A short History of Amniocentesis, Fetoscopy and Chorionic Villus Sampling

Dr. Joseph Woo



Amniocentesis

Tapping of amniotic fluid had been practised for over a 100 years although many cases had not been recorded. In the literature, transabdominal amniocentesis in the third trimester has been reported by Prochownick, Von Schatz and Lambl in 1877 and Schatz in the 1890s. In 1919 there was a report from Hinkel describing release of amniotic fluid from a patient with polyhydramnios. Menees et. al. reported in 1930 removal of amniotic fluid by transabdominal needling. Radio-opaque contrast was injected to outline the fetus and placenta. Bevis in 1953 obtained samples of liquor by abdominal paracentesis, at two-weekly intervals, in the management of rhesus isoimmunized patients, and to predict the gravity of the condition.

Liley in Auckland, New Zealand in 1961 published the well-known correlation between the deviation of the spectral absorption curve of liquor amnii resulting from bilirubin, and the severity of rhesus isoimmunization. Since Liley's studies, the practice of amniocentesis had become a standard procedure in Obstetric practice.

The first use of amniotic fluid examination in the diagnosis of genetic disease was reported by Fuchs and Riis in 1956 in their seminal article in "Nature". They determined fetal sex from cells found in amniotic fluid, basing on the presence or absence of the Barr body. John Edward in England, also discussed for the first time in 1956 the possibility of the "antenatal detection of hereditary disorders". The determination of fetal sex led to the prenatal management of patients with Haemophilia A in 1960, and Duchenne muscular dystrophy in 1964.

Steele and Breg very importantly demonstrated in their seminal paper in the Lancet in 1966 that cultured amniotic fluid cells were suitable for karyotyping. Thiede, Creasman and Metcalfe published similar findings later on in the same year. In 1968, Nadler reported on enzyme assays utilizing cultured fetal cells in the amniotic fluid and in the same year reported one of the first diagnoses of Trisomy 21. Their group used cultured cells for a full chromosome analysis. Milunsky and Littlefield discussed the diagnosis of inborn errors of metabolism in 1972. Brock and Sutcliffe in 1972 discovered that excessive amounts of alpha-fetoprotein (AFP) were present in the amniotic fluid of pregnancies with neural tube defects. Other biochemical substances were investigated. Nadler and Gerbie published the important article "Role of amniocentesis in the intra-uterine diagnosis of genetic defects" in the New England Journal of Medicine in 1970. This was the real impetus in genetic amniocentesis and diagnosis, and from then on, genetic laboratories for analysis of amniotic fluid had become prevalent and indications for genetic amniocentesis included the detection of chromosomal abnormalities, X-Iinked conditons, inborn errors of metabolism, and the neural tube defects.


16 cm Non-disposable re-use steel needles used in the late 1960s and early 70s.
This was replaced by 9 cm disposable ones in the mid 70s.

Gluck et al in 1971 discovered that fetal lung maturity was found to be related to the surface active phospholipid lecithin. When compared with another phospholipid, sphingomyelin, the lecithin/ sphingomyelin ratio was found to be predictive of severe idiopathic respiratory distress syndrome. Ultrasound guidance was started to be employed in amniocentesis with reports from Jens Bang and Allen Northeved from Copenhagen in 1972, where they worked with Hans Hendrik Holm at the Gentofe Hospital, a center which became famous of interventional imaging.


As early as 1967, and basing on the Vidoson, Hofmann and Hollander in Germany had discussed the importance of placental localization using ultrasound before amniocentesis. Jens Bang and Allen Northeved in Copenhagen described ultrasound-guided amniocentesis in 1972. Prior to the mid 1970s many of the genetic amniocentesis were done 'blind', ie the puncture site located merely by external palpation of the uterus in the abdomen. In the mid 1970s to mid 80s, amniocentesis was performed with the assistence of a static or realtime B-scan. A scan was first performed to locate a feasible pocket of amniotic fluid before a tap, the skin on top of that area was marked and the puncture was done without actually seeing the needle tip going into the fluid pocket. With improving resolution of the realtime scanners, a small number of centers had in the late 1970s started to perform amniocentesis with the simultaneous visualization of the puncture needle tip on the scanner monitor. One such pioneer was the Birnholz group at Harvard who used an early phased array for the purpose. Needle-guide adapters soon became available from ultrasound manufacturers which could be coupled to the linear array or phased array sector probes where the needle passed through a fixed path either parallel or at an angle to the ultrasonic beam. These were cumbersome to use however, particularly in a busy setting. They also had serious problem of keeping the equipment sterile. The adapters may also increase the risk of traumatisation as it did not allow for the 'desired' and sensitive placement of needles.

Many centers started to do it freehand with an assistent holding onto the transducer probe that was commonly wrapped in a sterile adhesive drape. In 1984, Holzgreve in Basel, Switzerland described a large series of over 3000 'freehand' amniocentesis with low complication rate. Similar experience was also reported by Platt in Los Angeles, who emphasised on the need for the transducer probe to be manipulated by the same operator which resulted in better hand-eye co-ordination. In the following year, Romero at Yale formally described the single operator two-hands technique in amniocentesis and the reduction in the number of multiple taps and bloody taps associated with the procedure. Most centers soon adopted the single operator technique, which had become popular because of its convenience and effectiveness. Newer needles were marketed with special external coating and echo-luminence to enhance needle placement. Complication rates were reportedly lower with each successive improvement in technique.

The Benacerraf group reported early amniocentesis (11-14 weeks) in 1988, following some initial reports from Hanson et al. in 1987. In 1990, the Benacerraf group reported an early fetal loss rate of over 2.3%. Several important reviews in the mid-90s confirmed this high incidence of fetal loss. For this reason, the practice was not met with general acceptance.



Fetoscopy and fetal blood sampling

The first attempts at fetoscopy were carried out by Westin in 1954 using a 10 mm diameter hysteroscope introduced through the cervix of patients who were to have therapeutic abortions between 14 and 18 weeks. A transabdominal approach was used by Mandelbaum et al in 1967 during attempts at intrauterine fetal transfusion for haemolytic disease. Fetal skin samples were obtained prior to termination of pregnancy by Valenti in 1972, using a 5mm needlescope which he modified from an 18 French pediatric cystoscope and which he called an endoamnioscope. The term Fetoscopy was introduced by Scrimgeour in 1973. He exposed the uterus at laparotomy and introduced a 2.2 mm needlescope to view the amniotic cavity and fetus. The procedure was performed in six women whose offspring were at high risk of recurring fetal neural tube defect. Three healthy infants were delivered but a fourth had spina bifida.

Valenti in 1973 used the 'endoamnioscope' and reported the first aspiration of fetal blood and the diagnosis of haemoglobinopathy. The newer Dyonics® Needlescope became available in the following year, which was 1.7mm in diameter with a 2mm cannula. General anaesthetics was not required for its use.

Pioneering work came from Hobbins and Mahoney at Yale and Patrick, Perry and KInch in Canada in the same year. Initial work was performed on patients between 15 and 20 weeks of gestation. The use of sonography prior to the procedure was much emphasised. Fetal blood aspiration was performed via a 27-gauge needle inserted through a special cannula allowing aspiration under direct vision. The special cannula was named the Hobbins cannula. It was noted that there was no evidence of any vessel trauma at postmortem examination and blood samples were more successfully obtained after 18 weeks and peripheral parts better visualized than central ones.


In 1977, Hobbins and Mahoney reported successful exclusion of beta-thalassemia and diagnosis of sickle cell disease without aparent risk to the mother and fetus. Other important workers included Alter and Nathan, and Fairweather in London. Rodeck and Campbell reported the diagnosis of spina bifida using this method. In 1979 the group reported a success rate of obtaining pure blood samples of 94% in 51 attempts. They introduced the method of aspirating from one of the larger vessels at the base of the cord. Most investigators started with the diagnosis of haemoglobinopahies, in which maternal cell contamination did not affect the accuracy of the results

Other reported diseases diagnosed via fetoscopy included haemophilia (1979, Firsheim), chronic granulomatous disease (1979, Newburger), galactosaemia (1979, Fensom), and Tay-Sachs disease (1979, Perry). Fetal skin biopsy successfully diagnosed congenital bullous ichthyosiform erythroderma ichthyosis by the Golbus group in San Francisco in 1979 and epydermolysis bullosa letalis by the Rodeck group in 1980. In 1982, the Rodeck group reported fetal liver biopsy for prenatal diagnosis of ornithine carbamyltransferace deficiency.

Fetoscopic guided Laser occlusion of chorioangiopagous vessels (FLOC) was first pioneered by De Lia in 1988 at the University of Utah for the treatment of the Twin-to-Twin-Transfusion Syndrome (TTTS) . Nicolaides at King's and Ville in France introduced the technique to Britain and Europe in 1991. It is now standard treatment for this condition in many perinatal centers.

After fetoscopy, ultrasound-guided pure fetal blood cordocentesis was pioneered in France in 1983 by Daffos. Pure fetal blood was aspirated in-utero at around 18 weeks from the umbilical vein near the placental insertion of the cord using a twenty gauge needle under ultrasound guidance. Their group reported the first case of Haemophilia A diagnosed in-utero by this method. The procedure was also popularised around the same time in England by the Campbell and Rodeck group at King's College Hospital. The Hobbins group at Yale described their technique in 1985 and called the procedure percutaneous umbilical blood sampling (PUBS). This replaced blood sampling via fetoscopy which the group had pioneered in 1974.

Nicolaides at King's developed the single operator two-hands method and became a leading figure in cordocentesis exploring many important aspects of fetal physiology and pathophysiology. With the advent of color flow mapping, the technique has become even more accessible. In 1988, Nicolini, working with Rodeck at the Queen Charlotte's Maternity Hospital in London, first described fetal blood sampling from the intrahepatic portion of the umbilical vein in the fetus, as an alternative procedure in cases where cord needling was unsuccessful.

In the late 1980s fetoscopy has mainly been reserved for tissue or organ sampling, and fetal blood sampling are always done via the ultrasonic-guidance needle procedure. The commonest indication of fetal blood sampling had evolved to become one of quick confirmation of abnormal karyotype in the 22-24 weeks fetus, when a chromosomal abnorrmality has been suggested on ultrasound scan.

In 1990, Cullen, Reece, Whethaam and Hobbins described the new technique of "Embryoscopy', a transabdominal thin gauge embryo-fetoscopy procedure in the first trimester. Quintero, Abuhamad, Hobbins and Mahonney reviewed the clinical application of the procedure in 1993 and reported the early prenatal diagnosis of a case of Meckel Gruber Syndrome using this technique.



Chorionic villus Sampling (Biopsy)

In 1968 Mohr in Scandinavia introduced the concept of antenatal genetic diagnosis using sampled chorionic villi. He performed transcervical biopsy of the chorion under direct endoscopic vision, using a straight 5mm endoscope. He reported a 96% success rate in obtaining chorionic material but with a high incidence of bleeding, infection and failed culture. The approach was slowly abandoned in the midst of increasing safety from mid-trimester amniocentesis. Kullander and Sandahl in 1973 and Hahnemann in 1974 reported fetal chromosome analysis from transcervical placental biopsy prior to termination in early pregnancies. The first successful prenatal diagnostic use of chorionic villi biopsy was apparently reported in 1975 from the Department of Obstetrics and Gynaecology at the Tietung Hospital in Anshan, China, where fetal sex was diagnosed for the purpose of sex pre-selection. This was reported in the first issue of the (new) Chinese Medical Journal. They performed blind aspirations using a 3mm metal cannula on a group of 100 patients. When a soft resistence was met, a smaller internal tube was advanced further and placental material obtained by syringe suction. They claimed to have 6 wrong diagnosis out of 99 successful attempts and only 4 prenatal losses. Investigators in the United States were, however unable to duplicate the results and the idea of first trimester antenatal diagnosis was again shelfed for some time.

Apparently with the advent of ultrasound and advancement in molecular genetics the desire for an earlier antenatal diagnosis was rekindled. Kazy et at. in 1980, in the USSR reported fetal sexing and enzyme assay on chorion biopsies taken at 6 -12 weeks' gestation, using either an endoscopic or ultrasound-guided approach. Biopsy forceps were used instead of cannulas. This was the first report in the literature of using ultrasound guidance during chorion sampling. Niazi et al. in 1981 at the St. Mary's Hospital, London reported improved methods for culturing of fibroblasts from trophoblast villi.

In 1983, Ward in London performed transcervical chorionic sampling under ultrasonic guidence using a 1.5 mm malleable polyethylene catheter and syringe suction. His group reported 67% sampling success rate, including 7 patients for the diagnosis of haemoglobinopathies. The Brambati group in Milan demonstrated in 1983 that with ultrasonic guidance, success rate of obtaining chorionic material rose from 75% to 96%. Brambati used a 1.5mm polyethylene tube with a soft stainless steel malleable obturator inserted into the 1 mm internal barrel. This design has been the most common design in use today. Other workers like Dumez in Paris used a simple 2 mm biopsy forceps. The Simoni and Brambati group in Milan described in 1983 a technique for direct chromosome and biochemical analysis on first trimester chorionic villi (direct prep), without preliminary culture. Chorionic villi were obtained by aspiration or direct biopsy from the chorion frondosum, at the edge of the placental disc. The inner cytotrophoblastic layer beneath the outer syncytiotrophoblast layer contains actively mitotic cells in freshly sampled villus which could be recovered with their technique. Virtually all analyses could be performed with these fresh whole villus.

In 1984, Smidt-Jensen and Hahnemann in Copenhagen introduced transabdominal fine-needle villus aspiration under ultrasound guidance. With less chance of infective complications and re-insertions the procedure has become more popular than the transcervical counterpart in many prenatal diagnostic centers. Other adjunctive ultrasonic techniques and modifications were reported by the Brambati and Simoni group in Milan and the Golbus group in San Francisco in 1985. The Golbus group reported in 1986 initial experience with 1000 cases of CVS and reported a fetal loss rate of 3.8% and a 1.7% incidence of chromosome mosaicism not found in the fetus. A much lower miscarriage rate of less than 1.5% was subsequently reported by many other centers making the procedure acceptable for routine use.






References:

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