\r\n\t[2] J. V. Moloney, A. C. Newell. Nonlinear Optics. Westview Press, Oxford, 2004.
\r\n\t[3] M. Kauranen, A. V. Zayats. Nonlinear Plasmonics. Nature Photonics, vol. 6, 2012, pp. 737-748.
\r\n\t[4] P. Dombi, Z. Pápa, J. Vogelsang et al. Strong-field nano-optics. Reviews of Modern Physics, vol. 92, 2020, pp. 025003-1 – 025003-66.
\r\n\t[5] N. C. Panoiu, W. E. I. Sha, D.Y. Lei, G.-C. Li. Nonlinear optics in plasmonic nanostructures. Journal of Optics, 20, 2018, pp. 1-36.
\r\n\t[6] A. Krasnok, A. Alu. Active nanophotonics. Proceedings of IEEE, vol. 108, 2020, pp. 628-654.
\r\n\t[7] M. Lapine, I.V. Shadrivov, Yu. S. Kivshar. Colloquium: Nonlinear metamaterials. Reviews of Modern Physics, vol. 86, 2014, pp. 1093-1123.
\r\n\t[8] Iam Choon Khoo. Nonlinear optics, active plasmonics and metamaterials with liquid crystals. Progress in Quantum Electronics, vol. 38, 2014, pp. 77- 117.
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Autogenous arteriovenous fistulas (AVF) are the preferred vascular access for patients with end-stage kidney disease. They are cheap and easy to construct, have excellent patency rates and require minimal maintenance by the patient and the health care staff. However, they can develop various complications, which have different rates of incidence, morbidity and mortality. Most of them threaten the functionality of the fistula and some of them even pose an immediate vital risk. We believe it is important that all health care professionals who deal with patients on whom an AVF is performed should have thorough knowledge of the types, physiopathology, risks and treatment of these complications.
Our team has performed 832 surgical constructions of autogenous AFV in the last 5 years. The number of complications that required surgical revision was 61 (7.3%). This is comparable to a 9% rate of complications reported in a study of 628 patients, by Fokou et al. in Cameroon [1]. The patients in this population have numerous comorbidities besides the end-stage kidney disease; among them, diabetes mellitus, hypertension and chronic viral hepatitis. These 4 are factors who augment the complication rate after any surgical intervention. However, the number of events requiring surgical exploration following AFV construction is relatively low, probably because of increasing experience and technical skills of vascular surgeons.
The complications can be divided in 2 categories:
Acute complications
Chronic complications
These are complications that occur in the first hours or days after the construction of an AVF and always require evaluation by a vascular surgeon.
Thrombosis of the fistula occurs when there is inadequate flow through the fistula, which leads to stasis and thrombosis. Thrombosis of the fistula occurs mostly in patients with inadequate venous run-off, i.e. history of subclavian vein catheters, multiple venous punctions with local fibrosis [2]. We do not use preoperative Duplex exam to assess the vein [3]. Local inspection at the time of surgery should be performed, and if the vein is small, fibrotic or with a visibile thrombus inside, another vein should be used. We also assess the vein by flushing it with a heparinated saline solution via a catheter; if there is resistance in advancing the catheter, injecting the solution or no backflow through the catheter, a proximal stenosis of the vein should be suspected, which leaves no alternative but using a different vein. Building an anastomosis that is too tight, restricting the blood flow, coupled with systemic hypotension can also be incriminated in acute thrombosis. We advise our patients to maintain their blood pressures in the 130-150 mmHg interval during the fistula’s maturation period. Hypotension sometimes occurs during the first hemodialysis (HD) session performed after the operation, using an indwelling HD catheter. This is the reason why a newly constructed fistula should be assessed by the medical staff at the beginning and end of all HD sessions.
Introducing a catheter on the subclavian vein of an arm with a functional AVF can lead to thrombosis, either immediate or after the first HD session.
Other causes of thrombosis are extrinsic compression of the operated arm, e.g. wearing clothes with tight sleeves or sleeping on the respective arm.
In the acute setting (during the first 12-24 hours), thrombosis can be solved by surgical thrombectomy. If, on palpation, the vein is tender, pulsatile in the initial segment but with no thrill, the vein can be opened longitudinally and a Fogarty catheter passed both distally (towards the subclavian vein) and proximally (towards the anastomosis). Flushing the vein with a heparinated saline solution is mandatory. A thrill should be obtained after removing the cross clamp. There is an increased risk of pulmonary embolism associated with this procedure, making its’ use subject to a very careful evaluation of the patient and close monitoring. In the past 5 years, only 3 patients were operated on for acute thrombosis of the fistula (0.3%) by our team – compared to an incidence of 2% in other studies [1]. All three cases preserved the AVF after thrombectomy.
Bleeding is the most common acute complication. Spontaneous bleedings are not uncommon in uremic patients, in whom the primary mechanisms of hemostasis are compromised, including thrombocytopenia, platelet dysfunction and von Willebrand factor’s changes. Chronic anemia, which is common in uremic patients, also negatively influences the rheologic component of the platelet – vascular wall interaction. All of these factors concur to the fact that, in the postoperative setting, a bleeding is unlikely to spontaneously stop.
Bleeding sources have several causes. There are smaller sources, with no significant hemodynamic impact, but with a continuous flow, generally overestimated by the patient and his family. These smaller sources are dermal, subdermal or from the subcutaneous tissue. If the patient undergoes a session of hemodialysis (HD) or heparination of the hemodialysis catheter shortly after the AVF has been constructed, bleeding is usually the norm. In our practice, we have observed that a delay of 36 hours between the operation and the HD session makes bleeding complications exceptional. We routinely recommend to all patients abstention from HD during this time period.
The wound is inspected, and if only a dermal bleeding point is found, with no hematoma, then the source is sutured under local anesthesia. This maneuver can be performed in the emergency room. Local digital compression or applying a hemostatic sponge generally does not stop the bleeding. Compressive dressings are to be avoided, as they can stop the blood flow through the fistula.
There are also larger sources, with a higher flow and a life-threatening potential. They are usually found at the site of the anastomosis or a slipped vessel ligature and are accompanied by a hematoma.
In the past 5 years, 4 of our 832 patients (0.5%) presented for bleeding requiring surgical exploration. In all the cases, the bleeding source was a slipped ligature on the distal end of the vein used for the AVF, with accompanying hematoma. The incision was reopened, the hematoma removed and bleeding source sutured. The wound was then flushed with an antiseptic solution and closed.
Although uremic patients are prone to bleeding due to their pathophysiological changes to the mechanisms of hemostasis, in our experience, the small number of bleedings and the fact that a ”mechanical” cause is found, we believe that there is no benefit in running a series of extensive tests on these patients (thrombelastogram, von Willebrand’s factor determination, clotting time etc). There is no doubt that each and every one of these patients’ coagulation pathways are malfunctioning and are unlikely to spontaneously stop a bleeding. However, we feel that good surgical technique avoid bleeding in all patients.
Hematoma formation, with or without associated active bleeding, can demand surgical exploration of the wound. There are several situations that can be encountered. A hematoma with no active bleeding through the sutures may not impart on the fistula’s functionality. If the hematoma is small and the AVF’s thrill is present, there is no surgical indication and the patient is routinely monitored. If the hematoma is larger, and the thrill is modified or absent, the hematoma must be evacuated, followed by closing the bleeding source and AVF repermeation. Sometimes, removing the hematoma can bring back the thrill; if this does not occur, thrombectomy of the AVF or even construction of a new AVF should be performed.
Hematoma associated with bleeding with dark red blood is accompanied by an alteration of the thrill, rendering it sharp, dull, short and systolic only. Surgical exploration and hematoma removal usually turn the thrill back to normal. The bleeding source is probably a slipped ligature from the distal end of the vein used for the fistula. The volume of blood flowing from the wound can appear quite high; in this situation, the patient or untrained medical personnel can interpret this as anastomosis disruption and can apply a tourniquet on the arm, which completely closes the flow through the fistula, making it unsalvageable. As previously stated, we have operated on 4 patients with active bleeding and hematoma. The bleeding source was found to be a slipped ligature on the distal end of the vein. In 2 patients, a tourniquet had been placed on the arm prior to presentation, so the fistula could not be salvaged, but only the bleeding stopped. In the other 2 cases, the fistula was preserved and later matured and was used for HD.
Hematoma accompanied by bright red blood oozing through the sutures has an arterial source – at the anastomotic level or a collateral arterial branch. The flow through the fistula is severely compromised due to the compression, leading to venous and possibly arterial thrombosis. After suturing the source, arterial and venous thrombectomy with a Foley catheter are performed; making sure not to injure the arterial or venous wall with the balloon catheter.
These are complications that occur days or months after the construction of an AVF.
Thrombosis is caused by inadequate flow through the fistula, which leads to stasis. Causes of inadequate flow are discussed earlier. Other causes include intimal hyperplasia of the anastomosis, thrombosis of a venous pseudoaneurysm with consecutive thrombosis of the whole vein and extrinsic compression of the vein during its’ maturation period (for example, during sleep) [4] [5]. If the patients presents promptly, an attempt to salvage the fistula can be made via a surgical thrombectomy with a Fogarty catheter [6] [7]; if the vein has aneurysmal changes, it is probably not amenable to surgical treatment. If the fistula is unsalvageable, a new one must be constructed under the protection of a temporary hemodialysis catheter.
Anastomotic pseudoaneurysm is a rare complication with severe consequences, which requires emergency surgery. In our group, 7 patients (0.8%) developed this complication. A pseudotumoral, pulsatile mass appears at the level of the incision used to create the fistula; this mass is tender, increasing in size and may be painful. The overlying skin has inflammatory and necrotic modifications. A septic process is quite always involved, which disrupts the anastomosis. The origin of the infection can be intraoperative or a clinically silent infection in a patient wearing a HD catheter. The main risk is of overlying skin necrosis with massive bleeding. Surgical exploration is mandatory. Usually, a partially thrombosed false aneurysm is found, with partial anastomosis disruption. A fragment of the pseudoaneurysm’s wall is sent for a bacteriological exam and a full course of antibiotics is given after the operation.
Further action depends on the artery used for the fistula and the patient’s general condition. If the radial artery is used, it is ligated; we have seen this scenario in only 3 cases and there were no ischemic complications after interruption of the radial artery. In the case of the brachial artery, which has a higher ischemic potential, the main goal is pseudoaneurysm removal and rebuilding the arterial continuity. This can be performed via a termino-terminal arterial anastomosis (as one of our patients has received) or by a venous graft interposition, using either an arterialized venous segment, or with a greater saphenous vein segment, if there are signs that the arterialized vein is infected. In cases with severe septic potential and aggravated general condition, the brachial artery can be ligated. Three of our patients received this treatment, fortunately without secondary ischemic events.
Venous aneurysm occurs in uncorrected hypertensive patients, months or years after fistula construction, irrespective of the fact that the fistula has or has not been used for HD (figure 1). The incidence of this complication was 3.6% (30 patients) in our group and 4.2% in the group from Cameroon [1].
\n\t\t\tAneurysm of the cephalic vein in a patient with a radio-cephalic fistula
A Doppler examination of the aneurysm shows turbulent blood flow and parietal thrombus (figure 2). The natural evolution of this complication is with total thrombotic occlusion or spontaneous rupture. Other associated processes are thrombophlebitis, infection, skin necrosis with imminent perforation and hyperdynamic syndrome[8]; these all require surgical treatment. Also, a quickly evolving aneurysm requires surgical intervention. Otherwise, the undilated segments of the fistula can be used for hemodialysis access[9].
Aneurysm of the cephalic vein with parietal thrombus
The fistula is ligated and a new one is constructed using a different vein. The aneurysm can be removed or left in place. Further control of blood pressure values ensures that the new fistula does not develop the same complication.
Among the 30 patients venous aneurysms in our group, we operated on 21. The fistula was ligated and a new one created with an available vein. These new fistulas developed no aneurysm once the blood pressure valued were kept in the normal range.
Venous pseudoaneurysm develops due to a common mistake made in hemodialysis services, which is repeated punctions at the same site. In time, the arterialized vein can grow to impressive sizes, develop a false aneurysm with partial or complete thrombosis. After repeated punctions, the overlying skin undergoes fibrotic changes, followed by necrosis, with a high risk of disruption and massive bleeding. This potential course of events makes surgery mandatory as soon as possible. The most common intervention is fistula ligation, followed by creating a new fistula with a different vein. In selected patients, who have no aneurysmal thrombi on Doppler exam or on palpation, a reductional plasty of the aneurysm can be performed. The entire aneurysm is exposed through a longitudinal incision, followed by proximal and distal cross clamping and wedge resection of the anterior wall of the aneurysm. The vein is rebuilt with a 7-0 Prolene continuous suture. The proximal segment of the vein can be used for HD after 36 hours and the dissected segment, after 3 weeks.
Eight of our 832 patients (0.9%) presented for venous pseudoaneurysm and were operated on immediately. We performed fistula ligation in 5 cases, followed by creation of a new fistula after 3 weeks, during which time the patient underwent HD sessions via a temporary catheter. In the other 3 cases, after assessing the pseudoaneurysms with palpation and Doppler exam, we found them suitable for remodeling and a reductional plasty was performed in the described manner.
Skin necrosis also develops at the site of repeated punctions. It occurs after superficialization of a basilic or brachial vein, if the wound had been closed with a thin layer of skin overlying the fistula (figure 3). This heals poorly between HD sessions, as it has an inadequate blood supply, and becomes even thinner and necrotic; the venous wall is also thin and very fragile. Bleeding is the risk with this complication, and can be massive, life-threatening due to the high flow through the fistula (figure 4).
\n\t\t\tSkin necrosis at the level of a superficalized basilic vein
Bleeding from the necrotic skin area
Surgical treatment involves the bleeding point skin suture, then making a circular incision around the necrotic segment and carefully dissecting it away from the vein, without entering the vein.
Then the hemostasis can be easily performed with a 5-0 Prolene suture and the necrotic skin removed. The skin is then approximated with interrupted Prolene sutures. If bleeding occurs, the assistant compresses the fistula at the anastomotic level and proximally, on the arm, until hemostasis has been performed with interrupted 5-0 Prolene sutures. We routinely give an antibiotic regimen to our operated patients, usually 2 grams of Oxacillin per day, for 5 days.
We have seen this complication in 3 of our 832 patients (0.3%). Two of them bled from the necrotic area before presenting to the hospital. They were all operated on and made an uneventful recovery.
Hand ischemia is the most serious complication of vascular access surgery. The patients have all the clinical manifestations of chronic limb ischemia: muscular atrophy of the thenar and hypothenar eminences with functional impotence of the fingers, cold extremities, pain at rest, which becomes excruciating during HD sessions [10]. Gangrenous changes of the fingers are sometimes present (figure 5).
\n\t\t\tIschemic hand and necrosis of the fingers in a patient with a brachio-cephalic fistula
The patient is usually diabetic and has atherosclerotic lesions distal to the anastomosis. Blood flow is diverted through the vessel with a lower resistance, which is the vein – the “steal syndrome” [11]. Under normal conditions, when the radial artery is used for the fistula, the hand is still supplied with blood via the ulnar artery and the vascular arcades of the hand. However, there are cases when the arcades have clinically silent lesions (i.e. negative Allen test), which become significant if the distal radial artery is interrupted while constructing the AVF. This is why we attempt to maintain the distal radial artery open after creating the fistula. Hand ischemia can also occur if the brachial artery is used and is usually more serious.
All attempts should be made to salvage the limb firstly, and the fistula, secondly. The most direct and simple technique is outflow ligation. The vein is exposed close to the anastomosis and doubly ligated with a number 5 Nylon tape. The thrill should disappear and distal perfusion is immediately improved, with quick remission of symptoms. The major drawback is that the AVF is lost for further access.
Other AVF preserving techniques aim to decrease the flow through the fistula. These are banding of the vein, prosthetic graft interposition (ePTFE nr.5) and venous by-pass using the accessory radial vein. These techniques will be discussed in the hyperdynamic syndrome paragraph.
The DRIL procedure (Distal Revascularization Interval-Ligation) has been described by Schanzer in 1988 [12]. The artery is ligated distal to the anastomosis. An arterio-arterial by-pass is performed between the proximal artery (usually, the brachial artery) and the distal arterial territory (usually, the radial artery). Immediate technical success rates are excellent, with an overall reduction in ischemic events; however, if graft failure occurs, the entire distal extremity is at risk of gangrene and may require amputation [13][14].
In patients with a brachio-cephalic fistula and pseudoischemic symptoms accompanied by venous engorgement, we have found a patent accessory radial artery, which originates high in the arm, from the cephalic vein. This vein had a retrograde flow which impeded the venous outflow of the cubital region and the forearm. Ligation of this vein led to the disappearance of the venous engorgement and the ischemic symptoms.
Hand ischemia can also have technical reasons, if the anastomosis causes reduction in diameter or even occlusion of the distal brachial artery. In this setting, the fistula is also sacrificed, this time by ligation followed by arterial reconstruction at the site of the anastomosis.
This complication occured in 7 of our 832 patients (0.7%). We were forced to ligate the fistula in 6 cases and perform vein banding in one other case. There have also been cases of ischemia associated with hyperdynamic syndrome; these cases will be discussed below.
Hyperdynamic syndrome is a consequence of greatly increased blood flow through the fistula, with consecutive volume overload of the right heart and cardiac failure. It is a relatively rare complication and can occur irrespective of the age of the fistula. It is associated with brachial artery use, which has a larger diameter and thus a higher flow (1-1.1 L/min) when compared to the radial artery (0.65 L/min) [15] [16] [17]. After the maturation period, Doppler examinations show flows of 8-10 L/min through the fistula. Local examination shows venous dilatations and the patients are restless and show dyspnea, orthopnea and sinus tachycardia [18]. Almost all of them are hypertensive, with uncorrected BP values in spite of treatment. The aim of the surgical treatment is to decrease the flow through the fistula.
Fistula closure promptly makes this syndrome disappear. However, this means that the heart has to rapidly adapt to new hemodynamic conditions (with severely decreased venous return). Transient bradycardia, hypotension and syncope can occur. With this patients subgroup, we always ligate the fistula under close monitoring (EKG, blood pressure and SpO2).
As previously stated, there are also techniques which aim to preserve the AVF. Banding the vein decreases the vein’s diameter and thus increases the resistance flow and decreases the flow. The vein is dissected and encircled with a tape which is progressively tightened until the thrill becomes less intense, the heart rate drops below 100 beats/minute and the dyspnea gets clinically better. It is sometimes difficult to establish a precise amount of banding that prevents the steal syndrome but still allows fistula patency. In the setting of reduced flow that results from fistula banding, thrombosis can occur with further transient flow decrease, for example in hypotensive states [15][19]. Also, in our experience, banding offers only a momentary decrease of symptoms. For this reason, we prefer to use alternate techniques and have used this technique in only 3 patients in the last 5 years.
Prosthetic graft interposition uses a nr.5 ePTFE graft, which obviously has a much smaller diameter than the arterialized vein and thus a higher resistance. A 4-5 cm segment of the vein is dissected; 3-5 cm are removed and the graft is interposed via 2 end-to-end anastomoses. Approximating the end of the vein and the graft can be difficult, due to the difference in size. Alternatively, the vein can be left in place and the graft sutured via 2 end-to-side anastomoses, followed by ligating the fistula between the 2 anastomoses. This eliminates the size-mismatch. The surgeon must resist the urge of using a larger graft, as this does not reduce the flow in a significant manner.
To decrease flow, we have also created a venous by-pass using the accessory radial vein. This is usually found in the forearm, where it merges with the median cephalic vein, creating the cephalic vein. But there are cases when it has a high origin, in the arm, lateral to the cephalic vein. Even after arterialization of the cephalic vein, this branch maintains a small diameter and can be used to divert the blood flow from the larger cephalic vein (figure 6).
Accessory radial vein with a high origin in a patient with a brachio-cephalic fistula
During surgery, it is dissected from its’ origin in the cephalic vein for a distance of 5 cm, then anastomosed end-to-side to the cephalic vein after the arterio-venous anastomosis. The cephalic vein is then interrupted between the newly created anastomosis and the origin of the accessory radial vein (figure 7). The patients receive one week of antibiotics after the intervention.
The anastomosis is complete and the cephalic vein is ligated distal to the anastomosis
In 4 of our patients (0.4%) we performed a by-pass with a PTFE graft; 3 other cases (0.3%) received a venous by-pass. The results of by-pass (either using a prosthetic graft or the accessory radial vein) are very good at short and mid-term follow-up. Heart rate is maintained at less than 100 beats/minute with great clinical improvement. Doppler echography shows diminished flows, of 4-5 L/min. The fistula remains functional with no residual steal syndrome. In conclusion, the surgical treatment that we favor for hyperdynamic syndrome is venous by-pass with the accessory radial vein, whenever available; if not, graft interposition is the next option.
Hand edema is a relatively frequent, but usually transient complication in vascular access surgery. It is more frequent when the superficial veins have been used up and a brachio-brachial fistula is constructed. Venous hypertension occurs shortly after AVF creation, but it diminishes after collaterals develop and outflow improves. Outflow obstruction due to stenosis of a central vein provoked by a long-term indwelling catheter or by neointimal hyperplasia from the turbulent flow of the AVF also cause venous hypertension. Sometimes, venous tributaries become dilated, incompetent and perfuse retrograde toward the forearm and the hand, thus increasing the capillary pressure. If the hypertension does not subside, it is accompanied by the classic symptoms of a venous stasis syndrome: edema, pigmentation and ulceration. The whole upper extremity can become involved in the edema, which sometimes includes the chest wall and the breast. A rich collateral venous circulation also develops. There are rare cases when the edema is so important that it produces ischemic phenomena. Treatment consists of repair of the fistula outflow or ligation of the fistula; improvement is immediate and dramatic, with edema reduction and healing of ulcerations within 1-2 weeks.
We have seen no cases of edema requiring surgical correction during the past 5 years.
Lymphorhea is a relatively rare complication (<1% of operated patients)[7]. Patients with a thick layer of subcutaneous tissue, which has been extensively dissected, complicated with postoperative upper arm edema sometimes develop it. We have never seen it in conjunction with radio-cephalic fistula. In our experience, it is more frequent with the brachio-brachial fistula. The wound closes and heals following several (sometimes daily) sessions of HD, and frequent changing of dressings. If a septic process develops, surgical debridement and antibiotherapy become necessary.
Infection is a rare complication with severe repercussions [20]. In the past 5 years, only one of our patients developed it (0.1%). If intraoperative contamination occurs, after a short period of time the wound becomes inflamed, painful, with purulent discharge, accompanied by fever. Vascular access creation is forbidden in a patient which carries a HD catheter but presents with fever and leucocytosis; in this case, the anastomosis becomes infected due to bacteremia and is extremely susceptible to disruption. These patients should be postponed until a new catheter is implanted in a different site and the old catheter removed and its’ tip sent for bacteriological examination, followed by proper antibiotherapy. The most common infectious agents encountered are S. aureus and S. epidermidis. Reinterventions for bleeding or fistula thrombosis also increase the risk of infection. The higher the number of reexploration, the higher is the chance of acquiring an infection. For this reason, we believe that the maximum number of reinterventions is 2 in 24 hours. If the fistula is not functional after these 2 reinterventions, we wait until the incision heals before trying to create a new fistula using the same incision. Late anastomotic pseudoaneurysm formation is also a septic complication, which can develop even if the incision is healed.
If the wound shows a purulent discharge, the patient must be evaluated by a vascular surgeon. There are 2 therapeutic options. The conservative one is drainage of the collection, followed by washing with an antiseptic solution. A more aggressive option is closure of the fistula, also followed by antiseptisation of the wound. For a radio-cephalic fistula, the radial artery can be ligated without any ischemic consequences. For a fistula using the brachial artery, the fistula must be closed and arterial reconstruction performed. In the setting of acute bleeding, with fragile arterial wall, arterial ligature is mandatory; ischemic phenomena may occur, but this is not the rule.
In all cases, antibiotherapy is indicated.
Rice is such an agricultural commodity that covers the third-highest worldwide production making it one of the most important cereal crops [1]. With its wide geographic distribution extending from 50°N to 35°S, rice is expected to be the most vulnerable cultivated crop to changing climates in future [2, 3]. Rice production is dwindled mainly because of biotic and abiotic stresses due to the complexity of interaction between the stress factors and various molecular, biochemical and physiological phenomena affecting plant growth and development [4, 5]. To battle with these situations, development of adaptive rice varieties is one of the best strategies. Since aboveground parts are often taken into consideration for making stress tolerant varieties, root study remains backward in this aspect. Roots, the hidden portion of the plant have not yet been much focused. Because exploring the root traits of the plant are much more difficult compared to its above-ground traits. But when it comes to the fact of studying the optimal developmental plasticity system and characteristic features of plant growth, the root system is given the first priority [6]. Root system is the site of water and nutrient uptake from the soil, a sensor of abiotic and biotic stresses, and a structural anchor to support the shoot. The root system communicates with the shoot, and the shoot in turn sends signals to the roots [7]. Soil type, moisture and nutrients all strongly influence the architecture of the root system [8, 9, 10]. Recently it has been emphasized that root architectural traits play a decent role for the adaptation of crop varieties under different abiotic stresses [11, 12]. Root interaction with changing environment is a complex phenomenon that differs with genotypes and intensity of stress [13, 14, 15, 16, 17]. For that, different species and also genotypes under the same species may respond contrarily under stress conditions and show different magnitudes of tolerance or susceptibility to stress. These diversities can be exploited by plant breeders to improve stress tolerance in plants. Scientists assume that selection for yield will indirectly select for varieties with the optimum root system. But the fact is, more directed selection for specific root architectural traits could enhance yields for different soil environments [18]. As by 2035, a predicted 26% increase in rice production will be essential to feed the rising population [19], it is imperative to develop high yielding rice cultivars with efficient root systems for better exploitation of natural resources under stressed conditions.
\nBeing the hidden half of the plants, the root system performs several functions like water and nutrient acquisition, mechanical support to the plant and storage of reserve assimilates [7]. In plant, roots are the first organ for sensing the water limitation and the roots are also the signal transmitter to other plant parts through xylem sap and phytohormone which is known as one of the most important root-shoot stress signal mechanism [20, 21, 22, 23]. Development of the root system is a major agronomic trait and proper architecture in a given environment permits plants to survive in water and nutrient deficit conditions and gives the ability to utilize minimum resources efficiently [6].
\nCrop loss in rice production has become severe now-a-days due to abiotic stresses. Therefore, having a clear knowledge about the architecture and development of roots of rice toward optimizing water and nutrient uptake has become crucial for exploitation and manipulation of root characteristics for enhancing yield under unfavorable conditions [24, 25]. In general, root study comprises the study of the entire root system or a large portion of the plant’s root system [26, 27]. To understand the functional characteristic of root system and the necessity to exploit heterogeneous environment, root architecture study has become crucial in plant productivity as root system architecture is strongly linked with plasticity to the plant through which plant can alter its root structure according to its heterogeneous environment [26].
\nElongation and branching are the mode of plant root growth. Local environmental conditions, physiological status of the plants and the type of root determine the magnitude and direction of root elongation [6]. Root system architecture (RSA) is thus the three-dimensional geometry of the root system including the primary root, branch roots, and root hairs [6, 26, 28, 29]. Topological, distributional and morphological features combine to form the root system architecture [8, 26, 30]. Topology denotes the branching pattern of individual roots including features like lengths and diameters, number of roots originating from a node, root insertion angles, magnitude and the altitude of root [31, 32]. Measures of the spatial distribution of roots simplify the dissection of root systems [26]. Root morphology refers to the external features of a root axis and may include properties of roots hairs, root diameter and trend of secondary root emergence. Acceleration or inhibition of primary root growth, increment of lateral roots (LRs) and a rise in root hairs and also the formation of adventitious roots are the ways of modification of root system architecture. The primary root is formed during embryogenesis. This primary root produces secondary roots those in turn produce tertiary roots [6, 33]. Root system architecture has proved to be a critical factor in plant survival, contributing to water and nutrient acquisition efficiency and competitive fitness in a given environment [34]. Composition of soil specially water and mineral nutrients availability and plant species have impact on root architecture [6].
\nMonocot cereals have a complex fibrous root system consisting of an adventitious root (ARs) bunch. Adventitious roots originate from the shoot or subterranean stem. This type of root is sometimes referred to as a nodal or crown root [35]. Root systems of rice plants (Oryza sativa L.) comprise numerous nodal roots of relatively short length: a mature rice plant usually has several hundreds of nodal roots, most of which are less than 40 cm in length [36]. Rice (Oryza sativa L.) is a model cereal crop with seminal roots that die during the growing period [36]. Thus, lateral roots and adventitious roots are the key determinants of nutrient and water use efficiency in rice [37].
\nSeveral embryonic and postembryonic roots including the radicle, the embryonic crown roots, the postembryonic crown roots, the large lateral roots (L-type), and the small lateral roots (S-type) [38] form the rice root systems (see Figure 1). Lateral rice roots can appear on any primary root, including embryonic and crown roots, and can be classified into two main anatomical types [39]. Numerous small lateral roots (S-type) are thin with determinate growth that can be formed from large lateral roots (L-type) and they never bear any lateral roots. Whereas large lateral (L-type) roots are few in number, thinner compared to primary roots that show indeterminate growth. Additionally, lateral elongation of small lateral roots and downward elongation of large lateral roots indicate non-responsiveness of the small lateral roots to gravity. Higher orders of branching can also be observed in the large lateral roots of the crown roots that emerge at later growth stages [40]. These small and large lateral roots exhibit differential growth and lateral root bearing pattern signifying unlike purposes for these two types of lateral roots [37].
\nA typical root system architecture at the tiller axis of Oryza sativa L. Black disks indicate individual root bearing phytomer with progressive development chronologically from top to downward. Root hairs form on main axis and all the lateral roots [41].
The concept of a phytomer was established around 6–7 decades ago [40, 42]. Clear knowledge about phytomer is required for better understanding of plant development and architecture. Many higher plants, including rice, are composed of successive stem segments called phytomer [43, 44, 45]. Each phytomer consists of an internode of the stem with one leaf, one tiller bud and several adventitious (nodal) roots [36]. The phytomer concept has long been recognized among grass scientists [46, 47]. The coordinated development of stem, tiller bud, and adventitious roots in each phytomer corresponds to the phyllochronic time in rice [43, 44, 48]. This indicates that genotypic variation in root-and-shoot growth can be ascribed to the variation of stem and adventitious root development at the phytomer level [49].
\nDetailed study of root morphology and architecture at the phytomer level become more obvious with the attainment of new knowledge about segmental architecture of poaceous crops [50, 51, 52, 53]. As the higher plant structure is formed by the repetitive unit of plant growth called phytomer [54], so phytomer formation, its growth and senescence ultimately determine development of plant canopy [47]. Therefore the phytomer components have become the interest of the plant breeder.
\nRoot axes of rice plants serve functions of anchorage and typically establish overall root system architecture [55]. The lateral roots are the functionally active part of the root system involved in nutrient acquisition and water uptake. The size, type and distribution of lateral roots eventually decide the ultimate length and surface area of an individual root and finally of a whole tiller. Understanding morphology of the lateral roots is therefore important to develop rice cultivars with an efficient root system [11, 56].
\nIn rice, there are two types of lateral roots; long and thick roots, and short and slender roots [57, 58, 59]. It has been designated that the first type as L-type and the latter as S-type [60]. The L-type lateral roots are usually long and thick and are capable of producing higher-order lateral roots, whereas S-type ones are short, slender, and non-branching. In rice plants, these two types of lateral roots are visually distinguishable. The L-type lateral roots show basically identical tissue arrangement with seminal and nodal roots, whereas S-types are anatomically different wherein their vascular systems are simplified [35].
\nIn rice plants, the observed average diameter of S-type lateral roots (first-order) that were produced on mature nodal roots of a one-month-old plant was 80 μm, whereas that of L-type roots was almost double that, i.e., 159 μm. Average length was 7.6 mm for S-type and about 30 mm for L-type. The S-type laterals were almost similar in length, and only very few S-type laterals exceeded 10 mm in length. The L-type laterals varied greatly in length and some of them elongated to more than 300 mm [60]. The small laterals are less effective in water and nutrient uptake than even root hairs [61].
\nThe changes in lateral root development were triggered by changes in water status in the root zone, and these developmental changes were induced by genetic [62, 63] and environmental factors. With regard to the environmental factors, it is shown that phenotypic plasticity promoted lateral root development and that nodal root production was the key trait that ensured stable growth of rice plants grown under changing soil moisture levels [64]. As far as the literature explored, developmental morphology of the individual roots with special reference to different lateral root branches was not studied in detail, probably due to lack of the most appropriate tools and methods [11].
\nRoot hairs are tubular-shaped cells that arise from root epidermal cells called trichoblast; they are thought to increase the absorptive capacity of the root by increasing the surface area [65]. Root hairs contribute as much as 77% of the root surface area of the cultivated crops, forming the major point of contact between the plant and the rhizosphere. Root hair is a long and narrow tube like structure originating from a single cell through tip growth (the deposition of new membrane and cell wall material at a growing tip). For being the major water and nutrient uptake site of plants, root hairs form a progressively significant model system for development studies and cell biology of higher plants [66]. Root hairs had the highest contribution toward total length and surface area of an individual root whereas main axis and first order laterals mostly contributed root volume [11].
\nRoot hairs are localized for many water channels [67], phosphate [68], nitrogen [69], potassium [70], calcium [70], and sulfate transporters [71], all of which are beneficial to water and nutrient uptake by plants [72]. There is significant inter- and intra-specific variation exists for root hair traits, and this has been linked to P uptake. Plants with longer, denser root hairs exhibit greater P uptake and plant growth in P-deficient soils [73, 74, 75]. So, the root hair traits, especially root hair length can be exploited in breeding for improved nutrient uptake and increased fertilizer use efficiency [76]. Considerable researches support an important role for root hairs in P attainment [73, 74, 75, 77, 78]. Root hair length and root hair density (which is usually correlated with root hair length) have clear value for the acquisition of P and probably other diffusion-limited nutrients such as K and ammonium [79].
\nUsually root hair traits have a low heritability and their expression is influenced by soil type resulting in lack of research in this field [6, 80, 81]. It has been proposed that plasticity in root epidermis development as a response to a variety of environmental conditions might reflect a function of root hairs in sensing environmental signals, after which plants adjust themselves to the stress conditions, such as by increasing nutrient acquisition and water uptake or by helping to anchor the plant to the soil [82, 83, 84, 85, 86, 87]. Root hair elongation increases root surface area. Root surface area increment is a common phenomenon when the plants are subjected to the stress condition like salinity, drought or other abiotic stresses [79, 88, 89, 90, 91].
\nPlants recurrently face several stresses like salinity, drought, submergence, low temperature, heat, oxidative stress and heavy metal toxicity while exposed to the nature. Growth and grain production in cereals is often limited by these stresses under field conditions. All these stresses either directly or indirectly impose osmotic stress to plants that ultimately affect the final yield of rice. Root is the first part which can sense these stresses better than other plant parts. So researchers prioritize the fact of understanding the root adaptive responses of plants upon osmotic stress. In the last 30 years, comprehensive studies have been performed focusing on architecture and developmental morphology of roots and their genetic and molecular basis [11]. Morphological and anatomical development of the rice root system was thoroughly reviewed [92] whereas the mystery of root length was also reviewed [93]. A recent study highlighting the growth, development and genetic reasons of root morphology and function of crop plants was provided by [94]. An outstanding study on root system architecture and its molecular and genetic background also greatly contributed to the relevant literature recently [37]. The physiological background of root branching was also studied [7, 33]. The root parameters that are focused by the studies comprising root anatomy, plant height, root-shoot ratio, length, diameter, density, surface area and volume of root, root elongation rate, root branching, expansion of root regarding tiller development, maximum root depth, distribution pattern of root in soil column, root hydraulic conductivity, hardpan penetrability, all of which possess innumerable functional implication [95]. Roots of large diameter show greater penetration ability [96, 97, 98] and branching [8, 99] because of having larger radii of xylem vessel and poorer axial resistance to water flux [100].
\nWater is essential for survival and plant growth. As a sessile organism, plants constantly encounter water deficit, which is the most severe environmental stress limiting plant growth and productivity in natural and agricultural systems [101, 102]. Thus, water stress tolerance has been a fundamental scientific question in plant biology.
\nPlants have evolved complex adaptive mechanisms that enable them to survive drought conditions. Over more than five decades, researchers have identified osmotic adjustment, antioxidant protection, and stomatal movement as key adaptive mechanisms for survival where both osmotic adjustment and reactive oxygen species (ROS) are involved in this plastic development process [103]. To cope with the changing water status in the growing environment, plants have evolved various adaptive mechanisms by which plants can modify root allocation and root system architecture to obtain more water [104].
\nNumerous studies have provided evidence to show that when plants are subjected to water stress, root growth is strongly inhibited, although root development is less sensitive to water stress than that of shoots [105, 106, 107].
\nRoot system architecture is regulated by osmotica [108]. The osmotic potential of the soil alters the depth of the root system, its overall mass, the rate of root elongation and the number of lateral roots in many plants, including Arabidopsis [8, 9, 107, 109, 110].
\nRoot length, root dry weight, and root production are limited by drought stress [111, 112]. Roots are the significant plant part which increase plant adaptability power to soil water deficits by maintaining water uptake under dry conditions [113]. Root and other root components such as root hair, root-shoot ratio, and root length are found to be decreased in drought sensitive varieties. But the resistant varieties which possess tolerance capacity against drought showed increase in root hair, high root to shoot ratio and root length [114]. Roots are considered as the most efficient plant organ which helps plant to uptake water and minerals from the soil and during drought stress. Root proliferation and changes in root parts occurs to take more water from deeper regions of the soil [25]. Different types of changes are observed in root growth of drought resistant rice varieties such as a deeper and highly branched root system than drought- sensitive varieties [115]. Plant also extends its roots for more nutrients (such as phosphorus) and water uptake which results in more root to shoot ratio [116]. In recent years breeding for developing larger and more efficient root systems has become the hotspot in research in some crops such as rice, as there is a relation between root system size and tolerance to water stress [81, 117].
\nThe change in lateral root development, i.e. in the plasticity of the root system, exhibited under water deficit conditions may play an important role in drought stress tolerance [35]. From an agronomical view, the knowledge about lateral root development is useful for breeding varieties with drought stress tolerance [118].
\nThe importance of root system structure is particularly recognizable when its significance in relation to its function is clearly identified. The significance of root system structure in nutrient and water uptake was stressed in previous study [119].
\nUnder waterlogged conditions, the plant roots have to function in anaerobic soil, and there are at least two morphological adaptations that roots exhibit in response to anaerobiosis, i.e., development of new adventitious roots [120, 121] and superficial rooting (i.e., the concentration of new root growth in the upper layers of the soil) [122]. Nodal root production (increase in number) continued to take place, however, in the sense that when adventitious roots in the lower nodal position of the plant’s stem die due to waterlogging injury, new adventitious roots appear at the next highest nodal position. There appears to be a direct relationship between the death of older adventitious roots and the development of new ones. Progressively waterlogged plants generally show smaller root system size than those grown in a well-drained condition. It is considered that the turgor pressure affects the cell elongation and growth of plants [123, 124]. Aerobic cultivars of rice have greater ability for plastic lateral root production than irrigated lowland cultivars under transient moisture stresses [125].
\nWe have a little understanding of the responses of roots and root hairs to salinity stress and their function in stress tolerance. The efficient root system can either avoid or lessen the osmotic stress. Usually, growth, morphology, and physiology of the roots alter first under salinity stress and the whole plant is then affected. Therefore, the responses and characteristics of the roots under saline conditions are of primary importance for plant salt-tolerance [126]. It is supposed that root morphology affects salt accumulation around the roots impeding uptake of water from saline areas. Modification of root morphology has a big potential to develop crop salt tolerance [127]. Root hairs have higher sensitivity to salt than other root traits and shoots [128]. Environmental factors also regulate the root hair development [128]. The development of root epidermal cells has great plasticity where the differentiation programs can be switched from one to another in response to external factors [17]. Plasticity in development of root epidermis as a response to a variety of environmental conditions might reflect a function of root hairs in sensing environmental signals, after which plants adjust themselves to the stress conditions [82, 84, 85, 86, 87, 129].
\nRoot hair growth and development and their physiological role in response to salt stress are largely unknown [128]. The development of root epidermis cells has great plasticity where the differentiation programs can be switched from one to another in response to external factors [17]. Root hairs have higher sensitivity to salinity than do roots and shoots [128]. Systematic study on root hair plasticity induced by salt stress and the possible role in plant adaptation/tolerance to salinity is still lacking [128]. Usually root hair traits have a low heritability and their expression is influenced by soil type resulting in lack of research in this field [6, 80, 81].
\nEarlier many scientists had reported root morphology and its distribution were greatly varied based on genotypes of plant species [13, 14, 15, 16]. There is widespread evidence that root architecture and different root characteristics of many crop species varies among genotypes [14, 130, 131, 132, 133]. In a few quite recent studies, the importance of studying root architectural traits has been emphasized for the adaptation of the crop varieties to various abiotic stress conditions. Genotypic variation has a significant role in adapting the adverse environmental and edaphic effects [14]. Inter- and intra-species variations in root architectural traits are very useful to breed the crops for root features optimum for diverse environmental conditions [134, 135, 136].
\nRoot anatomical and morphological traits have been well studied in rice [92]. Varietal differences in root morphological characteristics such as length and thickness have been reported in cultivated rice (Oryza sativa L.) in various studies [11, 14, 41, 137]. In general, the roots of upland rice cultivars are thicker and penetrate more deeply into the soil than those of lowland cultivars [14]. Root distribution has also been quantitatively characterized by using several traits, including root length, volume, and density in the soil at different depths, and these characteristics differed among cultivars [92, 138, 139, 140].
\nUnderstanding and improvement of root system and its genetics plays a pivotal role to become self-sufficient and to achieve sustainability in rice production. Actually more yields from the limited input rely on our capability to unambiguously manipulate the plants. And exploring the diversity of root architecture both in genetic and phenotypic basis will directly connect to this concern. Although great strides have been made to understand the root morphology but in future, more intense investigations to elucidate the functional implication of root morphological variation may aid in selection of root system with anticipated characteristics.
\nFuture exploration of stress responses regulated by roots at cellular or tissue level will open the door of further breeding research. Besides the modern gene pools, exploration of genes and alleles in wild relatives and landraces will also provide interesting features that will be easier to transfer to cultivated rice. Further it is important to have a better understanding on the epigenetic regulation of roots and root development under stressful conditions. There will be a need for high throughput phenotyping systems coupled with automated data analysis for accelerating the development. Endorsement of approaches including both root ideotype-based screening and selection for grain yield may establish a fruitful screening system. Alongside designing new genetic screening methods based on a better knowledge of the integrated stress responses will be also appreciated. Dynamic root/soil interaction modeling will aid in integrating different functional parameters (e.g. water uptake per length of root) under a variety of environmental conditions. Overall the root system being less accessible and more complex than other agronomic traits, achieving the ambitious goal of future rice root research, coordinated effort and joint resources are required. The sensible and appropriate efforts will have a crucial role to play in future crop production in vulnerable climate and resource scarcity prioritizing the objective of serving food to 9 billion world populations by the year 2050.
\n“The authors declare no conflict of interest.”
Edited by Jan Oxholm Gordeladze, ISBN 978-953-51-3020-8, Print ISBN 978-953-51-3019-2, 336 pages,
\nPublisher: IntechOpen
\nChapters published March 22, 2017 under CC BY 3.0 license
\nDOI: 10.5772/61430
\nEdited Volume
This book serves as a comprehensive survey of the impact of vitamin K2 on cellular functions and organ systems, indicating that vitamin K2 plays an important role in the differentiation/preservation of various cell phenotypes and as a stimulator and/or mediator of interorgan cross talk. Vitamin K2 binds to the transcription factor SXR/PXR, thus acting like a hormone (very much in the same manner as vitamin A and vitamin D). Therefore, vitamin K2 affects a multitude of organ systems, and it is reckoned to be one positive factor in bringing about "longevity" to the human body, e.g., supporting the functions/health of different organ systems, as well as correcting the functioning or even "curing" ailments striking several organs in our body.
\\n\\nChapter 1 Introductory Chapter: Vitamin K2 by Jan Oxholm Gordeladze
\\n\\nChapter 2 Vitamin K, SXR, and GGCX by Kotaro Azuma and Satoshi Inoue
\\n\\nChapter 3 Vitamin K2 Rich Food Products by Muhammad Yasin, Masood Sadiq Butt and Aurang Zeb
\\n\\nChapter 4 Menaquinones, Bacteria, and Foods: Vitamin K2 in the Diet by Barbara Walther and Magali Chollet
\\n\\nChapter 5 The Impact of Vitamin K2 on Energy Metabolism by Mona Møller, Serena Tonstad, Tone Bathen and Jan Oxholm Gordeladze
\\n\\nChapter 6 Vitamin K2 and Bone Health by Niels Erik Frandsen and Jan Oxholm Gordeladze
\\n\\nChapter 7 Vitamin K2 and its Impact on Tooth Epigenetics by Jan Oxholm Gordeladze, Maria A. Landin, Gaute Floer Johnsen, Håvard Jostein Haugen and Harald Osmundsen
\\n\\nChapter 8 Anti-Inflammatory Actions of Vitamin K by Stephen J. Hodges, Andrew A. Pitsillides, Lars M. Ytrebø and Robin Soper
\\n\\nChapter 9 Vitamin K2: Implications for Cardiovascular Health in the Context of Plant-Based Diets, with Applications for Prostate Health by Michael S. Donaldson
\\n\\nChapter 11 Vitamin K2 Facilitating Inter-Organ Cross-Talk by Jan O. Gordeladze, Håvard J. Haugen, Gaute Floer Johnsen and Mona Møller
\\n\\nChapter 13 Medicinal Chemistry of Vitamin K Derivatives and Metabolites by Shinya Fujii and Hiroyuki Kagechika
\\n"}]'},components:[{type:"htmlEditorComponent",content:'This book serves as a comprehensive survey of the impact of vitamin K2 on cellular functions and organ systems, indicating that vitamin K2 plays an important role in the differentiation/preservation of various cell phenotypes and as a stimulator and/or mediator of interorgan cross talk. Vitamin K2 binds to the transcription factor SXR/PXR, thus acting like a hormone (very much in the same manner as vitamin A and vitamin D). Therefore, vitamin K2 affects a multitude of organ systems, and it is reckoned to be one positive factor in bringing about "longevity" to the human body, e.g., supporting the functions/health of different organ systems, as well as correcting the functioning or even "curing" ailments striking several organs in our body.
\n\nChapter 1 Introductory Chapter: Vitamin K2 by Jan Oxholm Gordeladze
\n\nChapter 2 Vitamin K, SXR, and GGCX by Kotaro Azuma and Satoshi Inoue
\n\nChapter 3 Vitamin K2 Rich Food Products by Muhammad Yasin, Masood Sadiq Butt and Aurang Zeb
\n\nChapter 4 Menaquinones, Bacteria, and Foods: Vitamin K2 in the Diet by Barbara Walther and Magali Chollet
\n\nChapter 5 The Impact of Vitamin K2 on Energy Metabolism by Mona Møller, Serena Tonstad, Tone Bathen and Jan Oxholm Gordeladze
\n\nChapter 6 Vitamin K2 and Bone Health by Niels Erik Frandsen and Jan Oxholm Gordeladze
\n\nChapter 7 Vitamin K2 and its Impact on Tooth Epigenetics by Jan Oxholm Gordeladze, Maria A. Landin, Gaute Floer Johnsen, Håvard Jostein Haugen and Harald Osmundsen
\n\nChapter 8 Anti-Inflammatory Actions of Vitamin K by Stephen J. Hodges, Andrew A. Pitsillides, Lars M. Ytrebø and Robin Soper
\n\nChapter 9 Vitamin K2: Implications for Cardiovascular Health in the Context of Plant-Based Diets, with Applications for Prostate Health by Michael S. Donaldson
\n\nChapter 11 Vitamin K2 Facilitating Inter-Organ Cross-Talk by Jan O. Gordeladze, Håvard J. Haugen, Gaute Floer Johnsen and Mona Møller
\n\nChapter 13 Medicinal Chemistry of Vitamin K Derivatives and Metabolites by Shinya Fujii and Hiroyuki Kagechika
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