. These data were compared with the expected linear measurements and SDs at various postmenstrual gestational age as given by Archie et al. [8] In our series, the CHL, CRL and CC were more than one SD low in majority of cases. Only the FL was high in 50% of cases (18 out of 36 cases). This is altogether a new revelation in our knowledge since we didn't get any literature for comparison of our findings.

It is difficult to calculate the birth weight of NTD cases especially those with anencephaly since 11-13% of birth weight is brain weight. [17] Since major portion of brain is missing in anencephalic fetuses, we had to adjust the birth weight by adding the brain weight according to gestational age. [8] After that, 69.4% of all cases of NTD showed a low birth weight upto one SD The percentage was still higher with cranial NTDs where 40 out of 56 cases (71.4%) had low birth weight. The reason for high value may be that many had intra uterine growth retardation due to either nutritional or other maternal causes and in some cases may be due to deficiency of insulin as put forth by Liggins. [18] Certain organ weights are known to deviate from normal range. In our series, most common deviation was seen with adrenals followed by lungs. 51 out of 72 cases, that is, 72.2% had decrease or absence of adrenals (49 adrenal hypoplasia with absence of adrenals in 2 cases). Adrenal hypoplasia in anencephalic patients can be of two types. Predominant type in our series was absence of fetal adrenal cortex and few showed disorganisation of zona fasciculata and glomerulosa. The cases of adrenal agenesis showed fetal kidney with complete absence of adrenal and replacement by smooth muscle cells in histology [Figure 5]a. This is a common finding in study of other authors also. [19],[20] It is hypothesized to be caused by impaired hypothalamus-pituitary-adrenal axis. Hyplplasia of lungs has also been found out by other authors n anencephalic foetuses. [21],[22] But in study of all types of NTD cases, we find normal lungs more commonly than hypoplastic lungs (54.1% in comparison to 37.5%). Pulmonary hypoplasia may be explained by deformed thoracic cage. In our series this was not a common finding which perhaps explains the higher rate of normal lungs in our study. In case of organs like heart, liver and kidneys, majority were in the normal range (61.1%, 59.7% and 62.5% respectively). We have got two cases of multicystic kidney with many diffusely present small cystic spaces [Figure 4]. In histological examination, morphology of all the organs didn't reveal any abnormality.

The most common associated congenital malformation in case of spina bifida was hydrocephalus seen in 8.3% of cases. This goes with the findings of Nielsen et al. where it was the predominant abnormality and was observed in 47% of spina bifida cases. The cause for decreased incidence of hydrocephalus in our series may be due to less number of cases studied and also hydrocephalus is more common with higher location of the defect in the spinal cord. In the present study the common location of spina bifida was lumbosacral and not higher resulting in less association with hydrocephalus. Among anencephalic fetuses, skeletal abnormality like absence of vertebral bodies, scoliosis were most common finding followed by urogenital abnormalities like absence of one kidney, cystic kidney and renal hypoplasia with one case of dysplasia. In one case multiple congenital anomalies were seen in face like fusion of two eye balls.Cleft lip and cleft palate were noted in one case of encephalocele [Figure 3]a and b. Even though there were fusion of eyes or cyclopia, there were no associated characteristic craniofacial abnormalities like single cerebral ventricle, single tubular nose and other features of midline defect ruling out the possibility of holoprosencephaly: syndromic and nonsyndromic. Associated mature teratoma was noted in one case which was confirmed histopathologically. This was not observed in studies of other authors.

Concluding NTDs are among the most common congenital anomalies that we encountered in our series. Young age of mother, low parity, poverty, polyhydramnios and a negative history of folate consumption might be contributing factors for its occurrence.Therefore, supplementation of Folic Acid and prenatal screening by determination of serum Fetoprotein level could decrease NTDs and other devastating conditions. Since NTDs occurs very early in pregnancy and many pregnancies are not planned, the Centers for Disease Control (CDC) and Prevention has recommended the adminstration of 0.4 mg of FA daily to all women of childbearing age. [23]

The purpose of doing this study is to know in detail about demographic factors of NTD cases about which literatures are scanty, to reduce the incidence by use of folate, and also if other organs of these unfortunate infants are normal so that in future attempts can be made to transplant them to their more fortunate counterparts. The detail study done on NTD revealed that the weights of heart, liver and kidney are predominantly normal and histological examination also did not show any abnormality. So we conclude that if the ethical and religious issues can be solved, the NTD infants can be kept on respirators and their organs can be donated to those infants who need them.

Limitations of this study are small number of cases and lack of chromosomal analysis. Chromosomal analysis in these cases is difficult since most of the fetuses are still born or terminated and parents do not cooperate and don't want to spend for babies which have dismal prognosis. Also sending samples to other institutions as in our case had the problem of disintegration and sample being unsuitable for karyotyping.

 
   References Top

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Nielsen LA, Maroun LL, Broholm H, Laursen H, Graem N. Neural tube defects and associated anomalies in a fetal and perinatal autopsy series. APMIS 2006;114:239-46.  Back to cited text no. 1
    
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Frey L, Hauser WA. Epidemiology of neural tube defects. Epilepsia 2003;44 Suppl 3:4-13.  Back to cited text no. 3
    
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Sperber GH, Gorlin RJ. Head and neck. In: Gilbert-Barness E, editor. Potter′s Pathology of the Fetus and Infant. St. Louis, MO, USA: Mosby-Year Book; 1997.  Back to cited text no. 4
    
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Larroche JC, Encha-Razzavi F, de Vries L. Central nervous system and hydrocephalus. In: Gilbert-Barness E, editor. Potter′s Pathology of the Fetus and Infant. St. Louis, MO, USA: Mosby-Year Book; 1997.  Back to cited text no. 5
    
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Khaskheli M, Baloch S, Khushk IA, Shah SS. Pattern of fetal deaths at a university hospital of Sindh. J Ayub Med Coll Abbottabad 2007;19:32-4.  Back to cited text no. 12
    
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Whiteman D, Murphy M, Hey K, O′Donnell M, Goldacre M. Reproductive factors, subfertility, and risk of neural tube defects: A case-control study based on the Oxford Record Linkage Study Register. Am J Epidemiol 2000;152:823-8.  Back to cited text no. 15
    
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Mastroiacovo P, Castilla EE, Arpino C, Botting B, Cocchi G, Goujard J, et al. Congenital malformations in twins: An international study. Am J Med Genet 1999;83:117-24.  Back to cited text no. 16
    
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Liggins GC. The driveto fetal growth. In: Beard RW, Nathancisz PW, editors. Fetal Pathology and Medicine. Philadelphia: WB Saunders; 1976. p. 254-70.  Back to cited text no. 18
    
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Sadovnick AD, Baird PA. Congenital malformations associated with anencephaly in liveborn and stillborn infants. Teratology 1985;32:355-61.  Back to cited text no. 19
    
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Mazzitelli N, Vauthay L, Grandi C, Fuksman R, Rittler M. Reviewing old concepts at the start of a new millenium: Growth restriction, adrenal hypoplasia, and thymomegaly in human anencephaly. Teratology 2002;66:105-14.  Back to cited text no. 20
    
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Correspondence Address:
Dr. Asaranti Kar
Department of Pathology, S. C. B. Medical College, Qrs. No. JO-1, Cuttack - 753 007, Odisha
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0377-4929.162832

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