This chapter is relevant to Section G1(iv)  of the 2017 CICM Primary Syllabus, which asks the exam candidate to "describe the fetal circulation". By tracking this occurence of an Americanised spelling in an Australian professional document, one can suppose that, like many syllabus items, this was cut-and-pasted from the ANZCA Syllabus for the Basic Sciences. Incidentally, as a member of a Commonwealth country where etymological fallacies are viewed as a marker of cultured literary prestige, the author has chosen to keep his foetuses full of Oe.

This has never appeared in the First Part papers, which is somewhat weird. The topic of foetal circulation and the circulatory changes which occur at birth has appeared multiple times in the Fellowship exam (Question 10 from the second paper of 2007, Question 11 from the first paper of 2005, Question 6 from the first paper of 2001), but vanished completely with the establishment of the CICM Primary Exam, which did not exist pre-2007. 

The key to learning this subject would be to find an explanation which focuses on the reasons behind the structural and functional differences between adult and in-utero circulations. Without that rationale to stimulate their faculties, the trainee turns to mindlessly memorising the list of differences. This produces suboptimal trainees, but also answers the SAQs, i.e. either approach has merit. The author himself has understood and re-forgotten this topic on at least eight separate occasions, in spite of epic efforts to self-educate. 

In summary:

Anatomical peculiarities:

  • The umbilical vein carries blood from the placenta to the IVC via the ductus venosus
  • From the IVC, blood splits into two parallel circuits:
    • via the foramen ovale into the LA
    • via the RV into the pulmonary circulation 
    • From the pulmonary trunk to the aorta via the ductus arteriosus
  • From the aorta, some of the blood flow returns to the placenta via the umbilical artery

Functional peculiarities

Systemic oxygen saturation 65% (in the left atrium) 97-100% (in the aorta)
Venous oxygen saturation 25-40% (IVC) 65-70% (pulmonary artery)
Arrangement of circulation Parallel circuit with shunts Serial circuit
Pulmonary blood flow 8% of the cardiac output 100% of the cardiac output
Pulmonary vascular resistance High Low
Pressures in the ventricles Equal Left ventricle has a much higher pressure than right
Mean arterial pressure
(normal range)
15-40 mmHg 65-90 mmHg
Compensation Minimal capacity to increase stroke volume; must increase heart rate to increase cardiac output Can increase stroke volume (by Starling mechanism) as well as heart rate

As far as peer-reviewed articles go, the best one would probably have to be the free BJA article by Murphy (2013), because it's short and to the point. Kiserud (2005) or Kiserud & Acharya (2004) might also be useful, depending on which links die first (in fact, anything by Torvid Kiserud seems to be gold). All of these authors have one flaw, which is the insistence on trying to represent the circulatory system with some semblance of anatomical accuracy. One could, however, make the arguments that CICM trainees are a) never going to operate on the unborn, and b) have a very function-oriented focus in the primary exams, which makes anatomy completely superfluous in this specific topic area. Therefore, a purely functional flowchart diagram is offered, to liberate the trainees from confusing tangles of poorly drawn greater vessels.

Structure of the foetal circulation

This diagram of the foetal circulation is an uncharacteristically austere version which should be reasonably easy to reproduce in an exam setting. 

circulation of the foetus - austere diagram

In summary, the path of blood flow is,

  • Oxygenated blood from the placenta returns via the umbilical vein
  • The umbilical vein distributes
    • 40% of its flow to the liver
    • 60% of its flow to the inferior vena cava, via the ductus venosus
  • The inferior vena cava drains into the right atrium
  • From the right atrium, the flow splits into parallel circuits:
    • Into the right ventricle, and then
      • Into pulmonary circulation, then back to the left atrium and left ventricle
      • Into the systemic circulation via the ductus arteriosus, which connects the pulmonary trunk to the proximal descending aorta
    • Into the left atrium via the foramen ovale,  and then to the left ventricle (this is mainly IVC blood, directed there by the Eustachian valve)
  • From the left ventricle, into the aorta
    • From the aorta, upper body blood flow (brain and arms) is purely from the left ventricle, whereas lower body blood flow is the combined output of the LV and RV (via the ductus arteriosus)
  • From the systemic circulation, venous blood returns:
    • From the common iliac arteries, via the umbilical arteries, to the placenta
    • From the upper body, to the right atrium
    • From the lower body, to the right atrium

In case this information is ever of interest, MRI imaging has been able to measure the following flow rates in these vessels, (indexed to kilograms of body mass in the 37 week foetus):

circulation of the foetus - austere diagram with flow rates.jpg

Characteristic structural features of the foetal circulation

There are a few structures which the trainee should probably know a little bit about, because they are unique to prenatal life. These will be discussed in order of circulatory appearance:

  • The umbilical vein is the major vessel carrying oxygenated blood to the foetus from the placenta; the saturation of its contents is usually about 70%. (Spurway et al, 2012). It sits alongside the umbilical ateries in the umbilical cord, packed in Wharton's Jelly. This vessel is of a reasonably large diameter; at term, it is expected to be about 8mm wide. It is a low pressure system;  umbilical venous pressure increases from 4.5 mmHg at 18 weeks gestation to 6 mmHg at term. It is connected to the IVC by the ductus venosus.
  • Ductus venosus is a "thin, trumpet-shaped vessel connecting the intra-abdominal umbilical vein to the inferior vena cava" (Kisserud, 2001). It basically points the flow of umbilical venous blood directly at the opening of the foramen ovale, with a little help from the Eustachian valve. The intrathoracic IVC being virtually nonexistant in the foetus, there is really only a very short distance between the opening of the ductus and the foramen, and well -oxygenated blood from the umbilical vein can be projected directly into the systemic circulation without mixing overmuch with the relatively hypoxic blood returning from the foetal lower body. 
  • Foramen ovale is a small atrial septal defect which closes at birth and forms the fossa ovalis (or not, in up to 25% of people). Blood flow through this opening is approximately the same as the flow through the pulmonary circulation, and half of what is pupted through the ductus arteriosus.
  • Ductus arteriosus is a short wide blood vessel which connects the pulmonary trunk to the descending aorta. As you can see on this image from Ho & Anderson (1979), it is approximately the same size as the pulmonary trunk, and conveys about twice the blood flow of the pulmonary circulation before birth.
    ductus arteriosus from Ho & Anderson, 1979
    Anyway. This thing closes with the action of prostacyclines at birth, and eventually becomes the ligamentum arteriosus in the adult. While patent, it supplies well-oxygenated blood to the upper body of the foetus. Some blood with reasonable oxygen content also emerges from the left ventricle via the ascending aorta, after having passed through the foramen ovale and the lungs. 
  • Umbilical arteries  are conduits for deoxygenated blood from the foetus to the placenta. When one describes this stuff as "deoxygenated", it is important to remember that it is the same level of oxygen as what supplies the foetal lower body.  These vessels originate from the common iliac arteries and wind spirally up the umbilical cord together with the umbilical vein. 

Functional differences between adult and foetal circulation

Apart from being structurally quite unlike the adult system, the foetal circulation has enough functional weirdness to fill an extensive list:

  • It operates at an extremely low pressure, as might be expected in a tiny organism. At a gestational age of around 19-21 weeks, Castle & Mackenzie (1986) were able to directly measure a MAP of around 15-10 mmHg. It apparently increases to about 40mmHg by the 28th week of pregnancy, which - though low - is at least no longer resembling the blood pressure of a medium sized bird. 
  • The oxygen saturation is much lower no matter where you sample. Acheson et al (1957)  measured an SaO2 of 65% in the carotid and 52% in the pulmonary trunk of foetal lambs, which appears to be consistent with human estimates. However, in spite of this, because the haematocrit is very high (Hb 150-170g/L), foetal blood maintains a high oxygen content - in fact often higher than that of the relatively well-oxygenated mother.
  • Combined ventricular output (CVO) rather than the cardiac output (CO) is used to describe the volume of blood pumped by the foetal heart per minute, as the ventricles are in parallel rather than in series. For the term foetus, this is quite high - about 400-500ml/kg/min. To compare, that would be about 28-35 L/min for a 70kg adult, well in excess of what is thought to be the uppermost limit of cardiovascular performance in humans.
  • The output of the RV and LV are not equal. The right ventricle receives about 65% of the venous return and the left ventricle receives about 35% (via the patent foramen ovale and the useless pulmonary circulation). Mielke et al (2001), with the aid of high resolution colour Doppler, were able to determine that right cardiac output was 59% and left cardiac output was 41% of biventricular cardiac output.
  • Cardiac output is heart rate-dependent. Contrary to popular belief, the Frank-Starling mechanism does operate in the foetal heart; it's just not very good. Kirkpatrick et al (1976) were able to demonstrate a significant change in LV shortening with increased end-diastolic pressure (at least in "chronically instrumented foetal lambs"). However, the foetal heart can only do this over a very narrow range of preload values, with the preload-contractility relationship limited to the flat part of the ascending limb of the Frank-Starling curve. The diagram below is plagiarised from a textbook on cardiac development, where it appears without a reference.
    https://academic.oup.com/eurheartj/article-abstract/13/suppl_E/40/486026
    The reason for this is thought to be a dearth of mature contractile units. It might seem very limiting, but one must be reminded that the intrauterine life is rather coddled from a haemodynamic perspective, such that the foetus is never exposed to wild swings in cardiovascular parameters.  The foetal circulation is so venodilated and intravascular volume is so abundantly available and easily replaced from the maternal circulation that there are minimal changes in foetal preload during a normal gestation.

Though these differences have never been a topic of an SAQ (none of this has), they are a ripe low-hanging fruit for an easily graded question, where a tabulated answer is expected.  Where possible, the oxygenation values and other numbers came from the Murphy article.

Differences between
the Foetal and Adult Circulatory Systems
Domain Foetus Adult
Source of oxygenated blood Placenta Lungs
Systemic oxygen saturation 65% (in the left atrium) 97-100% (in the aorta)
Venous oxygen saturation 25-40% (IVC) 65-70% (pulmonary artery)
Arrangement of circulation Parallel circuit with shunts Serial circuit
Pulmonary blood flow 8% of the cardiac output 100% of the cardiac output
Pulmonary vascular resistance High Low
Pressures in the ventricles Equal Left ventricle has a much higher pressure than right
Mean arterial pressure
(normal range)
15-40 mmHg 65-90 mmHg
Compensation Minimal capacity to increase stroke volume; must increase heart rate to increase cardiac output Can increase stroke volume (by Starling mechanism) as well as heart rate

References

Murphy, Peter John. "The fetal circulation." Continuing Education in Anaesthesia, Critical Care & Pain 5.4 (2005): 107-112.

Kiserud, Torvid. "Physiology of the fetal circulation." Seminars in Fetal and Neonatal Medicine. Vol. 10. No. 6. WB Saunders, 2005.

Kiserud, Torvid, and Ganesh Acharya. "The fetal circulation." Prenatal Diagnosis: Published in Affiliation With the International Society for Prenatal Diagnosis 24.13 (2004): 1049-1059.

Seed, Mike, et al. "Feasibility of quantification of the distribution of blood flow in the normal human fetal circulation using CMR: a cross-sectional study." Journal of cardiovascular magnetic resonance 14.1 (2012): 79.

Castle, B., and I. Z. Mackenzie. "In vivo observations on intravascular blood pressure in the fetus during mid-pregnancy." Fetal physiological measurements. Butterworth-Heinemann, 1986. 65-69.

Spurway, Jacqueline, Patricia Logan, and Sokcheon Pak. "The development, structure and blood flow within the umbilical cord with particular reference to the venous system." Australasian journal of ultrasound in medicine 15.3 (2012): 97-102.

Kiserud, Torvid. "The ductus venosus." Seminars in perinatology. Vol. 25. No. 1. WB Saunders, 2001.

Ho, S. Yen, and ROBERT H. Anderson. "Coarctation, tubular hypoplasia, and the ductus arteriosus. Histological study of 35 specimens." Heart 41.3 (1979): 268-274.

Acheson, G. H., G. S. Dawes, and Joan C. Mott. "Oxygen consumption and the arterial oxygen saturation in foetal and new-born lambs." The Journal of physiology 135.3 (1957): 623.

Kirkpatrick, STANLEY E., et al. "Frank-Starling relationship as an important determinant of fetal cardiac output." American Journal of Physiology-Legacy Content 231.2 (1976): 495-500.

Mott, J. C. "Control of the foetal circulation." Journal of Experimental Biology 100.1 (1982): 129-146.

Teitel, D. F., et al. "The end-systolic pressure–volume relationship in young animals using the conductance technique.European heart journal 13.suppl_E (1992): 40-46.

Mielke, Gunther, and Norbert Benda. "Cardiac output and central distribution of blood flow in the human fetus." Circulation 103.12 (2001): 1662-1668.