A Clinical Study of the Korotkoff Phases of Blood Pressure in Children

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Journal of Human Hypertension (2001) 15, 197–201  2001 Nature Publishing Group All rights reserved 0950-9240/01 $15.00 www.nature.com/jhh ORIGINAL ARTICLE A clinical study of the Korotkoff phases of blood pressure in children

J O’Sullivan1, J Allen2 and A Murray2 Departments of 1Paediatric Cardiology and 2Regional Medical Physics Department, Freeman Hospital, Newcastle upon Tyne, UK

Background: Five Korotkoff phases are described in re-assessed there was no significant difference in the adults, but there are no studies of the Korotkoff phase phase distribution of the sounds. All five phases were distribution in children. This study determines the pres- present in 40% (28/70). Phase III only occurred in the ence and length of Korotkoff phases in children, provid- presence of phase II (P Ͻ 0.0001). There was no signifi- ing data on the repeatability of these measurements, the cant relationship between the presence of the different relationship between the phases, and finally the phases and heart rate or blood pressure. Arm circumfer- relationship between the phases and heart rate, blood ence was significantly larger in children with phase V pressure and arm circumference. present (P Ͻ 0.02). Methods: Seventy, 11-year-old children were studied. Conclusions: The Korotkoff sounds and phase distri- The Korotkoff sounds were recorded from the bell of a bution present in normal children is described. Korot- stethoscope to a MiniDisc system and each sound koff sounds were consistently allocated to the various described twice on separate occasions as phase I, II, III Korotkoff phases. This study provides insights into the or IV, with phase V meaning disappearance of the problems of accurate diastolic blood pressure measure- sound. ment. Phase V was more likely to be present with Results: Phases I, II, III, IV and V were present in 97% increasing arm circumference, but the variation in the (68/70), 61% (43/70), 51% (36/70), 88% (62/70) and 80% occurrence of phases II and III remains unexplained. (56/70) respectively. When the recordings were blindly Journal of Human Hypertension (2001) 15, 197–201

Keywords: Korotkoff sounds; diastolic blood pressure

Introduction the Korotkoff sounds present in normal children; how consistently the sounds could be allocated to The measurement of blood pressure using the Korot- the various phases on repeat assessment, the koff method is done by listening over the brachial relationship between phases, and how the Korotkoff artery during deflation of an upper arm cuff. In 1905 1,2 phases relate to heart rate, systolic and diastolic Korotkoff described three different sounds that blood pressure, and arm circumference. could be distinguished by listening with a stethoscope placed over the brachial artery. The original description of the sounds has been slightly modified Subjects and methods over the years and we now recognise four different Subjects types of sound (and five phases).2 The pressure in the mercury sphygmomanometer A local secondary school agreed to participate in the when the first sounds are heard represents systolic study. Following a visit to the school, children took blood pressure and there is continuing debate as to a consent form home to their parent/guardian. The whether disappearance (phase V) or muffling of study was carried out on a normal school day that sounds (phase IV) best represents diastolic pressure did not include a physical education class. Formal in children.3 Even though it is recognised that phase approval was obtained from the local Ethics Com- V (disappearance of sounds) may be absent in chil- mittee. dren, the presence or otherwise of the other four phases has not been described. This study describes Recording equipment The Korotkoff sound measurement system is illus- Correspondence: Dr John O’Sullivan, Department of Paediatric trated in Figure 1. The bell of a Littmann cardiology Cardiology, Freeman Hospital, Newcastle upon Tyne, NE7 7DN, UK. E-mail: J.J.OsullivanȰncl.ac.uk grade stethoscope (No 2151, 3M) was attached to a Received 22 May 2000; revised 5 August 2000; accepted 11 miniature high sensitivity ceramic microphone (BL- August 2000 1994, Knowles Electronics Co) using 60 cm of Korotkoff sounds in children J O’Sullivan et al 198 dren of this age the 5th centile for diastolic pressure is over 40 mm Hg.4

Korotkoff sound analysis The Korotkoff phases were identified by the character of the sounds, as outlined by Geddes;2 phase I sounds are loud with a clear-cut and snapping tone, phase II sounds have a murmur-like quality, phase III sounds are similar in character to first phase sounds, and phase IV sounds have a dull or muffled tone. The fifth phase represents the complete disap- Figure 1 The figure shows the arm cuff which is inflated auto- pearance of the sounds. One of the investigators matically and which is deflated at an approximate constant rate. The stethoscope is connected to a microphone, allowing the (JO’S) allocated each of the sounds to one of these investigator to listen through headphones to the sounds being phases and repeated it 2 months later (blinded) to recorded onto MiniDisc. check consistency. Since the cuff deflated rapidly below 30 mm Hg it was not possible to say if phase V was absent, but for the purposes of analysis, if sounds persisted to 30 mm Hg then phase V was stethoscope tubing. An amplifier was connected to said to be absent. If the first sounds heard had a mur- the microphone with the highest frequency range of mur-like quality then phase I was said to be absent. the amplifier chosen to provide realistic and faithful The number of beats heard in phases I to IV was audio-quality reproduction on listening. In addition, counted and the length of each phase measured. all components of the measurement system were chosen to extend down to 10 Hz to cover the audible hearing range in humans. The signal was then Statistical methods passed to a Sony MDS-JB930 MiniDisc digital The relationship between the blood pressure and recorder which provided high quality sound repro- arm circumference was analysed using standard ductions with low noise. The operator listened regression plots. The differences in phase lengths through a set of studio quality audio headphones and also arm circumference for the phase groups (Beyer, DT150) during recording and playback. To were assessed using the Mann-Whitney test. The obtain a consistent and controlled release of air from inter-relationship between phases II and III was the arm cuff an automatic blood pressure monitoring assessed using the Chi-squared test. In assessing device (A&D Blood Pressure Monitor, TM2421) was paired differences in repeat data the confidence modified to provide consistent cuff deflation from intervals of ±2 standard deviations about a mean dif- 130 down to 30 mm Hg at a mean deflation rate of ference level, as recommended by Bland and Alt- −3.3 mm Hg/s. man, were calculated.5

Measurement procedure Results Children were studied in a quiet room in the school. Blood pressure and arm circumference Each child sat quietly for at least 10 min before the Seventy children (31 males), all aged 11 years, were measurements. An appropriate sized pressure cuff studied. Median height was 150 cm (Interquartile (bladder width at least 40% of the arm range (IQR): 146–155 cm) and median arm circum- circumference) was placed around the left arm and ference was 22 cm (IQR: 21–24 cm). The systolic was supported near to heart level using a cushion. blood pressure ranged from 84 mm Hg to 130 mm Hg A Doppler ultrasound probe (Dopplex, Huntleigh and diastolic pressure from 50 mm Hg to 78 mm Hg. Healthcare) was used to locate the clearest pulsatile These parameters are presented for boys and girls signal at the antecubital fossa and the skin marked. separately in Table 1. There was a significant corre- Blood pressure was first measured with a mercury Table 1 The table details some of the measurements obtained in sphygmomanometer, using phase V (if present) for boys and girls separately. The mean values (± standard deviation) diastolic. The Korotkoff sounds were then recorded for heart rate (beats per minute), systolic blood pressure, diastolic using the equipment described above. There were blood pressure (phase V), arm circumference (cm) and standing two stages: a first one to preview the sounds and the height (cm) are provided second to make a recording to MiniDisc. Subjects were asked to keep still but relaxed during the Male Female measurement. Each recording lasted for 1 min ± ± allowing ample time for the deflation cycle. A Heart rate 80.2 ( 11.4) 83.8 ( 12.3) Systolic BP 99.9 (±9.2) 99.7 (±9.6) ‘bleep’ was generated once the cuff pressure fell Diastolic BP 61.7 (±9.2) 63.1 (±9.5) below the start of rapid deflation at 30 mm Hg, as Arm Circumference 22.8 (±4.5) 23.3 (±4.5) this allowed the listener to ignore any sounds after Height 150.8 (±27.4) 150 (±8.8) this point. This was considered valid since in chil-

Journal of Human Hypertension Korotkoff sounds in children J O’Sullivan et al 199 lation between the systolic and diastolic blood The largest difference was in phase IV with a differ- pressure (r = 0.32, P Ͻ 0.01). There was a significant ence of less than one beat. The discrepancy in phase correlation between arm circumference and height IV sounds (muffling) was due to their low amplitude (r = 0.44; P Ͻ 0.001). There was also a significant and these sounds faded rather than abruptly ceased relationship between arm circumference and both making it difficult to decide whether the sound had systolic and diastolic blood pressure (r = 0.44, P Ͻ disappeared or was still faintly present. 0.001 and r = 0.29, P Ͻ 0.05), with larger arm cir- cumferences associated with higher pressures. Pattern of Korotkoff phases present The patterns of Korotkoff phases present is Reproducibility of the Korotkoff sound analysis presented in Table 2. In virtually all children phase When the same investigator (blinded) listened again I was present (68/70, 97%) and phase IV (muffling) to the recordings, the phases identified in each child was identified in 62/70 (88%). Sounds persisted to were identical to those identified on the first except the end of the controlled deflation (30 mm Hg) in for two children where phases IV was thought to be 14 children suggesting that under these conditions present on one occasion but not on the other. The phase V does not occur in approximately 20% of number of beats allocated to each phase on both children. Phase II and phase III sounds were present occasions is shown in Figure 2. There was no sig- in 43/70 (61%) and 36/70 (51%) respectively. Less nificant difference with the repeats for any phase. than half of the children (28/70) had all five phases. Phase III only occurred with phase II, with phase II being present without phase III in only seven children. This was highly significant (P Ͻ 0.0001). The proportions of the phases are shown in Figure 3. There was no significant difference in the proportion of each phase in the repeat assessment. The length of the phases is shown in Figure 4. Phase I was significantly longer in those children where phases II and III were absent (8.2 s [IQR 6.4– 10.9] compared to 3.2 s [IQR 2.4–4.6], P Ͻ 0.00001), and similarly for the number of beats (10.5 beats [IQR 9–15] compared to 4.0 beats [IQR 4.0–6.0], P Ͻ 0.00001). Phase IV was significantly longer when phase V was absent (13.7 s [IQR 12.0–15.4] compared to 3.7 s [IQR 1.7–8.7], P Ͻ 0.00001), and similarly for the number of beats (17.0 beats [IQR 14.8– 22.3] compared to 7.3 beats [IQR 2.3–11.8], P Ͻ 0.00001).

Relationship between Korotkoff phases and other parameters There was no significant relationship between the relative duration of the various phases and heart rate. Also, the presence or absence of the various phases had no significant relationship with heart rate, sex, systolic or diastolic blood pressure. We did, however, find that arm circumference (Figure 5) was significantly larger in those with phase V (23.0 cm, [IQR 22.0–25.0]) versus those with no phase V (21.5 cm, [21.0–22.0], P Ͻ 0.02).

Discussion The only previous studies on the clinical description of all Korotkoff phases in the literature were undertaken in adults over 80 years ago. Swan6 Figure 2 (a) The number of beats allocated to the various phases described the Korotkoff phases in 200 adults. All when the recordings were assessed on the ﬁrst (1) and second (2) phases were present in about 40% and phase IV was occasions (median ± Inter-quartile range (IQR). (b) The difference in the number of beats allocated to the different phases when detected in less than half of the subjects. Goodman 7,8 the recordings were assessed on the second occasion. The mean and Howell measured the proportion of the pulse difference ±2 standard deviations are shown in the ﬁgure. pressure that the phases occupied and reported that

Journal of Human Hypertension Korotkoff sounds in children J O’Sullivan et al 200 Table 2 The table shows the different patterns of phases present in the 70 children. The area is shaded if that phase is present. No. = number of children with the different patterns of phase distribution

I II III IV V No. (=70)

28 15 7 6 5 3 2 1 1 1 1 68 43 36 62 56

Figure 5 Children were divided into those with (yes) and those Figure 3 The duration of the Korotkoff sounds for each individ- without (no) phase V. The difference in arm circumference ual was measured and the proportion occupied by each phase between these two groups is presented with each individual calculated. These proportions are presented in the figure (median value shown as an open circle and the group median (± Inter- ± Inter-quartile range (IQR)) for each phase and for the two quartile range) as the closed circles. occasions when the sounds were assessed. The numbers 1 and 2 on the figure refer to the first and second assessments (respectively) of the recordings. phase II was the longest phase. In these studies the Korotkoff sounds were analysed during the actual blood pressure measurement which has large poten- tial errors as it is very difficult to achieve consistent rate of manual cuff deflation and the investigator had only one opportunity to allocate the sounds to the various phases. Our method allowed consistent cuff deflation and recording of the sounds for later analysis. Using this approach each sound was described as phase I, II, III or IV and the allocation of the sounds was consistent when the recordings were analysed again. A number of interesting observations could be made. Less than half the children had all 5 phases and a number of different patterns were observed. Phase II was present in about two-thirds and was strongly associated with phase III, which itself was present in about 50% of children. The length of the individual Figure 4 The length of each phase was measured, in seconds, and phases also showed much variation and when some is shown in the figure as the median duration, ± Inter-quartile phases were absent the remaining phase(s) were range. longer. We found that phase V was more likely to

Journal of Human Hypertension Korotkoff sounds in children J O’Sullivan et al 201 be present in children with larger arm circumfer- in understanding the clinical significance of the Kor- ence. Arm circumference is positively associated otkoff phases of blood pressure. with increasing height and weight and therefore larger arm circumference may be the main expla- Acknowledgements nation for the fact that phase V is virtually always present in normal adults. However other factors We are grateful to the parents, teachers and children such as pulse pressure and arterial wall compliance of Heaton Manor school who supported the study, may also be important. As there is no consensus on and to Mrs Toni Allen who helped to organise the how the Korotkoff phases are produced,9,10 one can study and was funded by the Children’s Heart Unit only speculate as to the significance of the observed Fund (CHUF). The equipment for this study was variation in the presence and length of the phases in purchased by a grant from the Freeman Hospital Special Trustees. children with similar blood pressure. The apparent differences between our findings and those reported in historical adult studies6,7 might suggest that References arterial wall compliance is an important factor, but 1 Korotkoff NS. On the subject of methods of determin- methodological differences between the studies ing blood pressure [in Russian]. Bull Imperial Military make comparisons difficult. Med Academy, St. Petersburg 1905: 11: 365. Our study also provides some insights into the 2 Geddes LA, Hoff HE, Badger AS. Introduction of the problems of accurate diastolic blood pressure auscultatory method of measuring blood pressure – measurement in children. It was clear that phase IV including a translation of Korotkoff’s original paper. Cardiovasc Res Center Bull 1966; 5: 57–74. (muffling) sounds are of low amplitude and often 3 Gillman MW, Cook NR. Blood pressure measurement difficult to hear. Under the optimal listening con- in childhood epidemiological studies. Circulation ditions of our study phase IV could not be detected 1995; 92: 1049–1057. in 12% of children. The difficulty with the reliable 4 de Man SA et al. Blood pressure in childhood: pooled detection of phase IV is highlighted by the widely findings of six European studies. J Hypertens 1991; 9: different results of two large studies. A Finnish 109–114. study found that phase IV sounds were not detected 5 Bland JM, Altman DG. Statistical methods for in 3% of over 1000 12-year-old children11 and an assessing agreement between two methods of clinical measurement. Lancet 1986; i: 307–310. American study on children aged 10–15 years found 12 6 Swan JM. The auscultatory method of blood pressure no phase IV in over 50%. Using phase V for dias- determination: a clinical study. Int Clin 1914; 4: tolic blood pressure measurement is also prone to 130–190. error as the phase IV sounds generally fade rather 7 Goodman EH, Howell AA. Further clinical studies in than abruptly cease. The small difference in the the auscultatory method of determining blood press- length of phase IV when the recordings were reana- ure. Am J Med Sci 1911; 142: 334–353. lysed suggests that under standard clinical con- 8 Goodman EH, Howell AA. Clinical studies in the aus- ditions the reproducibility would be much poorer. cultatory method of determining blood pressure. Uni- versity Penn Med Bull 1910; 23: 469–475. This was the case in a study on between- and 9 Drzewiecki GM, Melbin J, Noordergraaf A. The Korot- within-visit variance of blood pressure, which con- koff sound. Annals of Biomed Engineering 1989; 17: cluded that diastolic blood pressure (using phase IV 325–359. or V) was a ‘strikingly imprecise measurement’ for 10 McCutcheon EP, Rushmer RF. Korotkoff sounds. An children aged 8–12 years.13 experimental critique. Circ Res 1967; 20: 149–161. Our study describes in detail the Korotkoff phases 11 Uhari M, Nuutinen M, Turtinen J, Pokka T. Pulse detectable in normal children under optimal listen- sounds and measurement of diastolic blood pressure ing conditions. This is the first study to describe all in children. Lancet 1991; 338: 159–161. the Korotkoff phases in children and it provides 12 Sinalko AR, Gomez-Marin O, Prineas RJ. Diastolic fourth and fifth phase blood pressure in 10–15 year old insight into the problems of accurate clinical children. Am J Epidemiol 1990; 132: 647–655. measurement of diastolic blood pressure in this age 13 Rosner B et al. Reproducibility and predictive values group. It is noteworthy that almost 100 years since of routine blood pressure measurements in children. their initial description we have made little progress Am J Epidemiol 1987; 126: 1115–1125.

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