Table 1.
Data on relationship between H. pylori infection (HPI) and bone status/osteoporosis.
| First Author, Year, Reference No, Country/Region | Population, Gender (F/M) |
Mean Age, Years |
HPI Detection Method | HPI Strain Identification |
Bone Status Assessment Methods, Skeletal Location |
HPI+ and OP, n (%) | HPI+ and Non -OP/Controls |
Association (Yes/No) |
|---|---|---|---|---|---|---|---|---|
| Figura N, 2005 [98], Italy | 240, M | 65 (55–82) | Serum antibody | CagA | DEXA, LS, FN; Urinary cross-laps, serum bALP, PTH, Ca, PO4, 25(OH)D |
51/80 (63.7%); CagA+: 30 (58.8%) |
107/160 (66.8%); CagA+: 43 (40.1%) |
Yes, if CagA+; increased levels of urinary cross-laps |
| Ozdem S, 2007 [105], Turkey | 61, 36/25 | 11.8 ± 3 (F) 10.1 ± 3 (M) |
RUT, histology | Serum P1NP, βCTX, OC, ALP, PTH, Ca, PO4 |
No | |||
| Kakehasi A, 2007 [107], Brazil | 50, F | 61.7 ± 7 (50–70) | RUT, histology, 13C-UBT |
DEXA, LS | 10/18 (55%) |
24/32 (75%) |
No | |
| Kakehasi A, 2009 [108], Brazil | 85, F | 63.7 ± 7.3 (HPI+); 62.5 ± 7.0 (HPI−) |
RUT, histology, 13C-UBT |
DEXA, LS, H | No | |||
| Figura N, 2010 [99], Italy | 1118, 935/183 | 62.5 ± 6 (F); 65.9 ± 6 (M) |
Serum antibody | CagA | DEXA | 41.5%; CagA + 30% |
43.9%; CagA + 21% |
Yes, if CagA+ |
| Akkaya N, 2011 [109], Turkey | 105, F | 65.3 ± 6.1 (OP+) 63.6 ± 6.5 (OP−) |
Serum antibodies | DEXA, LS, H | 41/58 (IgG+) (70.7%) |
35/47 (IgG+) (74.5%) |
No | |
| Asaoka D, 2014 [110], Japan | 200, 105/95 | 62.8 ± 7.7 (M) 63.4 ± 9 (F) |
Serum antibody, 13C-UBT |
DEXA, LS; serum bALP, NTX |
25/41 (61.0%) | 57/159 (35.8%) |
Yes, OR 5.33 (1.73–16.42) in PUD |
|
| Lin S, 2014 [111], Taiwan | 365, F | 77.3 (65–97) | RUT, histology | DEXA or osteoporosis medication use | 77/101 (76.2%) | 24/101 (23.8%) |
Yes, OR 2.03 (1.14–3.62) |
|
| Asaoka D, 2015 [106], Japan | 255, 135/120 |
63.2 ± 8.5 | Serum antibody, 13C-UBT |
DEXA, LS; serum bALP, NTX | 25/43 (58.1%) | 69/212 (32.5%) | Yes, OR 3.0 (1.31–6.88) |
|
| Mizuro S, 2015 [112], Japan | 230, M | >50; 62.1 ± 5.0 (TBD low), 58.4 ± 5.4 (TBD normal) |
Serum antibody | QUS, radius | 61/116 (52.5%) | 38/114 (33.3%) | Yes, OR 1.83 (1.04–3.21) |
|
| Fotouk-Kiai M, 2015 [113], Iran | 967, 392/575; H.p.+ 758, H.p.− 209 (controls) |
68.3 ± 6.8 (H.p.+) 69.3 ± 7.4 (H.p.−) |
Serum antibody | DEXA, LS, FN | 236/758 (31.1%) | 522/758 (68.9%) |
No, OR 0.76 (0.55–1.05) |
|
| Chung Y, 2015 [97], Korea | I, 126, M H.p.+ 657 H.p.− 469 |
54.4 ± 10.7 (H.p.+) 51.9 ± 12.1 (H.p.−) |
Serum antibody | DEXA, LS (L1-L4) |
173 */657 (26.3%) (LS); 114/657 (17.4%) (FN) |
484/657 (73.7%) (LS); 543/657 (82.6) (FN) |
Yes, only for lumbar BMD (not for total femur or femoral neck) | |
| Kalantarhormozi M, 2016 [96], Iran | 250, F; 16 (OP), 234 (controls) | 58.9 ± 8.0 | Serum antibody | DEXA, LS, F; bone turnover markers, OPG, RANK, Ca, PO4 | No | |||
| Shih H, 2016 [95], Taiwan | 5447 (H.p.+), 21,788 (controls) |
>20 | H.p. eradication treatment for PUD | DEXA | Yes, HR 1.62 (1.06–2.47) |
|||
| Chen L, 2017 [114], Taiwan | 2689, 1792/897 | >40 | 13C-UBT | FRAX (without BMD) |
F: 177/324↑ (54.6%); M: 54/93 (58.1%) |
No, for 10-year fracture risk prediction | ||
| Chinda D, 2017 [115], Japan | 473 F (healthy) | 52.2 ± 15.2 | Serum antibody (IgG), H.p. antigen in stool sample | QUS, calcaneus | 65 */118 (55.1%) | 53/118 (44.9%) |
No, OR 0.95 (0.55–1.63) for osteopenia |
|
| Abdolahi N, 2017 [116], Iran | 107 F, 34 with OP, 73 controls |
Post- menopausal |
Serum antibodies (IgA, IgG) | 70.6% IgA+ 82.0% IgG+ |
54.8% IgA+ 75.3% IgG+ |
No | ||
| Lu L, 2018 [19], China | 1867, 393/1474 | 13C-UBT | QUS, calcaneus | No, for BMD | ||||
| Pan B, 2018 [117], Taiwan |
867, 299/568 | 55.9 ± 11.3 | RUT | DEXA | 257/556 (46.2%) | 124/311 (39.9%) | Yes, OR 1.62, (1.12–2.35) for decreased BMD |
|
| Chinda D, 2019 [118], Japan | 268 M (healthy) | 49.1 ± 15.1 | Serum antibody (IgG), H.p. antigen in stool sample, serum pepsinogens | QUS, calcaneus | No, OR 1.31 (0.54–3.21) for atrophic gastritis, OR 0.74 (0.29–1.90) without gastritis |
Abbreviations: ALP, alkaline phosphatase; bALP, bone-specific ALP; βCTX, β-collagen1 carboxy-terminal telopeptide; Ca, calcium; DEXA, dual energy X-ray absorption; CagA, cytotoxin associated antigen A; DM, type 2 diabetes mellitus; FN, femur neck; H, hip; H.p, H. pylori; LS, lumbar spine; HR, hazard ratio; LS, lumbar spine; NTX, collagen type-1cross-linked N-telopeptide; OC, N-mid-osteocalcin; crosLaps, urinary type 1 collagen C-telopeptides; OPG, osteoprotegerin; OR, odds ratio (in brackets 95% confidential intervals); P1NP, N-terminal cross-links of human procollagen type1; PO4, phosphate; PTH, parathyroid hormone; QUS, quantitative ultrasonic densitometry; RANK, receptor activator of nuclear factor κB; RUT, rapid urease test; 25(OH)D, 25-hydroxy vitamin D; Serum antibody, serum anti-H.pylori antibody (ELISA kits); TBD, trabecular bone density; UBT, urea breast test; ↑, high 10-year fracture risk using the Fracture Risk Assessment tool (FRAX) scale without BMD; *, osteoporosis and osteopenia combined. Empty cells indicate that data were not mentioned.