Martin, Kathy PT, DHS; Kaltenmark, Tiffany DPT, PTA; Lewallen, Amanda DPT, ATC, LAT; Smith, Catherine DPT; Yoshida, Aika
Children presenting with weakness, low muscle tone, abnormal reflexes, and sensory and motor problems are commonly considered hypotonic by physicians and physical therapists.1–4 Many disorders, including neurological diseases, endocrine and systemic metabolic diseases, Down syndrome, nonspecific neuromuscular expression of malnutrition, chronic systemic illness, Prader–Willi syndrome, cerebral palsy, and spinal muscle atrophy often have hypotonia as a component of the clinical presentation.5–8 This partial list of medical diagnoses and disorders that are associated with hypotonia represents a wide variety of etiologies, including central nervous system pathology, peripheral nerve pathology, metabolic disturbances, and hypotonia of unknown origin.
Understanding of the global concept of muscle tone is necessary before hypotonicity can be correctly identified and quantified. Muscle tone is defined as “resistance to passive stretch while the patient is attempting to maintain a relaxed state of muscle activity.”9(p. 91) It can also be described as the amount of tension or stiffness in the resting muscle that is typically assessed by performing passive movement of the limb being tested.10 Leonard11 states muscle tone is influenced by both the mechanical-elastic properties of the muscle and the neural drive to the muscle. Crawford3 notes that the arousal level of the child must also be taken into consideration when assessing muscle tone. The clinical reality of examining muscle tone is that its assessment is subjective3,10,12,13 and even controversial.13 Thus, the concept of muscle tone is complex at best and challenging to quantify.
Although the term hypotonia is used frequently among healthcare professionals, a universal definition for this specific end of the muscle tone continuum does not yet exist. According to Ratliffe et al.,14 hypotonicity is “low muscle tone, characterized by lack of resistance to passive movement, poor definition of muscles, hypermobility of joints and sometimes decreased strength and endurance.”14(p. 432) Without a specific definition, quantification of hypotonia is difficult. A general muscle tone assessment scale has been published that includes definitions of levels of hypotonia (mild, moderate, and severe) and provides a grading system; however, no information on the development of this scale or its reliability and validity has been offered.15 The French Angles Factor of the Infant Neurological International Battery (INFANIB)16 is also said to examine hypotonia, but it fails to distinguish hypotonia from joint hypermobility. Thus, the currently available literature on hypotonia represents only descriptions or vague attempts to quantify hypotonia without sufficient evidence of reliability or validity.
The diagnosis of hypotonia made by physicians using various criteria are subjective in nature, as is assessment of muscle tone in general. In a retrospective study conducted by Paro-Panjan and Neubauer,12 newborns were considered to have hypotonia if they “looked floppy, felt floppy, and had hyperextensible joints.”12(p. 439) Other diagnostic criteria reported in the literature include decreased resistance to passive range of motion,17 decreased antigravity movements of the head and limbs,17,18 frogged posture (hip external rotation and abduction),17,18 and motor delays.19,20 Many of these authors make a distinction between hypotonia of central origin versus peripheral origin and cite numerous diagnostic studies that should be conducted to help with the differential diagnosis, including muscle biopsy, electromyographic studies, and nerve conduction velocity studies. However, the differential diagnosis process is still initiated based on a subjective clinical opinion about muscle tone, posture and antigravity movements.
Other health care professionals, including physical therapists (PTs) and occupational therapists (OTs), have not been able to do much better with defining and quantifying hypotonia. Recently, a study conducted by Martin et al.21 attempted to characterize hypotonia in children. The researchers surveyed pediatric PTs and OTs regarding the characteristics of hypotonia. According to this study, children with hypotonia displayed the following characteristics: decreased strength, hypermobile joints, increased flexibility, rounded shoulder posture, poor attention and motivation, leaning on supports, decreased activity tolerance, and delayed motor skill development. The results of this study gave a list of characteristics observed in children with hypotonia, but the study did not provide any objective criteria for quantifying or defining hypotonia. This study was also limited by the low response rate of 26.6% with a small sample size of 300, thus it may not have provided an accurate representation of the majority of practicing PTs and OTs.
Without a precise definition of hypotonia, proper examination or diagnostic tools cannot be developed. These tools are necessary for more accurate documentation of a child’s status. Currently, hypotonia is diagnosed by physicians using a process of exclusion following normal muscle biopsies and cerebellar imaging, or by the subjective judgments of the examiner using observation and passive range of motion.4,5,17,18 Therefore, the purpose of this study was to further develop and begin to confirm the previous study’s21 findings identifying eight clinical characteristics of hypotonia as described by PTs and OTs. This study also sought to increase the sample size of PTs and OTs to perhaps provide an opinion about hypotonia that is more representative of therapists in each profession. Results of this research will potentially contribute to the ongoing dialogue to operationally define hypotonia among health care professionals.
The Developmental Delay section of the American Occupational Therapy Association (AOTA) and the Section on Pediatrics of the American Physical Therapy Association (APTA) were contacted to obtain a mailing list of 500 randomly selected members from each group. The selection of members from these two professional groups helped assure that individuals surveyed had professional experience treating children with developmental delays and neuromuscular conditions.
The survey (Appendix 1) was developed based on the results of Martin et al.21 and consisted of both open- and closed-ended questions. The open-ended questions related to clinical observations that illustrated the eight characteristics found in the previous study. The survey also asked participants to describe any diagnostic/objective measures used to determine the presence of hypotonia or to quantify it. The last two open-ended questions on the survey pertained to long-term prognosis and asked for a definition of hypotonia.
The closed-ended questions pertained to participants’ level of agreement with the previous study’s21 list of characteristics of hypotonia. The participants were asked to rank these characteristics in order of frequency of occurrence as well as decide whether or not the characteristics improve with therapy services. The remainder of the closed-ended questions gathered demographic information about the professional experience of the participants.
Before the initiation of this research the study was approved by the University of Indianapolis’ Institutional Review Board. After receiving the mailing lists from the APTA and the AOTA, the researchers assigned each participant a randomly chosen number code from 1100–2500, where the first number represented the profession code (1 = APTA, 2 = AOTA). The surveys were then distributed by the United States Postal Service with a cover letter that also offered participants the opportunity to complete the survey online at http://www.surveyshare.com. The numeric codes were used to track nonrespondents for the purpose of mailing a second survey to enhance the response rate. Participants did not receive a consent form; however, the cover letter contained a statement that indicated return of the survey implied informed consent from the participants.
Data analysis began with an assessment of the reliability of data entry into an Excel spreadsheet. A random sample of 10% of the returned surveys was selected, and entry of the data for those surveys was reviewed by two members of the research team. No errors in data entry were found in this random sample. Qualitative analyses of two of the open-ended questions regarding objective measures (#5, Appendix 1) and effects of intervention (#6, Appendix 1) were analyzed and coded using a system developed from a random selection of 10 returned surveys (five from PTs and five from OTs). Three groups of researchers (two groups of DPT students, and one group of PT faculty members) independently reviewed all 10 surveys to develop thematic categories for the responses to these open-ended questions. Three groups were chosen to allow for consideration of possible differences in opinion about interpretation of the survey responses. After these reviews, all researchers met and negotiated to develop a consensus for the categories to be included in the coding system. All responses to these open-ended questions of the remaining surveys were coded based upon these categories. Responses that did not adequately match the established categories were noted and new categories were developed as needed through collaboration of the research team. Data analysis for the six closed-ended questions was performed using SPSS (version 12.0) to determine frequencies, means, and standard deviations for each response. The open-ended questions seeking clarification of characteristics (#3), prognosis (#7), and the respondent’s definition of hypotonia (#8) are reported in a separate manuscript.
Response Rate and Demographics
Among the 1000 distributed surveys, 268 were returned resulting in a 26.8% response rate. PTs returned 147 of the surveys and OTs returned 121. Of the returned surveys, 256 (25.6%; 116 PT and 140 OT) were returned by mail while 12 (1.2%; 7 PT and 5 OT) were submitted electronically. Partially completed surveys were also included in the data analysis. A summary of the respondents’ demographic data is included in Table 1. Most of the respondents had greater than 10 years of experience, practiced in either a school or outpatient setting, and treated more than 20 children per week.
Level of Agreement with Previously Identified Characteristics
Table 2 presents the percentage of respondents indicating each level of agreement for each of the eight characteristics. Respondents showed the highest levels of agreement, by indicating agree or strongly agree, for the following characteristics: hypermobile joints (89%), increased flexibility (85%), and decreased strength (83%). The lowest level of agreement (agree or strongly agree) was found for poor attention and motivation (30%) while 32% indicated they either disagreed or strongly disagreed that children with hypotonia displayed this characteristic.
Frequency of Occurrence for Characteristics
When forced to rank order the prevalence of each characteristic in children with hypotonia, 57% of the respondents assigned decreased strength with a rank of 1 or 2 (1 represented most common, 8 represented least common). Hypermobile joints was ranked as either 1 or 2 by 53% of our respondents, while 48% gave increased flexibility one of the top two ranks. Poor attention and motivation was assigned the least common rank order of 8 by 53% of the respondents. The mean ranks and standard deviations for the eight characteristics are provided in Table 3.
Assessment Tools and Diagnostic Tests
Observation and passive range of motion most often were reported as the primary examination methods used by respondents (Fig. 1). Approximately 20.5% of the respondents reported that they did not use an examination tool for hypotonia, and 53% of respondents stated that they used observation to examine hypotonia. Therefore, a total of 73.5% of our respondents indicated that they did not use a formal examination tool to evaluate for hypotonia.
Characteristics and Changes with Therapy
Most clinicians (85.4%) indicated that characteristics observed with hypotonia improve with therapy, while only 14.6% reported no improvement. The respondents who reported hypotonia improved with therapy indicated that change was greatest in the areas of strength (41.4%), meeting developmental milestones (22%), increased endurance (18.3%), and increased function (16.8%). Figure 2 represents the most common changes reported for PT and OT interventions.
Nearly 75% of our respondents stated that no objective tool was available to examine hypotonia. Nonetheless, PTs and OTs reported that they try to find objective measures to help document a child’s status. Developmental milestones tests, strength testing, and observation of posture and antigravity movements were cited by some as ways to attempt to examine hypotonia. Similar strategies have been reported in published articles. Clinical opinion based on observation of the infant by a neonatologist was cited as the basis for the diagnosis of hypotonia in one study.12 Delayed milestones7; posture assessment7,17; and antigravity control of limbs, head, and trunk (pull to sit, ventral suspension)7,10,12,17 all have been reported as examination techniques. No objective criteria have been published for the quantification of hypotonia.
Most of the respondents (83%) agreed or strongly agreed that decreased strength was a characteristic observed in children with hypotonia. Strength can be quantified in most cases and maximal force production can be examined through manual muscle testing and use of dynamometers. PTs and OTs may identify decreased strength as a common characteristic of hypotonia because they are searching for an objective way to document a child’s muscle tone and strength is more readily examined and quantified than tone. However, Jacobson10 wrote that “weakness and hypotonia are different aspects of motor control that should not be used interchangeably.”10(p. 156) Further confusing the issue is Crawford’s3 opinion that ‘weak infants are always hypotonic but hypotonia may exist without weakness.”3(p. 348) Thus, the majority opinion in our results that decreased strength is a part of the clinical picture of hypotonia needs to be interpreted carefully, and quantification of strength may not be an appropriate examination for hypotonia.
Most authors agree that the presence or absence of weakness with hypotonia depends on the etiology of the hypotonia, and that weakness implies involvement of the motor unit in some way.3,17,22 The challenge for PTs and OTs is to link muscle tone with motor performance in a way that can be objectively documented. Electromyographic studies have attempted to establish a link between muscle tone, the function of the motor unit, and force production, or strength, but have had conflicting results.13,23 Thus, the validity of linking strength and hypotonia is not yet established in the literature.
Hypermobile Joints and Increased Flexibility
Most respondents in this study either agreed or strongly agreed that hypermobile joints (89%) and increased flexibility (85%) were characteristics observed in children with hypotonia. Numerous authors acknowledge that hypermobile joints are often associated with hypotonia.3,4,7,12,14,20,24 The INFANIB16 is said to examine hypotonia by assessing mobility at several joints, but some authors acknowledge that this tool does not fully capture the concept of muscle tone.4 Jacobson10 noted that care should be taken when examining hypermobility to assess the contributions of ligamentous laxity versus muscle extensibility, and it is our opinion that the INFANIB does not differentiate the source (muscle tone, muscle extensibility or ligamentous structures) of hypermobility.
Lautenslager et al.2 proposed that hypermobile joints present confounding variables. These variables are a “lack of stabilizing myogenous contractions around joints (co-contractions), proprioception, and hypermobility of joints.”2(p. 11) Several authors wrote that joint laxity may be the result of a genetic defect resulting in abnormal collagen and thus ligamentous and joint capsule laxity.4,24 However, other authors suggest that joint laxity may be the result of not only ligamentous laxity, but of hypotonia itself.4,20 Thus, although there is agreement that hypotonia and hypermobility frequently occur together, the exact nature of this relationship and what factors contribute to the relationship remains unclear.
Our respondents also agreed that increased flexibility was often a characteristic of hypotonia. Increased flexibility can be caused either by muscle properties, including increased fiber length, or joint properties such as ligamentous laxity. Our results did not offer a clear distinction between joint hypermobility and increased flexibility, and the literature reviewed failed to establish a clear relationship between hypermobile joints, increased flexibility and hypotonia. In fact, the studies we reviewed focused on hypermobility and did not address increased flexibility as a separate phenomenon. The respondents for this study were not asked to differentiate between the two characteristics, nor were the terms operationally defined in our survey.
Rounded Shoulder Posture
The results of this study showed that 67% of respondents either agreed or strongly agreed that rounded shoulder posture was a characteristic of hypotonia. However, there is a lack of literature to support the specific presentation of rounded shoulder posture in children with hypotonia. Kovacs17 noted atypical sitting or standing postures in children with hypotonia, while Blackman7 commented on abnormal posture in ventral suspension of infants with hypotonia. Neither of these authors provides support for or refute the notion of a rounded shoulder posture that our respondents report. While reviewing the responses from our study, we discovered an individual who reported that children may ‘use protraction to create a stable posture, giving the appearance of rounded shoulders.‘ Thus, this posture could be a compensation for decreased muscular strength and endurance rather than a characteristic of hypotonia. More research is needed to determine the relationship between rounded shoulder posture and hypotonia.
Delayed Motor Skills
Eighty percent of our respondents either agreed or strongly agreed that delayed development of motor skills are evident in children with hypotonia. However, contradictions exist in the literature regarding this relationship. Crawford3 and Blackman7 both noted that delayed achievement of motor milestones may be the predominant complaint for older infants and children with hypotonia. Bodensteiner25 has noted that decreased axial tone may lead to a delay in acquisition of motor milestones. In contrast, Steifel26 noted that developmental delay is typically absent in benign congenital hypotonia. In another study the researchers specifically examined the relationship between hypotonia and developmental delay by doing a secondary analysis of longitudinal data and concluded that hypotonia, as measure by the INFANIB, was not related to motor delays at the ages of seven, 10 or 15 months.4 The authors acknowledged that their results contradicted many previously published articles, but suggested that differences in how muscle tone, joint laxity and motor development were assessed could explain the different conclusions. The authors also acknowledged that part of the challenge in this line of research is finding valid and reliable tools to examine the constructs of hypotonia and joint laxity.
Delay in motor development is a commonly accepted component of some conditions such as Down syndrome2,27 and Prader−Willi syndrome,8 which also are characterized by hypotonia. Our respondents did not address, nor were they prompted to identify, whether or not they were describing characteristics of a specific condition that included hypotonia as a component. Thus, it is unclear whether developmental delay may be associated with hypotonia itself or is the result of the multiple issues seen with a specific diagnosis that affects more than just muscle tone.
Despite the lack of agreement in the scientific literature on this topic, respondents from our study, as well as the report by Martin et al.21 indicate that delayed development of motor skills was associated with hypotonia. Additional research is needed to clarify the relationship between delayed motor skills and hypotonia.
Leaning on Supports
Our respondents supported the previous study’s21 results in that 76% either agreed or strongly agreed that children with hypotonia often lean on supports. Currently, the literature lacks evidence to support or contradict the need for external support for children with hypotonia. We believe that decreased strength, endurance, proximal stability, and delayed motor skills may all be factors that lead the child to require external support to maintain a posture. We also believe that PTs and OTs have increased contact with children while they are engaged in physical activity in comparison to other healthcare professions. This increased contact time with increased opportunity to observe activity may allow therapists to more frequently note this behavior. In order to adequately support or contradict our findings, more research needs to be conducted to determine reasons as to why supports are needed or used and the frequency of use by children with hypotonia.
Poor Attention and Motivation
Although decreased attention and motivation were noted by 32.5% of the respondents as a characteristic of hypotonia in the report by Martin et al.,21 our respondents failed to reach consensus on this characteristic. Only 30% agreed or strongly agreed and 32% disagreed or strongly disagreed. An even larger percentage (36%) were neutral on this topic; however, when the participants were asked to rank order the characteristics, 53% ranked decreased attention and motivation as the least commonly occurring characteristic.
We believe that decreased endurance or lack of ability to explore the environment secondary to decreased strength might be factors contributing to reports of poor attention and motivation. Lower levels of endurance may cause a child with hypotonia to readily quit tasks that require increased effort. Only one article that we reviewed addressed this issue. Crawford3 suggested that infants with hypotonia have learned not to attempt tasks for which they do not have adequate strength, thus they may have the appearance of having poor motivation. However, Crawford further stated that infants with hypotonia and normal intelligence often find creative ways to play and interact to compensate for their weakness. This could be interpreted to imply normal or even increased motivation. Considering this together with our results, we concluded that decreased attention and motivation may not be a characteristic of hypotonia as previously reported by Martin et al.21
Decreased Activity Tolerance
Respondents in this study identified decreased activity tolerance as a characteristic observed in children with hypotonia as 68% agreed or strongly agreed. Only one of the research articles we reviewed addressed this characteristic. Crawford3 noted that fatigue was challenging to examine in an infant because it required sustained maximal effort, and the examiner would have no way knowing if this actually occurred with an infant or young child. We found no published evidence to support or refute the presence of decreased activity tolerance with hypotonia as suggested by Crawford.3
Most of the research that exists regarding hypotonia addresses medical issues rather than the signs and clinical presentations that would be observed from the perspectives of practicing PTs and OTs. Therapists may have more opportunities to observe activity tolerance as it may present as a limiting factor during their intervention sessions. Previous literature has linked decreased strength to hypotonia, therefore it seems logical that decreased activity tolerance would be another characteristic that would be at least indirectly related. Children with hypotonia may exhibit decreased activity tolerance for bouts of activity that require strength. Results of the previous and current study revealed that decreased activity tolerance in children with hypotonia is a shared clinical observation of both OTs and PTs. This demonstrates the need for additional research to explore the relationship between activity tolerance and hypotonia.
Improvement with Therapy
Our survey asked whether or not children with hypotonia improved with PT and/or OT. The majority of respondents (85.4%) stated that children with hypotonia do improve with PT or OT and gave examples of improvements (Fig. 2). Improvements discussed in the literature are usually in reference to benign congenital hypotonia (BCH) or Down syndrome. BCH is a diagnosis of exclusion26 used to describe infants with hypotonia for which an etiology has not been identified. With respect to BCH, most authors report that the prognosis is good3,4,7,19,20 with improvement with neurological findings and even spontaneous recovery in some.19 In contrast, Down syndrome is arguably the most common condition associated with hypotonia and there is a lack of consensus in the literature about improvements as a result of therapy for children with Down syndrome.
According to Mahoney, Robinson, and Fewell,28 a year of early intervention was not shown to be any better than simply the passage of time (maturation) for children with Down syndrome. An earlier study reached a similar conclusion in that nine weeks of intervention (neurodevelopmental therapy) did not provide significant differences in motor development for a group of children with Down syndrome when compared to a matched control group.29 In contrast, a study that examined the use of an intense, skill- and task-specific intervention (treadmill training) showed that children with Down syndrome developed independent ambulation an average of 101 days earlier than a control group.30 Adding to the confusion about whether or not children with Down syndrome improve with therapy is a longitudinal study that noted that while early intervention programming improved outcomes for intellectual and adaptive functioning, adolescents continued to display deficits in postural control.31 Thus the literature on improvement with therapy for children with Down syndrome is mixed with some studies supporting the effectiveness of therapy and other studies contradicting this finding.
Differing reports about the prognosis for BCH also appear in the literature. Steifel26 noted that hypotonia persists into adult life, but weakness and developmental delay are usually absent. In contrast, some authors acknowledge that some lingering effects of hypotonia may exist as Crawford3 stated that children with BCH usually do well but also reported that clumsiness and even cognitive problems may be present in older children. Carboni et al.20 stated that hypotonic muscles that are weak will become progressively weaker without sufficient active exercise of those muscle groups.
Diagnoses are often the basis for establishing prognoses, but not everyone agrees that BCH is an appropriate diagnosis. Thompson32 insists that the term BCH should not be used and that its use has not been appropriate since the 1960s. She states that a thorough diagnostic work-up should be done to find the etiology of hypotonia in order to appropriately counsel the family. Carboni and colleagues20 acknowledged that the term BCH is confusing, and they proposed the term, “congenital hypotonia with favorable outcome.” In contrast to Thompson,32 Carboni and colleagues20 stated that the etiology of hypotonia and a specific diagnosis is not always possible to establish.
Regardless of the diagnostic label applied to children with hypotonia, the results of our study and the review of literature we conducted seem to favor a good prognosis in general. The question remains whether or not this improvement in motor skills is the result of therapeutic intervention or simply maturation with time. The results of our study represent the clinical opinions of the respondents and were not linked to a specific etiology of hypotonia or diagnosis. Therefore, conclusions about prognosis based on this study should be interpreted with caution.
A major limitation of the study was the low response rate. We anticipated a low response rate based on the rate from the previous survey on hypotonia.21 In an attempt to compensate for the anticipated low response rate, we dramatically increased the sample size (N = 1000) compared with the previous study (N = 300). Although the response rate of this study (25.6%) was slightly lower than the previous study’s rate (28.6%), we collected substantially more responses this time (268 vs 86). Nonetheless, the poor response rate means that this study may not represent the consensus opinion of pediatric PTs and OTs and the results should be interpreted with caution. It is possible that the response rate of this study was negatively affected by the difficult task of describing and defining hypotonia. Therapists who have not had much success treating children with hypotonia might have been less likely to respond, perhaps because they felt they did not have the answers to the questions posed in the survey. In contrast, the clinicians with the strongest opinions about hypotonia may have been more likely to respond, which could have skewed overall responses obtained in the study.
Other limitations could have been researcher and/or respondent bias. Despite efforts to minimize the effects of researcher bias, previously held opinions of the researchers could have shaped the wording of questions used in the survey and therefore may have had an effect on the way in which respondents answered questions. Finally, we did not attempt to differentiate between hypotonia of various etiologies (ie, central versus peripheral). Some of the literature we reviewed did make distinctions about clinical presentation of hypotonia based on its etiology. It is unclear whether our respondents were responding to hypotonia in general or to hypotonia associated with a specific etiology or diagnosis as we did not ask them to specify this in their answers.
The respondents of this study agreed with a previous study21 that children with hypotonia present with decreased strength, hypermobile joints, increased flexibility, rounded shoulder posture, delayed motor skills, decreased activity tolerance, and a need to lean on supports. However, respondents expressed less agreement about decreased attention and motivation as a characteristic of hypotonia. Review of existing literature and results of our current study demonstrate a substantial need for further research in determining the primary characteristics accompanying hypotonia and the nature of the relationship between these characteristics and hypotonia. This study took another step toward characterizing hypotonia, and the development of an operational definition of hypotonia will aid in the assessment of and intervention for pediatric patients with low tone. However, further studies need to compare these findings with responses with other health care professionals (pediatricians, neurologists, etc) who are frequently involved with the care of children with hypotonia.
We would like to express our appreciation to Clyde Killian, PT, PhD, for his assistance and guidance with the statistical analysis of our data.
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