ORIGINAL ARTICLE

A longitudinal study of radiological changes in the lumbarspine in asymptomatic Japanese military young adults

Osamu Nemoto & Akira Kitada & Yoshifumi Tsuda &

Junya Yokobe & Keitarou Matsukawa & You Ukegawa

Received: 13 October 2011 /Accepted: 23 May 2012 /Published online: 4 June 2012# EFORT 2012

AbstractObjective High prevalence of vertebral osteophytes hasbeen observed in men associated with heavy physical activ-ity and found to be associated with low back pain (LBP) inrecent reports. However, development of vertebral osteo-phytes and identification of their predictors in longitudinalobservational studies are not well known.Materials and methods In 1984, 45 Japanese Self DefenseForces male military parachutists aged 18 or 19 years, with-out a history of LBP and radiological abnormal findings,were investigated. After 25 years, 40 subjects were con-tacted and underwent repeated X-ray. At the 25-yearfollow-up evaluation, we studied developed lumbar degen-erative changes. All 40 subjects completed questionnaireson current LBP and lifestyle factors. Univariate analysis wasperformed to study the risk factors of LBP. Association ofvertebral osteophytes development with various factors wasstudied using univariate and multivariate analyses.Results The prevalence of vertebral osteophytes, disc spacenarrowing or facet joint osteoarthrosis was 70 %, 48 %, or57 % respectively. Current LBP rated as mild pain wasdemonstrated in 60 %. We did not find a significant associ-ation between LBP and various factors, although vertebralosteophytes showed a greater odds ratio. Among variousvariables in multiple logistic regression analysis, the numberof parachuting descents (≧250) and disc space narrowingwere significant predictors for the development of vertebralosteophytes.Discussion and Conclusions In asymptomatic and radiolog-ically normal young male parachutists, frequent parachuting

descents and disc space narrowing were associated withvertebral osteophytes formation.

Keywords Vertebral osteophytes . Longitudinal study .

Military parachutists . Disc space narrowing

Introduction

High prevalence rates of low back pain (LBP) resulting fromthe job-related physical activity have been demonstratedamong subjects with a history of military service [1–3].Disability discharges for LBP and physical limitation dutyrestriction profiles are issued in Japanese Self DefenseForces (JSDF). The relation between lumbar spine abnor-malities and LBP has been debated, presumably because ofpotential biases related to selection or its cross-sectionalobservation in nature. Another limitation presumes thatmost subjects show some degree of radiological abnormal-ities of the lumbar spine, even at young ages. Many radio-logical surveys have failed to demonstrate any significantcorrelations with LBP [4–7]. In contrast, several reportsshow a weak but significant association between degenera-tive changes and LBP [8–11]. Vertebral osteophytes (VOs)have not been regarded as important factors that influenceLBP; however, recent observational studies reported thatthey appear to play a role in the development of LBP [9,12]. In a cross-sectional study with middle aged men,O’Neill reported that VOs affecting the lumbar spine areassociated with LBP [12]. However, little data concerningthe natural history of lumbar VOs formation and associatedrisk factors exist [13–16].

Therefore, the aim of our study was to investigate thedevelopment of LBP and lumbar degenerative changes over25 years in initially asymptomatic and radiologically normal

O. Nemoto (*) :A. Kitada :Y. Tsuda : J. Yokobe :K. Matsukawa :Y. UkegawaOrthopaedic Surgery, Japanese Self Defense Forces Central Hospital,1-2-24, Ikejiri, Setagaya-ku Tokyo, Japane-mail: drsamusio@world.ocn.ne.jp

Eur Orthop Traumatol (2012) 3:135–139DOI 10.1007/s12570-012-0108-8

male young military parachutists. We also explored the riskfactors for the development of LBP and VOs.

Materials and methods

Subjects

For research on the incidence of lumbar degenerative change inmilitary parachutists approved by JSDF, 48male young recruitsaged 18 or 19 who enlisted for a certain parachute companywere investigated in 1984. Subjects included in this study hadno history of LBP, sciatica, or neurogenic claudication. Aftertaking anteroposterior, lateral, and bilateral oblique lumbarspine radiographs, subjects were excluded if they had abnormalradiologic findings such as VOs, disc space narrowing (DSN),spondylolysis, spinal deformity, wedged vertebra, or irregular-ity of the end-plate on plain X-ray. As a result, we selected 45JSDFmale recruits for entry. In 2009, three had retired from themilitary and could not be reached. Among 42 active dutypersonnel, 2 were excluded as they had lumbar surgery duringthe intervening period. Consequently, 40 subjects were able toparticipate in this follow-up study. For these subjects, the sameradiological entry examination and postal questionnaires wereperformed. The letter asked for information concerning epi-sodes of LBP, habit of smoking, alcohol consumption, andnumber of parachuting descents. Height and weight were takenfrom JSDF health records and BMI was calculated as weight(in kilograms) per height (in square meters).

All variables were expressed as binary outcomes foranalysis. Smoking versus nonsmoking history, alcohol con-sumption ≧3 days/week versus <3 days/week, BMI ≧25versus <25, increase of weight ≧10 kg versus <10 kg, num-ber of parachuting descent ≧250 versus <250. LBP wasdefined as a current pain lasting ≧7 consecutive days expe-rienced during the year prior to this study.

Radiological findings were assessed by a single trainedobserver (ON). The incidence of VO was defined as ≧2 mmin length according to the classification of Macnab et al. [17].DSNwas defined as≧1/3 decrease of the disc height, comparedto that of at entry. A summary grade reported by Lane et al. [18]was assigned to each lumbar spine based on the presence andseverity of VOs and DSN, grade00normal, grade10mild, andgrade20moderate–severe. Facet joint osteoarthrosis (FJOA)was evaluated by the semiquantitative method reported byPathria et al. [19], summarized as grade00normal, grade10narrowing, grade20narrowing+sclerosis or hypertrophy,grade30severe OAwith narrowing, sclerosis, and osteophytes,and scores≧grade2 were classified as FJOA.

Within-observer variation was assessed by test–retestanalysis of 20 randomly selected radiographs from thestudy. Good within-observer reproducibility (κ00.78–0.89)was found.

Statistical method

We calculated unadjusted odds ratios for outcomes of LBP orVOs in relation to the various factors, using logistic regres-sion. The independent variables for analysis were as follows;significant weight gain, habits of smoking or alcohol con-sumption, number of parachuting descents, and degenerativechanges such as DSN or FJOA during the intervening25 years. Variables that were significantly associated withVOs were subsequently included in a multiple logistic regres-sion analysis to determine their independent effects. Statisticalanalysis was performed by SPSS statistical software packageversion 11, and statistical significance was assigned to Pvalues less than 0.05.

Results

Table 1 shows the demographic data in 40 subjects at entryand at follow-up. The average follow-up period was 24.8±2.8 years. Analysis of lumbar radiographs made in 2009revealed that 10 of 40 subjects (25 %) had normal findingsand 30 subjects (75 %) had degenerative changes, including

Table 1 Demographic data of 40 subjects at entry and follow-up

Mean value±standard deviation

At entry At follow-up

Age (years) 18.1±0.3 43.0±0.9

Height (cm) 172.2±5.0 171.7±4.3

Weight (kg) 67.7±6.5 75.1±9.4

BMI 23.1±2.1 25.3±3.1

Fig. 1 Distribution of generative change

136 Eur Orthop Traumatol (2012) 3:135–139

19 subjects (48 %) with grade1 and 11 subjects (27 %) withgrade2. Incidence of degenerative changes was observed in27 subjects (68 %) for VOs, 19 subjects (48 %) for DSN, 23subjects (57 %) for FJOA, respectively. The distribution ofdegenerative changes is shown in Fig. 1. The number ofVOs or FJOA was greater in the lower spinal level. Incontrast, DSN showed relatively equal distribution withhighest prevalence at L3/4.

Twenty-four subjects (60 %) reported having a history ofpresent LBP, but no one had lost time from work because ofpain, indicating mild LBP in all subjects. Risk factors for LBPwere investigated in a univariate model. There was no signif-icant difference in age, height, weight and BMI between thosewith LBP and those without (Table 2). Although the numberof descents, weight gain, smoking, alcohol consumption,DSN and FJOA did not significantly predict LBP, develop-ment of VOs showed a nonsignificant but greater odds ratio insubjects with LBP (Table 3).

Next, we performed univariate analysis to clarify therelationship of various factors with VOs development. Thedemographic data of the subjects with or without VOsshowed no differences in age, height, weight and BMI.Table 4 demonstrates unadjusted odds ratios for develop-ment of VOs. Factors associated with an increased risk ofVOs were number of descents (≧250), DSN, and FJOA.Weight gain (≧10 kg) during follow-up, smoking and alcoholconsumption did not significantly predict VOs development.Nonsignificant variables at this stage were excluded. Threesignificant variables were selected for the multiple logisticregression analysis. The multiple logistic regression analysis

demonstrated that the number of descents (≧250) and DSNwere significantly associated with VOs (Table 5).

Discussion and conclusion

A number of studies on different athletes and heavy physicalworkers have reported high but variable rate of degenerativechanges in the lumbar spine [20–23]. In contrast, there arefew data concerning those changes in military parachutists.Among ex-military parachutists with a mean age of 55 years,Leslie et al. demonstrated that 85 % had some degree ofdegeneration, with 28 % showing moderate or greater de-generative change [24]. Our results also showed a high prev-alence rate of degenerative changes, even though our subjectswere younger. Accumulations of vertical stress on lumbarspine in parachuting and ordinary physical stress in militarybasic training might be contributing factors.

The development of VOs and FJOA was observed morefrequently in the lower lumbar spine, but DSN showed rela-tively equal distribution at each spinal level. This may reflectthe different degenerative or aging process in DSN, comparedto that of VOs and FJOA. The distribution of VOs is differentfrom that described in an autopsy series showing high preva-lence at L3/4 [25]. This may due to the fact that localizedrepetitive stress in the lower lumbar spine due to parachutingmay increase the formation of VOs.

Compared with the high prevalence of radiological abnor-malities, the intensity of current LBP was mild, not disruptingtheir military jobs, although 60 % of the subjects reportedLBP. Lundin et al. [22] also showed in the analysis of LBP andradiological abnormalities among athletes that regular partic-ipation in exercise and sports was associated with less backpain, despite an increase in degenerative disc changes. Thisfinding is similar to our military parachutists. The causeremains speculative, but there is a possibility that during theirtraining, military parachutists gain a higher tolerance for pain,as proposed by Granhed et al. [26] or perhaps active militarypersonnel more resemble athletes in their level of physicalactivity than the general population.

Table 2 Demographic data of subjects with or without LBP

Subjects with LBP Subjects without LBP P value(n024) (n016)

Age (years) 42.9±0.9 43.1±0.9 0.581

Height (cm) 172.2±4.4 171.1±6.0 0.940

Weight (kg) 75.0±9.9 75.1±9.0 0.973

BMI 25.3±3.5 25.3±2.4 0.968

Values are expressed as mean±SD

Table 3 Unadjusted oddsratio for various factorsrelated to LBP

LBP(+) LBP(−) OR (95%CI)(n024) (n016)No. of subjects (%) No. of subjects (%)

Increase of weight 8 (33) 5 (31) 1.10 (0.28–4.26)

Smoking 19 (79) 12 (75) 1.26 (0.28–5.69)

Alcohol 16 (67) 14 (88) 0.28 (0.05–1.57)

Descent 19 (79) 10 (63) 2.28 (0.55–9.36)

VO 12 (79) 8 (50) 3.80 (0.95–15.2)

DSN 12 (50) 7 (44) 1.28 (0.36–4.58)

FJOA 15 (63) 10 (63) 1.00 (0.27–3.69)

Eur Orthop Traumatol (2012) 3:135–139 137

With regard to the association of LBP with physicalcharacteristics or lifestyle factors, literature reviews provideconflicting views. Review of the literature by Leboeuf-Ydeet al. reveals that smoking should be considered a weak riskindicator and not a cause of LBP [27]. As for the linkbetween obesity or weight gain and LBP, the increasedmechanical demands resulting from these factors have beensuspected of causing LBP through excessive wear and tear.However, a closer examination of the literature also revealssome confusion [28]. Excessive alcohol consumption isanother prevalent lifestyle factor that is generally known tocontribute to certain diseases, such as cardiovascular diseaseand disorders of the liver. A review of the literature revealsthat alcohol in relation to LBP has not evoked the sameamount of interest as smoking and obesity in relation to LBP[29]. We found no significant associations of these factorswith LBP. With a larger sample size, some factors may wellprove to be significant contributors to LBP development.

The relation between radiological abnormalities in the lum-bar spine and LBP has been published in a number of reports.In a cross-sectional study, Kellgren and Lawrence [30] foundsome association between radiological changes and past, butnot present, LBP. Frymoyer [6], on the other hand, concludedthat single DSN and VO were equally prevalent in symptom-atic and asymptomatic men. The recent cross-sectional studyof middle aged subjects by O’Neill et al. [12] revealed thatVOs were associated with increased BMI and heavy physicalactivity, and lumbar VOs were associated with LBP, particu-larly in men. In the analysis of athletes of different sports,Lundin et al. [22] found no correlation between LBP and anyspecific radiologic abnormalities; however, they demonstrateda significant correlation between LBP and a decrease in discheight during a 13-year follow-up period. Thus, the relationbetween radiological abnormalities in lumbar spine and LBPhas been debated. This longitudinal study assessed the statusof degenerative changes of lumbar spine by plain X-ray atentry and follow-up in conjunction with various demographic,radiomorphologic, and occupational risk factors. While thedevelopment of VOs showed a trend toward predicting LBP,the result did not achieve statistical significance, probablyreflecting the small sample size.

We found clear predictive effects on VOs development ofDSN and the number of parachuting descents (>250). Thecause for the association of these factors remains speculative,but a recent study has shown significant correlations betweenosteophytes, end-plate sclerosis, and disc space narrowing inthe lumbar spine [31]. It is also suggested that degeneratedintervertebral discs shown as DSN on plain X-ray can lead tothe formation of VOs because the shock absorbing capacity ofthe vertebral column is impaired. In general, it would appearthat VOs begin to form whenever the compression forces onthe vertebral end-plates exceed the capacity of the vertebralbone to resist those compression forces. Additionally, the peakdeceleration g forces on the spine in a head–toe directionduring a military parachute landing have been shown to rangebetween 3.2 and 17.0 with a mean of 5.8 [32]. Consideringthese epidemiologic and pathophysiologic data, it is not sur-prising that the formation of VOs can be influenced by DSNor frequent parachuting.

As with any study, this study has several weak points thatmay limit potential generalization of the results. The smallsample size and the rather weak power associated with thestudy is a problem. Given the complexity of the initial andrepeated X-ray after 25 years, it was not easy to includemore subjects in this trial. Other drawbacks were not includ-ing female, a limited subject pool of military parachutists,and a restricted radiological analysis using plain X-ray.Therefore, we are planning to conduct a similar study target-ing the general population, including females, by MRI aswell as plain X-ray.

Despite the aforementioned limitations, this is the firststudy to investigate the development of VOs as well as theserisk factors with such a longitudinal design using asymp-tomatic young adults without radiological abnormalities atbaseline.

Table 4 Unadjusted oddsratio for various factors relatedto VOs

VOs (+) VOs (−) OR (95%CI)(n027) (n013)No. of subjects (%) No. of subjects (%)

Increase of weight 16 (59) 5 (38) 2.32 (0.60–9.02)

Smoking 13 (48) 6 (46) 1.08 (0.28–4.08)

Alcohol 18 (67) 12 (92) 0.16 (0.02–1.49)

Descent 23 (85) 10 (63) 6.70 (1.46–30.73)

DSN 17 (63) 2 (7) 9.35 (1.71–51.03)

FJOA 20 (74) 5 (28) 4.57 (1.11–18.73)

Table 5 Adjusted odds ratio for various factors related to VO

Odds ratio 95 % CI P value

Descent 7.979 1.298–49.036 0.025

DSN 10.819 1.618–72.338 0.014

138 Eur Orthop Traumatol (2012) 3:135–139

We conclude that frequent parachuting descent and newlydeveloped DSN are important predictors of VO formation inasymptomatic and radiologically normal young male para-chutists. Further studies will be needed to clarify the riskfactors for LBP.

Acknowledgment The authors did not receive any outside fundingor grants in support of their research for or preparation for this work.Neither they nor a member of their immediate families received pay-ments or other benefits or a commitment or agreement to provide suchbenefits from a commercial entity. No commercial entity paid ordirected, or agreed to pay or direct, any benefits to any research fund,foundation, division, center, clinical practice, or other charitable ornon-profit organization with which the authors, or a member of theirimmediate families, are affiliated or associated.

References

1. Cady LD, Bischoff DP, O’Connell ER, Thomas PC, Allan JH (1979)Strength and fitness and subsequent back injuries in firefighters. JOccup med 21(4):269–272

2. Mattila VM, Sahi T, Jormanainen V, Pihlajamaki H (2008) Lowback pain and its risk indicators: a survey of 7040 Finnish maleconscripts. Eur Spine J 17(1):64–69

3. Mattila VM, Sillanpaa P, Visuri T, Pihlajamaki H (2008) Incidenceand trends of low back pain hospitalization during military service—an analysis of 387070 Finnish young males. BMC MusculoskeletalDisord 10:10

4. Hult (1954) Cervical, dorsal and lumbar spinal syndromes. ActaOrthop Scandinavica 17:1–102

5. Fullenlove TM,Williams AJ (1957) Comparative Roentgen findingsin symptomatic and asymptomatic backs. Radiology 68(4):572–574

6. Frymoyer JW, Newberg A, Pope MH, Wilder DG, Clements J,MacPherson B (1984) Spine radiographs in patients with low backpain. J Bone and Joint Surg 66-A(7):1048–1054

7. Kalichman L, Kim DH, Li L, Guermazi A, Hunter DJ (2010)Computed tomography evaluated features of spinal degeneration:prevalence, intercorrelation, and association with self-reported lowback pain. Spine J10(3):200–208

8. Elfering A, Semmer N, Birkhofer D, Zanetti M, Hodler J, Boos N(2002) Risk factors for lumbar disc degeneration. Spine 27(2):125–134

9. Hicks GE, Morone N, Weiner DK (2009) Degenerative lumbardisc and facet disease in older adults. Spine 34(12):1301–1306

10. de SchepperEI DJ, van Meurs JB, Ginai AZ, Popham M, HofmanA, Koes BW, Bierma-Zienstra SM (2010) The association betweenlumbar disc degeneration and low back pain: the influence of age,gender, and individual radiographic features. Spine 35(5):531–536

11. Pye SR, Reid DM, Smith R, Adams JE, Nelson K, Silman AJ,O’Neill TW (2004) Radiographic features of lumbar disc degenera-tion and self-reported back pain. J Rheumatol 31(4):753–758

12. O’Neill TW, McCloskey EV, Kanis JA, Bhalla AK, Reeve J, ReidDM, Todd C, Woolf AD, Silman AJ (1999) The distribution,determinants, and clinical correlates of vertebral osteophytosis: apopulation based survey. J Rheumatol 26(4):842–848

13. Lane NE, Michel B, Bjorkengren A (1993) The risk of osteoar-thritis with running and aging: a 5-year longitudinal study. JRheumatol 20(3):461–468

14. Yasukawa Y (1994) Age changes in the lumbar spine: radiologicalfollow-up studies over more than 10 years. J Jpn Orthop Assoc 68(9):854–863

15. Symmonds DP, van Hemert AM, Vandenbroucke JP, ValkenburgHA (1991) A longitudinal study of back pain and radiologicalchanges in the lumbar spines of middle aged women. II.Radiographic findings. Ann Rheum Dis 50(3):162–166

16. Hassett G, Hart DJ, Manek NJ, Doyle DV, Spector TD (2003) Riskfactors for progression of lumbar spine disc degeneration. ArthritisRheum 48(11):3112–3117

17. Macnab I (1971) The traction spur. An indicator of segmentalinstability. J Bone Joint Sug Am 53(4):663–670

18. Lane NY, Nevitt MC, Genant H, Hochberg MC (1993) Reliabilityof new indices of radiographic osteoarthritis of the hand and hiplumbar disc degeneration. J Rheumatol 20(11):1911–1918

19. Pathria M, Sartoris DJ, Resnick D (1987) Osteoarthritis of the facetjoints: accuracy of oblique radiographic assessment. Radiology164(1):227–230

20. Goldstein JD, Berger PE, Windler GE, Jackson DW (1991) Spineinjuries in gymnasts and swimmers. An epidemiologic investiga-tion. Am J Sports Med 19(5):463–468

21. Iwamoto J, Abe H, Tsukimura Y, Wakano K (2004) Relationshipbetween radiographic abnormalities of lumbar spine and incidenceof low back pain in high school and college football players: aprospective study. Am J Sports Med 32(3):781–786

22. Lundin O, Hellstrom M, Nilsson I, Sward L (2001) Back pain andradiological changes in the thoraco-lumbar spine of athletes. Along-term follow up. Scand J Med Sci Sports 11(2):103–109

23. Schmitt H, Dubljanin E, Schneider S (2004) Radiographic changesin the lumbar spine in former elite athletes. Spine 29(22):2554–2559

24. Murray-Leslie CF, Lintott DJ, Wright V (1977) The spine in sportand veteran military parachutists. Ann Rheum Dis 36(4):337–342

25. Nathan H (1962) Osteophytes of the vertebral column. J BoneJoint Surg 42-A(1):243–268

26. Granhed H, Morelli B (1988) Low back pain among retiredwrestlers and heavyweight lifters. Am J Sports Med 16(5):530–533

27. Leboeuf-Yde C (1999) Smoking and low back pain. A systematicliterature review of 41 journal articles reporting 47 epidemiologicstudies. Spine 24(14):1463–1470

28. Leboeuf-Yde C (2000) Body weight and low back pain. A sys-tematic literature review of 56 journal articles reporting 65 epide-miologic studies. Spine 25(2):226–237

29. Leboeuf-Yde C (2000) Alcohol and low back pain: a systematicliterature review. J Manipulative Physiol Ther 23(5):343–346

30. Kellgren JH, Lawrence JS (1958) Osteo-arthrosis and diskdegeneration in an urban population. Ann Rheum Dis17:388–397

31. Pye SR, Reid DM, Lunt M, Adams JE, Silman AJ, O’Neill TW(2007) Lumbar disc degeneration: association between osteo-phytes, end-plate sclerosis and disc space narrowing. Ann RheumDis 66(3):330–333

32. Reid D, Doerr JE, Doshier HD, Ellertson DG (1971) Accelerationand opening shock forces during free fall parachuting via FM/AMtelemetry. Aerospace Medicine 42(11):1207–1212

Eur Orthop Traumatol (2012) 3:135–139 139