Measurements of craniofacial skeleton
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",isbn:"978-1-83968-460-9",printIsbn:"978-1-83968-459-3",pdfIsbn:"978-1-83969-232-1",doi:null,price:0,priceEur:0,priceUsd:0,slug:null,numberOfPages:0,isOpenForSubmission:!0,hash:"babca2dea1c80719111734cc57a21a4c",bookSignature:"Dr. Amin Talei",publishedDate:null,coverURL:"https://cdn.intechopen.com/books/images_new/10404.jpg",keywords:"Water Budget, Ground Measurement, Satellite Data, Empirical Models, Physical Models, Data-Driven Models, Artificial Neural Network, Neuro-Fuzzy Systems, Genetic Programming, Irrigation Management, Drought, Aquifer Management",numberOfDownloads:null,numberOfWosCitations:0,numberOfCrossrefCitations:null,numberOfDimensionsCitations:null,numberOfTotalCitations:null,isAvailableForWebshopOrdering:!0,dateEndFirstStepPublish:"October 29th 2020",dateEndSecondStepPublish:"November 26th 2020",dateEndThirdStepPublish:"January 25th 2021",dateEndFourthStepPublish:"April 15th 2021",dateEndFifthStepPublish:"June 14th 2021",remainingDaysToSecondStep:"2 months",secondStepPassed:!0,currentStepOfPublishingProcess:3,editedByType:null,kuFlag:!1,biosketch:"A pioneering researcher in developing hydrological models using adaptive neuro-fuzzy systems, a pioneering researcher in tropical biofiltration systems, appointed head of the Civil Engineering Discipline in Monash University Malaysia.",coeditorOneBiosketch:null,coeditorTwoBiosketch:null,coeditorThreeBiosketch:null,coeditorFourBiosketch:null,coeditorFiveBiosketch:null,editors:[{id:"335732",title:"Dr.",name:"Amin",middleName:null,surname:"Talei",slug:"amin-talei",fullName:"Amin Talei",profilePictureURL:"https://mts.intechopen.com/storage/users/335732/images/system/335732.jpg",biography:"Associate Professor Amin Talei joined Monash University Malaysia in January 2013 and currently is the head of Civil Engineering discipline. His previous appointment was as researcher in School of Civil & Environmental Engineering of Nanyang Technological University of Singapore where he studied for his PhD during 2008-2011. His research is predominantly focused on hydrological modeling and flood forecasting using artificial intelligence techniques. Most recently, he has been also involved in research projects dealing with sustainable urban water management. To date, he has published over 50 articles in reputable journals and international conference proceedings. He has supervised several PhD and Master students and won the Supervisor of the Year Award in Monash University Malaysia in 2017. 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Venkateswarlu",coverURL:"https://cdn.intechopen.com/books/images_new/371.jpg",editedByType:"Edited by",editors:[{id:"58592",title:"Dr.",name:"Arun",surname:"Shanker",slug:"arun-shanker",fullName:"Arun Shanker"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"878",title:"Phytochemicals",subtitle:"A Global Perspective of Their Role in Nutrition and Health",isOpenForSubmission:!1,hash:"ec77671f63975ef2d16192897deb6835",slug:"phytochemicals-a-global-perspective-of-their-role-in-nutrition-and-health",bookSignature:"Venketeshwer Rao",coverURL:"https://cdn.intechopen.com/books/images_new/878.jpg",editedByType:"Edited by",editors:[{id:"82663",title:"Dr.",name:"Venketeshwer",surname:"Rao",slug:"venketeshwer-rao",fullName:"Venketeshwer Rao"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}},{type:"book",id:"4816",title:"Face Recognition",subtitle:null,isOpenForSubmission:!1,hash:"146063b5359146b7718ea86bad47c8eb",slug:"face_recognition",bookSignature:"Kresimir Delac and Mislav Grgic",coverURL:"https://cdn.intechopen.com/books/images_new/4816.jpg",editedByType:"Edited by",editors:[{id:"528",title:"Dr.",name:"Kresimir",surname:"Delac",slug:"kresimir-delac",fullName:"Kresimir Delac"}],productType:{id:"1",chapterContentType:"chapter",authoredCaption:"Edited by"}}]},chapter:{item:{type:"chapter",id:"49504",title:"Complication of Type 1 Diabetes in Craniofacial and Dental Hard Tissue",doi:"10.5772/61885",slug:"complication-of-type-1-diabetes-in-craniofacial-and-dental-hard-tissue",body:'Type 1 diabetes is a chronic and a complex autoimmune disease arisen primarily due to β-cell destruction. Historically, type 1 diabetes was considered as a disorder in children and adolescents, but now it is known that symptomatic onset of type 1 diabetes may occur at any age. Three major symptoms, polydipsia, polyphagia, and polyuria along with overt hyperglycemia, are a diagnostic hallmark in young type 1 diabetes patients. Exogenous insulin replacement is needed immediately after the onset of type 1 diabetes and should be kept throughout their lifetime for survival.
To prevent the diabetic complication, patients with type 1 diabetes require a strict control of blood glucose level.
Although type 1 diabetes can be diagnosed at any age, it is one of the most common chronic diseases of childhood. Its prevalence increases between the ages 5 and 7 years or near puberty [1].
It has been reported that the incidence of type 1 diabetes is increasing worldwide for several decades [2] and it is likely to have been most pronounced in children aged 4 years and younger [3]. If these trends continue, the total prevalence of people with type 1 diabetes will increase in the coming years [4].
A continuous hyperglycemia in type 1 diabetes leads to various chronic complications. Recently, official healthcare providers have paid more attention to the prevention of disabling chronic complications, such as diabetic retinopathy, nephropathy, neuropathy, and atherosclerosis with cardiovascular disease, and much more attention has been paid for adverse bone metabolism in type 1 diabetes. [5] In this review, we provide a brief overview on the effects of type 1 diabetes on both bone in general and hard tissue in craniofacial region.
The relation between diabetes and bone metabolism has been considered for a long time; however, many questions still remain hidden and unclear. Pathophysiology of diabetes arises from the insufficient insulin action, and such insulin action may have an influence on the bone metabolism directly or indirectly. Clinically, it is well known that type 1 and type 2 diabetes are involved in an increased risk of fractures [6, 7]; on the other hand, bone mineral density (BMD) is decreased in type 1 diabetes than in type 2 diabetes [7]. The reasons for this discrepancy are not fully understood. Indeed both type 1 and type 2 diabetes are the same in terms of an abnormal glucose tolerance, but pathological condition is different. In this part, we discuss diabetic osteopenia in type 1 diabetes from the viewpoints of insulin deficiency and hyperglycemia.
It is widely recognized that bone volume and bone quality are decreased in type 1 diabetes patients, and it is thought that insulin has a pivotal role in bone formation [7]. In animal experiment, streptozotocin (STZ)-induced type 1 diabetes rat or mouse showed a decrease in bone volume (BV) and bone fragility by the decrease of bone formation [8–10].
In insulin receptor substrate-1 (IRS-1)-deficient mouse, osteoblast differentiation and function were impaired, and as a result, there is a decrease in BV [11].
Remarkable hyperglycemia exists with insulin deficiency in the type 1 diabetes model animals, and it seems to be thought that not only the insulin deficiency but also the hyperglycemic condition gives some influences on bone metabolism. On the other hand, it appears that decrease in anabolic action at the osteoblasts level in type 1 diabetes is the main cause of the bone metabolism disorder by serial animal experiments in which the disorder of glucose metabolism is slight under the normal breeding condition in IRS-1- or IRS-2-deficient mice. On the basis of these findings, one should consider the rise in onset, osteoporosis, and bone fracture frequency of the osteoporosis in type 1 diabetes mellitus depends on an osteoplasty disorder by the insulin deficiency.
In 1948, Albright and Reifenstein described for the first time the association between diabetes and reduced bone mass [12]. In 1976, Levin et al. demonstrated that almost 50% of the patients with type 1 diabetes had a reduction of BMD at the wrist [13]. Since then, many papers have been published. BMD seems to be reduced in patients with type 1 diabetes in most [14–17], but not all [18, 19]. The studies concerning the bone metabolism in type 1 diabetes can be categorized into two groups: 1) studies evaluating bone metabolism in diabetic children and adolescents who did not reach the peak of bone mass yet and 2) studies evaluating bone metabolism in adults who developed type 1 diabetes after having reached peak of bone mass.
It seems to be difficult to study bone metabolism in such population as children/adolescents whose skeleton is still in the way of growing. Moreover, the majority of studies included the children/adolescents at different stage of puberty and, therefore, at different stages of acquisition of bone mass. This probably has been one of the main reasons for the lack of concordant results about the impact of diabetes on growing bones.
Some reports showed no differences in BMD between type 1 diabetic children/adolescents and their peer without diabetes [20–26]. However, in other studies, low bone mineral content (BMC) and low BMD both at spine and at femoral neck in type 1 diabetic children/adolescents [27–33] have been described. Moreover, some longitudinal studies demonstrated a significant reduction of either lumber spine or femoral neck BMD in diabetic patients after 2–4 years of follow-up, despite normal BMD at baseline [20, 23]. Therefore, it seems that type 1 diabetes, appeared in childhood, may alter the acquisition of bone mass that can be registered in youth ages or later in adult life.
Indeed, the majority of studies, performed on the type 1 diabetes adults, consistently showed a reduction of BMD either at lumbar spine and/or at femur [34, 35, 36–40]. Only a few studies [41–43], which were conducted on small groups of diabetic patients (less than 40 cases), were discordant. Vestergaard et al. [44] having analyzed 80 studies regarding bone density in diabetes has proved in his meta-analysis that type 1 diabetes patients have lower BMD than the people without diabetes. Frequency of reduced BMD in type 1 diabetes varies largely from 3 to 40% [36–40]. Eller-Vainicher et al. [45] reported that about 30% of 175 type 1 diabetes patients had low bone mass (osteopenia/osteoporosis) at spine and/or femur, which was significantly higher in comparison with healthy controls.
In type 1 diabetes patients, the frequency of lifetime fractures at any site has been reported to be increased as compared to counterparts without diabetes. The meta-analysis of Vestergaard et al. [44] demonstrated a 6.94-fold increased risk of hip fracture in type 1 diabetes. Further, Zhukouskaya et al. [45] reported that type 1 diabetes patients were found to have an increased prevalence of asymptomatic vertebral fractures as well, which have been observed in 25% of diabetic subjects. In conclusion, there is strong evidence that bones in type 1 diabetes patients are characterized by poor mineralization and smaller and thinner size with reduced bone strength and quality, which can lead to a higher fracture incidence at any site, predominantly at femoral neck.
Type 1 diabetes is caused by absolute lack of insulin, and insulin has anabolic effect on bone. However, not only insulin but also hyperglycemia has some influence on the bone metabolism. In in vivo study, it is difficult to evaluate the influence on bone metabolism by hyperglycemia or insulin deficiency separately, so the influence of hyperglycemia on bone is considered at a cell level mainly.
In an experiment of osteoblastic cell, it was reported that the differentiation and function of osteoblastic cell were suppressed under osmolality-adjusted hyperglycemic condition [46].
In our previous experiment using MC3T3-E1 cell line, osteoblastic cells were cultured in medium containing normal (5.6 mM) or high (10, 20, or 30 mM) glucose with or without bone morphogenic protein 2 (BMP-2). Runx2 mRNA expression, which is a key transcription factor associated with osteoblast differentiation, was affected by glucose concentration and culture duration independently of the absence or presence of BMP-2 in the culture. (Fig. 1) [47]. Moreover, we could find both GLP-1 receptor (GLP-1R) and GIP receptor (GIPR) m RNA expression in osteoblastic cell first time ever (Fig. 2), and mRNA expression level of GLP-1R and GIPR were regulated by glucose concentrations in cells undergoing the differentiation induced by BMP-2 (Figs. 3, 4). GLP-1 or GIP belong to the incretin family. They both play important roles in regulating insulin secretion from pancreatic β-cells. GIPR and GLP-1R, the receptors of GIP and GLP-1, are expressed in various tissues, with a significant amount expressed in pancreas. Previous reports showed that GIPR is expressed in osteoblastic cells, but no study regarding GLP-1R expression had been conducted [48]. Although osteoblastic cells were thought to express a functional receptor for GLP-1, there is no direct evidence for the mRNA and protein expression of GLP-1R in these cells. GIP is known to have direct effects on bone, whereas the effects of GLP-1 on bone metabolism are mediated by thyroid hormone. [49] Our RT-PCR analysis revealed that MC3T3-E1 cells express GLP-1R and GIPR, suggesting that GLP-1 may directly affect bone, similar to GIP (Fig. 4). GLP-1R and GIPR are well-known G protein-coupled receptor (GPCR) and are potential targets for drug discovery [47]. It has been reported that the administration of insulin and thiazolidinediones increases fracture risk, whereas inhibitors of dipeptidyl peptidase-4 (DPP-4) were associated with reduced fracture risk. DPP-4 inactivates GLP-1, and its inhibitors improve glycemic control in patients with type 2 diabetes by preventing incretin degradation [50]. These findings show that GLP-1R links bone metabolism and glucose metabolism in osteoblasts and that GLP-1 might be a potential therapeutic target in bone diseases.
Effects of the glucose concentration on Runx2 mRNA expression. MC3T3-E1 cells were cultured in medium containing 5.6 (normal), or 10, 20, and 30 mM (high) concentrations of glucose in the absence or presence of bone morphogenetic protein-2 (BMP-2). Runx2 mRNA expression was determined after 24, 48, and 72 h of culture. Values are the means ± standard error of the mean (SEM) (n = 4/group). *P < 0.05 and **P < 0.01.
Reverse transcriptase-polymerase chain reaction (RT-PCR) analysis of glucagon-like peptide-1 receptor (GLP-1R) and glucose-dependent insulinotropic polypeptide receptor (GIPR) mRNA expression in MC3T3-E1 cells. Lane 1, negative control; lane 2, GLP-1R (337 bp); lane 3, GIPR (382 bp); lane 4, GAPDH (452 bp).
Effects of the glucose concentration on glucagon-like peptide-1 receptor (GLP-1R) mRNA expression. MC3T3-E1 cells were cultured in medium containing 5.6 (normal), or 10, 20 and 30 mM (high) concentrations of glucose in the absence or presence of bone morphogenetic protein-2 (BMP-2). GLP-1R mRNA expression after 24, 48, and 72 h of culture. Values are the means ± standard error of the mean (SEM) (n = 4/group). *P < 0.01.
Effects of glucose concentration on glucose- dependent insulinotropic polypeptide receptor (GIPR) mRNA expression. MC3T3-E1 cells were cultured in medium containing 5.6 (normal), or 10, 20, and 30 mM (high) concentrations of glucose in the absence or presence of bone morphogenetic protein-2 (BMP-2). GIPR mRNA expression after 24, 48, and 72 h of culture. Values are the means ± standard error of the mean (SEM) (n = 4/group). *P < 0.01.
Diabetes is one of the systemic diseases affecting a considerable number of patients worldwide [51]. Numerous clinical and experimental studies on the complications of diabetes have demonstrated extensive alterations in bone and mineral metabolism, linear growth, and body composition [52]. As we mentioned in the previous section, depletion of insulin in type 1 diabetes causes a reduction of bone composition, delay in fracture healing, and reduction of BMD in general. A long list of literature was dedicated to study the influence or complications of type 1 diabetes on general bones. However, there are few reports discussing the effects of type 1 diabetes on the craniofacial complex which is regulated by hormones, nutrients, mechanical forces, and various peripheral growth factors.
In craniofacial region, it is well known that bone metabolism in growth period is really intricate because there are mosaic growth sites where bones grow at different rates or mature at different times, which also depend on each individual’s growth stage, and the response to growth disruption is much more complicated than that of the appendicular skeleton. There are a few studies diabetes may significantly affect the bone remodeling process which is observed during treatments involving the application of mechanical or functional force to the craniofacial complex and the teeth as those applied during orthodontic tooth movement. Moreover, it is likely that the type 1 diabetes may have altered the growth of patients due to insulin deficiency and consequently led to skeletal mutation is it mutation or maturation?
Type 1 diabetes is well recognized in the endocrine disorders,, and a peak of onset is concentrated in childhood and adolescence, characterized by hyperglycemia as a cardinal biochemical feature that leads to several impairment of physical and emotional developments. There are some reports focusing on the altered bone remodeling in type 1 diabetes, which indicates the reduction of osteoblast activity or function. Bone mass decrease and rate of bone fracture risk increase have been often seen in type 1 diabetes patients. Impaired glucose metabolism results in adverse effects on bone metabolism, especially in type 1 diabetes patients who suffer from decreased bone mineral density (BMD) and increased risk of fractures. The pathophysiological mechanisms of increased risk of fracture in diabetes patients are divided into two reasons: osteopenia caused by decreased BMD and increased risk of fall and traumas caused by peripheral diabetic neuropathy. However, there are few reports about hard tissue in craniofacial region, in other words, cranium, maxilla, mandible, and teeth.
The aim of this chapter is to discuss the complexity of the dento-alveolar system and how it was affected by type 1 diabetes.
There are two processes of bone formation: “intramembranous ossification” and “endochondral ossification.” Endochondral ossification is a cartilage bone formation and it occurs in a replacement process within the cartilage models of the embryo and infant. Intramembranous bone forms through the activation of the osteoblastic cell or specialized bone forming cell in one of the layers of the fetal-connective tissue. The bones of the cranial vault, the face, and the clavicle are formed by the style of intramembranous ossification. All the other bones are formed in the manner of cartilage ossification. The bones formed by intramembranous ossification are the mandible, the maxilla, the premaxilla, the frontal bone, the palatine bone, the squamous part of temporal bone, the zygomatic bone, the medial plate of the pterygoid process, the vomer, the tympanic part of the temporal bone, the nasal bone, the lacrimal bone, and the parietal bone. The original pattern of intramembranous bone changes with progressive maturative growth when these bones begin to adapt to environmental influences. This accounts for deformities due to malfunction, disease, and other environmental factor [53].
It is thought that growth disturbance can be associated with specific anatomic or functional defects. Some kinds of endocrinal or metabolic disorders are known to cause a systemic growth disorder. Also, genetic, nutritional, or environmental factor can be the causes of growth disturbance. Disturbances in somatic growth show themselves in retardation or acceleration of the skeletal system, including the facial and cranial bones. Causes of growth problems usually fall into the following categories [54]:
familial short stature;
constitutional growth delay with delayed adolescence or delayed maturation;
illness that affects the whole body (systemic disease);
endocrine disease (hormonal disorder); and
congenital problems in the tissues where growth occurs.
Concerning juvenile diabetes, previous report about hand-wrist radiographs [55]. showed that usually, there is a delay in the development of appearance or ossification center of the carpal bone. These defects seem to occur twice as frequently in boys than in girls, and the total incidence of juvenile diabetes patients with abnormalities and developmental disorders was 24.3%.There was also a delay in the growth of bone, in 51% of diabetic males and in 60% of diabetic females. The trend of growth retardation in bone was large. The longer the disease duration of diabetes, the shorter the bone growth will be. Bone mass reduction in diabetic patients has been explained by the decrease in the proliferative capacity of fibroblasts. In addition, premature aging of all cells has been suggested as the basis for diabetes problems, which is believed to lead to early osteopenia. The yearly bone loss was reported to be 1.35% in patients with type 1 diabetes [56]. Moreover, reduction rate of bone mineral, along with the condition worsened in diabetes, was significantly faster despite of an increase in insulin dosage, when compared with patients with unchanged or improved insulin secretion. It was considered that exogenous insulin administration cannot fully compensate for the decrease in the endogenous insulin secretion. In addition, according to these studies, the bone resorption in patients with type 1 diabetes were increased, and vitamin D3 deficiency associated with the disease were not observed. Vertebral bone density has been studied in type 1 diabetic children [56]. In diabetic children, it has been found that the cortical bone density decreases slightly but significantly compared with control. The decrease in the cortical bone mineral density in diabetes did not correlate with age, gender, the duration of the diabetes, or glycosylated hemoglobin concentration. These results suggested that in children with uncomplicated type 1 diabetes, decreased vertebral bone density is a minor abnormality that affects only cortical bone [55].
To examine the dynamic bone metabolism and structure of craniofacial bone in diabetes, it is critically important in understanding the growth aspect and bone metabolism of the mandible. The next parts of this chapter are trying to focus on the following points:
The effects of juvenile diabetes on general craniofacial growth and skeletal maturation.
Analysis of the pattern of association between craniofacial morphology and skeletal maturation.
Determination of the mineral apposition rate and the bone formation rate in diabetic rat mandible using histomorphometric analysis.
Analysis of the diabetic effects on tooth (enamel and dentin formation).
It is well known that the streptozotocin-induced diabetic rat and the spontaneously diabetic BioBreeding rat were used as experimental type 1 diabetic models [57]. Pathogenesis of altered bone formation in long bones after inducing type 1 diabetes with streptozotocin (STZ) has been well documented [58, 59]. Streptozotocin-induced diabetes mellitus (STZ-DM) caused by the destruction of pancreatic β-cells and is similar to type 1 diabetes in human. It is characterized by mild-to-moderate hyperglycemia, glucosuria, polyphagia, hypoinsulinemia, hyperlipidemia, and weight loss. STZ-DM also exhibits many of the complications observed in human DM including enhanced susceptibility to infection and cardiovascular disease, retinopathy, alterations in angiogenesis, delayed wound healing, diminished growth factor expression, and reduced bone formation. [60].
We studied various changes on craniofacial hard tissue under DM condition using streptozotocin (STZ)-induced DM rat model. Three-week-old male Wistar rats (n = 12) were used for this study. They were randomly divided into two groups, the control group and the diabetes group (DM group), and each group consists of six rats. The rats in the control group were injected intraperitoneally with a single dose of 0.1M sodium citrate buffer (pH 4.5), while the rats in the DM group were injected intraperitoneally with a single dose of citrate buffer containing 60 mg/kg body weight of STZ (Sigma Chemical Co., St. Louis, MO, USA) [58, 61–63]. All animals were fed on standard rodent diet (Rodent Diet CE-2; Japan Clea Inc., Shizuoka, Japan) with free access to water. Body weights, the presence of glucose in urine, and blood glucose levels were recorded on days 0, 2, 7, 14, 21, and 28 after STZ injection. Diabetes condition was determined by the presence of glucose in urine and blood. The urine of the rats was tested using reagent strips (Uriace Ga; TERUMO) [64, 65]. Blood samples of the rats were obtained via vein puncture of a tail vein, and blood glucose levels were determined using a glucometer (Ascensia Brio; Bayer Medical). Rats with a positive urine test and a blood glucose level greater than 200 mg/dl were considered as diabetic. Time course of the animal experiment is shown in Fig. 5.
The time schedule of experiment
Cephalometric analysis
Cephalometric measurements are still one of the most widely spread diagnostic aids crucial for the diagnosis of various abnormalities in the craniofacial complex [66].
The protocol for examining the cephalometric measurements in Type 1 diabetic rats involved the following steps:
Prior to each radiographic session, the rats were anesthetized with diethyl ether and intraperitoneally injected with 8% chloral hydrate using 0.5 ml/100 g of body weight.
After anesthesia, the rats were placed in the same way using specially designed apparatus to maintain standardized head posture and contact with the film (SGP-3; Mitsutoyo, Tokyo, Japan) where the head of each rat was fixed firmly with a pair of ear rods oriented vertically to the sagittal plane, and the incisors were fixed into a plastic ring. The settings of lateral and dorsoventral cephalometric radiographs were 50/55 kVp, 15/10 mA, and 20/60-sec impulses, respectively [68].
Then, a 10-mm steel calibration rod was incorporated into the clear acrylic table on which the animals were positioned for the radiographs.
All the radiographs were developed and scanned at high resolution by the same operator (Fig. 6). The cephalometric landmarks were derived from previous studies on rodents [68–70]. The selected linear measurements were then obtained (Table 1). To ensure reliability and reproducibility of each measurement, each distance was digitized twice and the two values were averaged. In our studies, evaluation of the craniofacial growth of diabetic rats at the age of 7 weeks was carried out using lateral and dorsoventral cephalometric radiographs. All of the data in each experiment were confirmed for the normal distribution; that is, Student’s t-test was used to compare the mean of each data recorded in the control group and in the DM group. All statistical analyses were performed at a 5% significance level using statistic software (v. 10; SPSS, Chicago, IL, USA).
\n\t\t\t\tNeurocranium\n\t\t\t | \n\t\t\t\n\t\t\t\tMandible\n\t\t\t | \n\t\t
Po–N: total skull length | \n\t\t\tGo–Mn: posterior corpus length | \n\t\t
Po–E: cranial vault length | \n\t\t\tMl–Il: anterior corpus length | \n\t\t
Ba–E: total cranial base length | \n\t\t\tCo–Il: total mandibular length | \n\t\t
So–E: anterior cranial base length | \n\t\t\tCo–Gn: ramus height | \n\t\t
Ba–CB1: occipital bone length | \n\t\t\t\n\t\t\t\tTransverse X-ray\n\t\t\t | \n\t\t
CB1′–CB2: sphenoid bone length | \n\t\t\tGo1–Go2: bigonial width | \n\t\t
Ba–So: posterior cranial base length | \n\t\t\tC1–C2: maximum cranial width | \n\t\t
Po–Ba: posterior neurocranium height | \n\t\t\tP1–P2: palatal width | \n\t\t
\n\t\t\t\tViscerocranium\n\t\t\t | \n\t\t\tZ1–Z2: bizygomatic width | \n\t\t
E–N: nasal length | \n\t\t\t\n\t\t |
Mu2–Iu: palate length | \n\t\t\t\n\t\t |
CB2–Iu: midface length | \n\t\t\t\n\t\t |
E–Mu1: viscerocranial height | \n\t\t\t\n\t\t |
Measurements of craniofacial skeleton
Location of lateral cephalometric points on radiographs: (a) sagittal
The size of total skull, denoted by Po-N, was found to be significantly smaller in the DM group than in the control group (Fig. 7).
(A) Changes in the neurocranial measurements of the control and type 1 diabetes (DM) group. All the significant measurements are shown in this figure. Values are mean ± S.D. Significant differences between the two groups are marked with asterisks (P < 0.05). (B) Changes in the viscerocranial measurements of the control and DM groups. All the viscerocranial measurements are significant. Values are mean ± S.D. Significant differences between the two groups are marked with asterisks (P < 0.05). (C) Changes in the mandible measurements of the control and DM groups. Values are mean ± S.D. Significant differences between the two groups are marked with asterisks (P < 0.05). (D) Changes in the transverse X-ray measurements of the control and DM groups. Two measurements in the transverse X-ray were significant. Values are mean ± S.D. Significant differences between the two groups are marked with asterisks (P < 0.05).
Cranial vault length (Po-E), total cranial base length (Ba-E), anterior cranial base length (SoE), occipital bone length (Ba-CB1), and posterior cranial base length (Ba-So) were significantly shorter in DM group (Fig. 7), while the other dimensions showed no significant differences.
All measurements of the viscerocranium, including the nasal length (E-N), palatal length (Mu2-Iu), midface length (CB2-Iu), and viscerocranial height (E-Mu1), showed a statistically significant decrease in DM group (Fig. 7).
In the DM group, the posterior corpus length (Go-Mn), total mandibular length (Co-Il), and the ramus height (Co-Gn) were significantly shorter than in the control group (Fig. 7); on the other hand, there were no statistical differences in the remaining dimensions.
Fluorochromes are calcium-binding substances that are preferentially taken up at the site of active mineralization of bone known as the calcification front, thus labeling sites of new bone formation. They are detected using fluorescent microscopy on undecalcified sections. Labeling bones with fluorochrome markers provides a means to study the dynamics of bone formation. The rate and extent of bone deposition and resorption can be determined using double- and triple-fluorochrome labeling sequences. The sequential use of fluorochromes of clearly contrasting colors permits a more detailed record of events relating to calcification. Fluorochromes commonly used in mammals include tetracycline, calcein green, xylenol orange, alizarin red, and hematoporphyrin. Calcein gives bright green fluorescence when combined with calcium [71].
The detection of the double labeling involves the following steps:
Rats are subcutaneously injected with 50 mg/kg body weight calcein fluorescent marker on day 21 and day 28 after STZ injection [72]. The time difference between the two injections was one week to be able to compare the amount of bone formed during this period (Fig. 8).
All animals were sacrificed by transcardiac perfusion under deep anesthesia using 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4).
Mandibles were dissected and fixed in the same solution for 24 h and embedded in polystyrene resin (Rigolac; Nisshin EM Co. Ltd., Tokyo, Japan).
Undermineralized ground frontal sections were processed to show the crown and both apices of buccal and lingual roots of the lower second molar [72].
Frontal sections of the rat’s mandibular second molar area. Control, control rat; DM, type 1 diabetes rat. Fluorescent labeling on the periosteal surface indicates new bone formation.
The bone around the lower second molar is centrally located within the mandibular arch, and the parallel alignment of the buccal and lingual roots is used as a precise reference when frontal sections are produced [73]. To conduct the histomorphometric analysis, it is essential to use a digitizing morphometry system to measure bone formation indices. The system consists of a confocal laser scanning microscope (LSM510; Carl Zeiss Co. Ltd., Jena, Germany) and a morphometry program (LSM Image Browser; Carl Zeiss Co. Ltd., Jena, Germany). Bone formation indices of the periosteal surfaces of the alveolar/jaw bone include mineral apposition rate (μm/day) and bone formation rate (μm3/μm2/day), according to the standard nomenclature described by Parfitt and colleagues [74]. The calcein-labeled surface (CLS, in mm) is calculated as the sum of the length of double labels plus one half of the length of single labels (sL) along the entire endosteal or periosteal bone surfaces; that is, CLS = dL + 0.5sL [75]. The mineral apposition rate (MAR, in μm/day) is determined by dividing the mean of the width of the double labels by the interlabel time (7 days). The bone formation rate (BFR) is calculated by multiplying MAR by CLS [76]. Based on the reference line along the long axis of the buccal root, the area superior to the root apex was considered as an alveolar bone, while the area inferior to the root apex was considered as the jaw bone. The lingual side of the bone was excluded, because the existence of the incisor root might influence bone formation. The periosteal surfaces of the mandible were divided into four regions for analysis (Fig. 9).
Schematic drawing of observation regions for dynamic bone histomorphometry. The periosteal surfaces were delimited into four areas: alveolar crest (region 1), alveolar bone (region 2), buccal surface of the jaw bone (region 3), and inferior border of the jaw bone (region 4).
The obtained results in our study showed that in the alveolar bone (region 2), there was a significant decrease in the MAR (Fig. 10A) and the BFR (Fig. 10B) recorded in the DM group compared to the control group. However, in the alveolar crest (region 1), the MAR and the BFR in the control and the DM groups were not significantly different (P < 0.05). In the buccal surface (region 3) and inferior borders (region 4) of the jaw bone, the MAR (Fig. 10A) and BFR (Fig. 10B) were significantly suppressed compared with those in the control group (P < 0.05). Most of the periosteal surfaces in the mandibular regions of the control group showed significantly higher values recorded for the mineral apposition rate and the bone formation rate when compared to the DM group. These results agree with the previous studies that recorded diminished lamellar bone formation in DM rats’ femur and may suggest an association between the DM condition and the decreased number and function of osteoblasts [61]. The alveolar crest region was the only region that did not show a significant difference in the MAR and the BFR parameters between the two groups; this may be attributed to the unique nature of this region exhibiting a highly intensive bone remodeling process especially during the teeth eruption that decreases toward the base of the socket [77]; however, further studies are needed to elaborate the detailed pattern of bone growth at the alveolar crest region.
(A) Changes in the mineral apposition rate (MAR) of the mandible between the control group (red columns) and the type 1 diabetes mellitus (DM) group (blue columns). Alveolar crest (region 1, upper half of the tooth root, near the tooth crown). Alveolar bone (region 2, lower half of the tooth root, near the root apex). Buccal surface of the jaw bone (region 3). Inferior border of the jaw bone (region 4). The data are expressed as means ± S.D.; n = 5 for each group. Significantly different from controls, with *P < 0.05. (B) Changes in the bone formation rate (BFR/BS) of the mandible between the control group and the DM group. Alveolar crest (region 1, upper half of the tooth root, near the tooth crown). Alveolar bone (region 2, lower half of the tooth root, near the root apex). Buccal surface of the jaw bone (region 3). Inferior border of the jaw bone (region 4). The data are expressed as means ± S.D.; n = 5 for each group. Significantly different from controls, with *P < 0.05. In the buccal surface (region 3) and inferior borders (region 4) of the jaw bone, the MAR (Fig. 4A) and the BFR (Fig. 4B) are significantly suppressed compared with those in the control group (P < 0.05).
Type 1 diabetes exhibits various detrimental alterations on bones, and mineral metabolism [52, 58, 75]. However, there is scant information available on the possible effects exerted by the diabetic condition on tooth development and mineral content. Various clinical studies reported high caries prevalence in diabetic children when compared with healthy controls [78]. Previous studies suggested that the aforementioned increase in caries prevalence associated with type 1 diabetes may be due to alteration in the salivary gland functions resulting in decreased salivary flow. Alternative speculations were that type 1 diabetes produced increased salivary glucose levels which may have increased permeability of the parotid gland basement membrane to the elevated blood glucose. Understanding the factors contributing to the increased caries susceptibility of young patients suffering from the diabetic condition, especially young orthodontic patients who have high probability for the development of caries during their orthodontic treatment, may help dentists to plan suitable strategies for protecting such patients against the expected caries challenges. Moreover, it is of prime importance for dentists and orthodontists to explore any factors that might affect the dental tissues growth and thus the size of the teeth, which has a strong impact on the orthodontic treatment planning. Our study has employed the non-destructive micro-computed tomography (micro-CT) to examine the influence of induced type 1 diabetes on enamel and dentine mineral density and thickness using an experimental rat model. Micro-CT uses a focused beam to provide higher resolution on small samples in vitro. This method has been frequently used in experiments exploring bone and is considered as a promising technique for the assessment of tooth mineral density. In addition, a histomorphometric study was conducted to determine the effect of the type 1 diabetes condition on dentine formation and dentine mineral apposition rates in the continuously growing lower incisors of Wistar rats. This is an appropriate model for examining the effects of different factors on the development of hard tissues. The tested null hypotheses in this study were that the type 1 diabetes condition will not adversely affect thickness, mineral density, and the rate of tissue formation and mineral apposition in enamel and dentine.
Rats were subcutaneously injected with calcein fluorescent marker (50 mg/kg body weight) on day 21 and day 28 after STZ injection. All animals were anesthetized and sacrificed by transcardiac perfusion by 4% paraformaldehyde in 0.1 M phosphate buffer (pH 7.4). The right mandibles were removed and fixed in the same solution. After being embedded in polystyrene resin (Rigolac; Nisshin EM Co. Ltd., Tokyo, Japan), undemineralized ground mesial sections were cut using water-cooled diamond saw microtome (1600 Microtome; Leitz Wetzlar, Germany) parallel to the long axis of the rat molars just 2 mm to the mesial surface of the first lower molar crown; the distal second cut was done 2 mm distal to the crown of the first molar. The specimen mesial surface was then ground flat with water-cooled silicon carbide discs (600- and 1200-grade papers; Buehler) until it was possible to observe the two mesial canals and two mesial pulp chamber horns of the first molar. The ground mesial surface was glued on a glass slide, and the same grinding procedures were repeated from the distal surface until we can observe the two mesial canals and two mesial pulp horns of the first molar from the distal side. The obtained specimen is then wet-polished using diamond paste (1 mm; Buehler) to obtain a highly polished surface.
Dentine formation indices in control and type 1 diabetes groups were determined in the crown analogue area parallel to the long axis of the mesial surface of the first molar. A digitizing morphometry system was used to measure the dentine formation indices. The system consisted of a confocal laser scanning microscope (LSM510; Carl Zeiss Co. Ltd., Jena, Germany) and a morphometry program (LSM Image Browser; Carl Zeiss Co. Ltd., Germany). Dentine formation indices included dentine mineral apposition rate (mm/day) and dentine formation rate (μm3/μm2/day). The method for the calculation of bone indices was modified from a method described by Parfitt et al. [74] The calcein-labeled dentine surface (CLS, in mm) was calculated as the sum of the length of double labels (dL) plus one half of the length of single labels (sL) along the entire dentine surface; that is, CLS = dL + 0.5sL [17]. The mineral apposition rate (MAR, in μm/day and in μm2/day) was determined by dividing the mean of the width of the double labels by the interlabel time (7 days). The dentine formation rate (DFR) was calculated by multiplying MAR by CLS [18]. For the measurements of mineral apposition rate, the average of 3 inter-label widths at a 100-μm interval was calculated for each sample.
Green fluorescent lines labeled with calcein fluorescent marker at two different time points showed that dentine formation took place between day 21 and day 28 in the control and type 1 diabetes groups (Fig. 11A and B). In the type 1 diabetes group, there were significant decreases in both mineral apposition and dentine formation rates (Fig. 11C and D) when compared to control group (P < 0.05).
(A) Frontal section of the lower right mandible. *The lower first molar two roots that were considered the landmark for cutting all samples. (B, C) Frontal sections of the rat incisor mandibular first molar area. (B) Control; (C) T1DM. Fluorescent labelling indicates the new dentine formation. (D) The mineral apposition rate (MAR) of the dentine mandibular incisor for the control group and the T1DM group. The data are expressed as means ± SD. n = 10 for each group. Significant difference from controls, with *P < 0.05. (E) The dentine formation rate (DFR) of the dentine mandibular incisor for the control group and the DM group. The data are expressed as means ± S.D. n = 10 for each group. Significant difference from controls, with *P < 0.05).
Furthermore, our micro-CT results (details of method not shown) revealed that there was no significant difference in the enamel and dentine mineral densities between the control and experimental diabetes groups (Fig. 12). However, the type 1 diabetes group showed a significant decrease in the thickness of enamel and dentine surfaces when compared to the control group (Fig. 13) [79].
(A) Representative 3D reconstruction of the left mandible imaged by micro-CT. (B) The left mandible with the vertical reference line extending parallel to the mesial surface of the first molar. (C) Mineral density calibration curve based on the gray scale values obtained from the mineral reference phantoms (linear regression, R2 > 0.99). (D) Graph showing that there is no significant difference in the incisor enamel and dentine mineral densities between the control and T1DM groups.
(A) The micro-CT oriented image of the rat mandibular incisor showing the three zones (E1–E3) selected for evaluation of enamel thickness and the three zones (D1–D3) selected for evaluation of dentine thickness. B-buccal; M-middle; Li-lingual. (B) The T1DM group shows a significant decrease in the thickness of enamel surface when compared to control group in the three different zones. (C) The T1DM group shows a significant decrease in the thickness of dentine surface when compared to control group in the three different zones (P < 0.05).
Growth of the craniofacial or maxillofacial complex is regulated by genetic and environmental factors [57]. For normal growth and morphogenesis of the cranial and maxillofacial complex, a proper regulation by hormones, nutrients, mechanical forces, and various general and local growth factor is essential. Type 1 diabetes causes a deteriorating growth and metabolic disorder of bone in both humans and experimental animals [58]. Since studies in humans are generally limited by small sample size, cross-sectional designs, uncontrolled variables, and often retrospective natures; it often performed more rigorous analyses using animal models [56]. We have observed the growth of the rat from 3 weeks of age to 7 weeks of age in our study. According to the previous craniofacial growth studies, this period corresponds to the initial stage of growth in humans [80, 81]. Consequently, STZ-induced DM models in our study were used to investigate the effects of type 1 diabetes on the development of craniofacial complex. These STZ-induced DM rats showed a significant reduction in the growth of a large portion of the unit of craniofacial hard tissues compared with control rats, but regarding the rest of the craniofacial skeletal units (sphenoid bone length, posterior neurocranium height, anterior corpus length, bigonial width, and palatal width), no significant difference were observed between the control and the STZ-induced DM groups. In general, craniofacial skeletal growth was significantly lower in STZ-induced DM group compared to controls in all three dimensions. The previous study investigated the DM effect exclusively on the growth of the mandible and suggested that the diabetic condition had a differential effect on the osseous components and/or its associated non-skeletal tissues. They discussed that disharmony of the mandibular growth was due to the condition of the DM, such as renal failure, anemia, body weight change, or alteration in the food-intake qualities [58]. Thus, we hypothesize that the deficiency in the craniofacial growth in our experiment might be due to the diabetic condition in the DM group as it has been reported that specific changes in bone metabolism are associated with DM. In addition, some of the pathogenic potential, insulinopenia, microvascular bone, dysregulation of mineral metabolism, changes in local factors that regulate bone remodeling, and even an intrinsic disorder related to type 1 diabetes, have been proposed [82, 83]. It is thought that the aforementioned deficiency of the insulin associated with type 1 diabetes may have a direct effect on bone metabolism. It was reported that normal insulin levels exert a direct anabolic effect on bone cells [82]. Multiple osteoblast-like cell lines, expressing the insulin receptor on the cell surface, have a high capacity for insulin binding [84]. Moreover, osteoclast are known to reduce bone resorption in response to insulin stimulation [85]. These findings support the view that insulin in bone can act directly against osteoblasts in combination with the inhibition of osteoclasts [60, 85], and this mechanism of action can be used to explain the delay in the craniofacial growth in STZ-DM. Diabetes has a detrimental effect on osseous turnover due to decreased both osteoblast and osteoclast activities and numbers and, a lower percentage of osteoid surface and osteocalcin synthesis, as well as increased time for mineralization of osteoid [82]. In a separate stage in matrix-induced endochondral bone formation, the influence of diabetes was reported to have a significant impact on the biomechanical behavior of bone. In addition, chondrogenesis and calcification of bone were reduced by 50% in diabetic animals [86]. This was also consistent with our findings that showed a significant reduction in the craniofacial linear measurements of the DM group. In addition, insulin can exert synergistic effects with other anabolic agents on bone, such as parathyroid hormone (PTH) [60, 85]. Type 1 diabetes animal models frequently show the alteration in bone turnover, retarded growth, increased concentration of PTH, and reduced concentration of 1,25-dihydroxyvitamin D [82, 87]. The effects of PTH on the bones are rather complex; PTH stimulates resorption or bone formation depending on the concentration used, the duration of the exhibition, and the administration method [82, 86, 87, 88]. Moreover, 1,25-dihydroxivitamin D, like PTH, belongs to the most important group of bone regulatory hormones. It regulates osteoclastic differentiation from hematopoietic mononuclear cells, and osteoblastic functions and activity [82, 89].
Moreover, insulin may indirectly regulate the increase in the concentration of growth hormone (GH) in serum concentration by direct regulation of the hepatic growth hormone receptor. That would result in abnormalities in the insulin growth factor-1 (IGF-1) in T1DM [90] which consequently might have led to the retarded growth in uncontrolled DM, in our study. In the present study, the mineral appositional rates and bone formation rate in DM group were significantly lower in the most area of periosteal surface in mandible as compared to the control group. These results are in agreement with the previous studies that reported diminished lamellar bone formation in DM rats’ femur and may suggesting the putative association between the DM condition and the decreased number and function of osteoblasts [61]. The alveolar crest region was the only region that did not show a significant difference in the mineral apposition rate and the bone formation rate parameters between healthy and DM groups; this may be attributed to the unique nature of this region exhibiting a highly intensive bone remodeling process especially during the teeth eruption that decreases toward the base of the socket [77]. A significant decrease in bone volume fraction, trabecular thickness, and trabecular numbers was confirmed by micro-CT analysis in DM rats. DM rats also showed a significant increase in the trabecular separation and the trabecular space when compared with the control group. This finding indicated the deterioration of the bone quality in the DM group. These observations are in agreement with other works suggesting that the glycemic levels play an important role in modulating the trabecular architecture especially in mandibular bone [60]. In this context, these results may describe a state of osteopenia in experimental diabetic rats, which might be caused by an imbalance between bone formation and resorption. A histometric evaluation of bone resorption was performed by counting the number of osteoclast cells on the distal surface of the alveolar bone adjacent to the mesio-buccal root of the second molar. These evaluations revealed that the number of osteoclasts was significantly lower in the DM rats than in the controls, in line with the previous studies on DM rats’ mandible and long bones [58]. These studies confirm that the decreased rate of bone turnover may be associated with the DM condition. This worsening effect of the structure and dynamic bone formation on mandible might be due to a number of pathogenic potentials such as insulinopenia, bone microangiopathy, impaired regulation of mineral metabolism, alteration in local factors that regulate bone remodeling [57, 83]. However, the adverse effects observed may not be associated with the significant loss of rats’ weights observed in the diabetic group starting from day 14 because previous research [57, 60] showed that the mandibular growth was not affected in normal rats supplied with restricted diet and having same pattern of weight loss resembling weight loss pattern observed in DM rats.
Many investigations focused on the various detrimental effects exerted by the type 1 diabetes on different body organs; however, less attention was paid to the effect of such condition on teeth. A previous study suggested that the diabetic condition may exert detrimental effects on enamel formation [91]. However, that study was conducted on an extremely small sample size of different types of rodents suffering from diabetic conditions that were either genetically induced or drug induced and did not include a proper number of control rats. Thus, it was of an extreme importance to study the detrimental effect of diabetes on tooth structure formation using enough number of experimental animals and to use accurate methods of measurements as those adopted in the our studies. The null hypotheses tested in our previous study were partly accepted because the type 1 diabetes condition adversely affected the enamel and dentine thickness, and the dentine mineral apposition and dentine formation rates; however, there was no significant effect of the type 1 diabetes condition on the enamel and dentine mineral densities.
We have demonstrated that the type 1 diabetes condition induced detrimental changes on the thickness of enamel and dentine. Thus, it could be speculated that the metabolic functions of the ameloblasts and the odontoblasts may be hindered by the elevated blood glucose level associated with the type 1 diabetes condition. It was previously suggested that the type 1 diabetes condition affect ameloblasts and odontoblasts by a mechanism similar to the well-documented mechanism exerted by the type 1 diabetes condition on osteoblasts bone-forming cells due to the similarities between the process of dentine, enamel, and bone development [92]. Moreover, several genetic disorders were found to affect both the osteoblasts and odontoblasts and thus affecting the mineralization process of bone and dentine, respectively [92]. However, in contrast to bone, dentine and enamel do not remodel and are not involved in the regulation of the calcium and phosphate metabolism [93].
It was previously demonstrated that a glucose concentration similar to those observed in poorly controlled diabetic patients inhibited the osteoblast cells from depositing calcium during the mineralization process of the bone matrix [94]. One can speculate that a similar inhibitory effect was exhibited in the current study by the high glucose level on the activities of the odontoblasts and ameloblasts during the enamel and dentine formation. This inhibitory effect of increased glucose level on ameloblasts and odontoblasts was suggested by a previous study that showed that the total calcium content in rat teeth suffering from type 1 diabetes was significantly lower than those of their controls [95]. Another study reported a significant decrease in cultured pulp cells ability to proliferate and decreased mineralized nodule formation upon exposure to high levels of glucose [96]. Another mechanism that might explain the negative effects exerted by the type 1 diabetes condition on odontoblasts and ameloblasts activities may be attributed to the increase in blood glucose level that interferes with the maturation and the proper mineralization of the dentine collagen matrix during the dentine development stages [97]. Previous research work showed that the histological features of the ameloblast and its function might be affected by the increased glucose level associated with the type 1 diabetes condition [98]. Moreover, several clinical observations showed that enamel susceptibility to caries and the incidence of enamel hypoplasia increased in type 1 diabetes patients [99]. Furthermore, it was previously suggested that type 1 diabetes condition may exert a generalized decrease in the metabolic activities of bone cells. All of the aforementioned findings may suggest that the observed harmful effects exerted by the type 1 diabetes condition on enamel and dentine in this study may be a part of a generalized detrimental effect exerted by the diabetic condition on osteoblasts, odontoblasts, and ameloblasts.
It is obvious that type 1 diabetes condition significantly affects craniofacial growth, bone formation mechanism, and the quality of the bone formed, which may alter many aspects of planning and treatment of orthodontic patients affected by this globally increasing hormonal disturbance. Moreover, type 1 diabetes condition impairs the proper tooth development and alters the oral environment rendering teeth more susceptible to dental caries. There should be a new strategy for treating orthodontic patients suffering from metabolic disorders specially those disorders having direct and indirect effects on bone growth as the diabetic condition. The orthodontic craniofacial linear measurements were significantly decreased in the type 1 diabetes cases when compared to normal cases. Moreover, greater risks of developing dental caries and possible tooth loss are associated with patients suffering from type 1 diabetes; these risks may complicate the outcome of orthodontic treatment which is associated with less ability of orthodontic patients to implement proper oral hygiene measures due to increased areas of bacterial biofilm formation around orthodontic brackets. These comprehensive studies carried out on bone and craniofacial growth suggest that planning the treatment in craniofacial region for patients affected with hormonal disorders is more complex procedure than the treatment of normal patients. Up-to-date data also suggest that it is of prime importance to keep close attention to the general systemic condition of these patients and administer the proper hormonal therapy for these patients when needed to avoid any detrimental effects on bone resulting from any hormonal imbalance. Moreover, the results of tooth analysis in experimental type 1 diabetes model showed that the type 1 diabetes condition suppressed the enamel and dentine formation; however, the enamel and dentine densities were not affected. This indicates that diabetic patients may be more susceptible to dental caries and teeth size discrepancies. Type 1 diabetes patients’ dental problems should be handled carefully, and their diabetic condition monitoring is of prime importance, especially during early stage of tooth development.
Seed dormancy and germination are distinct physiological processes, and the transition from dormancy to germination is not only a critical developmental step in the life cycle of higher plants but also determines the failure or success of the subsequent seedling establishment and plant growth [1]. Seed germination begins with the water uptake of dry seed (imbibition) and ends with radicle protrusion. Seed germination is affected by adverse environmental conditions including salinity, high temperature, and drought [2].
\nIt is estimated that about approximately 7% of world land is affected by salinity and approximately 20% of 230 million ha irrigated land is salt-affected [3]. This number could be increased in the future due to increased land salinization as a consequence of contaminated artificial irrigation, climate change, and unsuitable land management. Salinity is a major stress responsible for the inhibition of seed germination or reduction in germination percentage and a delay in germination time in crops. At present, around 30 crop plants provide 90% of plant-based human food and the majority of these crops are not salt tolerant, even salt-sensitive, called glycophytes [4]. There have been high yield losses in these crops under moderate salinity (EC 4–8 dS m−1, approximately 40–80 mM NaCl) [5].
\nHigh salinity leads a decrease in osmotic potential of ambient soil water, resulting with a decrease in water uptake by dry seeds (imbibition). Besides, the absorption of excess Na+ and Cl− ions from soils creates ionic stress and cause toxicity which contributing to disruption in biochemical processes including nucleic and protein metabolism, energy production, and respiration [6]. Salinity also damages the nutrient and hormone balances, especially gibberellin (GA)/abscisic acid (ABA), during germination. As a result, high salinity level causes a delay in germination, even inhibition of seed germination depending on salt tolerance of plants. Dynamic balance between the generation and scavenging of reactive oxygen species (ROS) such as hydroxyl radicals, superoxide, and hydrogen peroxide could be disturbed by high salinity stress. ROS damage the macromolecules including proteins, carbohydrates, nucleic acids, and lipids, or cellular structures like membranes, resulting with inhibition of seed germination [7].
\nGermination has been found to be under strict regulation of plant hormones, especially GA and ABA [8]. ABA promotes seed dormancy and inhibits germination of seed, whereas GAs release dormancy and stimulate germination. Plant hormones ethylene (ET), and brassinosteroids (BRs) also have positive effect on seed germination by controlling the inhibitory effects of ABA on germination and rupturing testa and endosperm [9, 10]. The plant hormones widely took part in determining the physiological state of a seed and regulating the germination process by interacting each other [11]. Hormones are regulated by distinct transcription factors and signaling components including NO and H2O2, showing the complexity of seed germination regulation. While some plant genes control the activity of plant hormones, and the other plant genes are activated by plant hormones [10]. Signaling molecules, such as NO and H2O2, also promotes germination and reduce the dormancy by enhancing ABA catabolism and GA biosynthesis [12].
\nRapid seed germination and subsequent seedling establishment are important factors determining crop production and yield under salinity stress. One of the useful physiological approaches for glycophytes to adapt saline condition is seed priming [7]. Seed priming is an easy, low cost and low risk technique. The seeds are hydrated in specific solutions including plant hormones (GA3, ET, auxins, kinetin), antioxidant compounds (ascorbic acid, glutathione, tocopherone) organic solutes (proline, glycine betaine), inorganic salts (KNO3, CaCl2, and KCl), and particular bacteria and fungi species for a certain time to allow metabolic process of germination, followed by drying the seed to inhibit occurring of radicle protrusion [13].
\nPlants, being sessile nature, are simultaneously subjected to various adverse conditions including salinity, drought, cold, heat, excess water, and heavy metals, which limit their development and growth. Salinity is the major environmental stress source that restricts on agricultural productivity and sustainability in arid and semiarid regions [14]. Salinity is a global issue that affects about 7% of the world’s total land area, including 20% total cultivated lands and 33% of irrigated land, causing estimated yield losses of 20% worldwide [15, 16]. Besides, it is estimated that every year 10 million ha of agricultural land destroyed by salinized soil [17]. This rate can be increased by global climate change, use of contaminated irrigation water, intensive farming and poor drainage [18, 19, 20, 21, 22, 23, 24, 25, 26, 27, 28, 29, 30, 31, 32, 33, 34, 35, 36, 37, 38, 39, 40, 41, 42, 43, 44, 45, 46, 47, 48, 49, 50, 51, 52, 53, 54, 55, 56]. Without proper and sustainable control, salinity-affected areas will increase to more than 50% of the world’s total arable land by 2050 [15]. This rate can be accelerated by increase in sea water level by climate change, excessive use of groundwater for irrigation, increasing use of low-quality water for irrigation and massive introduction of irrigation associated with intensive farming and poor drainage [57].
\nSoil salinity is a measure of the concentration of all the soluble salts in soil water, and is usually expressed as electrical conductivity (EC) of the saturation extract (ECe) with units of deci siemens per meter (1 dS m−1) [58]. The soils were classified as saline, sodic or saline-sodic based on the total concentration of salt and the ratio of Na+ to Ca2+ and Mg2+ in the saturated extract of the soil [59]. When the ECe exceeds 4 dS m−1 (approximately 40 mM/L NaCl) and exchangeable sodium percentage is less than 15 with sodium adsorption ratio (SAR) < 13, the soil is saline. The major problem with saline soils is the presence of soluble salts, primarily Cl−, SO4\n2−, and sometimes NO3\n−. The pH of saline soils is usually below 8.5. Sodic (alkali) soils have an ECe < 4 dS m−1, ESP > 15, and SAR > 13. Therefore, Na+ is the major problem in these soils. Sodic soils have a pH between 8.5 and 10. Saline-sodic soils have an ECe > 4 dS m−1, SAR > 13, and an ESP > 15. Thus, both soluble salts and exchangeable Na+ are high in these soils. Saline-sodic soils have similar salt and pH levels as saline soils. USSL Staff [59] has described the general relationship of ECe and plant growth as the following:
non-saline (ECe ≤ 2 dS m−1): salinity effects mostly negligible;
very slightly saline (ECe = 2–4 dS m−1): yields of very sensitive crops may be restricted;
slightly saline (ECe = 4–8 dS m−1): yields of many crops are restricted;
moderately saline (ECe = 8–16 dS m−1): only salt tolerant crops yield satisfactorily; and
strongly saline (ECe ≥ 16 dS m−1): only a few very salt tolerant crops yield satisfactorily.
Seed germination is a complex multi-stage developmental process and regulated by internal and external factors. Internal factors include proteins, plant hormones (gibberellins/ABA balance, ethylene, and auxin), chromatin-related factors such as methylation, acetylation, histone ubiquitination, related genes (maturating genes and hormonal and epigenetics-regulating genes), non-enzymatic processes, seed age, seed size, and structural components of seed including (endosperm and seed coat). Besides, external factors containing moisture, light, salinity, temperature, acidity, and nutrient also affect the seed germination [60, 61].
\nSeed germination begins with imbibition, the uptake of water by the dry mature seed, and ends with visible protrusion of radicle through testa [62]. Successful germination requires optimum environmental conditions, including water, oxygen, and temperature to initiate this process. Germination/sprouting is regulated by plant hormones such as gibberellic acid (GA), abscisic acid (ABA), ethylene, auxins, cytokinins, and brassinosteroids [63]. Among them, ABA and GA are two important regulators, which play antagonistic roles in seed dormancy and germination [64].
\nThe process of seed germination can be divided into three phases (Figure 1) [65]. Phase I begins with imbibition of dry seeds and ends with the early plateau phase of water uptake. Phase II includes reactivation of metabolisms, significant induction of hormonal and enzyme activity using surviving structures and components in the desiccated cells, genes involved in amino acid and nucleic acid synthesis, restarting of cellular respiration with genesis of mitochondria, mobilization of reserved, RNA and protein synthesis machinery [66, 67]. Phase III is post-germination stage involves establishment of seedling and the induction of genes for photosynthetic metabolism after radicle cells elongate and divide [68].
\nMajor events associated with germination and subsequent post-germinative growth (based on [13, 65]).
Gibberellins and ABA are two key phytohormones regulating seed germination and seedling growth [69]. While GA breaks dormancy and enhances the seed germination and seedling, ABA inhibits germination and enhances seed dormancy [10] However, the ratio of the two hormones, rather than the absolute level of each hormone, plays a key role in regulating the breaking of seed dormancy and the onset of germination [70]. GA/ABA balance determines fate of the seed; germination or dormancy. Gibberellins induce the synthesis and production of α-amylase, proteases, and β-glucanases, resulting in the germination of seeds [71]. GAs also stimulate the genes involved in weakening of endosperm and expansion of embryo cell [10]. On the other hand, ABA suppresses expression of many hydrolytic enzyme genes to prevent viviparous germination and inhibits promoting effect of GA on radicle growth and embryo expansion by inhibiting water uptake and hence cell-wall loosening, which is a key step to start germination [72].
\nEthylene is a gaseous hormone involved in various processes, including positive regulation of seed germination. Ethylene breaks the primary and secondary dormancy and promotes seed germination by reducing ABA levels or sensitivity [73]. Brassinosteroids (BRs) and auxin induce the secretion of ethylene which works in conjunction with GAs to induce germination [10]. Auxins reduce seed sensitivity to ABA by overexpressing microRNAs and interacting with GAs to counteract ABA suppression during germination [74, 75].
\nLow temperature decreases seed dormancy and enhances germination in many species, while high temperature has the negative effect on germination and induces secondary dormancy [70]. High temperature down-regulates the genes involved in synthesis of GA synthesis and deactivation of ABA, whereas genes involved in ABA synthesis are up-regulated by high temperature. Therefore, transcriptional changes in ABA and GA metabolism and signal pathways results with inhibition of germination or a delay in germination [76]. Light has been considered both to stimulate germination and to terminate dormancy by increasing the expression of GA anabolic genes, GA3ox1 and GA3ox2, and repressing expression of GA catabolism gene GA2ox2 [77].
\nIn addition to phytohormones, several signal molecules, including as nitric oxide (NO) and reactive oxygen species (ROS), also regulate seed dormancy and germination [68]. ROS is an important regulator during seed germination because of the interaction with lipids, DNA, and protein molecules, as well as phytohormones including ABA and GA in the cell [78]. The biochemical and cellular reactions stimulated by water uptake are accompanied by the generation of ROS [79]. Hydrogen peroxide (H2O2) serves as a signaling hub for the regulation of seed dormancy and germination; the accurate regulation of H2O2 accumulation by the cell antioxidant mechanism is important to achieve a balance between oxidative signaling that enhances germination and oxidative damage that inhibits germination or delays in germination time [80]. N compounds, including NO, promotes seed germination through increasing amylase activities, adjusting K+/Na+ balance, and enhancing seed respiration and ATP production [81].
\nSalinity affects seed germination process through osmotic stress, ion-specific effects and oxidative stress, shown by decreasing germination rate and extended germination time [82]. Salinity increases external osmotic potential that reduces water uptake during imbibition [83]. Salinity may affect the germination of seeds by the toxic effects of excess sodium and chloride ions on embryo viability [84, 85]. The toxic effects include disruption to the structure of enzymes and other macromolecules, damage to cell organelles and the plasma membrane, the disruption of respiration, photosynthesis and protein synthesis [85, 86, 87].
\nIn general, seed germination progresses in three phases under normal conditions. Seed germination begins with the rapid water uptake by dry seed (imbibition) (Phase I). A plateau phase, known as phase II, follows this phase. The cellular metabolisms are reactivated, and water uptake is restricted in phase II. This is followed by phase III, a post-germination phase, which is characterized by continuous water uptake until germination is complete (Figure 1). Based on these three phases, the inhibition of seed germination or delaying in germination time under salinity stress may be generally ascribed to osmotic stress in the phase I and ionic stress in the phase II. Osmotic stress and ionic stress interact together to inhibit or delay germination of seed during the phase III [88].
\nSalinity may adversely influence seed germination by decreasing the amounts of seed germination stimulants such as GAs, enhancing ABA amounts, and altering membrane permeability and water behavior in the seed [89]. In higher plants, salinity has been demonstrated to change expression profiles of the genes encoding GA metabolic enzymes, including copalyl diphosphate synthase (CPS), ent-kaurene synthase (KS), ent-kaurene oxidase (KO), ent-kaurenoic acid oxidase (KOA), GA 20-oxidase (GA20ox), GA 3-oxidase (GA3ox) and GA 2-oxidase (GA2ox), resulting with change in endogenous GA levels during germination [12].
\nThe germination of seeds is characterized by transcriptional induction of hydrolytic enzymes such as α-amylase [90]. The α-amylase is excreted into the endosperm to break the stored starch to metabolizable sugars that provide ready energy and nutrients for the growing embryo and radicle. Salinity stress may have much effect on delayed germination time than on final germination percentage for most crops. A delay of water uptake and a decrease in the activity of α-amylase with an increase in the concentration of NaCl may be main reasons for delaying of the germination time [91]. The decrease in the α-amylase activity have been reported to be higher in the salt-sensitive genotypes than in the salt-tolerant genotypes. This reduction in the α-amylase activity results with a significant reduction in the translocation of sugars, essential for the developing embryo. Besides, decreasing sugar concentrations also change the osmotic potential of growing cells, resulting in a decrease in water uptake [88].
\nBoth osmotic and ionic effects of salt stress leads to generation of excess reactive oxygen species (ROS) and oxidative damage, which disrupts proteins, lipids, and nucleic acids or the cellular structure including lipid membrane [83].
\nPlants can be divided into two main groups based on their response to saline stress; salt-tolerant halophytes and salt-sensitive glycophytes (non-halophytes) [6]. The halophytes are plants that are able to grow in the presence of high salt concentrations that generate a low water potential of the soil and kill 99% of other species. They are adapted to survive and complete their life cycle under saline levels of higher than 200 mM NaCl. However, seed germination was also affected under salt stress and germination percentage was reduced to less than 10% under 1.7 M NaCl [92, 93]. In halophytes, maximum salt tolerance for seed germination has been reported to vary from 1.7 to 0.26 M NaCl depending on halophyte species and other environment conditions such as temperature, moisture, and light (Table 1).
\nPlant species | \n\n\n*\nMaximum salt tolerance | \nSalt tolerance type | \nReference | \n
---|---|---|---|
\nSalicornia herbacea\n | \n1.7 M NaCl | \nHalophyte | \n[93] | \n
\nSuaeda aralocapsica\n | \n1.5 M NaCl | \nHalophyte | \n[94] | \n
\nLimonium vulgare\n | \n1.5 M NaCl | \nHalophyte | \n[95] | \n
\nSarcocornia perennis\n | \n1.3 M NaCl | \nHalophyte | \n[96] | \n
\nHaloxylon ammodendron\n | \n1.3 M NaCl | \nHalophyte | \n[97] | \n
\nKochia scoparia\n | \n1.0 M NaCl | \nHalophyte | \n[98] | \n
\nKochia prostrata\n | \n0.85 M NaCl | \nHalophyte | \n[99] | \n
\nHaloxylon salicornicum\n | \n0.8 M NaCl | \nHalophyte | \n[100] | \n
\nProsopis juliflora\n | \n0.6 M NaCl | \nHalophyte | \n[100] | \n
\nLimonium mansanetianum\n | \n0.5 M NaCl | \nHalophyte | \n[101] | \n
\nLimonium stocksi\n | \n0.4 M NaCl | \nHalophyte | \n[102] | \n
\nLimonium lilacinum\n | \n0.3 M NaCl | \nHalophyte | \n[103] | \n
\nTanacetum cinerariifolium\n | \n0.26 M NaCl | \nHalophyte | \n[104] | \n
Quinoa (Chenopodium quinoa Willd.) | \n0.3 M NaCl | \nHalophyte | \n[105] | \n
Barley (Hordeum vulgare L.). | \n0.25 M NaCl | \nGlycophyte | \n[106] | \n
Maize (Zea mays) | \n0.24 M NaCl | \nGlycophyte | \n[107] | \n
Chicory (Cichorium intybus L.) | \n0.21 M NaCl | \nGlycophyte | \n[108] | \n
Lentil (Lens culinaris Medik.) | \n0.2 M NaCl | \nGlycophyte | \n[14] | \n
\nBrassica napus\n | \n0.2 M NaCl | \nGlycophyte | \n[109] | \n
Peanut (Arachis hypogaea) | \n0.2 M NaCl | \nGlycophyte | \n[110] | \n
Rice (Oryza sativa) | \n0.16 M NaCl | \nGlycophyte | \n[111] | \n
Fig (Ficus carica L.) | \n0.17 M NaCl | \nGlycophyte | \n[112] | \n
Button grass (Dactyloctenium radulans) | \n0.1 M NaCl | \nGlycophyte | \n[113] | \n
Sorghum (Sorghum bicolor Moench) | \n0.1 M NaCl | \nGlycophyte | \n[114] | \n
Ryegrass (Lolium rigidum) | \n0.1 M NaCl | \nGlycophyte | \n[115] | \n
Chickpea (Cicer arietinum L.) | \n0.09 M NaCl | \nGlycophyte | \n[116] | \n
Tomato (Solanum lycopersicum) | \n0.05 M NaCl | \nGlycophyte | \n[117] | \n
Maximum salt tolerance of halophytes and glycophytes at the germination stage.
Maximum NaCl concentration at which seed germination percentage reduced to 10–20%.
A majority of the common crops, such as tomato, bean, rice, corn, etc., are salinity sensitive or even hypersensitive and they are described as glycophytes [5]. The glycophytes contain 99% of the world’s flora and are susceptible to even low levels of salinity (ECe < 4 dS m−1, approximately 40 mM NaCl) [92]. Under conditions of moderate salinity (EC 4–8 dS m−1), all important glycophytic crops reduce average yields by 50–80% [118]. Seed germination in glycophytes is severely inhibited under salinity due to both osmotic stress and ionic toxicity stress, while halophytes are less affected by osmotic stress during germination [12].
\nMost crops are highly susceptible to saline soil, even when soil has electrical conductivity (ECe) as low as 3 dS m−1 [119]. Therefore, salinity stress appears to be a major limitation factor for crop productivity. Seed germination and seedling establishments are the two critical stages in plant growth. These stages are the most sensitive to environmental conditions including salinity [120]. Plants are usually seeded within the top layer of the soil which is more saline than lower layers [121]. Salinity stress may delay or prevent germination of germination of high quality seeds, resulting with crop loss. Rapid seed germination and subsequent seedling establishment are important factors affecting crop production under salinity conditions. Therefore, to decrease the negative effects of salinity stress on seed germination, it is important to know to what extent the genotypic variation in the water uptake pattern during these phases is associated with the salt tolerance of genotypes at the germination stage.
\nSeed priming is one of the useful physiological approaches for adaptation of glycophyte species to saline conditions during germination and subsequent seedling establishment. Seed priming is a simple, low cost and powerful biotechnological tool used to overcome the salinity problem by promoting seed germination and seedling establishment in agricultural lands [122]. Seed are exposed to an eliciting solution for a constant period that allows partial hydration, but radicle emergence does not occur by re-drying of seed. Seed germination occurs three distinct phases: (i) imbibition, (ii) lag phase (reactivation of metabolisms) and (iii) protrusion of the radicle through the testa. The goal of seed priming is to extend the lag phase, which allows pre-germinative physiological and biochemical processes, but prevent the seed transition towards full germination [123]. Enhanced and uniformed germination of primed seeds occurs by reduction in the lag time of imbibition, activation of enzyme involved in seed germination, initiation of biochemical mechanisms of cell repair, increase in the RNA content and DNA replication, decrease in ROS and lipid peroxidation with increased activity of antioxidant enzymes including as superoxide dismutase, catalase, and glutathione reductase, and increase in osmotic adjustment and starch metabolism [124, 125].
\nSeveral methods of seed priming have been developed in order to revive seeds under salt stress conditions. Some of these methods are hydro-priming, osmopriming, solid matrix priming, hormonal-priming, bio-priming, chemical priming, and nutripriming [13]. In recent years, many studies have been reported to exhibit the positive effects of seed priming on germination under salinity conditions in many crops (Table 2).
\nPlant | \nTreatment | \nAlleviating effect | \nReference | \n
---|---|---|---|
Barley (Hordeum vulgare cv. Bülbül 89) | \nPriming with aqueous solution of 30 μM H2O2 for 24 h at room temperature | \nH2O2 increased the germination index from 16.71 to 25.07%, and from 8.19 to 14.65% under 250 mM and 300 mM NaCl, respectively | \n[126] | \n
Tomato (Solanum lycopersicum cv. Hezuo 903) | \nPriming with 100 μM Epigallocatechin-3-Gallate (EGCG) at 28 ± 3°C | \nEGCG increased germination rate and index from 84.7 to 97.0%, and from 29.4 to 35.2%, respectively | \n[127] | \n
Wheat (Triticum aestivum cv. Chamran) | \nPriming with 0.5 mM spermidine for 24 h, 25 mM proline for 2 days, or 1.5 mM silicon (K2SiO3) for 6 h | \nSpermidine, proline, and K2SiO3 enhanced the germination rate by 32, 18, and 17%, respectively, under salinity stress (20 dS m−1) | \n[128] | \n
\nZea mays, Pisum sativum, Lathyrus sativus\n | \nPriming with 0.2 g/L GA3 solution for 12 h at room temperature without light. | \nGA3 enhanced germination percentage from 16.67, 26.67, and 50 to 60, 73.3, and 86.67% in Z. mays, P. sativum, and L. sativus, respectively, and resulted in 20% reduction in mean germination time under salinity stress (12 dS m−1) | \n[129] | \n
Pakchoi (Brassica chinensis L. cv Tiancuiqing) | \nPriming with sodium nitroprusside (SNP) for 2 h in dark at 25 ± 1°C | \nGermination potential, germination index, and vitality index were increased by 7.67%, 14.20% and 74.51% after 10 μM SNP pre-treatment under 100 mM NaCl | \n[130] | \n
\nMelilotus officinalis\n | \nSoaking with 10 mM Ca2+\n | \nCa2+ significantly increased the germination percentage and recovery germination percentage under 200 mM NaCl | \n[131] | \n
Melon (Cucumis melo) | \nPriming with 10–50 μM melatonin for 6 h | \nMelatonin increase the germination percentage from 50 to 80% under salinity stress (14 dS m−1) | \n[132] | \n
Wheat (Triticum aestivum cv. Khirman) | \nPriming with 50 mg L−1 ascorbate, 50 mM proline, 25 μM triacontanol, or 100 μM indole acetic acid for 12 h | \nPriming treatments significantly enhanced germination index and final germination percentage, and reduced mean germination time under salinity stress (12 dS m−1) | \n[133] | \n
Grain sorghum (Sorghum bicolor Moench) | \nPriming with 100–500 mg L−1 nano-iron oxide (n-Fe2O3) for 10 h and soaking with 10 mg L−1 n-Fe2O3 for 3 days | \nTreatments improved the speed and percent of germination under 150 mM NaCl | \n[134] | \n
Lentil (Lens culinaris cv. Ncir) | \nSoaking with 0.5 mM salicylic acid or 0.1 mM H2O2 at 25°C in the dark | \nSalicylic acid and H2O2 enhanced the germination percentage from 71 to 86 and 87%, respectively | \n[135] | \n
\nLimonium bicolor\n | \nPriming with 80 μM salicylic acid (SA) | \nSA significantly increased germination rate, germination potential, and germination index of the seeds under 200 mM NaCl | \n[136] | \n
Sweet sorghum (Sorghum bicolor cv. Chuntian 1) | \nPriming with 288 μM Gibberellin (GA3) for 32–48 h | \nGA3 significantly increased the water uptake, resulting with increased cumulative germination percentage and germination index under 100 mM NaCl | \n[122] | \n
Maize (Zea mays) | \nPriming with 2 mM silicon (K2SiO3) for 7 days at 25°C in the dark | \nSilicon significantly enhanced the germination rate and percentage, as well as vitality index under 90 mM NaCl | \n[137] | \n
Oat (Avena sativa cv. NDO-2) | \nPriming with 150 ppm gibberellin (GA3) for 24 h | \nGA3 enhanced the germination percentage from 56.64 to 76.03% under 100 mM NaCl | \n[138] | \n
Cucumber (Cucumis sativus cv. Jinyou 1) | \nPriming with 0.3 mM silicon (NaSi) for 36 h | \nSilicon enhanced the germination percentage and index, and seedling vigor index under 200 mM NaCl | \n[139] | \n
\nLimonium bicolor\n | \nPriming with 200 μM melatonin | \nMelatonin significantly increased germination rate, potential and index under 200 mM NaCl | \n[140]. | \n
\nCeratoides lanata\n | \nPriming with 10 mM ethephon, 5 μM fusicoccin or 50 μM kinetin | \nFusicoccin, kinetin, and ethephon increased the germination percentage from 10 to 40, 50, and 84%, respectively under 900 mM NaCl | \n[141] | \n
\nLeymus chinensis cv. Jisheng 3 | \nPriming with 200 μM gibberellins (GA4 + 7), 200 μM fluridone (FLU), 200 μM cytokinin (CK), 100 μM sodium nitroprusside (SNP), or 100 μM thiourea (TH) in the dark or light | \nGA and FLU significantly increased the germination percentage from 7 to 23 and 59% in the light, respectively, while SNP, CK and TH increased the germination percentage from 9 to 54, 55, and 30%, respectively, in the dark under 200 mM NaCl | \n[142] | \n
\nSalicornia ramosissima\n | \nInoculation with Bacillus aryabhattai SP1016-20 | \nInoculation with B. aryabhattai enhanced the final germination percentage and mean daily germination from 21.3 to 46.7%, and from 1.6 to 4.5%, respectively, under 510 mM NaCl | \n[143] | \n
The functions of seed priming in plant at the germination stage under salinity condition.
Hydro-priming is the simplest and one of the mostly used seed priming method. Hydro-priming depends on seed soaking in pure water without chemical substances for 6–24 h and re-drying to original moisture content prior to sowing without emergence of radicle [144]. This method is a low-cost and environmentally friendly due to no use of additional chemicals. The uncontrolled water uptake by seeds is major disadvantage of this technique. Rapid hydration may cause leakage of essential nutrients out of the seed during germination, resulting in seed damage in some species [145].
\nOsmo-priming, also known as osmotic conditioning, involves soaking seeds in aerated low water potential solution including sugar, polyethylene glycol (PEG), glycerol, sorbitol, or mannitol with low water potential instead of pure water, followed by air drying before sowing. Due to low water potential of osmotic solutions, water is absorbed slowly by dry seed, which allows gradual seed imbibition [146]. While osmo-priming promotes activation of early phases of germination, inhibiting radicle emergence. Osmo-priming improves seed germination and enhances general crop performance under salt conditions. Water potential of osmotic agent is critical factor since main purpose is to restrict oxidative damage caused by ROS by inhibiting excess water from entering [147]. If inorganic salts such as NaCl, KCl, KNO3, K3PO4, MgSO4, and CaCl2 are used as an osmo-priming agent, the method is generally referred as halopriming.
\nIn hormonal priming, seed imbibition occurs in the presence of plan hormones such as GA3, ethylene, auxins, and salicylic acid, which can gave effect on seed metabolism. Chemical priming is a promising seed priming technique to enhance germination under high salinity stress. Seeds were pre-treated with different chemical solutions used as priming agents. Chemical agents includes a wide range of both natural and synthetic compounds such as antioxidants (ascorbic acid, glutathione, tocopherol, and melatonin), sodium hydrosulfide, polyamines hydrogen peroxide, sodium nitroprusside, urea, selenium, chitosan, fungicide, etc. [13].
\nBiopriming involves seed imbibition together with particular bacteria or fungi. These microorganisms are able to create endophytic connections with the plant. As other priming method, this treatment increases rate and uniformity of germination under salt conditions, as well as protects seeds against the soil and seed-borne pathogens [147]. The most frequently used biopriming species are Bacillus spp., Enterobacter spp., Pseudomonas spp., and Trichoderma spp. [148].
\nSeed priming efficiency is influence by many factors and strongly depends on treated plant species and chosen priming technique. Physical and chemical factors including osmotica and water potential, priming agent, duration, temperature, presence or absence of light, aeration, and seed condition also influence priming success and determine germination rate and time, seedling vigor, and further plant development [13, 144].
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\\n\\nIntechOpen has the right to include/use the Author and Co-Authors names and likeness in connection with scientific dissemination, retrieval, archiving, web hosting and promotion and marketing of the Work and has the right to contact the Author and Co-Authors until the Work is publicly available on any platform owned and/or operated by IntechOpen.
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\\n\\nThird Party Rights: A person who is not a party to this Publication Agreement may not enforce any of its provisions under the Contracts (Rights of Third Parties) Act 1999.
\\n\\nEntire Agreement: This Publication Agreement constitutes the entire agreement between the parties in relation to its subject matter. It replaces all prior agreements, draft agreements, arrangements, collateral warranties, collateral contracts, statements, assurances, representations and undertakings of any nature made by, or on behalf of, the parties, whether oral or written, in relation to that subject matter. Each party acknowledges that in entering into this Publication Agreement it has not relied upon any oral or written statements, collateral or other warranties, assurances, representations or undertakings which were made by or on behalf of the other party in relation to the subject matter of this Publication Agreement at any time before its signature (known as the "Pre-Contractual Statements"), other than those which are set out in this Publication Agreement. Each party hereby waives all rights and remedies which might otherwise be available to it in relation to such Pre-Contractual Statements. Nothing in this clause shall exclude or restrict the liability of either party arising out of any fraudulent pre-contract misrepresentation or concealment.
\\n\\nWaiver: No failure or delay by a party to exercise any right or remedy provided under this Publication Agreement or by law shall constitute a waiver of that or any other right or remedy, nor shall it preclude or restrict the further exercise of that or any other right or remedy. No single or partial exercise of such right or remedy shall preclude or restrict the further exercise of that or any other right or remedy.
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\\n\\nNo partnership: Nothing in this Publication Agreement is intended to, or shall be deemed to, establish or create any partnership or joint venture or the relationship of principal and agent or employer and employee between IntechOpen and the Author or any Co-Author, nor authorize any party to make or enter into any commitments for, or on behalf of, any other party.
\\n\\nGoverning law: This Publication Agreement and any dispute or claim, including non-contractual disputes or claims arising out of, or in connection with it, or its subject matter or formation, shall be governed by and construed in accordance with the law of England and Wales. The parties submit to the exclusive jurisdiction of the English courts to settle any dispute or claim arising out of, or in connection with, this Publication Agreement, including any non-contractual disputes or claims.
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\n\nCORRESPONDING AUTHOR'S GRANT OF RIGHTS
\n\nSubject to the following Article, the Author grants to IntechOpen, during the full term of copyright, and any extensions or renewals of that term, the following:
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\n\nThe Author and Co-Authors also confirm and warrant that: (i) he/she has the power to enter into this Publication Agreement on his or her own behalf and on behalf of each Co-Author; and (ii) has the necessary rights and/or title in and to the Work to grant IntechOpen, on behalf of themselves and any Co-Author, the rights and licences in this Publication Agreement. If the Work was prepared jointly by the Author and Co-Authors, the Author confirms that: (i) all Co-Authors agree to the submission, license and publication of the Work on the terms of this Publication Agreement; and (ii) the Author has the authority to enter into this biding Publication Agreement on behalf of each Co-Author. The Author shall: (i) ensure each Co-Author complies with all relevant provisions of this Publication Agreement, including those relating to confidentiality, performance and standards, as if a party to this Publication Agreement; and (ii) remain primarily liable for all acts and/or omissions of each Co-Author.
\n\nThe Author agrees to indemnify IntechOpen harmless against all liabilities, costs, expenses, damages and losses, as well as all reasonable legal costs and expenses suffered or incurred by IntechOpen arising out of, or in connection with, any breach of the agreed confirmations and warranties. This indemnity shall not apply in a situation in which a claim results from IntechOpen's negligence or willful misconduct.
\n\nNothing in this Publication Agreement shall have the effect of excluding or limiting any liability for death or personal injury caused by negligence or any other liability that cannot be excluded or limited by applicable law.
\n\nTERMINATION
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\n\nIntechOpen agrees to offer free online access to readers and use reasonable efforts to promote the Publication to relevant audiences.
\n\nIntechOpen is granted the authority to enforce the rights from this Publication Agreement on behalf of the Author and Co-Authors against third parties, for example in cases of plagiarism or copyright infringements. In respect of any such infringement or suspected infringement of the copyright in the Work, IntechOpen shall have absolute discretion in addressing any such infringement that is likely to affect IntechOpen's rights under this Publication Agreement, including issuing and conducting proceedings against the suspected infringer.
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\n\nThird Party Rights: A person who is not a party to this Publication Agreement may not enforce any of its provisions under the Contracts (Rights of Third Parties) Act 1999.
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\n\nGoverning law: This Publication Agreement and any dispute or claim, including non-contractual disputes or claims arising out of, or in connection with it, or its subject matter or formation, shall be governed by and construed in accordance with the law of England and Wales. The parties submit to the exclusive jurisdiction of the English courts to settle any dispute or claim arising out of, or in connection with, this Publication Agreement, including any non-contractual disputes or claims.
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