Vol 82, No 3 (2023)
Review article
Published online: 2022-06-22

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REVIEW ARTICLE

Folia Morphol.

Vol. 82, No. 3, pp. 467–477

DOI: 10.5603/FM.a2022.0061

Copyright © 2023 Via Medica

ISSN 0015–5659

eISSN 1644–3284

journals.viamedica.pl

Clinical significance of morphological variations of the inferior phrenic arteries

W. Marcinkowska1M. Malicki1P. Karauda1R.S. Tubbs2-7N. Zielińska1Ł. Olewnik1
1Department of Anatomical Dissection and Donation, Medical University of Lodz, Poland
2Department of Neurosurgery, Tulane University School of Medicine, New Orleans, LA, United States
3Department of Neurology, Tulane University School of Medicine, New Orleans, LA, United States
4Department of Surgery, Tulane University School of Medicine, New Orleans, LA, United States
5Department of Structural and Cellular Biology, Tulane University School of Medicine, New Orleans, LA, United States
6Department of Neurosurgery and Ochsner Neuroscience Institute, Ochsner Health System, New Orleans, LA, United States
7Department of Anatomical Sciences, St. George’s University, Grenada, West Indies
8Department of Normal and Clinical Anatomy, Medical University of Lodz, Poland

[Received: 31 January 2022; Accepted: 29 April 2022; Early publication date: 22 June 2022]

The rapid development of sciences such as genetics and molecular biology offers hope that better therapeutic methods can be developed and diagnosis and treatment made more effective. However, we must not forget that the basis for understanding the complex mechanisms of diseases and associated symptoms is knowledge of the relevant location and correlation among organs. In the present study, we focus on the clinical significance of the inferior phrenic artery. The diaphragm is a muscular structure that separates the abdominal and chest cavities. Thanks to this position, the inferior phrenic artery is much more significant than formerly assumed. A rich network of collaterals makes this vessel important in the development of neoplasms and metastases. Knowledge of anatomical variants of the inferior phrenic artery is also crucial for radiological procedures such as embolisation. The main aim of this study is to review the involvement of the inferior phrenic artery in physiological and pathophysiological processes. This work has value for all practicing doctors, especially radiologists and surgeons. (Folia Morphol 2023; 82, 3: 467–477)
Key words: inferior phrenic artery, diaphragm vascularisation, morphological variations, accessory inferior artery, hepatocellular carcinoma, pseudoaneurysm, embolisation

INTRODUCTION

The diaphragm is a dome-shaped muscular structure that separates the thoracic and abdominal cavities [5]. It is vascularised from several sources. Its cranial side is supplied by the pericardiacophrenic, musculophrenic, and superior phrenic arteries [32, 33]. However, the main donors of arterial blood to the diaphragm are the inferior phrenic arteries (IPAs) [5]. In the most common anatomical pattern, these vessels branch off the abdominal aorta. Each then crosses the crus of the diaphragm. The IPAs are located on the abdominal surface at an angle. Each vessel then divides into ascending and descending branches. The bifurcation is near the dorsal part of the central tendon of the diaphragm [21]. The ascending branch creates anastomoses with other arteries that supply the organ, namely the musculophrenic and pericardiacophrenic arteries and the same vessels on the opposite side [21]. The ascending branch of the left inferior phrenic artery (LIPA) crosses behind the oesophagus. It is then located on the left side of the aortic hiatus. The ascending branch of the right inferior phrenic artery (RIPA) runs behind the inferior vena cava. Thereafter, it is located on the right side of the vena cava foramen [21]. The descending branches of the IPAs anastomose with branches of the 8th to 12th intercostal arteries and the musculophrenic artery [5].

The provision of fresh arterial blood rich in oxygen is a precondition for keeping every organ alive [36]. The RIPA and LIPA are the most important sources of arterial blood for the diaphragm. This is highly physiologically significant because the diaphragm is crucial for respiration. It enables the thoracic cavity to expand during inspiration so that fresh air reaches the chest. Moreover, it prevents the withdrawal of gastric contents from the stomach into the oesophagus by occluding the gastroesophageal junction [5]. Branches of both the RIPA and LIPA also supply other organs such as the stomach, spleen, and oesophagus [37].

Anatomical variations of the RIPA and LIPA are well-known. Arteries often branch off abdominal arteries such as the gastric and renal arteries. The most common variant for both IPAs is an origin from the coeliac trunk. Interestingly, they can originate independently or via a common trunk [2, 3, 6, 7, 21].

Apart from providing blood to the diaphragm, the IPAs are also implicated in pathological conditions including pseudoaneurysm. The rupture of an IPA is life-threatening and requires early diagnosis and treatment [32]. Moreover, IPAs are particularly involved in the formation of extrahepatic collateral pathways that especially supply hepatocellular carcinomas [7]. They are also important in disorders caused by thoracic trauma, such as haemothorax [1].

The aim of this study is to assemble current knowledge about the physiological and clinical importance of IPAs and their anatomical variants. An important part of this review is the description of clinical syndromes related to these vessels. This knowledge is necessary for clinical practice, especially for radiologists and surgeons performing procedures pertaining to IPAs such as embolisation.

ANATOMICAL VARIANTS

Various types of IPA origin have been thoroughly described in recent studies. Aslaner et al. [2] proposed an interesting division of these arteries, distinguishing two main groups:

  • arteries originating independently without a trunk (Table 1, Figs. 15);
  • arteries originating via a common trunk (Tables 2, 3, Fig. 6).
Table 1. Types of right inferior phrenic artery and left inferior phrenic artery origin by a common trunk

Types of origin

Greig et al., 1951

Loukas et al., 2005

Kimura et al., 2007

Basile et al., 2008

Gürses et al., 2015

Aslaner et al., 2017

Szewczyk et al., 2020

Abdominal aorta

18.1%

31%

21%

21%

11.53%

16.4%

6.24%

Coeliac trunk

12.1%

11%

9%

16%

7.69%

12.6%

Right renal artery

-

0.4%

Left gastric artery

0.7%

-

0.1%

Table 2. Types of separate origin of right inferior phrenic artery (without common trunk)

Types of origin

Greig et al., 1951

Loukas et al., 2005

Kimura et al., 2007

Basile et al., 2008

Gürses et al., 2015

Aslaner et al., 2017

Abdominal aorta

28%

30.67%

36%

28%

50%

25.2%

Coeliac trunk

29.2%

36%

20.79%

25%

3.85%

30.7%

Right renal artery

17%

11%

5.5%

7.69%

10.4%

Left gastric artery

1.9%

3%

2%

4%

3.85%

4.1%

Common hepatic artery

0.1%

Accessory right hepatic artery

0.2%

Spermatic artery

0.2%

Dorsal pancreatic artery

1%

Proper hepatic artery

2%

0.5%

Table 3. Types of separate origin of left inferior phrenic artery (without common trunk)

Types of origin

Greig et al., 1951

Loukas et al., 2005

Basile et al., 2008

Gürses et al., 2015

Aslaner et al., 2017

Abdominal aorta

25.9%

37.67%

26.5%

34.61%

25.2%

Coeliac trunk

40%

43%

28%

23.07%

40.3%

Left gastric artery

1.9%

2%

2.4%

Left renal artery

5%

1%

2%

Left hepatic artery

0.5%

Right renal artery

0.1%

Accessory left hepatic artery

0.2%

Proper hepatic artery

1%

Splenic artery

1%

Figure 1. A. Right inferior phrenic artery (RIPA) (without common trunk) from abdominal aorta; B. RIPA (without common trunk) from coeliac trunk; C. RIPA (without common trunk) from right renal artery; D. RIPA (without common trunk) from the left gastric artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery.
Figure 2. A. Right inferior phrenic artery (RIPA) (without common trunk) from common hepatic artery; B. RIPA (without common trunk) from accessory right hepatic artery; C. RIPA (without common trunk) from spermatic artery; D. RIPA (without common trunk) from the dorsal pancreatic artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery; LHA — left hepatic artery; RHA — right hepatic artery; PSP — posterior superior pancreaticoduodenal artery; PSA — superior pancreaticoduodenal artery; PHA — proper hepatic artery; AGD — gastroduodenal artery; aRHA — accessory right hepatic artery; SpA — spermatic artery; DPA — dorsal pancreatic artery.
Figure 3. A. Right inferior phrenic artery (RIPA) (without common trunk) from proper hepatic artery; B. Left inferior phrenic artery (LIPA) (without common trunk) from abdominal aorta; C. LIPA (without common trunk) from coeliac trunk; D. LIPA (without common trunk) from the left gastric artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery; LHA — left hepatic artery; RHA — right hepatic artery; PSP — posterior superior pancreaticoduodenal artery; PSA — superior pancreaticoduodenal artery; PHA — proper hepatic artery; AGD — gastroduodenal artery.
Figure 4. A. Left inferior phrenic artery (LIPA) (without common trunk) from left renal artery; B. LIPA (without common trunk) from left hepatic artery; C. LIPA (without common trunk) from right renal artery; D. LIPA (without common trunk) from accessory left hepatic artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery; LHA — left hepatic artery; RHA — right hepatic artery; PSP — posterior superior pancreaticoduodenal artery; PSA — superior pancreaticoduodenal artery; PHA — proper hepatic artery; AGD — gastroduodenal artery; aLHA — accessory left hepatic artery.
Figure 5. A. Left inferior phrenic artery (LIPA) (without common trunk) from proper hepatic artery; B. LIPA (without common trunk) from splenic artery; C, D. Accessory inferior phrenic artery from the inferior phrenic artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery; LHA — left hepatic artery; RHA — right hepatic artery; PSP — posterior superior pancreaticoduodenal artery; PSA — superior pancreaticoduodenal artery; PHA — proper hepatic artery; AGD — gastroduodenal artery; LaIPA — left accessory inferior phrenic artery; RaIPA — right accessory inferior phrenic artery.
Figure 6. A. Right inferior phrenic artery (RIPA) and left inferior phrenic artery (LIPA) origin by a common trunk from the abdominal aorta; B. RIPA and LIPA origin by a common trunk from coeliac artery; C. RIPA and LIPA origin by a common trunk from right renal artery; D. RIPA and LIPA origin by a common trunk from the left gastric artery; AA — abdominal aorta; CA — coeliac artery; SA — splenic artery; CHA — common hepatic artery; LGA — left gastric artery; RRA — right renal artery; LRA — left renal artery; SMA — superior mesenteric artery; IMA — inferior mesenteric artery.

The tables present the frequency of each type according to previous investigations. The papers by various researchers differ in the number of cases analysed, the type of arterial detection method, and the classification system [2, 3, 6, 7, 17, 21, 38].

Aslaner et al. [2] examined 1190 patients by abdominal computed tomography (CT) angiography (CTA). The images assessed included those obtained from patients with histories of mesenteric ischaemia, peripheral arterial disease, renal artery stenosis, and aortic aneurysm and donors for renal transplantation. Patients with histories of hepatocellular carcinoma, liver disease, or severe atherosclerosis and those who had undergone transarterial chemoembolisation or endovascular or surgical treatment of the aorta were excluded from this investigation. Each image was assessed for IPA origin by radiologists, followed by statistical analysis [2]. Their classification was very accurate. This is the only study that described four possible origins of the RIPA and LIPA via a common trunk (Table 1, Fig. 6). Greig et al. [6] examined 425 cases by dissection. American whites and blacks of both sexes were included in their study, which described all the patterns of arterial derivation found. Interestingly, Greig et al. [6] described a LIPA branching from the accessory left hepatic artery (Fig. 4) and a RIPA originating from the accessory right hepatic artery and spermatic artery (Fig. 2). These variants have not been described elsewhere.

Kimura et al. [17] analysed the type of origin of RIPA only. They examined 178 patients with hepatocellular carcinoma who required transcatheter arterial chemoembolisation via the RIPA. They used angiography to detect the origin pattern and relationship of the vessel to the coeliac, superior mesenteric, and right renal arteries. They described a RIPA arising from the dorsal pancreatic artery (Fig. 2). This type has not been reported in other investigations.

Gürses et al. [7] examined 26 cadavers (24 males and 2 females) by classical anatomical dissection. They resected the diaphragm, abdominal aorta, both kidneys, and the suprarenal glands in order to visualise the course of the IPAs. Their dissection also revealed branches of the RIPA and LIPA (Figs. 1, 3).

Szewczyk et al. [37] dissected the upper abdominal regions of 48 Caucasian cadavers (29 males and 19 females). All the specimens were free of trauma, pathology, or prior surgery in the upper abdominal organs. The authors examined the origins of the LIPA and RIPA and their diameters.

Loukas et al. [21] examined 300 adult human cadavers (120 females and 180 males) by dissection. They excised the inferior vena cava, liver, superior and inferior mesenteric arteries, stomach, pancreas, and coeliac and superior mesenteric nerve plexuses. This allowed a clear field of visualisation to be obtained. The spleen, both kidneys, and the suprarenal glands were not removed. In this study, the termination of the IPAs was also examined. The diameter of each IPA was measured. Interestingly, the authors described a case of a LIPA branching from the proper hepatic artery (Fig. 5). This has not been seen in other studies [21].

Basile et al. [3] examined 200 patients with hepatocellular carcinoma by 16-section CT during the arterial phase. They found a very rare case of a LIPA arising from the splenic artery (Fig. 5). This type of LIPA origin has not been presented in other investigations.

LIPA and RIPA branching by a common trunk have significantly less varied types. All authors presented in Table 1 agree that the most common type of such origin is from the abdominal aorta. Therefore, this trait is definitely well established in the human population.

According to Kimura et al. [17], Basile et al. [3], and Gürses et al. [7], RIPA branching from the abdominal aorta is the most common type of origin of this artery. These studies are in line with the classical anatomical pattern. However, according to Greig et al. [6], Loukas et al. [21], and Aslaner et al. [2], the RIPA arises much more frequently from the coeliac trunk. In our opinion, more investigations are necessary to determine whether the current anatomical pattern should be changed.

Interestingly, the most common type of LIPA origin according to Greig et al. [6], Loukas et al. [21], Basile et al. [3], and Aslaner et al. [2] is a branch from the coeliac trunk. This is not in line with the accepted anatomical pattern, which assumes that both the LIPA and RIPA arise most frequently from the abdominal aorta. The study by Gürses et al. [7] is the only one that confirmed the classical pattern accepted by medical universities, raising the question of whether it should be changed.

The foregoing tables present the frequency of occurrence of IPAs arising from various arterial vessels. However, we propose our own classification of IPA origins based on the available literature (Table 4). The most important feature of our classification is the presentation of complex correlations in a simple, easy-to-remember way. This system focuses on the location of origin only. We do not include the frequency, side of the body, or kind of branching (by a common trunk or direct). Therefore, it is more readable and potentially valuable in the clinical setting, where knowledge of the origins of various arteries is crucial for surgical or radiological procedures.

Table 4. New classification system based on the available literature proposed by Marcinkowska et al.

Type

Description

I

Hepatic arteries*

A — common hepatic artery

B — proper hepatic artery

C — left hepatic artery

D — accessory left hepatic artery

E — accessory right hepatic artery

II

Coeliac trunk and its branches**

A — coeliac trunk

B — left gastric artery

C — splenic artery

III

Renal arteries

A — right renal artery

B — left renal artery

IV

Abdominal aorta

V

Dorsal pancreatic artery

VI

Spermatic artery

RELATIONSHIP BETWEEN ORIGIN OF IPA AND AORTA

The above tables present the frequency of IPAs arising from the aorta. However, the exact location in relation to the aorta is not shown; these arteries can branch off from it at different levels or sides. Several researchers have described this type of IPA origin more precisely [3, 17, 35]. Basile et al. [3] found cases of the RIPA and LIPA originating via a common trunk from the aorta at the left side of the coeliac trunk (12%) or from the middle ventral aortic wall above the origin of the coeliac trunk (9%). Kimura et al. [17] distinguished three classes of RIPA branches from the aorta: supracoeliac (32%), between the coeliac trunk and superior mesenteric artery (17%), and between the superior mesenteric and right renal arteries (8%). So et al. [35] also examined RIPA origin sites and offered more precise descriptions. They distinguished five origin types: supracoeliac (20.5%), juxtacoeliac (11.7%), between the coeliac trunk and superior mesenteric artery (12.3%), juxta-superior mesenteric artery (7.9%), and suprarenal (5.5%).

BRANCHES OF THE INFERIOR PHRENIC ARTERY

Inferior phrenic arteries give off several branches and arteries that supply other structures [2, 6, 21, 22, 37]:

  • superior adrenal artery this vessel is one of three arteries that supply the suprarenal gland, which is known for its rich vascularity. The other two are the inferior adrenal and middle adrenal arteries, branching from the renal artery and aorta respectively;
  • branches to the spleen;
  • branches to the liver;
  • branches to the stomach;
  • branches to the oesophagus;
  • branches to the inferior vena cava;
  • branches to the retroperitoneum;
  • branches to the kidney and renal capsule.

It has also been reported that IPA scan gives off aberrant vessels:

  • accessory left gastric artery Heymann et al. [11] presented five cases of such abnormalities as revealed by angiography. In these patients, a conventional left gastric artery arose from the coeliac trunk, but each patient had an additional vessel supplying the gastric fundus. The frequency of an accessory gastric artery is unknown. However, its appearance can be significant in surgical procedures involving the gastric fundus; for example, in bariatric embolisation and angiography for upper gastrointestinal bleeding;
  • dorsal pancreatic artery this vessel supplies blood to the dorsal part of the pancreatic body. It is divided into two branches. The right branch creates anastomoses with branches from the gastroduodenal artery. The left branch (called the transverse pancreatic artery) anastomoses with the great pancreatic artery. A dorsal pancreatic artery arising from the splenic artery is the most common anatomical pattern. However, Hagiwara et al. [9] presented a case in which this artery branched from the IPA; it was noted during transarterial chemoembolisation and subsequently confirmed by computed tomography;
  • accessory inferior phrenic arteries.

Several studies have characterised the ascending and posterior branches of the LIPA, which can arise from various sources as independent arteries [7, 8]. Gürses et al. [7] presented an interesting case in which the ascending branch of the LIPA originated from the coeliac trunk and the posterior branch from the aorta. According to their statistical analysis, this variant occurs in 3.85% of cases. The same vascular variant was previously reported by Kim et al. [16].

A rare case of accessory phrenic arteries was described by Zeng et al. [38]. In a 69-year-old male, interventional radiography revealed a LIPA supplying the lesser curvature of the stomach and a right accessory phrenic artery conveying blood to the duodenum. Such variants of the gastrointestinal vascular system are significant in the planning of upper abdominal surgery.

DIAGNOSTICS

Effective surgical intervention for vascular disease depends on accurate diagnosis and identification of the location and type of lesion [26].Owing to the variable anatomy of the IPA, preoperative diagnosis is very helpful in planning surgical procedures and thus optimizing treatment outcomes [3].

A method that is currently widely used in the diagnosis of vascular pathology is magnetic resonance angiography [24]. It is gaining popularity because it is a safer and non-invasive alternative to digital X-ray angiography [14]. In addition, this technique avoids ionizing radiation and employs a contrast agent that is not nephrotoxic and is much less frequently associated with allergic reactions [12]. Magnetic resonance angiography (MRA) can be used with a variety of techniques. In particular, we distinguish between techniques that require contrast and those that do not [24]. One technique that does not use contrast is balanced steady-state free precession, which is a method of visualisation aneurysms. Imaging with this procedure allows differentiation of blood in the vessel lumen and thrombus. However, contrast-enhanced MRA (CE-MRA) is a more precise and reproducible technique that can be performed in seconds with relatively few artifacts, especially in comparison to non-contrast techniques [24]. Dynamic magnetic resonance (MR) imaging using three-dimensional (3D) gradient-echo with fat-suppression has become important in abdominal MR studies. Thin-segmented, multiphase, 3D contrast-enhanced dynamic MR sequences with fat suppression are potentially useful for imaging small abdominal vessels such as the IPAs [13]. These are clinically relevant because, for example, they can be a source of bleeding resulting from trauma or can be the vessels supplying hepatocellular carcinoma. Fat suppression is essential for evaluating small IPAs because high signals from fat and chemical shift artifacts impair the visualisation of these vessels. Fat suppression by increasing the contrast between enhanced vessels and low-signal fat can improve the visualisation of IPAs [13].

Computed tomography angiography is another important tool in vascular imaging. Furthermore, it is also employed to detect complications after treatment, such as thrombosis or internal leakage after aneurysm repair [18]. CTA is a quick diagnostic imaging procedure that produces images of blood vessels after injecting a contrast agent and using X-rays. Two-dimensional (2D) and 3D visualisation methods are routinely used in CTA to obtain images comparable to those obtained via catheter angiography. There are also several post-processing methods that include multiplanar reconstruction, maximum intensity projection (MIP), curved planar reconstruction, and volume rendering. Multiplanar reconstruction produces images in arbitrary planes, resulting in quantitative analysis of both the lumen and the vessel wall. However, it can only generate 2D images [20]. Curved planar reconstruction is also a 2D image, displaying a cross-section of the vessel along its entire length, which is clearly visualized [31]. Volume rendering images preserve the original anatomical spatial relationships and have a 3D appearance, so vascular interrelationships can be visualised. In contrast, MIP is valuable as an additional display, especially for imaging smaller vessels [29]. Noninvasive vascular imaging by CTA has become an increasingly relevant diagnostic technique. Multidetector computed tomography angiography (MDCTA) is a quick and precise method for vascular anatomical assessment and diagnosis of vascular abnormalities [15]. This technique allows the anatomy of the IPA to be assessed in a relatively short time, which can be valuable in planning embolisation treatment sessions [3]. Specific advantages of MDCTA vascular imaging include more accurate visualisation of details, including stenoses and the presence and location of vascular anomalies. In addition, MIP rendering is valuable as an additional display, especially when smaller vessels are imaged [29]. MDCTA can reveal the real sizes of lesions such as aneurysms, thrombi, or arterial ruptures. Advances in MDCTA technology have contributed significantly to diagnosis and treatment planning in vascular disease [15]. Owing to the variable anatomy of the IPA, preoperative diagnostic MDCTA is very helpful in planning surgical procedures. This technique is also significant in imaging the different variants of the IPA, which helps in selective catheterisation of the vessel and eliminates the need for repeated contrast injections and angiograms in different projections [3].

CLINICAL RELEVANCE

It has been reported in the literature that IPAs are involved in several disorders and pathologic conditions. We reviewed the role of these arteries in diseases and clinical management below.

Inferior phrenic arteries are the main vessels supplying the diaphragm. In addition, they constitute extrahepatic collateral arterial pathways that supply hepatic malignancies. The RIPA and LIPA constitute more than half of the collaterals involved in forming the arterial pathways supplying hepatic malignancies, the RIPA being the more common [7]. It has been estimated that RIPA is involved in 7083% of extrahepatic arteries supplying hepatocellular carcinoma. Because it runs in direct contact with the bare area of the liver, the RIPA can form anastomoses with intrahepatic arteries. This facilitates the blood supply from the extrahepatic arteries to hepatic lesions when the natural tumour supply is impaired [23]. Apart from being an important extrahepatic artery for tumours of the liver, especially those located in the uncovered part of this organ, IPA also provides the essential blood supply to lung metastases [39].

Branches of the LIPA supply blood to the stomach and oesophagus and can also be involved in arterial bleeding at the oesophagus-gastric junction and Mallory-Weiss tears [7, 27, 34].

The LIPA can also be involved in atherosclerotic ischaemic heart disease, anastomosing with trans-diaphragmatic collaterals, and the left anterior descending coronary artery. This anastomosis arises from a connection between the LIPA and pericardiophrenic musculophrenic arteries [2].

The development of IPA pseudoaneurysm also has been described in the literature [19, 25, 32]. Such disorders are a consequence of partial or complete rupture of the vessel wall, leading to haemorrhage [28]. It is worth emphasizing that IPAs can be responsible for haemoperitoneum or haemothorax as a result of their pseudoaneurysm rupture [10, 19].

The IPA can also have a role in diaphragm injury. A very rare case of diaphragmatic rupture during cardiopulmonary resuscitation has been reported. Digital subtraction angiography revealed active bleeding from a branch of the RIPA. Thus, it is important to recognize the possibility that organs such as the diaphragm can be injured during energetic cardiopulmonary resuscitation [30].

The IPAs can also have a major role in diaphragmatic hernia repair, especially when rare anatomical defects or abnormal-looking vessels are involved. Calin et al. [4] described a rare case of diaphragmatic hernia in which an abnormally-sized LIPA presented a challenge to surgery. Knowledge of IPA variants is also necessary for treating surgical and traumatic vessel injuries and haemoptysis, especially when caused by pulmonary pathologies. However, when the arteries of vital organs are stenosed, the IPAs are key to preventing the development of ischaemia in those organs [2].

CONLUSIONS

The IPA has the ability to form rich collaterals with other arteries located in the thoracic and abdominal cavities. Thanks to this, it has an important role in pathological processes, the most common of which is supplying hepatic malignancies. Moreover, the IPA can become a pathway of lung metastasis. IPA injuries almost always result in life-threatening bleeding. On the other hand, this arterial vessel has great potential for protecting vital organs when their main arteries are stenosed. The present study demonstrates that knowledge of the anatomy of human blood vessels is helpful for better understanding of physiological and pathophysiological processes.

Ethical approval and consent to participate

The cadavers belonged to the Department of Anatomical Dissection and Donation, Medical University of Lodz.

Acknowledgements

The author wishes to express his gratitude to all those who donated their bodies to medical science.

Conflict of interest: None declared

REFERENCES

  1. Ahn HJ, Lee JW, Kim KD, et al. Phrenic arterial injury presenting as delayed hemothorax complicating simple rib fracture. J Korean Med Sci. 2016; 31(4): 641–643, doi: 10.3346/jkms.2016.31.4.641, indexed in Pubmed: 27051252.
  2. Aslaner R, Pekcevik Y, Sahin H, et al. Variations in the origin of inferior phrenic arteries and their relationship to celiac axis variations on CT angiography. Korean J Radiol. 2017; 18(2): 336–344, doi: 10.3348/kjr.2017.18.2.336, indexed in Pubmed: 28246513.
  3. Basile A, Tsetis D, Montineri A, et al. MDCT anatomic assessment of right inferior phrenic artery origin related to potential supply to hepatocellular carcinoma and its embolization. Cardiovasc Intervent Radiol. 2008; 31(2): 349–358, doi: 10.1007/s00270-007-9236-x, indexed in Pubmed: 18071790.
  4. Calin ML, Arevalo G, Harris K, et al. Large sized left inferior phrenic artery and parahiatal type of diaphragmatic hernia generating confusion during robotic surgical repair. J Laparoendosc Adv Surg Tech A. 2017; 27(3): 283–287, doi: 10.1089/lap.2016.0392, indexed in Pubmed: 27585397.
  5. Downey R. Anatomy of the normal diaphragm. Thorac Surg Clin. 2011; 21(2): 273–279, ix, doi: 10.1016/j.thorsurg.2011.01.001, indexed in Pubmed: 21477776.
  6. Greig HW, Anson BJ, Coleman SS. The inferior phrenic artery; types of origin in 850 body-halves and diaphragmatic relationship. Q Bull Northwest Univ Med Sch. 1951; 25(4): 345–350, indexed in Pubmed: 14892223.
  7. Gürses İA, Gayretli Ö, Kale A, et al. Inferior phrenic arteries and their branches, their anatomy and possible clinical importance: an experimental cadaver study. Balkan Med J. 2015; 32(2): 189–195, doi: 10.5152/balkanmedj.2015.150052, indexed in Pubmed: 26167344.
  8. Gwon DIl, Ko GY, Yoon HK, et al. Inferior phrenic artery: anatomy, variations, pathologic conditions, and interventional management. Radiographics. 2007; 27(3): 687–705, doi: 10.1148/rg.273065036, indexed in Pubmed: 17495287.
  9. Hagiwara A, Akai H, Kosaka T, et al. A dorsal pancreatic artery originating from the right inferior phrenic artery. J Vasc Interv Radiol. 2016; 27(1): 143–145, doi: 10.1016/j.jvir.2015.06.010, indexed in Pubmed: 26723925.
  10. Handa A, Dhooria S, Sehgal IS, et al. Primary cavitary sarcoidosis: A case report, systematic review, and proposal of new diagnostic criteria. Lung India. 2018; 35(1): 41–46, doi: 10.4103/lungindia.lungindia_225_17, indexed in Pubmed: 29319033.
  11. Heymann G, Shin DS, Johnson GE. Accessory left gastric artery arising from inferior phrenic artery: angiographic findings in 5 patients. J Vasc Interv Radiol. 2019; 30(10): 1687–1689, doi: 10.1016/j.jvir.2019.07.004, indexed in Pubmed: 31547929.
  12. Insko EK, Carpenter JP. Magnetic resonance angiography. Semin Vasc Surg. 2004; 17(2): 83–101, doi: 10.1053/j.semvascsurg.2004.03.010, indexed in Pubmed: 15185174.
  13. Ito K, Kim MJ, Mitchell DG, et al. Inferior phrenic arteries: depiction with thin-section three-dimensional contrast-enhanced dynamic MR imaging with fat suppression. J Magn Reson Imaging. 2001; 13(2): 201–206, doi: 10.1002/1522-2586(200102)13:2<201::aid-jmri1030>3.0.co;2-l, indexed in Pubmed: 11169825.
  14. Ivancevic MK, Geerts L, Weadock WJ, et al. Technical principles of MR angiography methods. Magn Reson Imaging Clin N Am. 2009; 17(1): 1–11, doi: 10.1016/j.mric.2009.01.012, indexed in Pubmed: 19364596.
  15. Kang PS, Spain JW. Multidetector CT angiography of the abdomen. Radiol Clin North Am. 2005; 43(6): 963–976, vii, doi: 10.1016/j.rcl.2005.07.007, indexed in Pubmed: 16253657.
  16. Kim HC, Chung JW, An S, et al. Left inferior phrenic artery feeding hepatocellular carcinoma: angiographic anatomy using C-arm CT. Am J Roentgenol. 2009; 193(4): W288–W294, doi: 10.2214/AJR.09.2417, indexed in Pubmed: 19770297.
  17. Kimura S, Okazaki M, Higashihara H, et al. Analysis of the origin of the right inferior phrenic artery in 178 patients with hepatocellular carcinoma treated by chemoembolization via the right inferior phrenic artery. Acta Radiol. 2007; 48(7): 728–733, doi: 10.1080/02841850701376334, indexed in Pubmed: 17729002.
  18. Kumamaru KK, Hoppel BE, Mather RT, et al. CT angio­graphy: current technology and clinical use. Radiol Clin North Am. 2010; 48(2): 213–235, vii, doi: 10.1016/j.rcl.2010.02.006, indexed in Pubmed: 20609871.
  19. Lee JW, Kim S, Kim CW, et al. Massive hemoperitoneum due to ruptured inferior phrenic artery pseudoaneurysm after blunt trauma. Emerg Radiol. 2006; 13(3): 147–149, doi: 10.1007/s10140-006-0524-6, indexed in Pubmed: 17039340.
  20. Lell MM, Anders K, Uder M, et al. New techniques in CT angiography. Radiographics. 2006; 26 (Suppl 1): S45–S62, doi: 10.1148/rg.26si065508, indexed in Pubmed: 17050518.
  21. Loukas M, Hullett J, Wagner T. Clinical anatomy of the inferior phrenic artery. Clin Anat. 2005; 18(5): 357–365, doi: 10.1002/ca.20112, indexed in Pubmed: 15971218.
  22. Mitty HA. Embryology, anatomy, and anomalies of the adrenal gland. Semin Roentgenol. 1988; 23(4): 271–279, doi: 10.1016/s0037-198x(88)80037-3, indexed in Pubmed: 3055310.
  23. Moustafa AS, Abdel Aal AK, Ertel N, et al. Chemoembolization of hepatocellular carcinoma with extrahepatic collateral blood supply: anatomic and technical considerations. Radiographics. 2017; 37(3): 963–977, doi: 10.1148/rg.2017160122, indexed in Pubmed: 28362557.
  24. Muhs BE, Verhagen HJM, Huddle MG, et al. Theory, technique, and practice of magnetic resonance angiography. Vascular. 2007; 15(6): 376–383, doi: 10.2310/6670.2007.00052, indexed in Pubmed: 18053424.
  25. Nagar N, Dubale N, Jagadeesh R, et al. Unusual locations of pseudo aneurysms as a sequel of chronic pancreatitis. J Interv Gastroenterol. 2011; 1(1): 28–32, doi: 10.4161/jig.1.1.14597, indexed in Pubmed: 21686110.
  26. Nonent M, Thouveny F, Simons P, et al. Iodixanol in multidetector-row computed tomography angiography (MDCTA): diagnostic accuracy for abdominal aorta and abdominal aortic major-branch diseases using four-, eight- and 16-detector-row CT scanners. Acta Radiol. 2007; 48(1): 48–58, doi: 10.1080/02841850601067629, indexed in Pubmed: 17325925.
  27. Northrop CH, Studley MA, Smith GR. Hemorrhage from the gastroesophageal junction. A cryptic angiographic diagnosis. Radiology. 1975; 117(3 Pt 1): 531–532, doi: 10.1148/117.3.531, indexed in Pubmed: 1081239.
  28. Núñez DB, Torres-León M, Múnera F. Vascular injuries of the neck and thoracic inlet: helical CT-angiographic correlation. Radiographics. 2004; 24(4): 1087–1100, doi: 10.1148/rg.244035035, indexed in Pubmed: 15256630.
  29. Ozbulbul NI, Yurdakul M, Tola M, et al. Can multidetector row CT visualize the right and left inferior phrenic artery in a population without disease of the liver? Surg Radiol Anat. 2009; 31(9): 681–685, doi: 10.1007/s00276-009-0504-0, indexed in Pubmed: 19367353.
  30. Rossi UG, Ierardi AM, Cariati M. Diaphragmatic rupture with inferior phrenic artery bleeding caused by cardiopulmonary resuscitation. Clin Exp Emerg Med. 2020; 7(3): 238–240, doi: 10.15441/ceem.19.044, indexed in Pubmed: 32482019.
  31. Saba L, Mallarini G. Multidetector row CT angiography in the evaluation of the hepatic artery and its anatomical variants. Clin Radiol. 2008; 63(3): 312–321, doi: 10.1016/j.crad.2007.05.023, indexed in Pubmed: 18275872.
  32. Salem JF, Haydar A, Hallal A. Inferior phrenic artery pseudoaneurysm complicating drug-induced acute pancreatitis. BMJ Case Rep. 2014; 2014, doi: 10.1136/bcr-2013-201049, indexed in Pubmed: 24385392.
  33. Schumpelick V, Steinau G, Schlüper I, et al. Surgical embryology and anatomy of the diaphragm with surgical applications. Surg Clin North Am. 2000; 80(1): 213–239, xi, doi: 10.1016/s0039-6109(05)70403-5, indexed in Pubmed: 10685150.
  34. Smith DC, Kitching GB. Angiographic demonstration of esophagogastric bleeding from the inferior phrenic artery. Radiology. 1977; 125(3): 613–614, doi: 10.1148/125.3.613, indexed in Pubmed: 303782.
  35. So YH, Chung JW, Yin Y, et al. The right inferior phrenic artery: origin and proximal anatomy on digital subtraction angiography and thin-section helical computed tomography. J Vasc Interv Radiol. 2009; 20(9): 1164–1171, doi: 10.1016/j.jvir.2009.05.036, indexed in Pubmed: 19631560.
  36. Sperryn PN. Blood. Br J Sports Med. 1989; 23(2): 129–131, doi: 10.1136/bjsm.23.2.129, indexed in Pubmed: 2605442.
  37. Szewczyk B, Karauda P, Olewnik Ł, et al. Types of inferior phrenic arteries: a new point of view based on a cadaveric study. Folia Morphol. 2021; 80(3): 567–574, doi: 10.5603/FM.a2020.0079, indexed in Pubmed: 32710792.
  38. Zeng R, Yao Z, Chen Y, et al. Variant arterial supply to the lesser curvature of the stomach and duodenum from double inferior phrenic arteries. Surg Radiol Anat. 2015; 37(7): 867–869, doi: 10.1007/s00276-014-1392-5, indexed in Pubmed: 25380829.
  39. Zhu LZ, Yang RJ, Zhu Xu. Role of inferior phrenic artery in the interventional treatment of lung metastases tumor: a report of 11 cases. J Cancer Res Ther. 2018; 14(1): 61–67, doi: 10.4103/jcrt.JCRT_742_17, indexed in Pubmed: 29516961.

Address for correspondence: Ł. Olewnik, MD, PhD, Department of Anatomical Dissection and Donation, Chair of Anatomy and Histology, Medical University of Lodz, ul. Żeligowskiego 7/9, 90–410 Łódź, Poland, e-mail: lukasz.olewnik@umed.lodz.pl

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